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Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments

  • Shenghao Jin , Haitao Jiang , Yue Sun , Fang Li , Jianglan Xia , Yaxin Li , Jiwei Zheng EMAIL logo and Ying Qin
Published/Copyright: September 19, 2022
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Open Life Sciences
From the journal Open Life Sciences Volume 17 Issue 1

Abstract

Periodontitis is a common disease that is difficult to treat, and if not controlled in time, it causes severe conditions, such as alveolar bone resorption and tooth loosening and loss. Periodontal ligament stem cells constitute a promising cell source for regenerative treatment of periodontitis due to their high osteogenic differentiation capacity. PDLSC osteogenesis plays a central role in periodontal regeneration through successive cytokine-mediated signaling pathways and various biochemical and physicochemical factors. However, this process is inhibited in the inflammatory periodontitis environment due to high concentrations of lipopolysaccharide. Here, we review the mechanisms that influence the osteogenic differentiation of periodontal stem cells in this inflammatory microenvironment.

Keywords: periodontal membrane stem cells; osteogenic differentiation; inflammatory environment; lipopolysaccharide

Periodontitis is an infectious disorder that occurs in the supporting tissues of the teeth and, if left untreated, often results in loosening and loss of teeth and jawbone loss. The commonly used clinical treatments, such as physiotherapy and periodontal surgery, do not yield favorable results. Therefore, tissue regeneration and the use of stem cells to reconstruct periodontal and bone tissues have recently become a major research topic. In recent years, with the development of the field of oral tissue regeneration, the discovery of oral-derived seed cells has enabled the complete regeneration of the periodontal tissue. The cells [1] that have been found to play a regenerative role are partially used in clinical applications include dental pulp stem cells, stem cells from the apical papilla, dental follicle progenitor cells, and periodontal ligament stem cells (PDLSCs). Many studies [2,3,4] have shown that odontogenic stem cells are superior to non-dental stem cells in regenerative treatment, and periodontal stem cells are recognized as one of the safest and most effective stem cells for this process. PDLSCs are mesenchymal stem cells with self-renewal and multi-directional differentiation potentials (Figure 1), whereby they can differentiate into various types of mesenchymal cells [5], such as osteoblasts, adipocytes, and chondrocytes, in addition to cardiomyocytes, endothelial cells, and ectoderm-derived neural cells, namely neurons, oligodendrocytes, astrocytes, and Schwann cells. Thus, PDLSCs constitute a promising cell source for the repair of various types of tissues in regenerative medicine. Liu et al. [6] and Nagata et al. [7] have investigated the role of PDLSCs in the repair of periodontal bone defects and demonstrated that PDLSC-derived cells are highly effective in osteogenesis and in the formation of a periodontal-like tissue, whereby the regeneration and repair of the periodontal attachment tissue are promoted. These studies have laid the foundation for the development of regenerative treatment approaches in periodontitis.

Figure 1 Multi-directional differentiation potential of periodontal stem cells. (Description: This figure describes the multidirectional differentiation potential of PDLSCs. According to the sources of endoderm, mesoderm, and ectoderm, PDLSCs can differentiate into a variety of cells in the figure. We can use this feature to study its role in repairing bone and other tissue defects in the treatment of periodontitis.).
Figure 1

Multi-directional differentiation potential of periodontal stem cells. (Description: This figure describes the multidirectional differentiation potential of PDLSCs. According to the sources of endoderm, mesoderm, and ectoderm, PDLSCs can differentiate into a variety of cells in the figure. We can use this feature to study its role in repairing bone and other tissue defects in the treatment of periodontitis.).

The bacteria [8] that presumably cause periodontitis include 11 species, such as Actinobacillus, Actinomyces, Porphyromonas gingivalis, and Fosetanella, most of which are G-bacteria. Lipopolysaccharide (LPS) is an important component of the G-bacterial membrane, and the LPS-induced inflammatory microenvironment is an important and typical manifestation of periodontitis. This inflammatory microenvironment induces production of numerous inflammatory factors, such as TNF-ɑ, IL-6, and IL-1β, and involves various signaling pathways. According to the recent advances in periodontal disease microbiology, there is conclusive evidence [9] that some of these bacteria, such as P. gingivalis and Bacillus actinomycetemcomitans, play important roles in the pathogenesis of periodontitis, including the activation of the inflammatory response and promotion of bone loss, both of which are inextricably linked to the production of LPS by bacteria. Although the effects of different bacterial species on periodontal regeneration after bone loss are unclear, the effect of LPS on the osteogenic differentiation of stem cells has commonalities. Croes et al. have found [10] that osteogenesis is active after stimulation with small amounts of inactivated bacteria (low LPS levels). Based on this observation, numerous studies [11,12,13] have confirmed the protective, proliferative, and osteogenic effects of low concentrations of LPS (generally <5 μg/mL) on periodontal cells. The underlying mechanism may stem from an adaptive mechanism of PDLSCs at low concentrations of LPS. Alternatively, low concentrations of LPS may induce PDLSCs to activate the macrophage NRF2 signaling pathway to regulate the oxidative stress and downregulate macrophage pro-inflammatory factor expression. However, this is obviously not consistent with the microenvironment of severe periodontitis, and thus, high LPS concentrations should be considered in studies. At high LPS concentrations [14], cell proliferation and osteogenic differentiation are significantly reduced, presumably due to the induction of apoptosis through the classical NF-kB pathway and the action of cystein. Studies have generally explored LPS concentration gradients to identify the mechanism(s) underlying these two opposing effects of LPS. However, Albiero et al. [15] have observed that the osteogenic potential of LPS on periodontal stem cells is not affected. This observation has encouraged researchers to seek substances that favor the osteogenic differentiation of stem cells in the periodontitis environment, with the ultimate aim to improve the efficacy of current therapies and to find new therapeutic strategies. The following is a summary of the various mechanisms and factors influencing the osteogenic differentiation of PDLSCs under LPS-induced inflammatory conditions.

1 Roles of major signaling pathways

1.1 Wnt/β-catenin signaling pathway

Transcriptional co-activator with PDZ binding motif (TAZ, also known as WWTR1) is a transcriptional co-regulator that promotes the osteogenic differentiation of PDLSCs. Xing et al. [16] observed that LPS-induced osteogenic differentiation of PDLSCs is suppressed upon knocking down TAZ, indicating that TAZ is required for LPS-induced osteogenesis. They also found that the use of the Wnt/β-catenin pathway inhibitor DKK inhibits LPS-induced TAZ activation and osteogenesis, indirectly confirming that TAZ is a downstream component of the Wnt signaling pathway, thus inferring that low concentrations of Escherichia coli LPS promote the osteogenic differentiation of human PDLSCs (hPDLSCs) through Wnt/ntcatenin-induced TAZ upregulation. This result is encouraging as it explains to some extent the osteogenic effect of LPS at low concentrations. Furthermore, Li et al. [17] found that, in PDLSCs, removal of the histone acetyltransferase GCN5 downregulates DKK1, whereby the Wnt/β-catenin pathway is activated and osteogenesis is promoted. Thus, it is reasonable to infer that GCN5 regulates the osteogenic differentiation of periodontal stem cells in an inflammatory microenvironment through DKK1 acetylation (Figure 2).

Figure 2 Mechanism of Wnt/β-catenin signaling pathway (Description: Wnt/β-catenin pathway is important for osteogenic differentiation of PDLSCs. In the presence of LPS, histone acetyltransferase GCN5 can inhibit this pathway through the acetylation regulation of DDK1. TAZ, which is necessary for LPS-induced osteogenesis, is a downstream component of this signal pathway. Interference with it by ShRNA or under the influence of phospholipase notum can inhibit Wnt/β-catenin pathway-mediated osteogenic differentiation of PDLSCs, and LiCl could reverse the effect of Notum).
Figure 2

Mechanism of Wnt/β-catenin signaling pathway (Description: Wnt/β-catenin pathway is important for osteogenic differentiation of PDLSCs. In the presence of LPS, histone acetyltransferase GCN5 can inhibit this pathway through the acetylation regulation of DDK1. TAZ, which is necessary for LPS-induced osteogenesis, is a downstream component of this signal pathway. Interference with it by ShRNA or under the influence of phospholipase notum can inhibit Wnt/β-catenin pathway-mediated osteogenic differentiation of PDLSCs, and LiCl could reverse the effect of Notum).

Recently, Notum, a glycoprotein glycan and Wnt/β-catenin-associated ligand, has been discovered. It is a phospholipase shed on the cell surface. Yang et al. [18] examined the expression of Notum in LPS-treated PDLSCs and the osteogenic markers under the influence of Notum. By inhibiting the effect of Notum on the Wnt/β-catenin pathway, they found that this protein may inhibit the osteogenic differentiation of hPDLSCs through this pathway. In addition, lithium chloride [19,20] significantly suppressed the inhibitory effect of Notum on the osteogenic differentiation of hPDLSCs. These observations provide a new thinking for the treatment of periodontitis.

1.2 Toll-like receptor TLR 4/nuclear factor NF-κB signaling pathway

TLR4 is a transmembrane receptor involved in the activation of signaling pathways under inflammatory conditions. Yu et al. [21] applied TLR 4 agonists or antagonists to hPDLSCs extracted from patients with periodontitis alongside those from healthy individuals and analyzed indicators of cell proliferation and differentiation. The authors found that TLR4 activation decreases the ALP activity and expression of osteogenic markers but increases the expression of adipogenesis-related genes poly(AdP ribose) polymerase gamma and lipoprotein lipase, demonstrating that LPS can inhibit the osteogenic differentiation of hPDLSCs and induce their adipogenic differentiation under inflammatory conditions by activating the TLR4 signaling (Figure 3).

Figure 3 Mechanism of Toll-like receptor TLR 4/nuclear factor NF-κB signaling pathway (Description: transmembrane receptor TLR4 can participate in the activation of signal pathways under inflammatory conditions. In LPS-mediated environment, TLR4 receptor activation decreased the expression of osteogenic markers, such as ALP, Runx, and OCN, activated NF-kB pathway, and downregulated the mRNA expression of osteogenic marker EphrinB2. All these make the osteogenic differentiation of PDLSCs inhibited. The activation of TLR1,4,6 can inhibit the activation of Akt and osteogenic differentiation of PDLSCs through Myd88- or TRIF-dependent signaling pathways. In addition, some studies have found that the inhibition of NF-kb pathway can be reversed by rutin, extracellular vesicles or astaxanthin).
Figure 3

Mechanism of Toll-like receptor TLR 4/nuclear factor NF-κB signaling pathway (Description: transmembrane receptor TLR4 can participate in the activation of signal pathways under inflammatory conditions. In LPS-mediated environment, TLR4 receptor activation decreased the expression of osteogenic markers, such as ALP, Runx, and OCN, activated NF-kB pathway, and downregulated the mRNA expression of osteogenic marker EphrinB2. All these make the osteogenic differentiation of PDLSCs inhibited. The activation of TLR1,4,6 can inhibit the activation of Akt and osteogenic differentiation of PDLSCs through Myd88- or TRIF-dependent signaling pathways. In addition, some studies have found that the inhibition of NF-kb pathway can be reversed by rutin, extracellular vesicles or astaxanthin).

The TLR4 receptor-mediated signaling is common, and it is also closely associated with other inflammatory pathways. By using anti-TLR4 antibodies or antagonizers of the TLR4 or NF-κB signaling, Li et al. [14] found that LPS reduces the osteogenic differentiation of hPDLSCs by activating NF-κB through the TLR4 signaling pathway. The LPS-induced reduction in osteogenesis suppressed the alveolar bone loss in LPS-induced periodontitis in rats. Furthermore, Duan et al. [22] observed that salvianolic acid C promoted osteogenesis by attenuating LPS-induced inflammation and apoptosis through the inhibition of the TLR4/NF-κB pathway.

Many factors affect the TLR4 signaling pathway. Wang et al. [23] found that various concentrations of LPS downregulated the mRNA level of EphrinB2, a cellular marker of osteodifferentiation. In contrast, blocking the TLR4 pathway partially suppressed this effect of LPS. Therefore, it is inferred that LPS partially inhibits the osteogenesis of hPDLSCs by downregulating EphrinB2 through the TLR4 signaling.

In addition to TLR 4 receptor, experiments on other receptors of the same type confirmed that a common signaling feature of all TLRs is the activation of the transcription factor NF-κB, which controls the expression of inflammatory cytokines and factors involved in cell maturation. Through analyses based on polymerase chain reaction, Zhu et al. [24] found that high doses of TLR1, 4, and 6 ligands inhibit the expression of NF-κB. This inhibition occurs through Myd88 or the TRIF-dependent signaling pathway to inhibit Akt activation and hPDLSC osteogenic differentiation in turn. In addition, it has been shown that rutin [25] and extracellular vesicles [26] or astaxanthin [27] can increase the anti-oxidative stress capacity, proliferation, and osteogenic differentiation of PDLSCs by inhibiting the activity of the NFκB signaling, all of which lay the foundation for the development of new treatment strategies in periodontitis.

1.3 ERK1/2 signaling pathways [28]

It has been shown that activation of the ERK1/2 signaling pathways by LPS is at least partially involved in the alteration in the differentiation capacity of PDLSCs as well as in the acquisition of myofibroblast and immunoregulatory properties of these cells. LPS downregulates regulatory genes related to osteogenesis, such as Runx2, ALP, and Ocn, thereby altering the differentiation commitment of PDLSCs and acting as a suppressor of osteogenesis. In addition, LPS upregulates Sox9 and PPARγ, which promote chondrogenesis and adipogenesis. PDLSC-derived myofibroblasts acquire significant contractile motility upon activation of the ERK1/2 signaling, indicating the effect of this signaling pathway in cell differentiation.

2 Effect of microRNAs (miRs) and IncRNAs

miRs are a class of non-coding single-stranded RNAs that are approximately 22 nucleotides in length. They are encoded by endogenous genes and involved in post-transcriptional regulation in plants and animals. Bao et al. [29] found that miR-148a is upregulated whereas neurofibrillary protein1 (NRP1) is downregulated when LPS inhibits PDLSC proliferation. Conversely, downregulation of miR-148a or upregulation of NRP1 increased the osteogenic capacity of LPS-stimulated PDLSCs. Inhibition of NRP1 could negate the promotion of osteogenesis by miR-148a inhibitors. These two actions are complementary and not independent, confirming the osteogenic potential of PDLSCs in an LPS-induced inflammatory environment. The decrease in the osteogenic potential of PDLSCs in such an environment is associated with the miR-148a/NRP1 functional axis (Table 1).

Table 1

Effect of miRs and IncRNAs and other genes (description: the table lists some genes that affect the osteogenic differentiation of periodontal stem cells and their mechanisms, especially miRNA and IncRNA)

Gene Mechanism Effect on osteogenesis
miR-148a/NRP1 functional axis [29] Downregulating miR-148a or upregulatiing of NRP1 Promoting the osteogenic capacity of LPS-stimulated PDLSCs
miR-21 [30] Inhibiting a negative regulator (Spry1) of the ERK and FGF signaling pathways Promoting lipogenesis and osteogenesis of PDLSCs
miR-200cN [31] Inhibiting LPS-induced IL-6, IL-8, and CCL-5 production in hPDLSCs and increasing cellular calcium, ALP, and Runx2 levels Promoting osteogenic differentiation
miR-138 [31] Downregulating osteocalcin, Runx2, and type I collagen Inhibiting the osteogenic differentiation of PDLSCs
miR-26a-5p [32] Presumably targeting Wnt5a and thereby inhibiting the activation of the Wnt/Ca2+ signaling Promoting the osteogenic differentiation of PDLSCs
miR-302b [37] Using Chuanxiongzin (TMP) to reduce inflammation and apoptosis Promoting osteogenesis of LPS-stimulated human periodontal membrane cells
IncRNA [36] Presumably regulating the metabolism of various amino acids Promoting the osteogenic differentiation of PDLSCs
P2X7R [33,34] Affecting the PI3K/Akt/mTOR signaling Promoting the osteogenic differentiation of PDLSCs
HOXA10 [35] Regulating β-linked protein localization and DKK1 Inhibiting the osteogenic differentiation of periodontal stem cells
PLAP-1 [38] Using 1,25(OH)2D3 to inhibit the transcription of PLAP-1 Promoting osteogenesis

Yang et al. [30] found that miR-21 can promote the lipogenesis and osteogenesis of PDLSCs by directly inhibiting Spry1, a negative regulator of the ERK and FGF signaling pathways. However, TNF-α may control the expression of inflammatory cytokines, adipogenesis, and osteogenic differentiation of PDLSCs by targeting the miR-21/Spry1 functional axis.

In addition, several studies have identified other miRs that affect the osteogenic differentiation of PDLSCs. For instance, miR-200cN [31] inhibits LPS-induced IL-6, IL-8, and CCL-5 production in hPDLSCs and increases cellular calcium, ALP, and Runx2 levels, consequently promoting osteogenic differentiation. Another miRNA, miR-138, hinders the osteogenic differentiation of PDLSCs by downregulating osteocalcin, Runx2, and type I collagen. Conversely, miR-26a-5p [32] promotes the osteogenic differentiation of PDLSCs both in vitro and in vivo, presumably by targeting Wnt5a and thereby inhibiting the activation of the Wnt/Ca2+ signaling. Xu et al. [33,34] found that the inflammation-mediated changes in P2X7R-overexpressing PDLSCs in an inflammatory osteogenic microenvironment were significantly reduced. Another study revealed that P2X7R overexpression could significantly enhance the osteogenic differentiation of PDLSCs through the PI3K/Akt/mTOR signaling. These two studies paved the way for the gene modification of stem cells for the treatment of periodontitis. miR species and effects are far from that. Recently, Wang et al. [35] demonstrated experimentally that HOXA10 inhibits the osteogenic differentiation of periodontal stem cells through the regulation of β-linked protein localization and DKK1.

lncRNA is a non-coding RNA of >200 nucleotides. Based on the known IncRNAs, Zhang’s team [36] predicted 63 new lncRNAs that regulate the metabolism of various amino acids. They demonstrated that these metabolic pathways are important for the osteogenic differentiation of PDLSCs, thereby largely unraveling the mechanism underlying lncRNA regulation of osteogenesis. In addition, with the ultimate aim to improve the differentiation potential of periodontitis-derived PDLSCs, the same authors pursued the mechanism, whereby an inflammatory microenvironment hinders osteogenesis and consequently identified 318 differentially expressed lncRNAs between healthy PDLSCs and LPS-mediated PDLSCs. The list of these lncRNAs is expected to be a useful tool to study the osteogenic differentiation of PDLSCs under inflammatory microenvironment. These lncRNAs are expected to be valuable in studying the mechanisms underlying the osteogenic differentiation of PDLSCs in an inflammatory microenvironment. Such studies on the mechanisms whereby lncRNAs regulate the osteogenic differentiation of PDLSCs have recently flourished.

In addition, several scholars have explored chemical approaches to improve osteogenesis. For example, tetramethylpyrazine (TMP) [37] improved the osteogenesis of LPS-stimulated human periodontal membrane cells by reducing inflammation and apoptosis through downregulation of miR-302b. In addition, 1,25(OH)2D3 has been shown to promote osteogenesis by inhibiting the transcription of PLAP-1 [38], but clinical trials have not yielded promising results.

3 Effects of biochemical and other mechanisms

Epigenetic modifications, such as DNA methylation and histone acetylation, manifest at the molecular level. Diomede et al. [39] detected that protein levels are altered in association with DNA methylation and histone acetylation in LPS-treated hPDLSCs and inferred that LPS can affect the osteogenic differentiation of periodontal stem cells through epigenetic modifications.

Endoplasmic reticulum stress (ERS) is a pathophysiological process [40,41] in which an imbalance in the action of the endoplasmic reticulum in response to a noxious stimulus leads to a decrease in the ability of the endoplasmic reticulum to fold proteins and an increase in the amount of unfolded proteins. Xue et al. [42] applied endoplasmic reticulum activators to LPS-treated PDLSCs and detected significant downregulation of the osteogenic markers RUNX2 and ALP. Zhang et al. [43] found that inflammatory periodontal stem cells mediated IL-1β secretion by macrophages through regulation of macrophage endoplasmic reticulum stress, which is suggestive of the involvement of endoplasmic reticulum in osteogenesis. Zhai et al. [44] found that upregulation of mitochondrial fusion protein 2 (mitofusin 2, Mfn2), a factor mediating endoplasmic reticulum-mitochondria coupling, suppresses osteogenesis. Recently, Feng et al. have found that 4-phenylbutyric acid [45] can inhibit inflammation and improve osteogenesis through ERS-related mechanisms and the NF-κB pathway.

From a systemic perspective, Plemmenos and Piperi [46] found that AGEs, glycosylation end products in diabetic metabolism, enhance LPS-induced expression of inflammatory factors in hPDLSCs and reduce osteogenic differentiation. It is suggested that diabetes may exacerbate the inflammation in patients with periodontitis and thus must be considered in periodontal treatment.

4 Conclusion

Periodontitis is a common disease of the periodontal supporting tissues, and most patients present to the clinic with severe symptoms, such as significant alveolar bone resorption and tooth loosening or even loss. However, there is currently no effective therapeutic strategy in periodontitis. In recent years, the development of tissue stem cell engineering has led researchers to seek breakthroughs in periodontitis treatment from a new perspective, such as regenerative approaches using periodontal stem cells. However, in the oral cavity of patients with severe periodontitis, the inflammatory microenvironment [47] caused by the high concentrations of LPS hampers the osteogenic differentiation of periodontal stem cells and, thus, impedes the success of the regenerative therapy. Therefore, the mechanisms underlying this phenomenon should be elucidated to find effective solutions that can improve the success rate.

PDLSC osteogenesis is differentially affected by LPS through different signaling pathways. The osteogenic differentiation of hPDLSCs is promoted by E. coli LPS at low concentrations through the Wnt/β-catenin–induced upregulation of TAZ. However, both the histone acetyltransferase GCN5 and phospholipase Notum can suppress this pathway, thereby inhibiting the osteogenic differentiation. LPS can also inhibit osteogenesis and instead induce adipogenesis of hPDLSCs under inflammatory conditions by activating the TLR4 signaling and presumably through the resulting EphrinB2 downregulation, and by activating the NF-κB pathway. In addition, high doses of TLR1, 4, and 6 ligands inhibit Akt activation through the Myd88- or TRIF-dependent signaling pathways, which also inhibit hPDLSC osteogenesis. Activation of the ERK1/2 signaling can also affect cell differentiation. Studies at the gene level have revealed that the miR-148a/NRP1 functional axis and miR-138 have inhibitory effects on osteogenesis, whereas miR-200cN, miR-26a-5p, and P2X7R have stimulatory effects. Studies on micro-RNAs and lncRNAs have expanded the spectrum of mechanistic studies related to osteogenesis. In addition, epigenetic modifications, ERS, endoplasmic reticulum-mitochondrial coupling, and diabetic metabolites have inhibitory effects on the osteogenic differentiation of periodontal stem cells.

Immense progress [48] has been made on the mechanisms affecting the osteogenic differentiation of PDLSCs in an LPS-induced inflammatory environment. These stem cells constitute a physiologically suitable cell population that can be used for the regenerative treatment of periodontitis [49]. Furthermore, they can be easily obtained and cultured and are tolerant to the LPS-induced inflammatory microenvironment of periodontitis. Of course, there are still many mechanisms yet to be clarified. First, the connections between the signaling pathways should be studied to further investigate the mechanisms affecting the osteogenic differentiation of PDLSCs in an LPS-induced inflammatory environment. Second, PDLSCs should be compared with other stem cells in osteogenic capacity in such an environment. Finally, although many factors affecting osteogenesis have been clinically explored, only a few have been applied to clinical experiments, and thus, basic research findings should be evaluated through additional clinical studies for bench-to-bedside translation.

  1. Funding information: The research has been financially supported by: (1) Xuzhou science and technology program (kc15sh015); (2) Jiangsu Province’s “six talent peaks” funded project (2014-wsw-068); (3) General project of natural science research plan of colleges and universities in Jiangsu Province (12kjb320015); (4) Key project of Jiangsu college students’ innovation and entrepreneurship training program (202010313088y); and (5) Open project of Jiangsu Key Laboratory of oral diseases (jsklod-kf-1905)

  2. Author contributions: Jin conceived the idea and completed the writing and subsequent revision of the article. Jiang suggested ideas and participated in revisions. Sun, Fang Li, Xia, and Yaxin Li are members of the subject group and provided help with the conception and writing of the article. Zheng and Qin are supervisors and guided us through the article. Zheng is the corresponding author. The authors applied the SDC approach for the sequence of authors. Authors are sorted in order of upload (under the heading). Each author has consensus.

  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.

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Received: 2022-03-14
Revised: 2022-06-29
Accepted: 2022-07-07
Published Online: 2022-09-19

© 2022 Shenghao Jin et al., published by De Gruyter

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

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https://doi.org/10.1515/biol-2022-0474
Keywords for this article
periodontal membrane stem cells; osteogenic differentiation; inflammatory environment; lipopolysaccharide
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Effects of direct oral anticoagulants dabigatran and rivaroxaban on the blood coagulation function in rabbits
  3. The mother of all battles: Viruses vs humans. Can humans avoid extinction in 50–100 years?
  4. Knockdown of G1P3 inhibits cell proliferation and enhances the cytotoxicity of dexamethasone in acute lymphoblastic leukemia
  5. LINC00665 regulates hepatocellular carcinoma by modulating mRNA via the m6A enzyme
  6. Association study of CLDN14 variations in patients with kidney stones
  7. Concanavalin A-induced autoimmune hepatitis model in mice: Mechanisms and future outlook
  8. Regulation of miR-30b in cancer development, apoptosis, and drug resistance
  9. Informatic analysis of the pulmonary microecology in non-cystic fibrosis bronchiectasis at three different stages
  10. Swimming attenuates tumor growth in CT-26 tumor-bearing mice and suppresses angiogenesis by mediating the HIF-1α/VEGFA pathway
  11. Characterization of intestinal microbiota and serum metabolites in patients with mild hepatic encephalopathy
  12. Functional conservation and divergence in plant-specific GRF gene family revealed by sequences and expression analysis
  13. Application of the FLP/LoxP-FRT recombination system to switch the eGFP expression in a model prokaryote
  14. Biomedical evaluation of antioxidant properties of lamb meat enriched with iodine and selenium
  15. Intravenous infusion of the exosomes derived from human umbilical cord mesenchymal stem cells enhance neurological recovery after traumatic brain injury via suppressing the NF-κB pathway
  16. Effect of dietary pattern on pregnant women with gestational diabetes mellitus and its clinical significance
  17. Potential regulatory mechanism of TNF-α/TNFR1/ANXA1 in glioma cells and its role in glioma cell proliferation
  18. Effect of the genetic mutant G71R in uridine diphosphate-glucuronosyltransferase 1A1 on the conjugation of bilirubin
  19. Quercetin inhibits cytotoxicity of PC12 cells induced by amyloid-beta 25–35 via stimulating estrogen receptor α, activating ERK1/2, and inhibiting apoptosis
  20. Nutrition intervention in the management of novel coronavirus pneumonia patients
  21. circ-CFH promotes the development of HCC by regulating cell proliferation, apoptosis, migration, invasion, and glycolysis through the miR-377-3p/RNF38 axis
  22. Bmi-1 directly upregulates glucose transporter 1 in human gastric adenocarcinoma
  23. Lacunar infarction aggravates the cognitive deficit in the elderly with white matter lesion
  24. Hydroxysafflor yellow A improved retinopathy via Nrf2/HO-1 pathway in rats
  25. Comparison of axon extension: PTFE versus PLA formed by a 3D printer
  26. Elevated IL-35 level and iTr35 subset increase the bacterial burden and lung lesions in Mycobacterium tuberculosis-infected mice
  27. A case report of CAT gene and HNF1β gene variations in a patient with early-onset diabetes
  28. Study on the mechanism of inhibiting patulin production by fengycin
  29. SOX4 promotes high-glucose-induced inflammation and angiogenesis of retinal endothelial cells by activating NF-κB signaling pathway
  30. Relationship between blood clots and COVID-19 vaccines: A literature review
  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
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  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
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  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
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  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”
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