Research progress of endogenous repair strategy in intervertebral disc_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LIU Yang ¹ ,  LIU Hao ¹ , MENG Yang ¹ , ZHANG Liang ²

1. Department of Orthopedics, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;
2. Department of Orthopedics, Northern Jiangsu People’s Hospital, Yangzhou Jiangsu, 225000, P.R.China;

Corresponding author：

LIU Hao, Email: dr.liuhao6304@yahoo.com

Keywords：

Intervertebral disc degeneration; endogenous repair strategy; intervertebral disc; stem/progenitor cells

DOI：

10.7507/1002-1892.202012070

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To review the research progress of endogenous repair strategy (ERS) in intervertebral disc (IVD).Methods The domestic and foreign literature related to ERS in IVD in recent years was reviewed, and its characteristics, status, and prospect in the future were summarized.Results The key of ERS in IVD is to improve the vitality of stem/progenitor cells in IVD or promote its migration from stem cell Niche to the tissue that need to repair. These stem/progenitor cells in IVD are derived from nucleus pulposus, annulus fibrosus, and cartilaginous endplate, showing similar biological characteristics to mesenchymal stem cells including the expression of the specific stem/progenitor cell surface markers and gene, and also the capacity of multiple differentiations potential. However, the development, senescence, and degeneration of IVD have consumed these stem/progenitor cells, and the harsh internal microenvironment further impair their biological characteristics, which leads to the failure of endogenous repair in IVD. At present, relevant research mainly focuses on improving the biological characteristics of endogenous stem/progenitor cells, directly supplementing endogenous stem/progenitor cells, biomaterials and small molecule compounds to stimulate the endogenous repair in IVD, so as to improve the effect of endogenous repair.Conclusion At present, ERS has gotten some achievements in the treatment of IVD degeneration, but its related studies are still in the pre-clinical stage. So further studies regarding ERS should be carried out in the future, especially in vivo experiments and clinical transformation.

Citation： LIU Yang, LIU Hao, MENG Yang, ZHANG Liang. Research progress of endogenous repair strategy in intervertebral disc. Chinese Journal of Reparative and Reconstructive Surgery, 2021, 35(5): 636-641. doi: 10.7507/1002-1892.202012070 Copy

1.	GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet, 2016, 388(10053): 1545-1602.
2.	Wu A, Dong W, Liu S, et al. The prevalence and years lived with disability caused by low back pain in China, 1990 to 2016: findings from the global burden of disease study 2016. Pain, 2019, 160(1): 237-245.
3.	Makanji H, Schoenfeld AJ, Bhalla A, et al. Critical analysis of trends in lumbar fusion for degenerative disorders revisited: influence of technique on fusion rate and clinical outcomes. Eur Spine J, 2018, 27(8): 1868-1876.
4.	梁秋发, 原林, 王文军, 等. 颈椎前路融合术后临近节段退变的MRI分析. 医学临床研究, 2005, 22(6): 727-729.
5.	Sakai D, Andersson GB. Stem cell therapy for intervertebral disc regeneration: obstacles and solutions. Nat Rev Rheumatol, 2015, 11(4): 243-256.
6.	Liang C, Li H, Tao Y, et al. Responses of human adipose-derived mesenchymal stem cells to chemical microenvironment of the intervertebral disc. J Transl Med, 2012, 10: 49. doi: 10.1186/1479-5876-10-49.
7.	Wang Y, Han ZB, Song YP, et al. Safety of mesenchymal stem cells for clinical application. Stem Cells Int, 2012, 2012: 652034. doi: 10.1155/2012/652034.
8.	Vadalà G, Sowa G, Hubert M, et al. Mesenchymal stem cells injection in degenerated intervertebral disc: Cell leakage may induce osteophyte formation. J Tissue Eng Regen Med, 2012, 6(5): 348-355.
9.	Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 1978, 4(1-2): 7-25.
10.	Scadden DT. The stem-cell niche as an entity of action. Nature, 2006, 441(7097): 1075-1079.
11.	Ruddy RM, Morshead CM. Home sweet home: the neural stem cell niche throughout development and after injury. Cell Tissue Res, 2018, 371(1): 125-141.
12.	Seike M, Omatsu Y, Watanabe H, et al. Stem cell niche-specific Ebf3 maintains the bone marrow cavity. Genes Dev, 2018, 32(5-6): 359-372.
13.	Gong M, Zhang P, Li C, et al. Protective mechanism of adipose-derived stem cells in remodelling of the skin stem cell niche during photoaging. Cell Physiol Biochem, 2018, 51(5): 2456-2471.
14.	Bartfeld S, Koo BK. Adult gastric stem cells and their niches. Wiley Interdiscip Rev Dev Biol, 2017, 6(2). doi: 10.1002/wdev.261.
15.	Shi R, Wang F, Hong X, et al. The presence of stem cells in potential stem cell niches of the intervertebral disc region: an in vitro study on rats. Eur Spine J, 2015, 24(11): 2411-2424.
16.	Clouet J, Fusellier M, Camus A, et al. Intervertebral disc regeneration: From cell therapy to the development of novel bioinspired endogenous repair strategies. Adv Drug Deliv Reviews, 2019, 146: 306-324.
17.	Risbud MV, Shapiro IM. Role of cytokines in intervertebral disc degeneration: pain and disc content. Nat Rev Rheumatol, 2014, 10(1): 44-56.
18.	Blanco JF, Graciani IF, Sanchez-Guijo FM, et al. Isolation and characterization of mesenchymal stromal cells from human degenerated nucleus pulposus: Comparison with bone marrow mesenchymal stromal cells from the same subjects. Spine (Phila Pa 1976), 2010, 35(26): 2259-2265.
19.	Tao YQ, Liang CZ, Li H, et al. Potential of co-culture of nucleus pulposus mesenchymal stem cells and nucleus pulposus cells in hyperosmotic microenvironment for intervertebral disc regeneration. Cell Biol Int, 2013, 37: 826-834.
20.	Han B, Wang HC, Li H, et al. Nucleus pulposus mesenchymal stem cells in acidic conditions mimicking degenerative intervertebral discs give better performance than adipose tissue-derived mesenchymal stem cells. Cells Tissues Organs, 2014, 199(5-6): 342-352.
21.	Liu Y, Li Y, Huang ZN, et al. The effect of intervertebral disc degenerative change on biological characteristics of nucleus pulposus mesenchymal stem cell: an in vitro study in rats. Connect Tissue Res, 2019, 60(4): 376-388.
22.	Yu H, Vu TH, Cho KS, et al. Mobilizing endogenous stem cells for retinal repair. Transl Res, 2014, 163(4): 387-398.
23.	Lyu FJ, Cheung KM, Zheng Z, et al. IVD progenitor cells: a new horizon for understanding disc homeostasis and repair. Nat Rev Rheumatol, 2019, 15(2): 102-112.
24.	Liu LT, Huang B, Li CQ, et al. Characteristics of stem cells derived from the degenerated human intervertebral disc cartilage endplate. PLoS One, 2011, 6(10): e26285. doi: 10.1371/journal.pone.0026285.
25.	Liu J, Tao H, Wang H, et al. Biological behavior of human nucleus pulposus mesenchymal stem cells in response to changes in the acidic environment during intervertebral disc degeneration. Stem Cells Dev, 2017, 26(12): 901-911.
26.	Wu H, Zeng X, Yu J, et al. Comparison of nucleus pulposus stem/progenitor cells isolated from degenerated intervertebral discs with umbilical cord derived mesenchymal stem cells. Exp Cell Res, 2017, 361(2): 324-332.
27.	Li Z, Chen S, Ma K, et al. Comparison of different methods for the isolation and purification of rat nucleus pulposus-derived mesenchymal stem cells. Connect Tissue Res, 2020, 61(5): 426-434.
28.	Cheng S, Li X, Jia Z, et al. The inflammatory cytokine TNF-α regulates the biological behavior of rat nucleus pulposus mesenchymal stem cells through the NF-κb signaling pathway in vitro. J Cell Biochem, 2019, 120: 13664-13679.
29.	Lin L, Jia Z, Zhao Y, et al. Use of limiting dilution method for isolation of nucleus pulposus mesenchymal stem/progenitor cells and effects of plating density on biological characteristics and plasticity. Biomed Res Int, 2017, 2017: 9765843. doi: 10.1155/2017/9765843.
30.	Jia J, Wang SZ, Ma LY, et al. The differential effects of leukocyte-containing and pure platelet-rich plasma on nucleus pulposus-derived mesenchymal stem cells: Implications for the clinical treatment of intervertebral disc degeneration. Stem Cells Int, 2018, 2018: 7162084. doi: 10.1155/2018/7162084.
31.	Lazzarini R, Guarnieri S, Fulgenzi G, et al. Mesenchymal stem cells from nucleus pulposus and neural differentiation potential: A continuous challenge. J Mol Neurosci, 2019, 67(1): 111-124.
32.	Qi L, Wang R, Shi Q, et al. Umbilical cord mesenchymal stem cell conditioned medium restored the expression of collagen Ⅱ and aggrecan in nucleus pulposus mesenchymal stem cells exposed to high glucose. J Bone Miner Metab, 2019, 37(3): 455-466.
33.	Wang KH, Kao AP, Chang CC, et al. Upregulation of Nanog and Sox-2 genes following ectopic expression of Oct-4 in amniotic fluid mesenchymal stem cells. Biotechnol Appl Biochem, 2015, 62(5): 591-597.
34.	Zanotti S, Canalis E. Notch signaling and the skeleton. Endocr Rev, 2016, 37(3): 223-253.
35.	Ciria M, García NA, Ontoria-Oviedo I, et al. Mesenchymal stem cell migration and proliferation are mediated by hypoxia-inducible factor-1α upstream of notch and sumo pathways. Stem Cells Dev, 2017, 26(13): 973-985.
36.	Yasen M, Fei Q, Hutton WC, et al. Changes of number of cells expressing proliferation and progenitor cell markers with age in rabbit intervertebral discs. Acta Biochim Biophys Sin (Shanghai), 2013, 45(5): 368-376.
37.	Li XC, Tang Y, Wu JH, et al. Characteristics and potentials of stem cells derived from human degenerated nucleus pulposus: potential for regeneration of the intervertebral disc. BMC Musculoskelet Disord, 2017, 18(1): 242. doi: 10.1186/s12891-017-1567-4.
38.	Tekari A, Chan SCW, Sakai D, et al. Angiopoietin-1 receptor tie2 distinguishes multipotent differentiation capability in bovine coccygeal nucleus pulposus cells. Stem Cell Res Ther, 2016, 7(1): 75. doi: 10.1186/s13287-016-0337-9.
39.	Li XC, Wang MS, Liu W, et al. Co-culturing nucleus pulposus mesenchymal stem cells with notochordal cell-rich nucleus pulposus explants attenuates tumor necrosis factor-α-induced senescence. Stem Cell Res Ther, 2018, 9(1): 171. doi: 10.1186/s13287-018-0919-9.
40.	Jia Z, Yang P, Wu Y, et al. Comparison of biological characteristics of nucleus pulposus mesenchymal stem cells derived from non-degenerative and degenerative human nucleus pulposus. Exp Ther Med, 2017, 13: 3574-3580.
41.	Wang H, Zhou Y, Chu TW, et al. Distinguishing characteristics of stem cells derived from different anatomical regions of human degenerated intervertebral discs. Eur Spine J, 2016, 25(9): 2691-2704.
42.	Liang H, Chen S, Huang D, et al. Effect of compression loading on human nucleus pulposus-derived mesenchymal stem cells. Stem Cells Int, 2018, 2018: 1481243. doi: 10.1155/2018/1481243.
43.	Sakai D, Nakamura Y, Nakai T, et al. Exhaustion of nucleus pulposus progenitor cells with ageing and degeneration of the intervertebral disc. Nat Commun, 2012, 3: 1264. doi: 10.1038/ncomms2226.
44.	Chen S, Deng X, Ma K, et al. Icariin improves the viability and function of cryopreserved human nucleus pulposus-derived mesenchymal stem cells. Oxid Med Cell Longev, 2018, 2018: 3459612. doi: 10.1155/2018/3459612.
45.	Liu S, Liang H, Lee SM, et al. Isolation and identification of stem cells from degenerated human intervertebral discs and their migration characteristics. Acta Biochim Biophys Sin (Shanghai), 2017, 49(2): 101-109.
46.	Erwin WM, Islam D, Eftekarpour E, et al. Intervertebral disc-derived stem cells: Implications for regenerative medicine and neural repair. Spine (Phila Pa 1976), 2013, 38(3): 211-216.
47.	Liu Y, Li Y, Nan L, et al. The effect of high glucose on the biological characteristics of nucleus pulposus-derived mesenchymal stem cells. Cell Biochem Funct, 2020, 38: 130-140.
48.	Li Z, Chen S, Ma K, et al. CsA attenuates compression-induced nucleus pulposus mesenchymal stem cells apoptosis via alleviating mitochondrial dysfunction and oxidative stress. Life Sci, 2018, 205: 26-37.
49.	Huang YC, Leung VY, Lu WW, et al. The effects of microenvironment in mesenchymal stem cell-based regeneration of intervertebral disc. Spine J, 2013, 13(3): 352-362.
50.	Huang YC, Urban JP, Luk KD. Intervertebral disc regeneration: do nutrients lead the way? Nat Rev Rheumatol, 2014, 10(9): 561-566.
51.	Gilbert HTJ, Hodson N, Baird P, et al. Acidic ph promotes intervertebral disc degeneration: Acid-sensing ion channel-3 as a potential therapeutic target. Sci Rep, 2016, 6: 37360. doi: 10.1038/srep37360.
52.	Tao Y, Zhou X, Liang C, et al. TGF-β3 and IGF-1 synergy ameliorates nucleus pulposus mesenchymal stem cell differentiation towards the nucleus pulposus cell type through mapk/erk signaling. Growth Factors, 2015, 33(5-6): 326-336.
53.	Ying JW, Wen TY, Pei SS, et al. Stromal cell-derived factor-1α promotes recruitment and differentiation of nucleus pulposus-derived stem cells. World J Stem Cells, 2019, 11(3): 196-211.
54.	Feng C, Yang M, Lan M, et al. Ros: Crucial intermediators in the pathogenesis of intervertebral disc degeneration. Oxid Med Cell Longev, 2017, 2017: 5601593. doi: 10.1155/2017/5601593.
55.	Nan LP, Wang F, Ran D, et al. Naringin alleviates H₂O₂-induced apoptosis via the PI3K/Akt pathway in rat nucleus pulposus-derived mesenchymal stem cells. Connect Tissue Res, 2020, 61(6): 554-567.
56.	Chen S, Liu S, Zhao L, et al. Heme oxygenase-1-mediated autophagy protects against oxidative damage in rat nucleus pulposus-derived mesenchymal stem cells. Oxid Med Cell Longev, 2020, 2020: 9349762. doi: 10.1155/2020/9349762.
57.	He R, Wang Z, Cui M, et al. HIF1A alleviates compression-induced apoptosis of nucleus pulposus derived stem cells via upregulating autophagy. Autophagy, 2021, 18: 1-23.
58.	Hu B, Zhang S, Liu W, et al. Inhibiting heat shock protein 90 protects nucleus pulposus-derived stem/progenitor cells from compression-induced necroptosis and apoptosis. Front Cell Dev Biol, 2020, 8: 685. doi: 10.3389/fcell.2020.00685.
59.	Chen S, Lv X, Hu B, et al. RIPK1/RIPK3/MLKL-mediated necroptosis contributes to compression-induced rat nucleus pulposus cells death. Apoptosis, 2017, 22(5): 626-638.
60.	Yang F, Leung VY, Luk KD, et al. Mesenchymal stem cells arrest intervertebral disc degeneration through chondrocytic differentiation and stimulation of endogenous cells. Mol Ther, 2009, 17(11): 1959-1966.
61.	Wang F, Nan LP, Zhou SF, et al. Injectable hydrogel combined with nucleus pulposus-derived mesenchymal stem cells for the treatment of degenerative intervertebral disc in rats. Stem Cells Int, 2019, 2019: 8496025. doi: 10.1155/2019/8496025.
62.	Morris TJ, Picken A, Sharp DMC, et al. The effect of Me2SO overexposure during cryopreservation on HOS TE85 and hMSC viability, growth and quality. Cryobiology, 2016, 73(3): 367-375.
63.	Henry N, Clouet J, Le Bideau J, et al. Innovative strategies for intervertebral disc regenerative medicine: From cell therapies to multiscale delivery systems. Biotechnol Adv, 2018, 36(1): 281-294.
64.	Benz K, Stippich C, Fischer L, et al. Intervertebral disc cell- and hydrogel-supported and spontaneous intervertebral disc repair in nucleotomized sheep. Eur Spine J, 2012, 21(9): 1758-1768.
65.	Xu P, Guan J, Chen Y, et al. Stiffness of photocrosslinkable gelatin hydrogel influences nucleus pulposus cell properties in vitro. J Cell Mol Med, 2021, 25(2): 880-891.
66.	Frapin L, Clouet J, Chédeville C, et al. Controlled release of biological factors for endogenous progenitor cell migration and intervertebral disc extracellular matrix remodelling. Biomaterials, 2020, 253: 120107. doi: 10.1016/j.biomaterials.2020.120107.

1. GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet, 2016, 388(10053): 1545-1602.
2. Wu A, Dong W, Liu S, et al. The prevalence and years lived with disability caused by low back pain in China, 1990 to 2016: findings from the global burden of disease study 2016. Pain, 2019, 160(1): 237-245.
3. Makanji H, Schoenfeld AJ, Bhalla A, et al. Critical analysis of trends in lumbar fusion for degenerative disorders revisited: influence of technique on fusion rate and clinical outcomes. Eur Spine J, 2018, 27(8): 1868-1876.
4. 梁秋发, 原林, 王文军, 等. 颈椎前路融合术后临近节段退变的MRI分析. 医学临床研究, 2005, 22(6): 727-729.
5. Sakai D, Andersson GB. Stem cell therapy for intervertebral disc regeneration: obstacles and solutions. Nat Rev Rheumatol, 2015, 11(4): 243-256.
6. Liang C, Li H, Tao Y, et al. Responses of human adipose-derived mesenchymal stem cells to chemical microenvironment of the intervertebral disc. J Transl Med, 2012, 10: 49. doi: 10.1186/1479-5876-10-49.
7. Wang Y, Han ZB, Song YP, et al. Safety of mesenchymal stem cells for clinical application. Stem Cells Int, 2012, 2012: 652034. doi: 10.1155/2012/652034.
8. Vadalà G, Sowa G, Hubert M, et al. Mesenchymal stem cells injection in degenerated intervertebral disc: Cell leakage may induce osteophyte formation. J Tissue Eng Regen Med, 2012, 6(5): 348-355.
9. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 1978, 4(1-2): 7-25.
10. Scadden DT. The stem-cell niche as an entity of action. Nature, 2006, 441(7097): 1075-1079.
11. Ruddy RM, Morshead CM. Home sweet home: the neural stem cell niche throughout development and after injury. Cell Tissue Res, 2018, 371(1): 125-141.
12. Seike M, Omatsu Y, Watanabe H, et al. Stem cell niche-specific Ebf3 maintains the bone marrow cavity. Genes Dev, 2018, 32(5-6): 359-372.
13. Gong M, Zhang P, Li C, et al. Protective mechanism of adipose-derived stem cells in remodelling of the skin stem cell niche during photoaging. Cell Physiol Biochem, 2018, 51(5): 2456-2471.
14. Bartfeld S, Koo BK. Adult gastric stem cells and their niches. Wiley Interdiscip Rev Dev Biol, 2017, 6(2). doi: 10.1002/wdev.261.
15. Shi R, Wang F, Hong X, et al. The presence of stem cells in potential stem cell niches of the intervertebral disc region: an in vitro study on rats. Eur Spine J, 2015, 24(11): 2411-2424.
16. Clouet J, Fusellier M, Camus A, et al. Intervertebral disc regeneration: From cell therapy to the development of novel bioinspired endogenous repair strategies. Adv Drug Deliv Reviews, 2019, 146: 306-324.
17. Risbud MV, Shapiro IM. Role of cytokines in intervertebral disc degeneration: pain and disc content. Nat Rev Rheumatol, 2014, 10(1): 44-56.
18. Blanco JF, Graciani IF, Sanchez-Guijo FM, et al. Isolation and characterization of mesenchymal stromal cells from human degenerated nucleus pulposus: Comparison with bone marrow mesenchymal stromal cells from the same subjects. Spine (Phila Pa 1976), 2010, 35(26): 2259-2265.
19. Tao YQ, Liang CZ, Li H, et al. Potential of co-culture of nucleus pulposus mesenchymal stem cells and nucleus pulposus cells in hyperosmotic microenvironment for intervertebral disc regeneration. Cell Biol Int, 2013, 37: 826-834.
20. Han B, Wang HC, Li H, et al. Nucleus pulposus mesenchymal stem cells in acidic conditions mimicking degenerative intervertebral discs give better performance than adipose tissue-derived mesenchymal stem cells. Cells Tissues Organs, 2014, 199(5-6): 342-352.
21. Liu Y, Li Y, Huang ZN, et al. The effect of intervertebral disc degenerative change on biological characteristics of nucleus pulposus mesenchymal stem cell: an in vitro study in rats. Connect Tissue Res, 2019, 60(4): 376-388.
22. Yu H, Vu TH, Cho KS, et al. Mobilizing endogenous stem cells for retinal repair. Transl Res, 2014, 163(4): 387-398.
23. Lyu FJ, Cheung KM, Zheng Z, et al. IVD progenitor cells: a new horizon for understanding disc homeostasis and repair. Nat Rev Rheumatol, 2019, 15(2): 102-112.
24. Liu LT, Huang B, Li CQ, et al. Characteristics of stem cells derived from the degenerated human intervertebral disc cartilage endplate. PLoS One, 2011, 6(10): e26285. doi: 10.1371/journal.pone.0026285.
25. Liu J, Tao H, Wang H, et al. Biological behavior of human nucleus pulposus mesenchymal stem cells in response to changes in the acidic environment during intervertebral disc degeneration. Stem Cells Dev, 2017, 26(12): 901-911.
26. Wu H, Zeng X, Yu J, et al. Comparison of nucleus pulposus stem/progenitor cells isolated from degenerated intervertebral discs with umbilical cord derived mesenchymal stem cells. Exp Cell Res, 2017, 361(2): 324-332.
27. Li Z, Chen S, Ma K, et al. Comparison of different methods for the isolation and purification of rat nucleus pulposus-derived mesenchymal stem cells. Connect Tissue Res, 2020, 61(5): 426-434.
28. Cheng S, Li X, Jia Z, et al. The inflammatory cytokine TNF-α regulates the biological behavior of rat nucleus pulposus mesenchymal stem cells through the NF-κb signaling pathway in vitro. J Cell Biochem, 2019, 120: 13664-13679.
29. Lin L, Jia Z, Zhao Y, et al. Use of limiting dilution method for isolation of nucleus pulposus mesenchymal stem/progenitor cells and effects of plating density on biological characteristics and plasticity. Biomed Res Int, 2017, 2017: 9765843. doi: 10.1155/2017/9765843.
30. Jia J, Wang SZ, Ma LY, et al. The differential effects of leukocyte-containing and pure platelet-rich plasma on nucleus pulposus-derived mesenchymal stem cells: Implications for the clinical treatment of intervertebral disc degeneration. Stem Cells Int, 2018, 2018: 7162084. doi: 10.1155/2018/7162084.
31. Lazzarini R, Guarnieri S, Fulgenzi G, et al. Mesenchymal stem cells from nucleus pulposus and neural differentiation potential: A continuous challenge. J Mol Neurosci, 2019, 67(1): 111-124.
32. Qi L, Wang R, Shi Q, et al. Umbilical cord mesenchymal stem cell conditioned medium restored the expression of collagen Ⅱ and aggrecan in nucleus pulposus mesenchymal stem cells exposed to high glucose. J Bone Miner Metab, 2019, 37(3): 455-466.
33. Wang KH, Kao AP, Chang CC, et al. Upregulation of Nanog and Sox-2 genes following ectopic expression of Oct-4 in amniotic fluid mesenchymal stem cells. Biotechnol Appl Biochem, 2015, 62(5): 591-597.
34. Zanotti S, Canalis E. Notch signaling and the skeleton. Endocr Rev, 2016, 37(3): 223-253.
35. Ciria M, García NA, Ontoria-Oviedo I, et al. Mesenchymal stem cell migration and proliferation are mediated by hypoxia-inducible factor-1α upstream of notch and sumo pathways. Stem Cells Dev, 2017, 26(13): 973-985.
36. Yasen M, Fei Q, Hutton WC, et al. Changes of number of cells expressing proliferation and progenitor cell markers with age in rabbit intervertebral discs. Acta Biochim Biophys Sin (Shanghai), 2013, 45(5): 368-376.
37. Li XC, Tang Y, Wu JH, et al. Characteristics and potentials of stem cells derived from human degenerated nucleus pulposus: potential for regeneration of the intervertebral disc. BMC Musculoskelet Disord, 2017, 18(1): 242. doi: 10.1186/s12891-017-1567-4.
38. Tekari A, Chan SCW, Sakai D, et al. Angiopoietin-1 receptor tie2 distinguishes multipotent differentiation capability in bovine coccygeal nucleus pulposus cells. Stem Cell Res Ther, 2016, 7(1): 75. doi: 10.1186/s13287-016-0337-9.
39. Li XC, Wang MS, Liu W, et al. Co-culturing nucleus pulposus mesenchymal stem cells with notochordal cell-rich nucleus pulposus explants attenuates tumor necrosis factor-α-induced senescence. Stem Cell Res Ther, 2018, 9(1): 171. doi: 10.1186/s13287-018-0919-9.
40. Jia Z, Yang P, Wu Y, et al. Comparison of biological characteristics of nucleus pulposus mesenchymal stem cells derived from non-degenerative and degenerative human nucleus pulposus. Exp Ther Med, 2017, 13: 3574-3580.
41. Wang H, Zhou Y, Chu TW, et al. Distinguishing characteristics of stem cells derived from different anatomical regions of human degenerated intervertebral discs. Eur Spine J, 2016, 25(9): 2691-2704.
42. Liang H, Chen S, Huang D, et al. Effect of compression loading on human nucleus pulposus-derived mesenchymal stem cells. Stem Cells Int, 2018, 2018: 1481243. doi: 10.1155/2018/1481243.
43. Sakai D, Nakamura Y, Nakai T, et al. Exhaustion of nucleus pulposus progenitor cells with ageing and degeneration of the intervertebral disc. Nat Commun, 2012, 3: 1264. doi: 10.1038/ncomms2226.
44. Chen S, Deng X, Ma K, et al. Icariin improves the viability and function of cryopreserved human nucleus pulposus-derived mesenchymal stem cells. Oxid Med Cell Longev, 2018, 2018: 3459612. doi: 10.1155/2018/3459612.
45. Liu S, Liang H, Lee SM, et al. Isolation and identification of stem cells from degenerated human intervertebral discs and their migration characteristics. Acta Biochim Biophys Sin (Shanghai), 2017, 49(2): 101-109.
46. Erwin WM, Islam D, Eftekarpour E, et al. Intervertebral disc-derived stem cells: Implications for regenerative medicine and neural repair. Spine (Phila Pa 1976), 2013, 38(3): 211-216.
47. Liu Y, Li Y, Nan L, et al. The effect of high glucose on the biological characteristics of nucleus pulposus-derived mesenchymal stem cells. Cell Biochem Funct, 2020, 38: 130-140.
48. Li Z, Chen S, Ma K, et al. CsA attenuates compression-induced nucleus pulposus mesenchymal stem cells apoptosis via alleviating mitochondrial dysfunction and oxidative stress. Life Sci, 2018, 205: 26-37.
49. Huang YC, Leung VY, Lu WW, et al. The effects of microenvironment in mesenchymal stem cell-based regeneration of intervertebral disc. Spine J, 2013, 13(3): 352-362.
50. Huang YC, Urban JP, Luk KD. Intervertebral disc regeneration: do nutrients lead the way? Nat Rev Rheumatol, 2014, 10(9): 561-566.
51. Gilbert HTJ, Hodson N, Baird P, et al. Acidic ph promotes intervertebral disc degeneration: Acid-sensing ion channel-3 as a potential therapeutic target. Sci Rep, 2016, 6: 37360. doi: 10.1038/srep37360.
52. Tao Y, Zhou X, Liang C, et al. TGF-β3 and IGF-1 synergy ameliorates nucleus pulposus mesenchymal stem cell differentiation towards the nucleus pulposus cell type through mapk/erk signaling. Growth Factors, 2015, 33(5-6): 326-336.
53. Ying JW, Wen TY, Pei SS, et al. Stromal cell-derived factor-1α promotes recruitment and differentiation of nucleus pulposus-derived stem cells. World J Stem Cells, 2019, 11(3): 196-211.
54. Feng C, Yang M, Lan M, et al. Ros: Crucial intermediators in the pathogenesis of intervertebral disc degeneration. Oxid Med Cell Longev, 2017, 2017: 5601593. doi: 10.1155/2017/5601593.
55. Nan LP, Wang F, Ran D, et al. Naringin alleviates H₂O₂-induced apoptosis via the PI3K/Akt pathway in rat nucleus pulposus-derived mesenchymal stem cells. Connect Tissue Res, 2020, 61(6): 554-567.
56. Chen S, Liu S, Zhao L, et al. Heme oxygenase-1-mediated autophagy protects against oxidative damage in rat nucleus pulposus-derived mesenchymal stem cells. Oxid Med Cell Longev, 2020, 2020: 9349762. doi: 10.1155/2020/9349762.
57. He R, Wang Z, Cui M, et al. HIF1A alleviates compression-induced apoptosis of nucleus pulposus derived stem cells via upregulating autophagy. Autophagy, 2021, 18: 1-23.
58. Hu B, Zhang S, Liu W, et al. Inhibiting heat shock protein 90 protects nucleus pulposus-derived stem/progenitor cells from compression-induced necroptosis and apoptosis. Front Cell Dev Biol, 2020, 8: 685. doi: 10.3389/fcell.2020.00685.
59. Chen S, Lv X, Hu B, et al. RIPK1/RIPK3/MLKL-mediated necroptosis contributes to compression-induced rat nucleus pulposus cells death. Apoptosis, 2017, 22(5): 626-638.
60. Yang F, Leung VY, Luk KD, et al. Mesenchymal stem cells arrest intervertebral disc degeneration through chondrocytic differentiation and stimulation of endogenous cells. Mol Ther, 2009, 17(11): 1959-1966.
61. Wang F, Nan LP, Zhou SF, et al. Injectable hydrogel combined with nucleus pulposus-derived mesenchymal stem cells for the treatment of degenerative intervertebral disc in rats. Stem Cells Int, 2019, 2019: 8496025. doi: 10.1155/2019/8496025.
62. Morris TJ, Picken A, Sharp DMC, et al. The effect of Me2SO overexposure during cryopreservation on HOS TE85 and hMSC viability, growth and quality. Cryobiology, 2016, 73(3): 367-375.
63. Henry N, Clouet J, Le Bideau J, et al. Innovative strategies for intervertebral disc regenerative medicine: From cell therapies to multiscale delivery systems. Biotechnol Adv, 2018, 36(1): 281-294.
64. Benz K, Stippich C, Fischer L, et al. Intervertebral disc cell- and hydrogel-supported and spontaneous intervertebral disc repair in nucleotomized sheep. Eur Spine J, 2012, 21(9): 1758-1768.
65. Xu P, Guan J, Chen Y, et al. Stiffness of photocrosslinkable gelatin hydrogel influences nucleus pulposus cell properties in vitro. J Cell Mol Med, 2021, 25(2): 880-891.
66. Frapin L, Clouet J, Chédeville C, et al. Controlled release of biological factors for endogenous progenitor cell migration and intervertebral disc extracellular matrix remodelling. Biomaterials, 2020, 253: 120107. doi: 10.1016/j.biomaterials.2020.120107.

Previous Article
Research progress of in vivo bioreactor for bone tissue engineering
Next Article
Research progress of intramedullary lengthening nail technology

Chinese Journal of Reparative and Reconstructive Surgery

Research progress of endogenous repair strategy in intervertebral disc

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content