The role of CD146 in mesenchymal stem cells_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHA Kangkang ^1,2,3 , TIAN Guangzhao ^1,2,3 , YANG Zhen ^1,2,3 , SUN Zhiqiang ^1,2,3 , LIU Shuyun ² ,  GUO Quanyi ²

1. Medical School of Chinese PLA, Beijing, 100853, P.R.China;
2. Institute of Orthopaedics, the First Medical Centre, Chinese PLA General Hospital, Beijing Key Laboratory of Regenerative Medicine in Orthopaedics, Key Laboratory of Musculoskeletal Trauma & War Injuries, Beijing, 100853, P.R.China;
3. School of Medicine, Nankai University, Tianjin, 300071, P.R.China;

Corresponding author：

GUO Quanyi, Email: doctorguo_301@163.com

Keywords：

CD146; mesenchymal stem cells; heterogeneity; stem cell subset; regeneration

DOI：

10.7507/1002-1892.202005110

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the expression and role of CD146 in mesenchymal stem cells (MSCs).Methods The literature related to CD146 at home and abroad were extensively consulted, and the CD146 expression in MSCs and its function were summarized and analyzed.Results CD146 is a transmembrane protein that mediates the adhesion of cells to cells and extracellular matrix, and is expressed on the surface of various MSCs. More and more studies have shown that CD146⁺ MSCs have superior cell properties such as greater proliferation, differentiation, migration, and immune regulation abilities than CD146^- or unsorted MSCs, and the application of CD146⁺ MSCs in the treatment of specific diseases has also achieved better results. CD146 is also involved in mediating a variety of cellular signaling pathways, but whether it plays the same role in MSCs remains to be demonstrated by further experiments.Conclusion The utilization of CD146⁺ MSCs for tissue regeneration will be conducive to improving the therapeutic effect of MSCs.

Citation： ZHA Kangkang, TIAN Guangzhao, YANG Zhen, SUN Zhiqiang, LIU Shuyun, GUO Quanyi. The role of CD146 in mesenchymal stem cells. Chinese Journal of Reparative and Reconstructive Surgery, 2021, 35(2): 227-233. doi: 10.7507/1002-1892.202005110 Copy

1.	Reinisch A, Etchart N, Thomas D, et al. Epigenetic and in vivo comparison of diverse MSC sources reveals an endochondral signature for human hematopoietic niche formation. Blood, 2015, 125(2): 249-260.
2.	Costa LA, Eiro N, Fraile M, et al. Functional heterogeneity of mesenchymal stem cells from natural niches to culture conditions: implications for further clinical uses. Cell Mol Life Sci, 2020. doi: 10.1007/s00018-020-03600-0.
3.	Lehmann JM, Holzmann B, Breitbart EW, et al. Discrimination between benign and malignant cells of melanocytic lineage by two novel antigens, a glycoprotein with a molecular weight of 113, 000 and a protein with a molecular weight of 76, 000. Cancer Res, 1987, 47(3): 841-845.
4.	Shih IM, Nesbit M, Herlyn M, et al. A new Mel-CAM (CD146)-specific monoclonal antibody, MN-4, on paraffin-embedded tissue. Mod Pathol, 1998, 11(11): 1098-1106.
5.	Lv FJ, Tuan RS, Cheung KM, et al. Concise review: the surface markers and identity of human mesenchymal stem cells. Stem Cells, 2014, 32(6): 1408-1419.
6.	Wang Z, Yan X. CD146, a multi-functional molecule beyond adhesion. Cancer Lett, 2013, 330(2): 150-162.
7.	Yang YK, Ogando CR, Wang See C, et al. Changes in phenotype and differentiation potential of human mesenchymal stem cells aging in vitro. Stem Cell Res Ther, 2018, 9(1): 131.
8.	Tormin A, Li O, Brune JC, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood, 2011, 117(19): 5067-5077.
9.	Liu JW, Nagpal JK, Jeronimo C, et al. Hypermethylation of MCAM gene is associated with advanced tumor stage in prostate cancer. Prostate, 2008, 68(4): 418-426.
10.	Harkness L, Zaher W, Ditzel N, et al. CD146/MCAM defines functionality of human bone marrow stromal stem cell populations. Stem Cell Res Ther, 2016, 7: 4. doi: 10.1186/s13287-015-0266-z.
11.	Espagnolle N, Guilloton F, Deschaseaux F, et al. CD146 expression on mesenchymal stem cells is associated with their vascular smooth muscle commitment. J Cell Mol Med, 2014, 18(1): 104-114.
12.	Wangler S, Menzel U, Li Z, et al. CD146/MCAM distinguishes stem cell subpopulations with distinct migration and regenerative potential in degenerative intervertebral discs. Osteoarthritis Cartilage, 2019, 27(7): 1094-1105.
13.	Bowles AC, Kouroupis D, Willman MA, et al. Signature quality attributes of CD146+ mesenchymal stem/stromal cells correlate with high therapeutic and secretory potency. Stem Cells, 2020, 38(8): 1034-1049.
14.	Zhang B, Zhang J, Zhu D, et al. Mesenchymal stem cells rejuvenate cardiac muscle after ischemic injury. Aging (Albany NY), 2019, 11(1): 63-72.
15.	Wang Y, Xu J, Chang L, et al. Relative contributions of adipose-resident CD146(+) pericytes and CD34(+) adventitial progenitor cells in bone tissue engineering. NPJ Regen Med, 2019, 4: 1. doi: 10.1038/s41536-018-0063-2. eCollection 2019.
16.	Lauvrud AT, Kelk P, Wiberg M, et al. Characterization of human adipose tissue-derived stem cells with enhanced angiogenic and adipogenic properties. J Tissue Eng Regen Med, 2017, 11(9): 2490-2502.
17.	Liu F, Shi J, Zhang Y, et al. NANOG attenuates hair follicle-derived mesenchymal stem cell senescence by upregulating PBX1 and activating AKT signaling. Oxid Med Cell Longev, 2019, 2019: 4286213. doi: 10.1155/2019/4286213. eCollection 2019.
18.	Gomes JP, Coatti GC, Valadares MC, et al. Human Adipose-Derived CD146+ stem cells increase life span of a muscular dystrophy mouse model more efficiently than mesenchymal stromal cells. DNA Cell Biol, 2018, 37(9): 798-804.
19.	Jin HJ, Kwon JH, Kim M, et al. Downregulation of melanoma cell adhesion molecule (MCAM/CD146) accelerates cellular senescence in human umbilical cord blood-derived mesenchymal stem cells. Stem Cells Transl Med, 2016, 5(4): 427-439.
20.	Shafiei F, Tavangar MS, Razmkhah M, et al. Cytotoxic effect of silorane and methacrylate based composites on the human dental pulp stem cells and fibroblasts. Med Oral Patol Oral Cir Bucal, 2014, 19(4): e350-358.
21.	Tavangar MS, Attar A, Razmkhah M, et al. Differential expression of drug resistance genes in CD146 positive dental pulp derived stem cells and CD146 negative fibroblasts. Clin Exp Dent Res, 2020, 6(4): 448-456.
22.	Matsui M, Kobayashi T, Tsutsui TW. CD146 positive human dental pulp stem cells promote regeneration of dentin/pulp-like structures. Hum Cell, 2018, 31(2): 127-138.
23.	Ulrich C, Abruzzese T, Maerz JK, et al. Human placenta-derived CD146-positive mesenchymal stromal cells display a distinct osteogenic differentiation potential. Stem Cells Dev, 2015, 24(13): 1558-1569.
24.	Mikael PE, Golebiowska AA, Kumbar S, et al. Evaluation of autologously derived biomaterials and stem cells for bone tissue engineering. Tissue Eng Part A, 2020. doi: 10.1089/ten.TEA.2020.0011. Online ahead of print.
25.	Tripodo C, Di Bernardo A, Ternullo MP, et al. CD146(+) bone marrow osteoprogenitors increase in the advanced stages of primary myelofibrosis. Haematologica, 2009, 94(1): 127-130.
26.	Mangialardi G, Ferland-McCollough D, Maselli D, et al. Bone marrow pericyte dysfunction in individuals with type 2 diabetes. Diabetologia, 2019, 62(7): 1275-1290.
27.	Fodor PB, Paulseth SG. Adipose derived stromal cell (ADSC) injections for pain management of osteoarthritis in the human knee joint. Aesthet Surg J, 2016, 36(2): 229-236.
28.	Lotfy A, Salama M, Zahran F, et al. Characterization of mesenchymal stem cells derived from rat bone marrow and adipose tissue: a comparative study. Int J Stem Cells, 2014, 7(2): 135-142.
29.	Arulmoli J, Pathak MM, McDonnell LP, et al. Static stretch affects neural stem cell differentiation in an extracellular matrix-dependent manner. Sci Rep, 2015, 5: 8499.
30.	Kim HS, Mandakhbayar N, Kim HW, et al. Protein-reactive nanofibrils decorated with cartilage-derived decellularized extracellular matrix for osteochondral defects. Biomaterials, 2020: 120214.
31.	Zimmerlin L, Donnenberg VS, Rubin JP, et al. Mesenchymal markers on human adipose stem/progenitor cells. Cytometry A, 2013, 83(1): 134-140.
32.	Esteves CL, Sheldrake TA, Dawson L, et al. Equine mesenchymal stromal cells retain a pericyte-like phenotype. Stem Cells Dev, 2017, 26(13): 964-972.
33.	Lee NE, Kim SJ, Yang SJ, et al. Comparative characterization of mesenchymal stromal cells from multiple abdominal adipose tissues and enrichment of angiogenic ability via CD146 molecule. Cytotherapy, 2017, 19(2): 170-180.
34.	Dvoretskiy S, Garg K, Munroe M, et al. The impact of skeletal muscle contraction on CD146+ Lin- pericytes. Am J Physiol Cell Physiol, 2019, 317(5): C1011-C1024.
35.	Riordan NH, Morales I, Fernández G, et al. Clinical feasibility of umbilical cord tissue-derived mesenchymal stem cells in the treatment of multiple sclerosis. J Transl Med, 2018, 16(1): 57.
36.	Gökçinar-Yagci B, Özyüncü Ö, Çelebi-Saltik B. Isolation, characterisation and comparative analysis of human umbilical cord vein perivascular cells and cord blood mesenchymal stem cells. Cell Tissue Bank, 2016, 17(2): 345-352.
37.	Lin HD, Fong CY, Biswas A, et al. Hypoxic Wharton’s jelly stem cell conditioned medium induces immunogenic cell death in lymphoma cells. Stem Cells Int, 2020, 2020: 4670948. doi: 10.1155/2020/4670948. eCollection 2020.
38.	Xu L, Zhou J, Liu J, et al. Different angiogenic potentials of mesenchymal stem cells derived from umbilical artery, umbilical vein, and Wharton’s jelly. Stem Cells Int, 2017, 2017: 3175748. doi: 10.1155/2017/3175748. Epub 2017 Aug 10.
39.	Kouroupis D, Churchman SM, McGonagle D, et al. The assessment of CD146-based cell sorting and telomere length analysis for establishing the identity of mesenchymal stem cells in human umbilical cord. F1000Res, 2014, 3: 126. doi: 10.12688/f1000research.4260.2. eCollection 2014.
40.	Huang GT, Gronthos S, Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res, 2009, 88(9): 792-806.
41.	周鹏飞, 林静, 陈玉英, 等. 聚羟基乙酸-犬牙髓干细胞复合体修复犬牙周组织缺损. 中国组织工程研究, 2020, 24(34): 5526-5531.
42.	Ducret M, Farges JC, Pasdeloup M, et al. Phenotypic identification of dental pulp mesenchymal stem/stromal cells subpopulations with multiparametric flow cytometry. Methods Mol Biol, 2019, 1922: 77-90.
43.	Sivasankar V, Ranganathan K. Growth characteristics and expression of CD73 and CD146 in cells cultured from dental pulp. J Investig Clin Dent, 2016, 7(3): 278-285.
44.	Dmitrieva RI, Lelyavina TA, Komarova MY, et al. Skeletal muscle resident progenitor cells coexpress mesenchymal and myogenic markers and are not affected by chronic heart failure-induced dysregulations. Stem Cells Int, 2019, 2019: 5690345.
45.	Paduano F, Marrelli M, Palmieri F, et al. CD146 expression influences periapical cyst mesenchymal stem cell properties. Stem Cell Rev Rep, 2016, 12(5): 592-603.
46.	Collins JJP, Lithopoulos MA, Dos Santos CC, et al. Impaired angiogenic supportive capacity and altered gene expression profile of resident CD146+ mesenchymal stromal cells isolated from hyperoxia-injured neonatal rat lungs. Stem Cells Dev, 2018, 27(16): 1109-1124.
47.	Roson-Burgo B, Sanchez-Guijo F, Del Canizo C, et al. Transcriptomic portrait of human Mesenchymal Stromal/Stem Cells isolated from bone marrow and placenta. BMC Genomics, 2014, 15(1): 910.
48.	Pilz GA, Ulrich C, Ruh M, et al. Human term placenta-derived mesenchymal stromal cells are less prone to osteogenic differentiation than bone marrow-derived mesenchymal stromal cells. Stem Cells Dev, 2011, 20(4): 635-646.
49.	Xia T, Duan W, Zhang Z, et al. Polyphenol-rich extract of Zhenjiang aromatic vinegar ameliorates high glucose-induced insulin resistance by regulating JNK-IRS-1 and PI3K/Akt signaling pathways. Food Chem, 2020, 335: 127513.
50.	Cook SA, Comrie WA, Poli MC, et al. HEM1 deficiency disrupts mTORC2 and F-actin control in inherited immunodysregulatory disease. Science, 2020, 369(6500): 202-207.
51.	Li G, Kalabis J, Xu X, et al. Reciprocal regulation of MelCAM and AKT in human melanoma. Oncogene, 2003, 22(44): 6891-6899.
52.	Xu W, Hua H, Chiu YH, et al. CD146 regulates growth factor-induced mTORC2 activity independent of the PI3K and mTORC1 pathways. Cell Rep, 2019, 29(5): 1311-1322.
53.	Huang ZX, Mao XM, Wu RF, et al. RhoA/ROCK pathway mediates the effect of oestrogen on regulating epithelial-mesenchymal transition and proliferation in endometriosis. J Cell Mol Med, 2020. doi: 10.1111/jcmm.15689.
54.	王柳, 韩芮, 谢俊雄, 等. RhoA/ROCK 信号通路在骨性关节炎中的研究进展. 中国疼痛医学杂志, 2020, 26(5): 331-336.
55.	Luo Y, Zheng C, Zhang J, et al. Recognition of CD146 as an ERM-binding protein offers novel mechanisms for melanoma cell migration. Oncogene, 2012, 31(3): 306-321.
56.	Han L, Cui D, Li B, et al. MicroRNA-338-5p reverses chemoresistance and inhibits invasion of esophageal squamous cell carcinoma cells by targeting Id-1. Cancer Sci, 2019, 110(12): 3677-3688.
57.	Zigler M, Villares GJ, Dobroff AS, et al. Expression of Id-1 is regulated by MCAM/MUC18: a missing link in melanoma progression. Cancer Res, 2011, 71(10): 3494-3504.
58.	Ma Y, Zhang H, Xiong C, et al. CD146 mediates an E-cadherin-to-N-cadherin switch during TGF-β signaling-induced epithelial-mesenchymal transition. Cancer Lett, 2018, 430: 201-214.
59.	Jiang T, Zhuang J, Duan H, et al. CD146 is a coreceptor for VEGFR-2 in tumor angiogenesis. Blood, 2012, 120(11): 2330-2339.
60.	Meirelles Lda S, Fontes AM, Covas DT, et al. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev, 2009, 20(5-6): 419-427.
61.	Kohli N, Al-Delfi IRT, Snow M, et al. CD271-selected mesenchymal stem cells from adipose tissue enhance cartilage repair and are less angiogenic than plastic adherent mesenchymal stem cells. Sci Rep, 2019, 9(1): 3194.
62.	Fan W, Li J, Wang Y, et al. CD105 promotes chondrogenesis of synovium-derived mesenchymal stem cells through Smad2 signaling. Biochem Biophys Res Commun, 2016, 474(2): 338-344.
63.	Picke AK, Campbell GM, Bluher M, et al. Thy-1 (CD90) promotes bone formation and protects against obesity. Sci Transl Med, 2018, 10(453): eaao6806.
64.	Yang Z, Ma S, Cao R, et al. CD49f high defines a distinct skin mesenchymal stem cell population capable of hair follicle epithelial cell maintenance. J Invest Dermatol, 2020, 140(3): 544-555.

1. Reinisch A, Etchart N, Thomas D, et al. Epigenetic and in vivo comparison of diverse MSC sources reveals an endochondral signature for human hematopoietic niche formation. Blood, 2015, 125(2): 249-260.
2. Costa LA, Eiro N, Fraile M, et al. Functional heterogeneity of mesenchymal stem cells from natural niches to culture conditions: implications for further clinical uses. Cell Mol Life Sci, 2020. doi: 10.1007/s00018-020-03600-0.
3. Lehmann JM, Holzmann B, Breitbart EW, et al. Discrimination between benign and malignant cells of melanocytic lineage by two novel antigens, a glycoprotein with a molecular weight of 113, 000 and a protein with a molecular weight of 76, 000. Cancer Res, 1987, 47(3): 841-845.
4. Shih IM, Nesbit M, Herlyn M, et al. A new Mel-CAM (CD146)-specific monoclonal antibody, MN-4, on paraffin-embedded tissue. Mod Pathol, 1998, 11(11): 1098-1106.
5. Lv FJ, Tuan RS, Cheung KM, et al. Concise review: the surface markers and identity of human mesenchymal stem cells. Stem Cells, 2014, 32(6): 1408-1419.
6. Wang Z, Yan X. CD146, a multi-functional molecule beyond adhesion. Cancer Lett, 2013, 330(2): 150-162.
7. Yang YK, Ogando CR, Wang See C, et al. Changes in phenotype and differentiation potential of human mesenchymal stem cells aging in vitro. Stem Cell Res Ther, 2018, 9(1): 131.
8. Tormin A, Li O, Brune JC, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood, 2011, 117(19): 5067-5077.
9. Liu JW, Nagpal JK, Jeronimo C, et al. Hypermethylation of MCAM gene is associated with advanced tumor stage in prostate cancer. Prostate, 2008, 68(4): 418-426.
10. Harkness L, Zaher W, Ditzel N, et al. CD146/MCAM defines functionality of human bone marrow stromal stem cell populations. Stem Cell Res Ther, 2016, 7: 4. doi: 10.1186/s13287-015-0266-z.
11. Espagnolle N, Guilloton F, Deschaseaux F, et al. CD146 expression on mesenchymal stem cells is associated with their vascular smooth muscle commitment. J Cell Mol Med, 2014, 18(1): 104-114.
12. Wangler S, Menzel U, Li Z, et al. CD146/MCAM distinguishes stem cell subpopulations with distinct migration and regenerative potential in degenerative intervertebral discs. Osteoarthritis Cartilage, 2019, 27(7): 1094-1105.
13. Bowles AC, Kouroupis D, Willman MA, et al. Signature quality attributes of CD146+ mesenchymal stem/stromal cells correlate with high therapeutic and secretory potency. Stem Cells, 2020, 38(8): 1034-1049.
14. Zhang B, Zhang J, Zhu D, et al. Mesenchymal stem cells rejuvenate cardiac muscle after ischemic injury. Aging (Albany NY), 2019, 11(1): 63-72.
15. Wang Y, Xu J, Chang L, et al. Relative contributions of adipose-resident CD146(+) pericytes and CD34(+) adventitial progenitor cells in bone tissue engineering. NPJ Regen Med, 2019, 4: 1. doi: 10.1038/s41536-018-0063-2. eCollection 2019.
16. Lauvrud AT, Kelk P, Wiberg M, et al. Characterization of human adipose tissue-derived stem cells with enhanced angiogenic and adipogenic properties. J Tissue Eng Regen Med, 2017, 11(9): 2490-2502.
17. Liu F, Shi J, Zhang Y, et al. NANOG attenuates hair follicle-derived mesenchymal stem cell senescence by upregulating PBX1 and activating AKT signaling. Oxid Med Cell Longev, 2019, 2019: 4286213. doi: 10.1155/2019/4286213. eCollection 2019.
18. Gomes JP, Coatti GC, Valadares MC, et al. Human Adipose-Derived CD146+ stem cells increase life span of a muscular dystrophy mouse model more efficiently than mesenchymal stromal cells. DNA Cell Biol, 2018, 37(9): 798-804.
19. Jin HJ, Kwon JH, Kim M, et al. Downregulation of melanoma cell adhesion molecule (MCAM/CD146) accelerates cellular senescence in human umbilical cord blood-derived mesenchymal stem cells. Stem Cells Transl Med, 2016, 5(4): 427-439.
20. Shafiei F, Tavangar MS, Razmkhah M, et al. Cytotoxic effect of silorane and methacrylate based composites on the human dental pulp stem cells and fibroblasts. Med Oral Patol Oral Cir Bucal, 2014, 19(4): e350-358.
21. Tavangar MS, Attar A, Razmkhah M, et al. Differential expression of drug resistance genes in CD146 positive dental pulp derived stem cells and CD146 negative fibroblasts. Clin Exp Dent Res, 2020, 6(4): 448-456.
22. Matsui M, Kobayashi T, Tsutsui TW. CD146 positive human dental pulp stem cells promote regeneration of dentin/pulp-like structures. Hum Cell, 2018, 31(2): 127-138.
23. Ulrich C, Abruzzese T, Maerz JK, et al. Human placenta-derived CD146-positive mesenchymal stromal cells display a distinct osteogenic differentiation potential. Stem Cells Dev, 2015, 24(13): 1558-1569.
24. Mikael PE, Golebiowska AA, Kumbar S, et al. Evaluation of autologously derived biomaterials and stem cells for bone tissue engineering. Tissue Eng Part A, 2020. doi: 10.1089/ten.TEA.2020.0011. Online ahead of print.
25. Tripodo C, Di Bernardo A, Ternullo MP, et al. CD146(+) bone marrow osteoprogenitors increase in the advanced stages of primary myelofibrosis. Haematologica, 2009, 94(1): 127-130.
26. Mangialardi G, Ferland-McCollough D, Maselli D, et al. Bone marrow pericyte dysfunction in individuals with type 2 diabetes. Diabetologia, 2019, 62(7): 1275-1290.
27. Fodor PB, Paulseth SG. Adipose derived stromal cell (ADSC) injections for pain management of osteoarthritis in the human knee joint. Aesthet Surg J, 2016, 36(2): 229-236.
28. Lotfy A, Salama M, Zahran F, et al. Characterization of mesenchymal stem cells derived from rat bone marrow and adipose tissue: a comparative study. Int J Stem Cells, 2014, 7(2): 135-142.
29. Arulmoli J, Pathak MM, McDonnell LP, et al. Static stretch affects neural stem cell differentiation in an extracellular matrix-dependent manner. Sci Rep, 2015, 5: 8499.
30. Kim HS, Mandakhbayar N, Kim HW, et al. Protein-reactive nanofibrils decorated with cartilage-derived decellularized extracellular matrix for osteochondral defects. Biomaterials, 2020: 120214.
31. Zimmerlin L, Donnenberg VS, Rubin JP, et al. Mesenchymal markers on human adipose stem/progenitor cells. Cytometry A, 2013, 83(1): 134-140.
32. Esteves CL, Sheldrake TA, Dawson L, et al. Equine mesenchymal stromal cells retain a pericyte-like phenotype. Stem Cells Dev, 2017, 26(13): 964-972.
33. Lee NE, Kim SJ, Yang SJ, et al. Comparative characterization of mesenchymal stromal cells from multiple abdominal adipose tissues and enrichment of angiogenic ability via CD146 molecule. Cytotherapy, 2017, 19(2): 170-180.
34. Dvoretskiy S, Garg K, Munroe M, et al. The impact of skeletal muscle contraction on CD146+ Lin- pericytes. Am J Physiol Cell Physiol, 2019, 317(5): C1011-C1024.
35. Riordan NH, Morales I, Fernández G, et al. Clinical feasibility of umbilical cord tissue-derived mesenchymal stem cells in the treatment of multiple sclerosis. J Transl Med, 2018, 16(1): 57.
36. Gökçinar-Yagci B, Özyüncü Ö, Çelebi-Saltik B. Isolation, characterisation and comparative analysis of human umbilical cord vein perivascular cells and cord blood mesenchymal stem cells. Cell Tissue Bank, 2016, 17(2): 345-352.
37. Lin HD, Fong CY, Biswas A, et al. Hypoxic Wharton’s jelly stem cell conditioned medium induces immunogenic cell death in lymphoma cells. Stem Cells Int, 2020, 2020: 4670948. doi: 10.1155/2020/4670948. eCollection 2020.
38. Xu L, Zhou J, Liu J, et al. Different angiogenic potentials of mesenchymal stem cells derived from umbilical artery, umbilical vein, and Wharton’s jelly. Stem Cells Int, 2017, 2017: 3175748. doi: 10.1155/2017/3175748. Epub 2017 Aug 10.
39. Kouroupis D, Churchman SM, McGonagle D, et al. The assessment of CD146-based cell sorting and telomere length analysis for establishing the identity of mesenchymal stem cells in human umbilical cord. F1000Res, 2014, 3: 126. doi: 10.12688/f1000research.4260.2. eCollection 2014.
40. Huang GT, Gronthos S, Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res, 2009, 88(9): 792-806.
41. 周鹏飞, 林静, 陈玉英, 等. 聚羟基乙酸-犬牙髓干细胞复合体修复犬牙周组织缺损. 中国组织工程研究, 2020, 24(34): 5526-5531.
42. Ducret M, Farges JC, Pasdeloup M, et al. Phenotypic identification of dental pulp mesenchymal stem/stromal cells subpopulations with multiparametric flow cytometry. Methods Mol Biol, 2019, 1922: 77-90.
43. Sivasankar V, Ranganathan K. Growth characteristics and expression of CD73 and CD146 in cells cultured from dental pulp. J Investig Clin Dent, 2016, 7(3): 278-285.
44. Dmitrieva RI, Lelyavina TA, Komarova MY, et al. Skeletal muscle resident progenitor cells coexpress mesenchymal and myogenic markers and are not affected by chronic heart failure-induced dysregulations. Stem Cells Int, 2019, 2019: 5690345.
45. Paduano F, Marrelli M, Palmieri F, et al. CD146 expression influences periapical cyst mesenchymal stem cell properties. Stem Cell Rev Rep, 2016, 12(5): 592-603.
46. Collins JJP, Lithopoulos MA, Dos Santos CC, et al. Impaired angiogenic supportive capacity and altered gene expression profile of resident CD146+ mesenchymal stromal cells isolated from hyperoxia-injured neonatal rat lungs. Stem Cells Dev, 2018, 27(16): 1109-1124.
47. Roson-Burgo B, Sanchez-Guijo F, Del Canizo C, et al. Transcriptomic portrait of human Mesenchymal Stromal/Stem Cells isolated from bone marrow and placenta. BMC Genomics, 2014, 15(1): 910.
48. Pilz GA, Ulrich C, Ruh M, et al. Human term placenta-derived mesenchymal stromal cells are less prone to osteogenic differentiation than bone marrow-derived mesenchymal stromal cells. Stem Cells Dev, 2011, 20(4): 635-646.
49. Xia T, Duan W, Zhang Z, et al. Polyphenol-rich extract of Zhenjiang aromatic vinegar ameliorates high glucose-induced insulin resistance by regulating JNK-IRS-1 and PI3K/Akt signaling pathways. Food Chem, 2020, 335: 127513.
50. Cook SA, Comrie WA, Poli MC, et al. HEM1 deficiency disrupts mTORC2 and F-actin control in inherited immunodysregulatory disease. Science, 2020, 369(6500): 202-207.
51. Li G, Kalabis J, Xu X, et al. Reciprocal regulation of MelCAM and AKT in human melanoma. Oncogene, 2003, 22(44): 6891-6899.
52. Xu W, Hua H, Chiu YH, et al. CD146 regulates growth factor-induced mTORC2 activity independent of the PI3K and mTORC1 pathways. Cell Rep, 2019, 29(5): 1311-1322.
53. Huang ZX, Mao XM, Wu RF, et al. RhoA/ROCK pathway mediates the effect of oestrogen on regulating epithelial-mesenchymal transition and proliferation in endometriosis. J Cell Mol Med, 2020. doi: 10.1111/jcmm.15689.
54. 王柳, 韩芮, 谢俊雄, 等. RhoA/ROCK 信号通路在骨性关节炎中的研究进展. 中国疼痛医学杂志, 2020, 26(5): 331-336.
55. Luo Y, Zheng C, Zhang J, et al. Recognition of CD146 as an ERM-binding protein offers novel mechanisms for melanoma cell migration. Oncogene, 2012, 31(3): 306-321.
56. Han L, Cui D, Li B, et al. MicroRNA-338-5p reverses chemoresistance and inhibits invasion of esophageal squamous cell carcinoma cells by targeting Id-1. Cancer Sci, 2019, 110(12): 3677-3688.
57. Zigler M, Villares GJ, Dobroff AS, et al. Expression of Id-1 is regulated by MCAM/MUC18: a missing link in melanoma progression. Cancer Res, 2011, 71(10): 3494-3504.
58. Ma Y, Zhang H, Xiong C, et al. CD146 mediates an E-cadherin-to-N-cadherin switch during TGF-β signaling-induced epithelial-mesenchymal transition. Cancer Lett, 2018, 430: 201-214.
59. Jiang T, Zhuang J, Duan H, et al. CD146 is a coreceptor for VEGFR-2 in tumor angiogenesis. Blood, 2012, 120(11): 2330-2339.
60. Meirelles Lda S, Fontes AM, Covas DT, et al. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev, 2009, 20(5-6): 419-427.
61. Kohli N, Al-Delfi IRT, Snow M, et al. CD271-selected mesenchymal stem cells from adipose tissue enhance cartilage repair and are less angiogenic than plastic adherent mesenchymal stem cells. Sci Rep, 2019, 9(1): 3194.
62. Fan W, Li J, Wang Y, et al. CD105 promotes chondrogenesis of synovium-derived mesenchymal stem cells through Smad2 signaling. Biochem Biophys Res Commun, 2016, 474(2): 338-344.
63. Picke AK, Campbell GM, Bluher M, et al. Thy-1 (CD90) promotes bone formation and protects against obesity. Sci Transl Med, 2018, 10(453): eaao6806.
64. Yang Z, Ma S, Cao R, et al. CD49f high defines a distinct skin mesenchymal stem cell population capable of hair follicle epithelial cell maintenance. J Invest Dermatol, 2020, 140(3): 544-555.

Chinese Journal of Reparative and Reconstructive Surgery

The role of CD146 in mesenchymal stem cells

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