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In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma

  • Pei Shen , Xianjuan Shen , Guo Chen , Chunmei Zhao , Hua Cai , Xinxin Xu , Yinong Duan , Xudong Wang EMAIL logo and Shaoqing Ju EMAIL logo
Published/Copyright: August 30, 2022
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From the journal Open Life Sciences Volume 17 Issue 1

Abstract

TIPE1 is a gene in the TNFAIP8 family involved in immune regulation and tumorigenesis. Although previous studies demonstrated that TIPE1 might play different roles in different tumors, its expression and role in lymphoma are unclear. Here we observed TIPE1 expression in diffuse large B cell lymphoma (DLBCL). Two microarrays containing 96 tumor tissue specimens were obtained from the Affiliated Hospital of Nantong University biobank. All specimens came from patients with a clear pathological diagnosis of lymphoma, lymphadenitis, breast cancer, or bladder cancer, and we performed immunohistochemical experiments on these tissue specimens. GEPIA and TIMER platforms were used for bioinformatic analyses. We found higher TIPE1 expression in tumor tissues from patients with lymphoma compared with those with lymphadenitis, breast cancer, or bladder cancer. The GEPIA and TIMER analyses revealed that TIPE1 was upregulated in DLBCL tissues but not in invasive breast carcinoma, urothelial bladder carcinoma, or liver hepatocellular carcinoma tissues. TIPE1 expression was irrelevant for pathological stage, overall survival, or DLBCL immune infiltration levels. However, TIPE1 expression was correlated with MKI67 expression in DLBCL. Overall, TIPE1’s high expression levels in DLBCL may contribute to tumor growth in DLBCL.

Keywords: TIPE1; lymphoma; diffuse large B cell lymphoma

1 Introduction

Lymphoma is a malignant tumor exhibiting painless progressive lymph node enlargement and local mass lesions. It is usually classified into two categories, Hodgkin lymphoma (HL) and non-Hodgkin lymphoma (NHL), the latter of which can be further classified into B cell, T cell, and NK cell varieties according to the immunophenotype [1,2]. In NHL, diffuse large B cell lymphoma (DLBCL) is the most common lymphoma and often exhibits heterogeneous gene expression and leads to heterogeneous clinical outcomes [3,4,5,6]. In a Chinese population, polymorphism of tumor necrosis factor-alpha-induced protein (TNFAIP8, rs1045241C > T) may make the Chinese population particularly susceptible to NHL [7]. TNFAIP8 belongs to the TNFAIP8 family, which may be associated with carcinogenesis and inflammation [8,9].

TNFAIP8 gene family contain TNFAIP8, TIPE1, TIPE2, and TIPE3. The protein sequences of all four members show high homology [10]. Of these genes, TNFAIP8, TIPE1, and TIPE3 are known to greatly influence tumor occurrence and development, while TIPE2 is mainly involved in innate immunity and acquired immunity [11]. The expression of TNFAIP8 (also known as SCC-S2) has been found to be greater in invasive ductal breast carcinoma (BRCA) than in the adjacent tissues, suggesting that TNFAIP8 promotes the growth and migration of breast cancer cells [12,13]. As a phosphoinositide transfer protein, TIPE3 is highly expressed in tumor tissues of patients with lung and esophageal cancer possibly binding to phosphoinositides to promote tumor formation [11]. Contrary to what is seen with TNFAIP8 and TIPE3, TIPE2 expression is a lower expression in human non-small cell lung cancer tissues than in normal lung tissues [14]. Li et al. confirmed that over-expression of TIPE2 may inhibit cell proliferation and cell invasion of lung cancer cell lines H1299 and A549 cells [14]. TIPE2 was also downregulated in breast cancer cells, suggesting that TIPE2 can suppress the proliferation and migration of breast cancer cells [15]. This body of research shows that TNFAIP8 and TIPE3 may act as oncogenes, while TIPE2 is likely a tumor suppressor gene.

TIPE1, which may be involved in immune regulation and tumorigenesis, is known to be downregulated in ovarian cancer tissues, suggesting that TIPE1 may suppress the metastasis and tumorigenesis of ovarian cancer [16]. However, TIPE1 can be upregulated in nasopharyngeal carcinoma, suggesting a role in promoting the proliferation of nasopharyngeal carcinoma cells [17]. Hence, TIPE1 may play various important roles in different tumors. Some studies have not detected TIPE1 expression in mature lymphocytes [18]. However, TIPE1 is highly expressed in HMy2.CIR (a human B lymphoblast cell line) transformed with Epstein-Barr Viral DNA as well as in EL4 (a murine T cell line) [18]. The expression and potential role of TIPE1 in the development of lymphoma remain unclear. In this study, we observed TIPE1 expression in DLBCL, a type of B-cell lymphoma. Expression levels of TIPE1 in DLBCL and its correlation with immune infiltration level and survival, and MKI67 expression in DLBCL were analyzed using bioinformatics based on TCGA database and so on. These studies will provide basis for the further study of the role of TIPE1 in DLBCL.

2 Materials and methods

2.1 Patients

Two microarrays containing a total of 96 tumor tissue specimens from 96 patients were obtained from the biobank of the Affiliated Hospital of Nantong University. All samples came from patients who went to the hospital from March 2004 to December 2013 with a clear pathological diagnosis of HL, NHL, lymphadenitis, breast cancer, or bladder cancer.

  1. Informed consent: All data were fully anonymized and no other individual information was collected from patients 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 Ethics Committee of Affiliated Hospital of Nantong University (Approval number: 2016056).

2.2 Immunohistochemical experiments

The tissue microarrays were prepared as normal paraffin-embedded sections and were dewaxed in dimethylbenzene followed by heating at 90°C in an antigen retrieval solution (Dako, Denmark). Tissue microarrays were then treated with H2O2 for 15 min at room temperature. After being inoculated with donkey serum (Solarbio, China) for blocking, a TIPE1 antibody (1:100, Santa Cruz Biotechnology, USA) was added to the samples, which were then incubated at 4°C overnight. An associated secondary antibody (Santa Cruz Biotechnology, USA) was added and incubated at 37°C for 2 h. Subsequently, DAB color development (Solarbio, China) was performed according to the instructions, and images of the tissue microarrays were captured using a Leica DM5000 B microscope (Leica, Germany). Cells stained in brown were considered positive samples [9].

2.3 Bioinformatic analysis

The expression of TIPE1 in tumor tissues was analyzed using the Gene Expression Profiling Interactive Analysis (GEPIA2) platform (http://gepia2.cancer-pku.cn/#index). GEPIA2 is a tool to analyze RNA sequencing expression data from The Cancer Genome Atlas (TCGA) and the Genotype-Tissue Expression (GTEx) projects [19]. Using this platform, we performed differential expression analysis and survival analysis of TIPE1 expression in tumor tissues and its control tissues.

To assess the correlation between TIPE1 expression and immune infiltration level in DLBCL, we used the Gene module of Tumor Immune Estimation Resource platform (https://cistrome.shinyapps.io/timer/, TIMER) [20,21]. We also used TIMER to examine the correlation between TIPE1 and MKI67. In addition, we obtained TIPE1 expression information from The Human Protein Atlas (HPA, http://www.proteinatlas.org) [22,23,24].

3 Results

Overall, our findings suggest that TIPE1 expression is upregulated in malignant lymphomas. In the immunohistochemical experiments, the expression of TIPE1 was higher in malignant lymphomas than in lymphadenitis (Figure 1). Interestingly, TIPE1 expression from HL and NHL tissues was higher than in lymphadenitis samples. However, TIPE1 expression did not differ between HL tissues and NHL tissues. Furthermore, TIPE1 was also lower in breast and bladder cancer than in malignant lymphomas.

Figure 1 Expression of TIPE1 was upregulated in malignant lymphoma. The expression levels of TIPE1 in tissues from patients with HL and NHL were all higher than those in patients with lymphadenitis (100×). TIPE1 expression levels in tissues from patients with malignant lymphoma were higher than those in tissues from patients with lymphadenitis or other cancers (100×). Cells stained in brown were considered positive samples.
Figure 1

Expression of TIPE1 was upregulated in malignant lymphoma. The expression levels of TIPE1 in tissues from patients with HL and NHL were all higher than those in patients with lymphadenitis (100×). TIPE1 expression levels in tissues from patients with malignant lymphoma were higher than those in tissues from patients with lymphadenitis or other cancers (100×). Cells stained in brown were considered positive samples.

We also confirmed that TIPE1 expression was upregulated in tissues from DLBCL patients (Figure 2a). According to the data from GEPIA2, the expression of TIPE1 (Gene ID: ENSG00000185361.8) in DLBCL (n = 47) was higher than that in the normal group (n = 337, p < 0.05) (Figure 2b). TIPE1 expression did not differ between the invasive BRCA group (n = 1,085) and normal group (n = 291, p > 0.05), nor between the urothelial bladder carcinoma (BLCA) group (n = 404) and normal group (n = 28, p > 0.05) or liver hepatocellular carcinoma (LIHC) group (n = 369) and normal group (n = 160, p > 0.05).

Figure 2 Expression of TIPE1 was upregulated in DLBCL. (a) TIPE1 expression levels in tissues from patients with DLBCL were higher than those in patients with lymphadenitis (100×). Cells stained in brown were considered positive samples. (b) The expression of TIPE1 was upregulated in the DLBCL group compared to that in the normal group. No difference in TIPE1 expression existed between the BLCA group and the normal group, between the BRCA group and the normal group, or between the LIHC group and the normal group. All the data were obtained from GEPIA2. Red indicates tumor groups, while gray indicates the normal group. * represents statistically significant differences (p < 0.05).
Figure 2

Expression of TIPE1 was upregulated in DLBCL. (a) TIPE1 expression levels in tissues from patients with DLBCL were higher than those in patients with lymphadenitis (100×). Cells stained in brown were considered positive samples. (b) The expression of TIPE1 was upregulated in the DLBCL group compared to that in the normal group. No difference in TIPE1 expression existed between the BLCA group and the normal group, between the BRCA group and the normal group, or between the LIHC group and the normal group. All the data were obtained from GEPIA2. Red indicates tumor groups, while gray indicates the normal group. * represents statistically significant differences (p < 0.05).

TIPE1 expression was not correlated with pathological stage nor overall survival of DLBCL. Using the GEPIA2 platform, we found that the expression of TIPE1 was independent of the DLBCL pathological stage of the tissue (Figure 3a, F = 0.683, Pr(F) = 0.568). Furthermore, overall survival was unrelated to TIPE1 expression (Log rank p = 0.48, p(HR) = 0.48, Figure 3b). Meanwhile, TIPE1 expression did not predict disease-free survival of DLBCL (Figure A1). In addition, according to the data from GEPIA2, TNFAIP8 expression was upregulated in DLBCL tumor (n = 47, p < 0.05, Figure 3c), similar to that of TIPE1 (Figure 2b). However, TIPE2 and TIPE3 expression did not differ between DLBCL tumor group (n = 47) and normal group (n = 337) (p > 0.05, Figure 3d and e).

Figure 3 TIPE1 expression was unrelated to the pathological stage and overall survival of DLBCL. (a) TIPE1 expression and pathological stages of DLBCL were uncorrelated. (b) TIPE1 expression and overall survival were uncorrelated (p = 0.48). (c) The expression of TNFAIP8 was higher in DLBCL (p < 0.05). (d) and (e) Expression of TIPE2 and TIPE3, respectively, was not greater in DLBCL compared with those in the normal group. Red indicates tumor groups, while gray indicates the normal group.
Figure 3

TIPE1 expression was unrelated to the pathological stage and overall survival of DLBCL. (a) TIPE1 expression and pathological stages of DLBCL were uncorrelated. (b) TIPE1 expression and overall survival were uncorrelated (p = 0.48). (c) The expression of TNFAIP8 was higher in DLBCL (p < 0.05). (d) and (e) Expression of TIPE2 and TIPE3, respectively, was not greater in DLBCL compared with those in the normal group. Red indicates tumor groups, while gray indicates the normal group.

TIPE1 expression in DLBCL was unrelated to immune infiltration levels but correlated with MKI67. Using HPA (https://www.proteinatlas.org/ENSG00000185361-TNFAIP8L1/pathology) platform, we also found that TIPE1 was an intracellular protein whose expression level is higher in the liver than in other tissues. However, its RNA expression level has low cancer and immune cell specificity [22]. Then, according to the data from TIMER, TIPE1 expression was not related to the infiltration levels of B cells (p = 0.185), CD8 + T cells (p = 0.104), CD4 + T cells (p = 0.346), macrophages (p = 0.509), neutrophils (p = 0.688), and dendritic cells (p = 0.879) (Figure 4a). As such, TIPE1 expression may be unrelated to immune infiltration in DLBCL.

Figure 4 TIPE1 expression was unrelated to immune infiltration levels but correlated with MKI67 in DLBCL. (a) TIPE1 expression and immune infiltration levels of B cells, CD8 + T cells, CD4 + T cells, macrophages, neutrophils, and dendritic cells in DLBCL were uncorrelated. (b) and (c) TIPE1 expression was correlated to MKI67 expression in DLBCL (b, purity adjustment and c, age adjustment, p < 0.05). (d), (e), and (f) TIPE1 expression was related to MYC expression in DLBCL (p < 0.05), but unrelated to BCL6 or BCL2 expression (p > 0.05).
Figure 4

TIPE1 expression was unrelated to immune infiltration levels but correlated with MKI67 in DLBCL. (a) TIPE1 expression and immune infiltration levels of B cells, CD8 + T cells, CD4 + T cells, macrophages, neutrophils, and dendritic cells in DLBCL were uncorrelated. (b) and (c) TIPE1 expression was correlated to MKI67 expression in DLBCL (b, purity adjustment and c, age adjustment, p < 0.05). (d), (e), and (f) TIPE1 expression was related to MYC expression in DLBCL (p < 0.05), but unrelated to BCL6 or BCL2 expression (p > 0.05).

Using the TIMER platform, we found that TIPE1 expression in DLBCL was predicted to correlate with MKI67 expression, whether the association was adjusted by tumor purity (p < 0.05, Figure 4b) or age (p < 0.05, Figure 4c). In addition, the expression levels of MKI67, MYC, BCL2, and BCL6 are shown in Figure A2. TIPE1 expression in DLBCL also correlated with MYC expression (p < 0.05, Figure 4d), but unrelated to BCL6 (p > 0.05, Figure 4e) or BCL2 (p > 0.05, Figure 4f) expression.

4 Discussion

According to the data from HPA in our study, we found that TIPE1 was expressed in multiple human tissues (especially in the liver) and exhibited low immune cell specificity and low human brain regional specificity. Cui et al. also reported that TIPE1 was expressed in various tissues of C57BL/6 mice, including brain neurons, liver, male and female reproductive cells, and muscle tissues as well as in tumor cells transfected with related viruses [18]. Although TIPE1 may be a prognostic marker in renal cancer, TIPE1 is typically expressed in a variety of human tumor tissues with low cancer specificity (HPA database). However, we observed that TIPE1 expression in LIHC tissues did not differ from that in normal tissues based on the data from GEPIA2. Furthermore, expression levels of TIPE1 were not upregulated in BRCA and BLCA groups (Figure 1). This differs from the report of Zhang et al., who found that TIPE1 expression was substantially reduced in hepatocellular carcinoma (HCC) tissues compared to adjacent tissues [25]. They also found that TIPE1 promoted apoptosis of HCC cells and inhibited HCC cell growth. TIPE1 may also inhibit colony formation of HCC cells and slow the growth of transplanted tumors [25]. Hu et al. found that TIPE1 inhibited the growth of breast cancer cells and demonstrated that TIPE1 expression was negatively correlated to MKI67 expression in breast cancer tissues [9]. On the other hand, TIPE1 expression was elevated, and its expression was positively correlated to MKI67 expression in cervical cancer tissues [26]. In vitro experiments also demonstrate that TIPE1 promotes the proliferation of cervical cancer cells through p53 pathway [26]. As such, differential expression of TIPE1 in different tumors may result in different biological functions.

In this study, all our analyses suggested that TIPE1 expression was substantially higher in the DLBCL group than in the normal group. Additionally, TNFAIP8 was found to be more highly expressed in DLBCL groups compared to the non-cancer groups, while TIPE2 and TIPE3 expression did not differ between DLBCL and normal tissues. Although TIPE1 expression was unrelated to DLBCL immune infiltration levels, DLBCL pathological stage, and overall survival of patients with DLBCL, we confirmed that MKI67 expression was upregulated in DLBCL tissues compared to that in the normal tissues based on the data from GEPIA2 (Figure A2). TIPE1 expression was also positively correlated with MKI67 in DLBCL tissues. As MKI67 is a protein associated with cell proliferation [27], these results suggest that TIPE1 expression in DLBCL may contribute to tumor growth. Previous work has shown that TIPE1/Oxi-beta can competitively bind to FBXW5 with tuberous sclerosis complex 2 (TSC2), increasing the stability of TSC2 and promoting excessive autophagy in Parkinson’s disease [28]. We also confirmed that the TIPE1 protein interacted with FBXW5 in our previous study [29]. As the autonomous autophagy of tumor cell may also promote tumor growth [30], we speculate that the higher expression of TIPE1 in DLBCL may contribute to the autophagy of tumor cells, thereby causing tumor growth of DLBCL.

In conclusion, TIPE1 is highly expressed in DLBCL and may contribute to tumor growth in DLBCL. Further study needs to be performed to observe the function of TIPE1 in DLBCL.

# Pei Shen, Xianjuan Shen and Guo Chen contributed equally to this work.

  1. Funding information: Authors state that this work was supported by the Natural Science Foundation of Nantong City (JCZ20003). The funder had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

  2. Author contributions: Pei Shen and Shaoqing Ju conceived and designed the project. Pei Shen, Xianjuan Shen, Guo Chen, and Chunmei Zhao acquired the data. Pei Shen, Hua Cai, and Xudong Wang analyzed and interpreted the data. Xudong Wang, Yinong Duan, and Shaoqing Ju provided the materials. Pei Shen, Xinxin Xu, and Yinong Duan wrote and revised the article.

  3. Conflict of interest: 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 TIPE1 expression did not predict disease-free survival of DLBCL. TIPE1 expression was uncorrelated with overall survival (p = 0.76).
Figure A1

TIPE1 expression did not predict disease-free survival of DLBCL. TIPE1 expression was uncorrelated with overall survival (p = 0.76).

Figure A2 Expression of MKI67, MYC, BCL2, and BCL6 was influenced by DLBCL. MKI67 (a), MYC (b), and BCL2 (c) expression levels were upregulated in the DLBCL group compared to the normal group, while expression of BCL6 (d) was downregulated compared to the normal group. Red indicates tumor groups, while gray indicates the normal group. *represents statistically significant differences (p < 0.05).
Figure A2

Expression of MKI67, MYC, BCL2, and BCL6 was influenced by DLBCL. MKI67 (a), MYC (b), and BCL2 (c) expression levels were upregulated in the DLBCL group compared to the normal group, while expression of BCL6 (d) was downregulated compared to the normal group. Red indicates tumor groups, while gray indicates the normal group. *represents statistically significant differences (p < 0.05).

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Received: 2022-02-02
Revised: 2022-04-27
Accepted: 2022-05-18
Published Online: 2022-08-30

© 2022 Pei Shen et al., published by De Gruyter

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

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  31. Analysis of genetic characteristics of 436 children with dysplasia and detailed analysis of rare karyotype
  32. Bioinformatics network analyses of growth differentiation factor 11
  33. NR4A1 inhibits the epithelial–mesenchymal transition of hepatic stellate cells: Involvement of TGF-β–Smad2/3/4–ZEB signaling
  34. Expression of Zeb1 in the differentiation of mouse embryonic stem cell
  35. Study on the genetic damage caused by cadmium sulfide quantum dots in human lymphocytes
  36. Association between single-nucleotide polymorphisms of NKX2.5 and congenital heart disease in Chinese population: A meta-analysis
  37. Assessment of the anesthetic effect of modified pentothal sodium solution on Sprague-Dawley rats
  38. Genetic susceptibility to high myopia in Han Chinese population
  39. Potential biomarkers and molecular mechanisms in preeclampsia progression
  40. Silencing circular RNA-friend leukemia virus integration 1 restrained malignancy of CC cells and oxaliplatin resistance by disturbing dyskeratosis congenita 1
  41. Endostar plus pembrolizumab combined with a platinum-based dual chemotherapy regime for advanced pulmonary large-cell neuroendocrine carcinoma as a first-line treatment: A case report
  42. The significance of PAK4 in signaling and clinicopathology: A review
  43. Sorafenib inhibits ovarian cancer cell proliferation and mobility and induces radiosensitivity by targeting the tumor cell epithelial–mesenchymal transition
  44. Characterization of rabbit polyclonal antibody against camel recombinant nanobodies
  45. Active legumain promotes invasion and migration of neuroblastoma by regulating epithelial-mesenchymal transition
  46. Effect of cell receptors in the pathogenesis of osteoarthritis: Current insights
  47. MT-12 inhibits the proliferation of bladder cells in vitro and in vivo by enhancing autophagy through mitochondrial dysfunction
  48. Study of hsa_circRNA_000121 and hsa_circRNA_004183 in papillary thyroid microcarcinoma
  49. BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
  50. Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
  51. Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
  52. A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
  53. Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
  54. Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
  55. Correlation between peripheral blood lymphocyte subpopulations and primary systemic lupus erythematosus
  56. A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
  57. β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
  58. Identification of metabolic genes for the prediction of prognosis and tumor microenvironment infiltration in early-stage non-small cell lung cancer
  59. BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
  60. Mucormycosis co-infection in COVID-19 patients: An update
  61. Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
  62. Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
  63. Preparation and evaluation of LA-PEG-SPION, a targeted MRI contrast agent for liver cancer
  64. Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
  65. Nasopharyngeal tuberculosis: A case report
  66. Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
  67. Aberrant pulmonary immune response of obese mice to periodontal infection
  68. Bacteriospermia – A formidable player in male subfertility
  69. In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma
  70. Effects of KCa channels on biological behavior of trophoblasts
  71. Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
  72. Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
  73. Prognostic signature related to the immune environment of oral squamous cell carcinoma
  74. Primary and metastatic squamous cell carcinoma of the thyroid gland: Two case reports
  75. Neuroprotective effects of crocin and crocin-loaded niosomes against the paraquat-induced oxidative brain damage in rats
  76. Role of MMP-2 and CD147 in kidney fibrosis
  77. Geometric basis of action potential of skeletal muscle cells and neurons
  78. Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
  79. Role of cerebellar cortex in associative learning and memory in guinea pigs
  80. Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
  82. Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
  84. Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
  86. Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
  87. Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
  88. One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
  89. S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
  90. Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
  93. N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
  99. Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
  102. Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
  107. A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
  110. The role of erythrocytes and erythroid progenitor cells in tumors
  111. Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
https://doi.org/10.1515/biol-2022-0099
Keywords for this article
TIPE1; lymphoma; diffuse large B cell lymphoma
Creative Commons
BY 4.0

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  49. BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
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  52. A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
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  76. Role of MMP-2 and CD147 in kidney fibrosis
  77. Geometric basis of action potential of skeletal muscle cells and neurons
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  79. Role of cerebellar cortex in associative learning and memory in guinea pigs
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  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
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  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
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  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
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  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
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  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
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  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
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  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
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  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
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  114. Plant Sciences
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  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
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  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
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  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
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  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
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  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
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