Home Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
Article Open Access

Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway

  • YanMei Liu , WenLi Ji , Na Yue and Weidong Zhou EMAIL logo
Published/Copyright: October 1, 2021
Download Article (PDF)
Open Life Sciences
From the journal Open Life Sciences Volume 16 Issue 1

Abstract

Ubiquitin-conjugating enzyme E2T (UBE2T) functions as an E2 ubiquitin-conjugating enzyme in the ubiquitin-proteasome degradation system and mediates cellular processes, such as cell cycle, proliferation, and differentiation. UBE2T has been considered to be an oncogene in a variety of tumors. However, the oncogenic role of UBE2T in cervical cancer remains unclear. In this study, our results first showed that the expression of UBE2T was higher in both of cervical cancer tissues and cells than that in the normal tissues and cells. Knockdown of UBE2T reduced cervical cancer cell viability and suppressed the proliferation, invasion, and migration. However, overexpression of UBE2T contributed to cervical cancer cell growth and metastasis. Moreover, UBE2T overexpression cervical cancer cells demonstrated enhanced self-renewal capacity with upregulation of SOX2, Oct-4, and Nanog protein. Silencing of UBE2T downregulated protein expression of SOX2, Oct-4, and Nanog in cervical cancer cells reduced self-renewal capacity. Furthermore, ectopic UBE2T expression promoted protein expression of glucose-regulated protein 78 (GRP78) and focal adhesion kinase (FAK) phosphorylation in cervical cancer cells. The knockdown of UBE2T reduced protein expression of GRP78 and FAK phosphorylation. Collectively, UBE2T promoted cervical cancer stem cell traits and exerted an oncogenic role through activation of the GRP78/FAK pathway.

Keywords: UBE2T; stem cell; cervical cancer; progression; GRP 78; FAK

1 Introduction

Cervical cancer ranks as the fourth leading cause of malignance-related mortality in women worldwide and the third most common cancer [1,2]. Although the widespread implementation of screening programs has reduced morbidity and mortality of cervical cancer in recent years, it remains a major public health problem, particularly in advanced cases [3]. Recent advancements in therapeutic strategies, such as chemotherapy, surgery, and radiotherapy, have improved patients’ survival rate with primary cervical carcinoma [4]. However, the advanced cases of cervical cancer with local or distant metastasis reduce the 5-year survival rate to 50% [5]. Therefore, efforts that focus on the identification of tumor-specific markers that predict the biological behavior of cervical cancer would be crucial for the prevention of cervical cancer cell motility and aggressiveness, further repressing the cancer occurrence and development.

Ubiquitin-conjugating enzyme E2T (UBE2T) belongs to the ubiquitin-proteasome system that covalently links ubiquitin to the lysine residues of target proteins and chains [6]. Since polyubiquitin chains are known to play a key role in the regulation of tumor progression, UBE2T is regarded as a potential therapeutic target for tumors [6]. Study has shown that UBE2T was upregulated in bladder cancer tissues and cell lines, and knockdown of UBE2T reduced the proliferation of bladder cancer cells, induced cell cycle arrest in the G2/M phase, and increased the apoptosis [7]. UBE2T has also been shown to be an oncogene in non-small cell lung cancer [8], renal cell carcinoma [9], and hepatocellular carcinoma [10]. However, the role of UBE2T in cervical cancer is still not clear.

Glucose-regulated protein 78 (GRP78) is expressed in the lung, brain, or liver and functions as a stress-induced endoplasmic reticulum chaperone [11]. Overexpression of GRP78 in various tumors was found to be implicated in biological processes, including cell survival, invasion, and metastasis [11]. Focal adhesion kinase (FAK) is a nonreceptor tyrosine kinase that plays a key role in modulation of integrin-mediated signaling pathways between cells and the extracellular matrix [12]. FAK functions as a critical regulator in tumor cell survival, invasion, and metastasis [12]. GRP78 has been shown to promote tumor progression through activation of FAK pathway [13]. GRP78/FAK was also reported to be involved in the tumor metastasis of cervical cancer [14]. Downregulation of GRP78 was implicated in the suppression of cervical cancer development [15]. Since previous study has shown that UBE2T interacted with GRP78 and promoted glioma cell migration and invasion [16], we hypothesized that UBE2T may function as an oncogene in cervical cancer through GRP78/FAK pathway in this study.

2 Materials and methods

2.1 Clinical specimens

Forty pairs of cervical cancer and adjacent normal tissues were obtained from patients which were pathologically diagnosed as cervical cancer. Patients with written informed consents were recruited at Affiliated Cancer Hospital of Xinjiang Medical University from 2016 to 2019.

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies, and in accordance with the tenets of the Helsinki Declaration and has been approved by the Affiliated Cancer Hospital of Xinjiang Medical University.

2.2 qRT-PCR

RNAs were isolated from cervical cancer and normal tissues via Trizol (Invitrogen, Carlsbad, CA, USA). The RNAs were reverse-transcribed into cDNAs and conducted with qRT-PCR analysis of UBE2T using SYBR Green Master (Roche, Mannheim, Germany). The following primers for UBE2T (forward: 5′-TTGATTCTGCTGGAAGGATTTG-3′; reverse: 5′-CAGTTGCGATGTTGAGGGAT-3′) and GAPDH (forward: 5′-TGACCACAGTGGATGCCAT-3′; reverse: 5′-TTACTCCTTGGAGGCCATGT-3′) were used in this study. GAPDH was used as endogenous control.

2.3 Cell culture and transfection

Human cervical cancer cell lines (HeLa, Caski, Siha) and normal human endocervical epithelial cell line (Endl/E6E7) were obtained from Cell Resource Center of Shanghai Academy of Sciences (Shanghai, China). Cells were cultured in Dulbecco’s modified Eagle’s medium (GE Healthcare Life Sciences, Little Chalfont, UK) containing 10% fetal bovine serum (GE Healthcare Life Sciences) at a 37°C incubator. For cell transfection, siRNA-mediated knockdown (si-UBE2T), pcDNA-mediated overexpression of UBE2T (pcDNA–UBE2T), and pcDNA-GRP78 were provided by GenePharma (Suzhou, China). HeLa and Caski were seeded into a 6-well plate and transfected with siRNAs and pcDNAs by Lipofectamine 2000 (Invitrogen).

2.4 Western blot

RIPA buffer (Ding Guo Chang Sheng Biotech, Beijing, China) was used to lyse the tumor tissues and cells on ice. The protein concentration of the supernatants collected from the lysates was calculated using a bicinchoninic acid protein assay kit (Pierce Biotechnology, Rockford, IL, USA). Samples (30 µg) were separated by SDS-PAGE and then transferred to PVDF membrane. The membrane was probed with anti-UBE2T and anti-GAPDH (1:2,000; Abcam, Cambridge, MA, USA), anti-FAK and anti-p-FAK (1:2,500; Abcam), anti-SOX2 and anti-Oct4 (1:3,000; Abcam), anti-Nanog, or anti-GRP78 (1:4,000; Abcam). Following incubation with horseradish peroxidase-conjugated immunoglobulin G (1:5,000; Abcam), the blots were detected by enhanced chemiluminescence (KeyGen, Nanjin, China).

2.5 Cell viability and proliferation assays

HeLa and Caski under siRNAs or pcDNAs transfection were seeded into a 96-well plate for 24, 48, or 72 hours. MTT solution (5 mg/mL; Beyotime, Beijing, China) was added into each well and incubated for 4 h. Following dissolving of the formazan products by DMSO, absorbance at 490 nm was detected by a microplate reader (Bio-Rad, Hercules, CA, USA). For cell proliferation assay, HeLa and Caski under siRNAs or pcDNAs transfection were seeded in a 6-well plate and cultured for 14 days. Paraformaldehyde-fixed and crystal violet-stained cells were observed under a light microscope (Olympus, Tokyo, Japan).

2.6 Wound healing and invasion assays

For wound healing, HeLa and Caski cells under siRNAs or pcDNAs transfection were seeded into a six-well plate until 90% confluence. A pipette tip was used to induce a scratching wound in the well. Twenty-four hours later, the wound width was calculated under an inverted Olympus IX50 microscope. For invasion assay, HeLa and Caski cells in serum-free medium were placed into the upper chamber of Matrigel-coated Transwell chamber (Biosciences, San Jose, CA, USA). The lower chamber was supplied with medium containing 20% fetal bovine serum. After 24 h of incubation, cells in the lower chamber were fixed in 4% paraformaldehyde and stained with hematoxylin. Cells were counted under the light microscope.

2.7 Tumorsphere culture

HeLa and Caski under siRNAs or pcDNAs transfection were cultured in medium (DMEM/F12 basal medium containing 20 ng/mL basic fibroblastic growth factor, 20 ng/mL human recombinant epidermal growth factor, N2 and B27 supplements) (PeproTech Inc., Rocky Hill, NJ, USA) and seeded into a 24-well ultralow attachment plates at a density of 200 cells per well. Two weeks later, the tumorspheres were aroused and counted under the light microscope.

2.8 Statistical analysis

Results from three independent experiments were presented as mean ± SD. Statistical analyses between different groups were performed with one-way analysis of variance or Student’s t test under SPSS19.0 software. Values were considered significant at p < 0.05.

3 Results

3.1 Upregulation of UBE2T in cervical cancer

Microarray analysis based on GEPIA (Gene Expression Profiling Interactive Analysis) database showed that UBE2T was upregulated in the cervical cancer tissues (n = 306) compared to the normal tissues (n = 13) (Figure 1a). Western blotting assay also identified the upregulation of UBE2T in the tumor tissues (Figure 1b) and cervical cancer cell lines (Figure 1c). Moreover, mRNA expression of UBE2T was also upregulated in the cervical cancer tissues compared with normal tissues (Figure 2b). These results suggested that UBE2T might be related to cervical cancer progression.

Figure 1 Upregulation of UBE2T in cervical cancer. (a) UBE2T was upregulated in the cervical cancer tissues (n = 306) compared to the normal tissues (n = 13) based on GEPIA database shown. (b) Protein and mRNA expression of UBE2T were upregulated in the cervical cancer tissues compared to the normal tissues. (c) Protein expression of UBE2T was upregulated in the cervical cancer cells (HeLa, Caski, and Siha) compared to the normal cells (End1/E6E7).
Figure 1

Upregulation of UBE2T in cervical cancer. (a) UBE2T was upregulated in the cervical cancer tissues (n = 306) compared to the normal tissues (n = 13) based on GEPIA database shown. (b) Protein and mRNA expression of UBE2T were upregulated in the cervical cancer tissues compared to the normal tissues. (c) Protein expression of UBE2T was upregulated in the cervical cancer cells (HeLa, Caski, and Siha) compared to the normal cells (End1/E6E7).

Figure 2 UBE2T contributed to cervical cancer cell growth. (a) Transfection with si-UBE2T in HeLa cells decreased the protein expression of UBE2T, while pcDNA–UBE2T increased the expression. (b) Cell viability of HeLa and Caski was reduced by si-UBE2T, while enhanced by pcDNA–UBE2T. (c) Knockdown of UBE2T repressed the cell proliferation of HeLa and Caski, while overexpression of UBE2T promoted the proliferation. (d) Knockdown of UBE2T repressed the cell invasion of HeLa and Caski, while overexpression of UBE2T promoted the invasion. (e) Knockdown of UBE2T repressed the cell migration of HeLa and Caski, while overexpression of UBE2T promoted the migration. *, ** vs siNC, p < 0.05, p < 0.01. ## vs pcDNA, p < 0.01.
Figure 2

UBE2T contributed to cervical cancer cell growth. (a) Transfection with si-UBE2T in HeLa cells decreased the protein expression of UBE2T, while pcDNA–UBE2T increased the expression. (b) Cell viability of HeLa and Caski was reduced by si-UBE2T, while enhanced by pcDNA–UBE2T. (c) Knockdown of UBE2T repressed the cell proliferation of HeLa and Caski, while overexpression of UBE2T promoted the proliferation. (d) Knockdown of UBE2T repressed the cell invasion of HeLa and Caski, while overexpression of UBE2T promoted the invasion. (e) Knockdown of UBE2T repressed the cell migration of HeLa and Caski, while overexpression of UBE2T promoted the migration. *, ** vs siNC, p < 0.05, p < 0.01. ## vs pcDNA, p < 0.01.

3.2 UBE2T contributed to cervical cancer cell growth

HeLa and Caski were conducted with gain- and loss-of-functional assays through transfection with siRNA and pcDNA, respectively. Transfection with si-UBE2T decreased the protein expression of UBE2T, while pcDNA–UBE2T increased its expression (Figure 2a). Cell viability of HeLa and Caski was reduced by si-UBE2T, while enhanced by pcDNA–UBE2T (Figure 2b). Moreover, knockdown of UBE2T repressed the cell proliferation (Figure 2c), invasion (Figure 2d), and migration (Figure 2e) of HeLa and Caski. However, the cell proliferation (Figure 2c), invasion (Figure 2d), and migration (Figure 2e) of HeLa and Caski were promoted by overexpression of UBE2T. These results indicated the proliferative and pro-invasive effects of UBE2T on cervical cancer.

3.3 UBE2T contributed to stemness of cervical cancer cell

The effect of UBE2T on self-renewal capacity of cervical cancer cell was assessed through tumorsphere formation assay. UBE2T-silenced HeLa and Caski cells showed reduced typical tumorspheres compared with the control (Figure 3a), while overexpression of UBE2T enhanced the tumorspheres (Figure 3a). The stem cell-related transcription factors, including SOX2, Oct4, and Nanog, were decreased in UBE2T-silenced cells (Figure 3b) and increased in UBE2T-overexpressed cells (Figure 3b), revealing that cervical cancer stem cell traits were promoted by UBE2T.

Figure 3 UBE2T contributed to stemness of cervical cancer cell. (a) UBE2T-silenced HeLa and Caski cells showed reduced typical tumorspheres compared to the control, while overexpression of UBE2T enhanced the tumorspheres. (b) Knockdown of UBE2T decreased protein expression of SOX2, Oct4, and Nanog in HeLa cells, while overexpression of UBE2T increased the protein expression. ** vs siNC, p < 0.01. ## vs pcDNA, p < 0.01.
Figure 3

UBE2T contributed to stemness of cervical cancer cell. (a) UBE2T-silenced HeLa and Caski cells showed reduced typical tumorspheres compared to the control, while overexpression of UBE2T enhanced the tumorspheres. (b) Knockdown of UBE2T decreased protein expression of SOX2, Oct4, and Nanog in HeLa cells, while overexpression of UBE2T increased the protein expression. ** vs siNC, p < 0.01. ## vs pcDNA, p < 0.01.

3.4 UBE2T contributed to GRP78/FAK activation

Protein expression of FAK was not affected by UBE2T-silencing or UBE2T-overexpressing in HeLa cells (Figure 4). However, FAK phosphorylation was reduced in UBE2T-silenced HeLa cells and enhanced in UBE2T-overexpressing HeLa cells (Figure 4). Moreover, GRP78 was also downregulated by knockdown of UBE2T, while upregulated by overexpression of UBE2T (Figure 4). HeLa was cotransfected with si-UBE2T and pcDNA-GRP78. Overexpression of GRP78 attenuated UBE2T silencing-induced decrease in p-FAK (Figure A1). Decreased cell viability in HeLa induced by silencing of UBE2T was also restored by overexpression of GRP78 (Figure A1), demonstrating that UBE2T contributed to cervical cancer cell growth and metastasis through GRP78/FAK activation.

Figure 4 UBE2T contributed to GRP78/FAK activation. Knockdown of UBE2T decreased protein expression of FAK phosphorylation and GRP78 in HeLa cells, while overexpression of UBE2T increased the protein expression. ** vs siNC, p < 0.01. ## vs pcDNA, p < 0.01.
Figure 4

UBE2T contributed to GRP78/FAK activation. Knockdown of UBE2T decreased protein expression of FAK phosphorylation and GRP78 in HeLa cells, while overexpression of UBE2T increased the protein expression. ** vs siNC, p < 0.01. ## vs pcDNA, p < 0.01.

4 Discussion

Ubiquitin-mediated degradation system, including E1, E2, and E3 enzymes, was implicated in the physiologic processes of tumor cells [17]. E2 enzymes are found to be dysregulated in a variety of cancers and function as diagnostic, prognostic, or therapeutic targets of tumors through modulation of the stability of target proteins [17]. For example, E2-EPF, an ubiquitin-conjugating enzyme, was overexpressed in the cervical cancer and associated with the aggressivity and growth of tumor cells [18]. Since UBE2T has been shown to be involved in the maintenance of chromosome stability and cell proliferation, thereby indicating the oncogenic nature in various tumors [17], the role of UBE2T in cervical cancer was then investigated in this study.

Higher expression of UBE2T in cervical cancer tissues and cells was first identified in this study. Previous study has shown that UBE2T was overexpressed in gastric cancer and predicted the poor prognosis [19]. The correlation between UBE2T and the clinical characteristics of patients with cervical cancer should be investigated to validate the diagnostic or prognostic roles in the future.

The oncogenic role of UBE2T in cervical cancer was then confirmed by the functions assays in this study. Results showed that ectopic expression of UBE2T enhanced the cell viability, cell proliferation, invasion, and migration of HeLa cells. Moreover, the cervical cancer cell growth and metastasis were suppressed by knockdown of UBE2T. Cervical cancer cells gain the mesenchymal phenotype and lose the epithelial characteristic features during tumor progression [20], and UBE2T promoted the ubiquitination-mediated FOXO1 degradation to facilitate the epithelial-mesenchymal transition of non-small cell lung cancer [21]. The effect of UBE2T on epithelial-mesenchymal transition of cervical cancer cells should be investigated in further researches.

Cervical cancer stem cells have self-renewal property and could differentiate into tumor cells for the tumorigenesis, thus representing a potential therapeutic target for the treatment of cervical cancer [22]. Leucine-rich repeat-containing G-protein-coupled receptor 5 promoted the cervical cancer stem cell traits, and knockdown of leucine-rich repeat-containing G-protein-coupled receptor 5 suppressed the tumorigenicity of cervical cancer cells [23]. UBE2T is first identified in the hematopoietic stem cells and plays critical role in the maintaining of hepatocellular carcinoma stem cells [24]. The stem cell-related transcription factors, including SOX2, Oct4, and Nanog, were decreased in UBE2T-silenced HeLa cells in this study, suggesting that knockdown of UBE2T might suppress the stem cell-like features in cervical cancer.

Different pathways, including PI3K/AKT [9], wnt/β-catenin [8], and GRP78 [16], were involved in UBE2T-mediated tumor progression. Results in this study showed that protein expression of phosphorylated FAK and GRP78 was enhanced in cervical cells with UBE2T overexpression and reduced by UBE2T silencing. GRP78, upregulated in the cervical cancer [25], has been shown to activate FAK to promote the hepatocellular carcinoma progression [26]. FAK activation was involved in the tumorigenesis of cervical cancer [27]. Therefore, results in this study indicated that UBE2T contributed to cervical cancer cell growth through activation of GRP78/FAK pathway.

In summary, UBE2T promoted the growth and metastasis of cervical cancer and facilitated the maintaining of the stem cell-like features in cervical cancer. Suppression of GRP78/FAK activation was implicated in the suppressive effect of UBE2T silencing on cervical cancer. Therefore, UBE2T might be a novel target for the treatment of cervical cancer.

tel: +86-0912-564-1770

  1. Funding information: The authors state no funding involved.

  2. Author contributions: YanMei Liu and WenLi Ji designed the study and supervised the data collection; Na Yue analyzed the data and interpreted the data; and Weidong Zhou prepared the manuscript for publication and reviewed the draft of the manuscript. All authors have read and approved the manuscript.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Appendix

Figure A1 Overexpression of GRP78 attenuated UBE2T silence-induced decrease of p-FAK. (a) Decrease of cell viability in HeLa induced by silence of UBE2T was also restored by overexpression of GRP78 (b). *, ** vs siNC, p < 0.05, p < 0.01. #, ## vs si-UBE2T, p < 0.05, p < 0.01.
Figure A1

Overexpression of GRP78 attenuated UBE2T silence-induced decrease of p-FAK. (a) Decrease of cell viability in HeLa induced by silence of UBE2T was also restored by overexpression of GRP78 (b). *, ** vs siNC, p < 0.05, p < 0.01. #, ## vs si-UBE2T, p < 0.05, p < 0.01.

References

[1] Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70(1):7–30.10.3322/caac.21590Search in Google Scholar PubMed

[2] Hanikezi T, Shaadaiti W, Mayinuer A, Zhao J, Guzainuer M, Mourboul A, et al. Impacts of isoliquiritigenin on proliferation and apoptosis of human cervical cancer cells. Eur J Gynaecol Oncol. 2019;40(3):425–30.Search in Google Scholar

[3] Wang J, Bai Z, Gao X, Zhang N, Wang Z. The effects of age, period, and cohort on the mortality of cervical cancer in three high-income countries: Canada, Korea, and Italy. Biomed Res Int [Internet]. 2021;2021:8829122. Available from: http://europepmc.org/abstract/MED/33490279. Available from: https://europepmc.org/articles/PMC7803425. Available from: https://europepmc.org/articles/PMC7803425?pdf=render. 10.1155/2021/8829122.Search in Google Scholar PubMed PubMed Central

[4] Lin M, Ye M, Zhou J, Wang ZP, Zhu X. Recent advances on the molecular mechanism of cervical carcinogenesis based on systems biology technologies. Comput Struct Biotechnol J. 2019;17:241–50.10.1016/j.csbj.2019.02.001Search in Google Scholar PubMed PubMed Central

[5] Schmid MP, Franckena M, Kirchheiner K, Sturdza A, Georg P, Dörr W, et al. Distant metastasis in patients with cervical cancer after primary radiotherapy with or without chemotherapy and image guided adaptive brachytherapy. Gynecol Oncol. 2014;133(2):256–62.10.1016/j.ygyno.2014.02.004Search in Google Scholar PubMed

[6] Perez-Peña J, Corrales-Sánchez V, Amir E, Pandiella A, Ocana A. Ubiquitin-conjugating enzyme E2T (UBE2T) and denticleless protein homolog (DTL) are linked to poor outcome in breast and lung cancers. Sci Rep. 2017;7(1):17530.10.1038/s41598-017-17836-7Search in Google Scholar PubMed PubMed Central

[7] Gong YQ, Peng D, Ning XH, Yang XY, Li XS, Zhou LQ, et al. UBE2T silencing suppresses proliferation and induces cell cycle arrest and apoptosis in bladder cancer cells. Oncol Lett. 2016;12(6):4485–92.10.3892/ol.2016.5237Search in Google Scholar PubMed PubMed Central

[8] Liu J, Liu X. UBE2T silencing inhibited non-small cell lung cancer cell proliferation and invasion by suppressing the wnt/β-catenin signaling pathway. Int J Clin Exp Pathol. 2017;10(9):9482–8.Search in Google Scholar

[9] Zhang Z, Li H, Zhao Y, Guo Q, Yu Y, Zhu S, et al. Asporin promotes cell proliferation via interacting with PSMD2 in gastric cancer. Front Biosci (Landmark Ed). 2019;24:1178–89.10.2741/4774Search in Google Scholar PubMed

[10] Wu M, Li X, Huang W, Chen Y, Wang B, Liu X. Ubiquitin-conjugating enzyme E2T(UBE2T) promotes colorectal cancer progression by facilitating ubiquitination and degradation of p53. Clin Res Hepatol Gastroenterol. 2021;45(2):101493.10.1016/j.clinre.2020.06.018Search in Google Scholar PubMed

[11] Ciortea R, Angheluta LM, Pintican D, Baltoaica R, Bucuri C, Măluțan A, et al. Glucose-regulated protein 78, an important biomarker in cancer etiopathogenesis. Ginecoeu. 2014;10:123–5.10.18643/gieu.2014.123Search in Google Scholar

[12] van Nimwegen MJ, van de Water B. Focal adhesion kinase: A potential target in cancer therapy. Biochem Pharmacol. 2007;73(5):597–609.10.1016/j.bcp.2006.08.011Search in Google Scholar PubMed

[13] Su R, Li Z, Li H, Song H, Bao C, Wei J, et al. Grp78 promotes the invasion of hepatocellular carcinoma. BMC Cancer. 2010;10:20.10.1186/1471-2407-10-20Search in Google Scholar PubMed PubMed Central

[14] Qiu J, Zhou S, Cheng W, Luo C. LINC00294 induced by GRP78 promotes cervical cancer development by promoting cell cycle transition. Oncol Lett. 2020;20(5):262.10.3892/ol.2020.12125Search in Google Scholar PubMed PubMed Central

[15] Luo C, Qiu J. miR-181a inhibits cervical cancer development via downregulating GRP78. Oncol Res. 2017;25(8):1341–8.10.3727/096504017X14867268787969Search in Google Scholar PubMed PubMed Central

[16] Huang P, Guo Y, Zhao Z, Ning W, Wang H, Gu C, et al. UBE2T promotes glioblastoma invasion and migration via stabilizing GRP78 and regulating EMT. Aging (Albany NY). 2020;12(11):10275–89.10.18632/aging.103239Search in Google Scholar PubMed PubMed Central

[17] Hosseini SM, Okoye I, Chaleshtari MG, Hazhirkarzar B, Mohamadnejad J, Azizi G, et al. E2 ubiquitin-conjugating enzymes in cancer: implications for immunotherapeutic interventions. Clinica Chim Acta. 2019;498:126–34.10.1016/j.cca.2019.08.020Search in Google Scholar PubMed

[18] Liang J, Nishi H, Bian M-L, Higuma C, Sasaki T, Ito H, et al. The ubiquitin-conjugating enzyme E2-EPF is overexpressed in cervical cancer and associates with tumor growth. Oncol Rep. 2012;28(4):1519–25.10.3892/or.2012.1949Search in Google Scholar PubMed

[19] Yu H, Xiang P, Pan Q, Huang Y, Xie N, Zhu W. Ubiquitin-conjugating enzyme E2T is an independent prognostic factor and promotes gastric cancer progression. Tumor Biol. 2016;37(9):11723–32.10.1007/s13277-016-5020-3Search in Google Scholar PubMed

[20] Lee M-Y, Shen M-R. Epithelial-mesenchymal transition in cervical carcinoma. Am J Transl Res. 2012;4(1):1–13.Search in Google Scholar

[21] Yin H, Wang X, Zhang X, Zeng Y, Xu Q, Wang W, et al. UBE2T promotes radiation resistance in non-small cell lung cancer via inducing epithelial-mesenchymal transition and the ubiquitination-mediated FOXO1 degradation. Cancer Lett. 2020;494:121–31.10.1016/j.canlet.2020.06.005Search in Google Scholar PubMed

[22] Chhabra R. Cervical cancer stem cells: opportunities and challenges. J Cancer Res Clin Oncol. 2015;141(11):1889–97.10.1007/s00432-014-1905-ySearch in Google Scholar PubMed

[23] Cao H-Z, Liu X-F, Yang W-T, Chen Q, Zheng P-S. LGR5 promotes cancer stem cell traits and chemoresistance in cervical cancer. Cell Death Dis. 2017;8(9):e3039.10.1038/cddis.2017.393Search in Google Scholar PubMed PubMed Central

[24] Ho NPY, Leung CON, Wong TL, Lau EYT, Lei MML, Mok EHK, et al. The interplay of UBE2T and Mule in regulating Wnt/β-catenin activation to promote hepatocellular carcinoma progression. Cell Death Dis. 2021;12(2):148.10.1038/s41419-021-03403-6Search in Google Scholar PubMed PubMed Central

[25] Luo C, Fan W, Jiang Y, Zhou S, Cheng W. Glucose-related protein 78 expression and its effects on cisplatin-resistance in cervical cancer. Med Sci Monit. 2018;24:2197–209.10.12659/MSM.906413Search in Google Scholar PubMed PubMed Central

[26] Li H, Song H, Luo J, Liang J, Zhao S, Su R. Knockdown of glucose-regulated protein 78 decreases the invasion, metalloproteinase expression and ECM degradation in hepatocellular carcinoma cells. J Exp Clin Cancer Res. 2012;31(1):39.10.1186/1756-9966-31-39Search in Google Scholar PubMed PubMed Central

[27] Zhou Y, Shu C, Huang Y. Fibronectin promotes cervical cancer tumorigenesis through activating FAK signaling pathway. J Cell Biochem. 2019;120(7):10988–97.10.1002/jcb.28282Search in Google Scholar PubMed

Received: 2021-05-21
Revised: 2021-08-19
Accepted: 2021-08-21
Published Online: 2021-10-01

© 2021 YanMei Liu et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Articles in the same Issue

  1. Biomedical Sciences
  2. Research progress on the mechanism of orexin in pain regulation in different brain regions
  3. Adriamycin-resistant cells are significantly less fit than adriamycin-sensitive cells in cervical cancer
  4. Exogenous spermidine affects polyamine metabolism in the mouse hypothalamus
  5. Iris metastasis of diffuse large B-cell lymphoma misdiagnosed as primary angle-closure glaucoma: A case report and review of the literature
  6. LncRNA PVT1 promotes cervical cancer progression by sponging miR-503 to upregulate ARL2 expression
  7. Two new inflammatory markers related to the CURB-65 score for disease severity in patients with community-acquired pneumonia: The hypersensitive C-reactive protein to albumin ratio and fibrinogen to albumin ratio
  8. Circ_0091579 enhances the malignancy of hepatocellular carcinoma via miR-1287/PDK2 axis
  9. Silencing XIST mitigated lipopolysaccharide (LPS)-induced inflammatory injury in human lung fibroblast WI-38 cells through modulating miR-30b-5p/CCL16 axis and TLR4/NF-κB signaling pathway
  10. Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats
  11. ABCB1 polymorphism in clopidogrel-treated Montenegrin patients
  12. Metabolic profiling of fatty acids in Tripterygium wilfordii multiglucoside- and triptolide-induced liver-injured rats
  13. miR-338-3p inhibits cell growth, invasion, and EMT process in neuroblastoma through targeting MMP-2
  14. Verification of neuroprotective effects of alpha-lipoic acid on chronic neuropathic pain in a chronic constriction injury rat model
  15. Circ_WWC3 overexpression decelerates the progression of osteosarcoma by regulating miR-421/PDE7B axis
  16. Knockdown of TUG1 rescues cardiomyocyte hypertrophy through targeting the miR-497/MEF2C axis
  17. MiR-146b-3p protects against AR42J cell injury in cerulein-induced acute pancreatitis model through targeting Anxa2
  18. miR-299-3p suppresses cell progression and induces apoptosis by downregulating PAX3 in gastric cancer
  19. Diabetes and COVID-19
  20. Discovery of novel potential KIT inhibitors for the treatment of gastrointestinal stromal tumor
  21. TEAD4 is a novel independent predictor of prognosis in LGG patients with IDH mutation
  22. circTLK1 facilitates the proliferation and metastasis of renal cell carcinoma by regulating miR-495-3p/CBL axis
  23. microRNA-9-5p protects liver sinusoidal endothelial cell against oxygen glucose deprivation/reperfusion injury
  24. Long noncoding RNA TUG1 regulates degradation of chondrocyte extracellular matrix via miR-320c/MMP-13 axis in osteoarthritis
  25. Duodenal adenocarcinoma with skin metastasis as initial manifestation: A case report
  26. Effects of Loofah cylindrica extract on learning and memory ability, brain tissue morphology, and immune function of aging mice
  27. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways
  28. Blocking circ_UBR4 suppressed proliferation, migration, and cell cycle progression of human vascular smooth muscle cells in atherosclerosis
  29. Gene therapy in PIDs, hemoglobin, ocular, neurodegenerative, and hemophilia B disorders
  30. Downregulation of circ_0037655 impedes glioma formation and metastasis via the regulation of miR-1229-3p/ITGB8 axis
  31. Vitamin D deficiency and cardiovascular risk in type 2 diabetes population
  32. Circ_0013359 facilitates the tumorigenicity of melanoma by regulating miR-136-5p/RAB9A axis
  33. Mechanisms of circular RNA circ_0066147 on pancreatic cancer progression
  34. lncRNA myocardial infarction-associated transcript (MIAT) knockdown alleviates LPS-induced chondrocytes inflammatory injury via regulating miR-488-3p/sex determining region Y-related HMG-box 11 (SOX11) axis
  35. Identification of circRNA circ-CSPP1 as a potent driver of colorectal cancer by directly targeting the miR-431/LASP1 axis
  36. Hyperhomocysteinemia exacerbates ischemia-reperfusion injury-induced acute kidney injury by mediating oxidative stress, DNA damage, JNK pathway, and apoptosis
  37. Potential prognostic markers and significant lncRNA–mRNA co-expression pairs in laryngeal squamous cell carcinoma
  38. Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: Potential application for SARS-CoV-2 inactivated vaccine development
  39. ADHFE1 is a correlative factor of patient survival in cancer
  40. The association of transcription factor Prox1 with the proliferation, migration, and invasion of lung cancer
  41. Is there a relationship between the prevalence of autoimmune thyroid disease and diabetic kidney disease?
  42. Immunoregulatory function of Dictyophora echinovolvata spore polysaccharides in immunocompromised mice induced by cyclophosphamide
  43. T cell epitopes of SARS-CoV-2 spike protein and conserved surface protein of Plasmodium malariae share sequence homology
  44. Anti-obesity effect and mechanism of mesenchymal stem cells influence on obese mice
  45. Long noncoding RNA HULC contributes to paclitaxel resistance in ovarian cancer via miR-137/ITGB8 axis
  46. Glucocorticoids protect HEI-OC1 cells from tunicamycin-induced cell damage via inhibiting endoplasmic reticulum stress
  47. Prognostic value of the neutrophil-to-lymphocyte ratio in acute organophosphorus pesticide poisoning
  48. Gastroprotective effects of diosgenin against HCl/ethanol-induced gastric mucosal injury through suppression of NF-κβ and myeloperoxidase activities
  49. Silencing of LINC00707 suppresses cell proliferation, migration, and invasion of osteosarcoma cells by modulating miR-338-3p/AHSA1 axis
  50. Successful extracorporeal membrane oxygenation resuscitation of patient with cardiogenic shock induced by phaeochromocytoma crisis mimicking hyperthyroidism: A case report
  51. Effects of miR-185-5p on replication of hepatitis C virus
  52. Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis
  53. Primary localized cutaneous nodular amyloidosis presenting as lymphatic malformation: A case report
  54. Multimodal magnetic resonance imaging analysis in the characteristics of Wilson’s disease: A case report and literature review
  55. Therapeutic potential of anticoagulant therapy in association with cytokine storm inhibition in severe cases of COVID-19: A case report
  56. Neoadjuvant immunotherapy combined with chemotherapy for locally advanced squamous cell lung carcinoma: A case report and literature review
  57. Rufinamide (RUF) suppresses inflammation and maintains the integrity of the blood–brain barrier during kainic acid-induced brain damage
  58. Inhibition of ADAM10 ameliorates doxorubicin-induced cardiac remodeling by suppressing N-cadherin cleavage
  59. Invasive ductal carcinoma and small lymphocytic lymphoma/chronic lymphocytic leukemia manifesting as a collision breast tumor: A case report and literature review
  60. Clonal diversity of the B cell receptor repertoire in patients with coronary in-stent restenosis and type 2 diabetes
  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
  67. A two-microRNA signature predicts the progression of male thyroid cancer
  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
  85. Red blood cell distribution width-standard deviation but not red blood cell distribution width-coefficient of variation as a potential index for the diagnosis of iron-deficiency anemia in mid-pregnancy women
  86. Small cell neuroendocrine carcinoma expressing alpha fetoprotein in the endometrium
  87. Superoxide dismutase and the sigma1 receptor as key elements of the antioxidant system in human gastrointestinal tract cancers
  88. Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
  89. ITGB5 mutation discovered in a Chinese family with blepharophimosis-ptosis-epicanthus inversus syndrome
  90. ACTB and GAPDH appear at multiple SDS-PAGE positions, thus not suitable as reference genes for determining protein loading in techniques like Western blotting
  91. Facilitation of mouse skin-derived precursor growth and yield by optimizing plating density
  92. 3,4-Dihydroxyphenylethanol ameliorates lipopolysaccharide-induced septic cardiac injury in a murine model
  93. Downregulation of PITX2 inhibits the proliferation and migration of liver cancer cells and induces cell apoptosis
  94. Expression of CDK9 in endometrial cancer tissues and its effect on the proliferation of HEC-1B
  95. Novel predictor of the occurrence of DKA in T1DM patients without infection: A combination of neutrophil/lymphocyte ratio and white blood cells
  96. Investigation of molecular regulation mechanism under the pathophysiology of subarachnoid hemorrhage
  97. miR-25-3p protects renal tubular epithelial cells from apoptosis induced by renal IRI by targeting DKK3
  98. Bioengineering and Biotechnology
  99. Green fabrication of Co and Co3O4 nanoparticles and their biomedical applications: A review
  100. Agriculture
  101. Effects of inorganic and organic selenium sources on the growth performance of broilers in China: A meta-analysis
  102. Crop-livestock integration practices, knowledge, and attitudes among smallholder farmers: Hedging against climate change-induced shocks in semi-arid Zimbabwe
  103. Food Science and Nutrition
  104. Effect of food processing on the antioxidant activity of flavones from Polygonatum odoratum (Mill.) Druce
  105. Vitamin D and iodine status was associated with the risk and complication of type 2 diabetes mellitus in China
  106. Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”
  107. Comparison between voltammetric detection methods for abalone-flavoring liquid
  108. Composition of low-molecular-weight glutenin subunits in common wheat (Triticum aestivum L.) and their effects on the rheological properties of dough
  109. Application of culture, PCR, and PacBio sequencing for determination of microbial composition of milk from subclinical mastitis dairy cows of smallholder farms
  110. Investigating microplastics and potentially toxic elements contamination in canned Tuna, Salmon, and Sardine fishes from Taif markets, KSA
  111. From bench to bar side: Evaluating the red wine storage lesion
  112. Establishment of an iodine model for prevention of iodine-excess-induced thyroid dysfunction in pregnant women
  113. Plant Sciences
  114. Characterization of GMPP from Dendrobium huoshanense yielding GDP-D-mannose
  115. Comparative analysis of the SPL gene family in five Rosaceae species: Fragaria vesca, Malus domestica, Prunus persica, Rubus occidentalis, and Pyrus pyrifolia
  116. Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR
  117. Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry
  118. Morphological structures and histochemistry of roots and shoots in Myricaria laxiflora (Tamaricaceae)
  119. Transcriptome analysis of resistance mechanism to potato wart disease
  120. In silico analysis of glycosyltransferase 2 family genes in duckweed (Spirodela polyrhiza) and its role in salt stress tolerance
  121. Comparative study on growth traits and ions regulation of zoysiagrasses under varied salinity treatments
  122. Role of MS1 homolog Ntms1 gene of tobacco infertility
  123. Biological characteristics and fungicide sensitivity of Pyricularia variabilis
  124. In silico/computational analysis of mevalonate pyrophosphate decarboxylase gene families in Campanulids
  125. Identification of novel drought-responsive miRNA regulatory network of drought stress response in common vetch (Vicia sativa)
  126. How photoautotrophy, photomixotrophy, and ventilation affect the stomata and fluorescence emission of pistachios rootstock?
  127. Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention
  128. Ecology and Environmental Sciences
  129. The impact of sewage sludge on the fungal communities in the rhizosphere and roots of barley and on barley yield
  130. Domestication of wild animals may provide a springboard for rapid variation of coronavirus
  131. Response of benthic invertebrate assemblages to seasonal and habitat condition in the Wewe River, Ashanti region (Ghana)
  132. Molecular record for the first authentication of Isaria cicadae from Vietnam
  133. Twig biomass allocation of Betula platyphylla in different habitats in Wudalianchi Volcano, northeast China
  134. Animal Sciences
  135. Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens
  136. Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
  137. Honey in wound healing: An updated review
  138. NONMMUT140591.1 may serve as a ceRNA to regulate Gata5 in UT-B knockout-induced cardiac conduction block
  139. Radiotherapy for the treatment of pulmonary hydatidosis in sheep
  140. Retraction
  141. Retraction of “Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating microRNA-34a-5p/NOTCH1 signaling pathway”
  142. Special Issue on Reuse of Agro-Industrial By-Products
  143. An effect of positional isomerism of benzoic acid derivatives on antibacterial activity against Escherichia coli
  144. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part II
  145. Relationship of Gensini score with retinal vessel diameter and arteriovenous ratio in senile CHD
  146. Effects of different enantiomers of amlodipine on lipid profiles and vasomotor factors in atherosclerotic rabbits
  147. Establishment of the New Zealand white rabbit animal model of fatty keratopathy associated with corneal neovascularization
  148. lncRNA MALAT1/miR-143 axis is a potential biomarker for in-stent restenosis and is involved in the multiplication of vascular smooth muscle cells
https://doi.org/10.1515/biol-2021-0108
Keywords for this article
UBE2T; stem cell; cervical cancer; progression; GRP 78; FAK
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Research progress on the mechanism of orexin in pain regulation in different brain regions
  3. Adriamycin-resistant cells are significantly less fit than adriamycin-sensitive cells in cervical cancer
  4. Exogenous spermidine affects polyamine metabolism in the mouse hypothalamus
  5. Iris metastasis of diffuse large B-cell lymphoma misdiagnosed as primary angle-closure glaucoma: A case report and review of the literature
  6. LncRNA PVT1 promotes cervical cancer progression by sponging miR-503 to upregulate ARL2 expression
  7. Two new inflammatory markers related to the CURB-65 score for disease severity in patients with community-acquired pneumonia: The hypersensitive C-reactive protein to albumin ratio and fibrinogen to albumin ratio
  8. Circ_0091579 enhances the malignancy of hepatocellular carcinoma via miR-1287/PDK2 axis
  9. Silencing XIST mitigated lipopolysaccharide (LPS)-induced inflammatory injury in human lung fibroblast WI-38 cells through modulating miR-30b-5p/CCL16 axis and TLR4/NF-κB signaling pathway
  10. Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats
  11. ABCB1 polymorphism in clopidogrel-treated Montenegrin patients
  12. Metabolic profiling of fatty acids in Tripterygium wilfordii multiglucoside- and triptolide-induced liver-injured rats
  13. miR-338-3p inhibits cell growth, invasion, and EMT process in neuroblastoma through targeting MMP-2
  14. Verification of neuroprotective effects of alpha-lipoic acid on chronic neuropathic pain in a chronic constriction injury rat model
  15. Circ_WWC3 overexpression decelerates the progression of osteosarcoma by regulating miR-421/PDE7B axis
  16. Knockdown of TUG1 rescues cardiomyocyte hypertrophy through targeting the miR-497/MEF2C axis
  17. MiR-146b-3p protects against AR42J cell injury in cerulein-induced acute pancreatitis model through targeting Anxa2
  18. miR-299-3p suppresses cell progression and induces apoptosis by downregulating PAX3 in gastric cancer
  19. Diabetes and COVID-19
  20. Discovery of novel potential KIT inhibitors for the treatment of gastrointestinal stromal tumor
  21. TEAD4 is a novel independent predictor of prognosis in LGG patients with IDH mutation
  22. circTLK1 facilitates the proliferation and metastasis of renal cell carcinoma by regulating miR-495-3p/CBL axis
  23. microRNA-9-5p protects liver sinusoidal endothelial cell against oxygen glucose deprivation/reperfusion injury
  24. Long noncoding RNA TUG1 regulates degradation of chondrocyte extracellular matrix via miR-320c/MMP-13 axis in osteoarthritis
  25. Duodenal adenocarcinoma with skin metastasis as initial manifestation: A case report
  26. Effects of Loofah cylindrica extract on learning and memory ability, brain tissue morphology, and immune function of aging mice
  27. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways
  28. Blocking circ_UBR4 suppressed proliferation, migration, and cell cycle progression of human vascular smooth muscle cells in atherosclerosis
  29. Gene therapy in PIDs, hemoglobin, ocular, neurodegenerative, and hemophilia B disorders
  30. Downregulation of circ_0037655 impedes glioma formation and metastasis via the regulation of miR-1229-3p/ITGB8 axis
  31. Vitamin D deficiency and cardiovascular risk in type 2 diabetes population
  32. Circ_0013359 facilitates the tumorigenicity of melanoma by regulating miR-136-5p/RAB9A axis
  33. Mechanisms of circular RNA circ_0066147 on pancreatic cancer progression
  34. lncRNA myocardial infarction-associated transcript (MIAT) knockdown alleviates LPS-induced chondrocytes inflammatory injury via regulating miR-488-3p/sex determining region Y-related HMG-box 11 (SOX11) axis
  35. Identification of circRNA circ-CSPP1 as a potent driver of colorectal cancer by directly targeting the miR-431/LASP1 axis
  36. Hyperhomocysteinemia exacerbates ischemia-reperfusion injury-induced acute kidney injury by mediating oxidative stress, DNA damage, JNK pathway, and apoptosis
  37. Potential prognostic markers and significant lncRNA–mRNA co-expression pairs in laryngeal squamous cell carcinoma
  38. Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: Potential application for SARS-CoV-2 inactivated vaccine development
  39. ADHFE1 is a correlative factor of patient survival in cancer
  40. The association of transcription factor Prox1 with the proliferation, migration, and invasion of lung cancer
  41. Is there a relationship between the prevalence of autoimmune thyroid disease and diabetic kidney disease?
  42. Immunoregulatory function of Dictyophora echinovolvata spore polysaccharides in immunocompromised mice induced by cyclophosphamide
  43. T cell epitopes of SARS-CoV-2 spike protein and conserved surface protein of Plasmodium malariae share sequence homology
  44. Anti-obesity effect and mechanism of mesenchymal stem cells influence on obese mice
  45. Long noncoding RNA HULC contributes to paclitaxel resistance in ovarian cancer via miR-137/ITGB8 axis
  46. Glucocorticoids protect HEI-OC1 cells from tunicamycin-induced cell damage via inhibiting endoplasmic reticulum stress
  47. Prognostic value of the neutrophil-to-lymphocyte ratio in acute organophosphorus pesticide poisoning
  48. Gastroprotective effects of diosgenin against HCl/ethanol-induced gastric mucosal injury through suppression of NF-κβ and myeloperoxidase activities
  49. Silencing of LINC00707 suppresses cell proliferation, migration, and invasion of osteosarcoma cells by modulating miR-338-3p/AHSA1 axis
  50. Successful extracorporeal membrane oxygenation resuscitation of patient with cardiogenic shock induced by phaeochromocytoma crisis mimicking hyperthyroidism: A case report
  51. Effects of miR-185-5p on replication of hepatitis C virus
  52. Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis
  53. Primary localized cutaneous nodular amyloidosis presenting as lymphatic malformation: A case report
  54. Multimodal magnetic resonance imaging analysis in the characteristics of Wilson’s disease: A case report and literature review
  55. Therapeutic potential of anticoagulant therapy in association with cytokine storm inhibition in severe cases of COVID-19: A case report
  56. Neoadjuvant immunotherapy combined with chemotherapy for locally advanced squamous cell lung carcinoma: A case report and literature review
  57. Rufinamide (RUF) suppresses inflammation and maintains the integrity of the blood–brain barrier during kainic acid-induced brain damage
  58. Inhibition of ADAM10 ameliorates doxorubicin-induced cardiac remodeling by suppressing N-cadherin cleavage
  59. Invasive ductal carcinoma and small lymphocytic lymphoma/chronic lymphocytic leukemia manifesting as a collision breast tumor: A case report and literature review
  60. Clonal diversity of the B cell receptor repertoire in patients with coronary in-stent restenosis and type 2 diabetes
  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
  67. A two-microRNA signature predicts the progression of male thyroid cancer
  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
  85. Red blood cell distribution width-standard deviation but not red blood cell distribution width-coefficient of variation as a potential index for the diagnosis of iron-deficiency anemia in mid-pregnancy women
  86. Small cell neuroendocrine carcinoma expressing alpha fetoprotein in the endometrium
  87. Superoxide dismutase and the sigma1 receptor as key elements of the antioxidant system in human gastrointestinal tract cancers
  88. Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
  89. ITGB5 mutation discovered in a Chinese family with blepharophimosis-ptosis-epicanthus inversus syndrome
  90. ACTB and GAPDH appear at multiple SDS-PAGE positions, thus not suitable as reference genes for determining protein loading in techniques like Western blotting
  91. Facilitation of mouse skin-derived precursor growth and yield by optimizing plating density
  92. 3,4-Dihydroxyphenylethanol ameliorates lipopolysaccharide-induced septic cardiac injury in a murine model
  93. Downregulation of PITX2 inhibits the proliferation and migration of liver cancer cells and induces cell apoptosis
  94. Expression of CDK9 in endometrial cancer tissues and its effect on the proliferation of HEC-1B
  95. Novel predictor of the occurrence of DKA in T1DM patients without infection: A combination of neutrophil/lymphocyte ratio and white blood cells
  96. Investigation of molecular regulation mechanism under the pathophysiology of subarachnoid hemorrhage
  97. miR-25-3p protects renal tubular epithelial cells from apoptosis induced by renal IRI by targeting DKK3
  98. Bioengineering and Biotechnology
  99. Green fabrication of Co and Co3O4 nanoparticles and their biomedical applications: A review
  100. Agriculture
  101. Effects of inorganic and organic selenium sources on the growth performance of broilers in China: A meta-analysis
  102. Crop-livestock integration practices, knowledge, and attitudes among smallholder farmers: Hedging against climate change-induced shocks in semi-arid Zimbabwe
  103. Food Science and Nutrition
  104. Effect of food processing on the antioxidant activity of flavones from Polygonatum odoratum (Mill.) Druce
  105. Vitamin D and iodine status was associated with the risk and complication of type 2 diabetes mellitus in China
  106. Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”
  107. Comparison between voltammetric detection methods for abalone-flavoring liquid
  108. Composition of low-molecular-weight glutenin subunits in common wheat (Triticum aestivum L.) and their effects on the rheological properties of dough
  109. Application of culture, PCR, and PacBio sequencing for determination of microbial composition of milk from subclinical mastitis dairy cows of smallholder farms
  110. Investigating microplastics and potentially toxic elements contamination in canned Tuna, Salmon, and Sardine fishes from Taif markets, KSA
  111. From bench to bar side: Evaluating the red wine storage lesion
  112. Establishment of an iodine model for prevention of iodine-excess-induced thyroid dysfunction in pregnant women
  113. Plant Sciences
  114. Characterization of GMPP from Dendrobium huoshanense yielding GDP-D-mannose
  115. Comparative analysis of the SPL gene family in five Rosaceae species: Fragaria vesca, Malus domestica, Prunus persica, Rubus occidentalis, and Pyrus pyrifolia
  116. Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR
  117. Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry
  118. Morphological structures and histochemistry of roots and shoots in Myricaria laxiflora (Tamaricaceae)
  119. Transcriptome analysis of resistance mechanism to potato wart disease
  120. In silico analysis of glycosyltransferase 2 family genes in duckweed (Spirodela polyrhiza) and its role in salt stress tolerance
  121. Comparative study on growth traits and ions regulation of zoysiagrasses under varied salinity treatments
  122. Role of MS1 homolog Ntms1 gene of tobacco infertility
  123. Biological characteristics and fungicide sensitivity of Pyricularia variabilis
  124. In silico/computational analysis of mevalonate pyrophosphate decarboxylase gene families in Campanulids
  125. Identification of novel drought-responsive miRNA regulatory network of drought stress response in common vetch (Vicia sativa)
  126. How photoautotrophy, photomixotrophy, and ventilation affect the stomata and fluorescence emission of pistachios rootstock?
  127. Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention
  128. Ecology and Environmental Sciences
  129. The impact of sewage sludge on the fungal communities in the rhizosphere and roots of barley and on barley yield
  130. Domestication of wild animals may provide a springboard for rapid variation of coronavirus
  131. Response of benthic invertebrate assemblages to seasonal and habitat condition in the Wewe River, Ashanti region (Ghana)
  132. Molecular record for the first authentication of Isaria cicadae from Vietnam
  133. Twig biomass allocation of Betula platyphylla in different habitats in Wudalianchi Volcano, northeast China
  134. Animal Sciences
  135. Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens
  136. Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
  137. Honey in wound healing: An updated review
  138. NONMMUT140591.1 may serve as a ceRNA to regulate Gata5 in UT-B knockout-induced cardiac conduction block
  139. Radiotherapy for the treatment of pulmonary hydatidosis in sheep
  140. Retraction
  141. Retraction of “Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating microRNA-34a-5p/NOTCH1 signaling pathway”
  142. Special Issue on Reuse of Agro-Industrial By-Products
  143. An effect of positional isomerism of benzoic acid derivatives on antibacterial activity against Escherichia coli
  144. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part II
  145. Relationship of Gensini score with retinal vessel diameter and arteriovenous ratio in senile CHD
  146. Effects of different enantiomers of amlodipine on lipid profiles and vasomotor factors in atherosclerotic rabbits
  147. Establishment of the New Zealand white rabbit animal model of fatty keratopathy associated with corneal neovascularization
  148. lncRNA MALAT1/miR-143 axis is a potential biomarker for in-stent restenosis and is involved in the multiplication of vascular smooth muscle cells
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 6.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/biol-2021-0108/html
Scroll to top button