RESEARCH SITUATION OF STEM CELLS TRANSPLANTATION FOR INTERVERTEBRAL DISC DEGENERATION_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

WANG Feng , WU Xiaotao , WANG Yuntao , BAO Junping.

Department of Orthopaedics, Affiliated Zhongda Hospital of Southeast University, Nanjing Jiangsu, 210009, P.R.China. Corresponding author: WU Xiaotao, E-mail: wuxiaotao@medmail.com.cn;

Corresponding author：

Keywords：

Stem cells; Intervertebral disc degeneration; Cell transplantation

DOI：

10.7507/1002-1892.20130127

Video：

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Objective To summarize the research situation of stem cells transplantation for intervertebral disc (IVD) degeneration. Methods The original articles about stem cells transplantation for repair of IVD degeneration were extensively reviewed; the clinical applications, the mechanisms, and related factors to influence repair effect were analyzed; and obstacles in stem cells transplantation for repair of IVD degeneration. Results Autogenic stem cells transplantation can repair IVD degeneration and effectively relieve the symptoms of low back and leg pain. Stem cells can differentiate into disc chondrocytes in the disc microenvironment, increase the production of various growth factors, and exert a trophic effect on disc cells. It is also evident that the transplanted stem cells can potentially protect disc cells from apoptosis and maintain an immune-privileged state in the IVD. Multiple factors such as tissue origin of stem cells, methods to pre-modulate the seeds, choice of injectable scaffolds, and even the severity of degeneration are closely related to the repair effects. To get a more efficient stem cell therapy, future researches are challenged to modulate the migration and distribution of stem cells in the IVD, avoid flow back, and better understand their ability to restore stemness properties within the degenerative disc niche. Conclusion Stem cells transplantation is proven to be a promising biological approach for repair of IVD degeneration.

Citation： WANG Feng,WU Xiaotao,WANG Yuntao,BAO Junping.. RESEARCH SITUATION OF STEM CELLS TRANSPLANTATION FOR INTERVERTEBRAL DISC DEGENERATION. Chinese Journal of Reparative and Reconstructive Surgery, 2013, 27(5): 575-579. doi: 10.7507/1002-1892.20130127 Copy

1.	Dagenais S, Caro J, Haldeman S. A systematic review of low back pain cost of illness studies in the United States and internationally. Spine J, 2008, 8(1): 8-20.
2.	王锋, 王运涛, 吴小涛. 髓核细胞修复椎间盘退行性变的研究进展. 中国修复重建外科杂志, 2009, 23(7): 864-867.
3.	Wang F, Wu XT, Zhuang SY, et al. Ex vivo observation of human nucleus pulposus chondrocytes isolated from degenerated intervertebral discs. Asian Spine J, 2011, 5(2): 73-81.
4.	Sakai D, Mochida J, Yamamoto Y, et al. Transplantation of mesenchymal stem cells embedded in Atelocollagen gel to the intervertebral disc: a potential therapeutic model for disc degeneration. Biomaterials, 2003, 24(20): 3531-3541.
5.	Wang YT, Wu XT, Wang F. Regeneration potential and mechanism of bone marrow mesenchymal stem cell transplantation for treating intervertebral disc degeneration. J Orthop Sci, 2010, 15(6): 707-719.
6.	Haufe SM, Mork AR. Intradiscal injection of hematopoietic stem cells in an attempt to rejuvenate the intervertebral discs. Stem Cells Dev, 2006, 15(1): 136-137.
7.	Yoshikawa T, Ueda Y, Miyazaki K, et al. Disc regeneration therapy using marrow mesenchymal cell transplantation: a report of two case studies. Spine (Phila Pa 1976), 2010, 35(11): E475-480.
8.	Orozco L, Soler R, Morera C, et al. Intervertebral disc repair by autologous mesenchymal bone marrow cells: a pilot study. Transplantation, 2011, 92(7): 822-828.
9.	Huang S, Tam V, Cheung KM, et al. Stem cell-based approaches for intervertebral disc regeneration. Curr Stem Cell Res Ther, 2011, 6(4): 317-326.
10.	严慧深, 吴小涛, 王运涛, 等. 骨髓间充质干细胞修复退变椎间盘中营养和分化效应的变化. 中华实验外科杂志, 2009, 26(6): 704-706.
11.	Wei A, Tao H, Chung SA, et al. The fate of transplanted xenogeneic bone marrow-derived stem cells in rat intervertebral discs. J Orthop Res, 2009, 27(3): 374-379.
12.	Henriksson HB, Svanvik T, Jonsson M, et al. Transplantation of human mesenchymal stems cells into intervertebral discs in a xenogeneic porcine model. Spine (Phila Pa 1976), 2009, 34(2): 141-148.
13.	Zhang Y, Drapeau S, Howard SA, et al. Transplantation of goat bone marrow stromal cells to the degenerating intervertebral disc in a goat disc injury model. Spine (Phila Pa 1976), 2011, 36(5): 372-377.
14.	Serigano K, Sakai D, Hiyama A, et al. Effect of cell number on mesenchymal stem cell transplantation in a canine disc degeneration model. J Orthop Res, 2010, 28(10): 1267-1275.
15.	Richardson SM, Walker RV, Parker S, et al. Intervertebral disc cell-mediated mesenchymal stem cell differentiation. Stem Cells, 2006, 24(3): 707-716.
16.	Yang SH, Wu CC, Shih TT, et al. In vitro study on interaction between human nucleus pulposus cells and mesenchymal stem cells through paracrine stimulation. Spine (Phila Pa 1976), 2008, 33(18): 1951-1957.
17.	Zhao CQ, Jiang LS, Dai LY. Programmed cell death in intervertebral disc degeneration. Apoptosis, 2006, 11(12): 2079-2088.
18.	Hiyama A, Mochida J, Iwashina T, et al. Transplantation of mesenchymal stem cells in a canine disc degeneration model. J Orthop Res, 2008, 26(5): 589-600.
19.	樊守刚, 吴小涛, 王运涛, 等. 移植骨髓间充质干细胞对兔退变椎间盘髓核细胞凋亡的影响. 中华实验外科杂志, 2010, 27(7): 979-982.
20.	王锋, 吴小涛, 王运涛, 等. 非接触共培养条件下人BMSCs 对氧化应激环境中退变髓核细胞凋亡的保护研究. 中国修复重建外科杂志, 2010, 24(4): 391-398.
21.	Gruber HE, Norton HJ, Hanley EN Jr. Anti-apoptotic effects of IGF-1 and PDGF on human intervertebral disc cells in vitro. Spine (Phila Pa 1976), 2000, 25(17): 2153-2157.
22.	Wei A, Brisby H, Chung SA, et al. Bone morphogenetic protein-7 protects human intervertebral disc cells in vitro from apoptosis. Spine J, 2008, 8(3): 466-474.
23.	Lwin T, Hazlehurst LA, Li Z, et al. Bone marrow stromal cells prevent apoptosis of lymphoma cells by upregulation of anti-apoptotic proteins associated with activation of NF-kappaB (RelB/p52) in non-Hodgkin’s lymphoma cells. Leukemia, 2007, 21(7): 1521-1531.
24.	Park JB, Lee JK, Park EY, et al. Fas/FasL interaction of nucleus pulposus and cancer cells with the activation of caspases. Int Orthop, 2008, 32(6): 835-840.
25.	Peng B, Hao J, Hou S, et al. Possible pathogenesis of painful intervertebral disc degeneration. Spine (Phila Pa 1976), 2006, 31(5): 560-566.
26.	Kaneyama S, Nishida K, Takada T, et al. Fas ligand expression on human nucleus pulposus cells decreases with disc degeneration processes. J Orthop Sci, 2008, 13(2): 130-135.
27.	Bertolo A, Thiede T, Aebli N, et al. Human mesenchymal stem cell co-culture modulates the immunological properties of human intervertebral disc tissue fragments in vitro. Eur Spine J, 2011, 20(4): 592-603.
28.	Kuhn NZ, Tuan RS. Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis. J Cell Physiol, 2010, 222(2): 268-277.
29.	Ganey T, Hutton WC, Moseley T, et al. Intervertebral disc repair using adipose tissue-derived stem and regenerative cells: experiments in a canine model. Spine (Phila Pa 1976), 2009, 34(21): 2297-2304.
30.	Vadalà G, Sobajima S, Lee JY, et al. In vitro interaction between muscle-derived stem cells and nucleus pulposus cells. Spine J, 2008, 8(5): 804-809.
31.	Miyamoto T, Muneta T, Tabuchi T, et al. Intradiscal transplantation of synovial mesenchymal stem cells prevents intervertebral disc degeneration through suppression of matrix metalloproteinase-related genes in nucleus pulposus cells in rabbits. Arthritis Res Ther, 2010, 12(6): R206.
32.	Murrell W, Sanford E, Anderberg L, et al. Olfactory stem cells can be induced to express chondrogenic phenotype in a rat intervertebral disc injury model. Spine J, 2009, 9(7): 585-594.
33.	Ruan D, Zhang Y, Wang D, et al. Differentiation of human Wharton’s jelly cells toward nucleus pulposus-like cells after coculture with nucleus pulposus cells in vitro. Tissue Eng Part A, 2012, 18(1-2): 167-175.
34.	Puetzer JL, Petitte JN, Loboa EG. Comparative review of growth factors for induction of three-dimensional in vitro chondrogenesis in human mesenchymal stem cells isolated from bone marrow and adipose tissue. Tissue Eng Part B Rev, 2010, 16(4): 435-444.
35.	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.
36.	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.
37.	Nerurkar NL, Elliott DM, Mauck RL. Mechanical design criteria for intervertebral disc tissue engineering. J Biomech, 2010, 43(6): 1017-1030.
38.	鲍军平, 吴小涛, 王运涛, 等. 干细胞移植延缓椎间盘退变及磁共振示踪研究. 东南大学学报: 医学版, 2008, 27 (3): 166-170.
39.	Sobajima S, Vadala G, Shimer A, et al. Feasibility of a stem cell therapy for intervertebral disc degeneration. Spine J, 2008, 8(6): 888-896.
40.	Illien-Jünger S, Pattappa G, Peroglio M, et al. Homing of mesenchymal stem cells in induced degenerative intervertebral discs in a whole organ culture system. Spine (Phila Pa 1976), 2012, 37(22): 1865-1873.
41.	孟晨, 吴小涛. SDF-1/CXCR4信号轴在调节干细胞迁移及发育中的作用. 东南大学学报: 医学版, 2011, 30(4): 625-629.
42.	Feng G, Jin X, Hu J, et al. Effects of hypoxias and scaffold architecture on rabbit mesenchymal stem cell differentiation towards a nucleus pulposus-like phenotype. Biomaterials, 2011, 32(32): 8182-8189.
43.	Markway BD, Tan GK, Brooke G, et al. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant, 2010, 19(1): 29-42.
44.	Thorpe SD, Buckley CT, Vinardell T, et al. The response of bone marrow-derived mesenchymal stem cells to dynamic compression following TGF-beta3 induced chondrogenic differentiation. Ann Biomed Eng, 2010, 38(9): 2896-2909.
45.	Sheikh H, Zakharian K, De La Torre RP, et al. In vivo intervertebral disc regeneration using stem cell-derived chondroprogenitors. J Neurosurg Spine, 2009, 10(3): 265-272.
46.	Roberts S, Johnson WE. Analysis of aging and degeneration of the human intervertebral disc. Spine (Phila Pa 1976), 1999, 24(5): 500-501.
47.	Acosta FL Jr, Metz L, Adkisson HD, et al. Porcine intervertebral disc repair using allogeneic juvenile articular chondrocytes or mesenchymal stem cells. Tissue Eng Part A, 2011, 17(23-24): 3045-3055.
48.	Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 2006, 8(4): 315-317.
49.	邵建树, 吴小涛, 王运涛, 等. 兔骨髓间充质干细胞与髓核细胞共培养后的营养效应和类髓核分化效应. 中国脊柱脊髓杂志, 2009, 19(5): 381-387.
50.	Risbud MV, Guttapalli A, Tsai TT, et al. Evidence for skeletal progenitor cells in the degenerate human intervertebral disc. Spine (Phila Pa 1976), 32(23): 537-2544.
51.	Henriksson H, Thornemo M, Karlsson C, et al. Identification of cell proliferation zones, progenitor cells and a potential stem cell niche in the intervertebral disc region: a study in four species. Spine (Phila Pa 1976), 2009, 34(21): 2278-2287.
52.	Henriksson HB, Svala E, Skioldebrand E, et al. Support of concept that migrating progenitor cells from stem cell niches contribute to normal regeneration of the adult mammal intervertebral disc: a descriptive study in the New Zealand white rabbit. Spine (Phila Pa 1976), 2012, 37(9): 722-732.
53.	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.
54.	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.
55.	Bendtsen M, Bünger CE, Zou X, et al. Autologous stem cell therapy maintains vertebral blood flow and contrast diffusion through the endplate in experimental intervertebral disc degeneration. Spine (Phila Pa 1976), 2011, 36(6): E373-E379.
56.	Ho G, Leung VY, Cheung KM, et al. Effect of severity of intervertebral disc injury on mesenchymal stem cell-based regeneration. Connect Tissue Res, 2008, 49(1): 15-21.

1. Dagenais S, Caro J, Haldeman S. A systematic review of low back pain cost of illness studies in the United States and internationally. Spine J, 2008, 8(1): 8-20.
2. 王锋, 王运涛, 吴小涛. 髓核细胞修复椎间盘退行性变的研究进展. 中国修复重建外科杂志, 2009, 23(7): 864-867.
3. Wang F, Wu XT, Zhuang SY, et al. Ex vivo observation of human nucleus pulposus chondrocytes isolated from degenerated intervertebral discs. Asian Spine J, 2011, 5(2): 73-81.
4. Sakai D, Mochida J, Yamamoto Y, et al. Transplantation of mesenchymal stem cells embedded in Atelocollagen gel to the intervertebral disc: a potential therapeutic model for disc degeneration. Biomaterials, 2003, 24(20): 3531-3541.
5. Wang YT, Wu XT, Wang F. Regeneration potential and mechanism of bone marrow mesenchymal stem cell transplantation for treating intervertebral disc degeneration. J Orthop Sci, 2010, 15(6): 707-719.
6. Haufe SM, Mork AR. Intradiscal injection of hematopoietic stem cells in an attempt to rejuvenate the intervertebral discs. Stem Cells Dev, 2006, 15(1): 136-137.
7. Yoshikawa T, Ueda Y, Miyazaki K, et al. Disc regeneration therapy using marrow mesenchymal cell transplantation: a report of two case studies. Spine (Phila Pa 1976), 2010, 35(11): E475-480.
8. Orozco L, Soler R, Morera C, et al. Intervertebral disc repair by autologous mesenchymal bone marrow cells: a pilot study. Transplantation, 2011, 92(7): 822-828.
9. Huang S, Tam V, Cheung KM, et al. Stem cell-based approaches for intervertebral disc regeneration. Curr Stem Cell Res Ther, 2011, 6(4): 317-326.
10. 严慧深, 吴小涛, 王运涛, 等. 骨髓间充质干细胞修复退变椎间盘中营养和分化效应的变化. 中华实验外科杂志, 2009, 26(6): 704-706.
11. Wei A, Tao H, Chung SA, et al. The fate of transplanted xenogeneic bone marrow-derived stem cells in rat intervertebral discs. J Orthop Res, 2009, 27(3): 374-379.
12. Henriksson HB, Svanvik T, Jonsson M, et al. Transplantation of human mesenchymal stems cells into intervertebral discs in a xenogeneic porcine model. Spine (Phila Pa 1976), 2009, 34(2): 141-148.
13. Zhang Y, Drapeau S, Howard SA, et al. Transplantation of goat bone marrow stromal cells to the degenerating intervertebral disc in a goat disc injury model. Spine (Phila Pa 1976), 2011, 36(5): 372-377.
14. Serigano K, Sakai D, Hiyama A, et al. Effect of cell number on mesenchymal stem cell transplantation in a canine disc degeneration model. J Orthop Res, 2010, 28(10): 1267-1275.
15. Richardson SM, Walker RV, Parker S, et al. Intervertebral disc cell-mediated mesenchymal stem cell differentiation. Stem Cells, 2006, 24(3): 707-716.
16. Yang SH, Wu CC, Shih TT, et al. In vitro study on interaction between human nucleus pulposus cells and mesenchymal stem cells through paracrine stimulation. Spine (Phila Pa 1976), 2008, 33(18): 1951-1957.
17. Zhao CQ, Jiang LS, Dai LY. Programmed cell death in intervertebral disc degeneration. Apoptosis, 2006, 11(12): 2079-2088.
18. Hiyama A, Mochida J, Iwashina T, et al. Transplantation of mesenchymal stem cells in a canine disc degeneration model. J Orthop Res, 2008, 26(5): 589-600.
19. 樊守刚, 吴小涛, 王运涛, 等. 移植骨髓间充质干细胞对兔退变椎间盘髓核细胞凋亡的影响. 中华实验外科杂志, 2010, 27(7): 979-982.
20. 王锋, 吴小涛, 王运涛, 等. 非接触共培养条件下人BMSCs 对氧化应激环境中退变髓核细胞凋亡的保护研究. 中国修复重建外科杂志, 2010, 24(4): 391-398.
21. Gruber HE, Norton HJ, Hanley EN Jr. Anti-apoptotic effects of IGF-1 and PDGF on human intervertebral disc cells in vitro. Spine (Phila Pa 1976), 2000, 25(17): 2153-2157.
22. Wei A, Brisby H, Chung SA, et al. Bone morphogenetic protein-7 protects human intervertebral disc cells in vitro from apoptosis. Spine J, 2008, 8(3): 466-474.
23. Lwin T, Hazlehurst LA, Li Z, et al. Bone marrow stromal cells prevent apoptosis of lymphoma cells by upregulation of anti-apoptotic proteins associated with activation of NF-kappaB (RelB/p52) in non-Hodgkin’s lymphoma cells. Leukemia, 2007, 21(7): 1521-1531.
24. Park JB, Lee JK, Park EY, et al. Fas/FasL interaction of nucleus pulposus and cancer cells with the activation of caspases. Int Orthop, 2008, 32(6): 835-840.
25. Peng B, Hao J, Hou S, et al. Possible pathogenesis of painful intervertebral disc degeneration. Spine (Phila Pa 1976), 2006, 31(5): 560-566.
26. Kaneyama S, Nishida K, Takada T, et al. Fas ligand expression on human nucleus pulposus cells decreases with disc degeneration processes. J Orthop Sci, 2008, 13(2): 130-135.
27. Bertolo A, Thiede T, Aebli N, et al. Human mesenchymal stem cell co-culture modulates the immunological properties of human intervertebral disc tissue fragments in vitro. Eur Spine J, 2011, 20(4): 592-603.
28. Kuhn NZ, Tuan RS. Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis. J Cell Physiol, 2010, 222(2): 268-277.
29. Ganey T, Hutton WC, Moseley T, et al. Intervertebral disc repair using adipose tissue-derived stem and regenerative cells: experiments in a canine model. Spine (Phila Pa 1976), 2009, 34(21): 2297-2304.
30. Vadalà G, Sobajima S, Lee JY, et al. In vitro interaction between muscle-derived stem cells and nucleus pulposus cells. Spine J, 2008, 8(5): 804-809.
31. Miyamoto T, Muneta T, Tabuchi T, et al. Intradiscal transplantation of synovial mesenchymal stem cells prevents intervertebral disc degeneration through suppression of matrix metalloproteinase-related genes in nucleus pulposus cells in rabbits. Arthritis Res Ther, 2010, 12(6): R206.
32. Murrell W, Sanford E, Anderberg L, et al. Olfactory stem cells can be induced to express chondrogenic phenotype in a rat intervertebral disc injury model. Spine J, 2009, 9(7): 585-594.
33. Ruan D, Zhang Y, Wang D, et al. Differentiation of human Wharton’s jelly cells toward nucleus pulposus-like cells after coculture with nucleus pulposus cells in vitro. Tissue Eng Part A, 2012, 18(1-2): 167-175.
34. Puetzer JL, Petitte JN, Loboa EG. Comparative review of growth factors for induction of three-dimensional in vitro chondrogenesis in human mesenchymal stem cells isolated from bone marrow and adipose tissue. Tissue Eng Part B Rev, 2010, 16(4): 435-444.
35. 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.
36. 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.
37. Nerurkar NL, Elliott DM, Mauck RL. Mechanical design criteria for intervertebral disc tissue engineering. J Biomech, 2010, 43(6): 1017-1030.
38. 鲍军平, 吴小涛, 王运涛, 等. 干细胞移植延缓椎间盘退变及磁共振示踪研究. 东南大学学报: 医学版, 2008, 27 (3): 166-170.
39. Sobajima S, Vadala G, Shimer A, et al. Feasibility of a stem cell therapy for intervertebral disc degeneration. Spine J, 2008, 8(6): 888-896.
40. Illien-Jünger S, Pattappa G, Peroglio M, et al. Homing of mesenchymal stem cells in induced degenerative intervertebral discs in a whole organ culture system. Spine (Phila Pa 1976), 2012, 37(22): 1865-1873.
41. 孟晨, 吴小涛. SDF-1/CXCR4信号轴在调节干细胞迁移及发育中的作用. 东南大学学报: 医学版, 2011, 30(4): 625-629.
42. Feng G, Jin X, Hu J, et al. Effects of hypoxias and scaffold architecture on rabbit mesenchymal stem cell differentiation towards a nucleus pulposus-like phenotype. Biomaterials, 2011, 32(32): 8182-8189.
43. Markway BD, Tan GK, Brooke G, et al. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant, 2010, 19(1): 29-42.
44. Thorpe SD, Buckley CT, Vinardell T, et al. The response of bone marrow-derived mesenchymal stem cells to dynamic compression following TGF-beta3 induced chondrogenic differentiation. Ann Biomed Eng, 2010, 38(9): 2896-2909.
45. Sheikh H, Zakharian K, De La Torre RP, et al. In vivo intervertebral disc regeneration using stem cell-derived chondroprogenitors. J Neurosurg Spine, 2009, 10(3): 265-272.
46. Roberts S, Johnson WE. Analysis of aging and degeneration of the human intervertebral disc. Spine (Phila Pa 1976), 1999, 24(5): 500-501.
47. Acosta FL Jr, Metz L, Adkisson HD, et al. Porcine intervertebral disc repair using allogeneic juvenile articular chondrocytes or mesenchymal stem cells. Tissue Eng Part A, 2011, 17(23-24): 3045-3055.
48. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 2006, 8(4): 315-317.
49. 邵建树, 吴小涛, 王运涛, 等. 兔骨髓间充质干细胞与髓核细胞共培养后的营养效应和类髓核分化效应. 中国脊柱脊髓杂志, 2009, 19(5): 381-387.
50. Risbud MV, Guttapalli A, Tsai TT, et al. Evidence for skeletal progenitor cells in the degenerate human intervertebral disc. Spine (Phila Pa 1976), 32(23): 537-2544.
51. Henriksson H, Thornemo M, Karlsson C, et al. Identification of cell proliferation zones, progenitor cells and a potential stem cell niche in the intervertebral disc region: a study in four species. Spine (Phila Pa 1976), 2009, 34(21): 2278-2287.
52. Henriksson HB, Svala E, Skioldebrand E, et al. Support of concept that migrating progenitor cells from stem cell niches contribute to normal regeneration of the adult mammal intervertebral disc: a descriptive study in the New Zealand white rabbit. Spine (Phila Pa 1976), 2012, 37(9): 722-732.
53. 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.
54. 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.
55. Bendtsen M, Bünger CE, Zou X, et al. Autologous stem cell therapy maintains vertebral blood flow and contrast diffusion through the endplate in experimental intervertebral disc degeneration. Spine (Phila Pa 1976), 2011, 36(6): E373-E379.
56. Ho G, Leung VY, Cheung KM, et al. Effect of severity of intervertebral disc injury on mesenchymal stem cell-based regeneration. Connect Tissue Res, 2008, 49(1): 15-21.

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