Influence of hypoxia in the intervertebral disc on the biological behaviors of rat adipose-and nucleus pulposus-derived mesenchymal stem cells

Cells Tissues Organs

Volumn 198, Issue 4, 2014, Pages 266-277

  Li, Hao ^a   Tao, Yiqing ^a   Liang, Chengzhen ^a   Han, Bin ^a   Li, Fangcai ^a   Chen, Gang ^a   Chen, Qixin ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Adipose derived mesenchymal stem cells; Disc degeneration; Hypoxia; Intervertebral disc; Nucleus pulposus derived mesenchymal stem cells

Indexed keywords

AGGRECAN; COLLAGEN TYPE 2; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIPOCORTIN 5; MESSENGER RNA; PROPIDIUM IODIDE; TRANSCRIPTION FACTOR SOX9; VASCULOTROPIN A; FLUORESCEIN ISOTHIOCYANATE;

ADIPOSE DERIVED MESENCHYMAL STEM CELL; ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL PROLIFERATION; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; HYPOXIA; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MTT ASSAY; NONHUMAN; NUCLEUS PULPOSUS; NUCLEUS PULPOSUS DERIVED MESENCHYMAL STEM CELL; PRIORITY JOURNAL; PROPIDIUM IODIDE ASSAY; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ADIPOSE TISSUE; ANIMAL; CELL CULTURE; CELL GROWTH; CELL HYPOXIA; CYTOLOGY; INTERVERTEBRAL DISK; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSPLANTATION; ANIMAL EXPERIMENT; BIOLOGICAL ACTIVITY; CELL THERAPY; INVESTIGATIVE PROCEDURES; QUANTITATIVE STUDY;

RATTUS;

ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELL HYPOXIA; CELLS, CULTURED; INTERVERTEBRAL DISC; MALE; MESENCHYMAL STROMAL CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84896729962     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000356505     Document Type: Article

References (40)

1. Agrawal, A., S. Gajghate, H. Smith, D.G. Anderson, T.J. Albert, I.M. Shapiro, M.V. Risbud (2008) Cited2 modulates hypoxia-inducible factor-dependent expression of vascular endothelial growth factor in nucleus pulposus cells of the rat intervertebral disc. Arthritis Rheum 58: 3798-3808.
2. Alini, M., P.J. Roughley, J. Antoniou, T. Stoll, M. Aebi (2002) A biological approach to treating disc degeneration: not for today, but maybe for tomorrow. Eur Spine J 11: S215-S220. (Pubitemid 35244957)
3. Balague, F., A.F. Mannion, F. Pellise, C. Cedraschi (2012) Non-specific low back pain. Lancet 379: 482-491.
4. Blanco, J.F., I.F. Graciani, F.M. Sanchez-Guijo, S. Muntion, P. Hernandez-Campo, C. Santamaria, S. Carrancio, M.V. Barbado, G. Cruz, S. Gutierrez-Cosio, C. Herrero, J.F. San Miguel, J.G. Brinon, M.C. del Canizo (2010) 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) 35: 2259-2265.
5. Choi, E.H., H. Park, K.S. Park, B.S. Kim, I.B. Han, D.A. Shin, S.H. Lee (2011) Effect of nucleus pulposus cells having different phenotypes on chondrogenic differentiation of adipose-derived stromal cells in a coculture system using porous membranes. Tissue Eng Part A 17: 2445-2451.
6. Chun, H.J., Y.S. Kim, B.K. Kim, E.H. Kim, J.H. Kim, B.R. Do, S.J. Hwang, J.Y. Hwang, Y.K. Lee (2012) Transplantation of human adipose-derived stem cells in a rabbit model of traumatic degeneration of lumbar discs. World Neurosurg 78: 364-371.
7. Ciapetti, G., D. Granchi, V. Devescovi, E. Leonardi, T. Greggi, M. Di Silvestre, N. Baldini (2012) Ex vivo observation of human intervertebral disc tissue and cells isolated from degenerated intervertebral discs. Eur Spine J 21: S10-S19.
8. Felka, T., R. Schafer, B. Schewe, K. Benz, W.K. Aicher (2009) Hypoxia reduces the inhibitory effect of IL-1beta on chondrogenic differentiation of FCS-free expanded MSC. Osteoarthritis Cartilage 17: 1368-1376.
9. Fujita, N., J. Imai, T. Suzuki, M. Yamada, K. Ninomiya, K. Miyamoto, R. Iwasaki, H. Morioka, M. Matsumoto, K. Chiba, S. Watanabe, T. Suda, Y. Toyama, T. Miyamoto (2008) Vascular endothelial growth factor-A is a survival factor for nucleus pulposus cells in the intervertebral disc. Biochem Biophys Res Commun 372: 367-372.
10. Galbusera, F., A. Mietsch, H. Schmidt, H.J. Wilke, C. Neidlinger-Wilke (2013) Effect of intervertebral disc degeneration on disc cell viability: a numerical investigation. Comput Methods Biomech Biomed Engin 16: 328-337.
11. Ganey, T., W.C. Hutton, T. Moseley, M. Hedrick, H.J. Meisel (2009) Intervertebral disc repair using adipose tissue-derived stem and regenerative cells: experiments in a canine model. Spine (Phila Pa 1976) 34: 2297-2304.
12. Gerber, H.P., A.K. Malik, G.P. Solar, D. Sherman, X.H. Liang, G. Meng, K. Hong, J.C. Marsters, N. Ferrara (2002) VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 417: 954-958. (Pubitemid 34716872)
13. Henriksson, H.B., H. Brisby (2013) Development and regeneration potential of the mammalian intervertebral disc. Cells Tissues Organs 197: 1-13.
14. Hu, J., K. Feng, X. Liu, P.X. Ma (2009) Chondrogenic and osteogenic differentiations of human bone marrow-derived mesenchymal stem cells on a nanofibrous scaffold with designed pore network. Biomaterials 30: 5061-5067.
15. Joost, H.G., G.I. Bell, J.D. Best, M.J. Birnbaum, M.J. Charron, Y.T. Chen, H. Doege, D.E. James, H.F. Lodish, K.H. Moley, J.F. Moley, M. Mueckler, S. Rogers, A. Schurmann, S. Seino, B. Thorens (2002) Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am J Physiol Endocrinol Metab 282: E974-E976. (Pubitemid 34654762)
16. Le Maitre, C.L., P. Baird, A.J. Freemont, J.A. Hoyland (2009) An in vitro study investigating the survival and phenotype of mesenchymal stem cells following injection into nucleus pulposus tissue. Arthritis Res Ther 11: R20.
17. Le Maitre, C.L., A. Pockert, D.J. Buttle, A.J. Freemont, J.A. Hoyland (2007) Matrix synthesis and degradation in human intervertebral disc degeneration. Biochem Soc Trans 35: 652-655. (Pubitemid 47310333)
18. Li, Y., S.R. Tew, A.M. Russell, K.R. Gonzalez, T.E. Hardingham, R.E. Hawkins (2004) Transduction of passaged human articular chondrocytes with adenoviral, retroviral, and lentiviral vectors and the effects of enhanced expression of SOX9. Tissue Eng 10: 575-584. (Pubitemid 38580278)
19. Liu, L.T., B. Huang, C.Q. Li, Y. Zhuang, J. Wang, Y. Zhou (2011) Characteristics of stem cells derived from the degenerated human intervertebral disc cartilage endplate. PLoS One 6: e26285.
20. Lu, Z.F., B.Z. Doulabi, P.I. Wuisman, R.A. Bank, M.N. Helder (2008) Influence of collagen type II and nucleus pulposus cells on aggregation and differentiation of adipose tissue-derived stem cells. J Cell Mol Med 12: 2812-2822.
21. Malladi, P., Y. Xu, M. Chiou, A.J. Giaccia, M.T. Longaker (2006) Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol 290: C1139-C1146.
22. Mark Erwin, W., D. Islam, E. Eftekarpour, R.D. Inman, M.Z. Karim, M.G. Fehlings (2013) Intervertebral disc-derived stem cells: implications for regenerative medicine and neural repair. Spine (Phila Pa 1976) 38: 211-216.
23. Moore, K.A., I.R. Lemischka (2006) Stem cells and their niches. Science 311: 1880-1885.
24. Mwale, F., I. Ciobanu, D. Giannitsios, P. Roughley, T. Steffen, J. Antoniou (2011) Effect of oxygen levels on proteoglycan synthesis by intervertebral disc cells. Spine (Phila Pa 1976) 36: E131-E138.
25. Risbud, M.V., T.J. Albert, A. Guttapalli, E.J. Vresilovic, A.S. Hillibrand, A.R. Vaccaro, I.M. Shapiro (2004) Differentiation of mesenchymal stem cells towards a nucleus pulposuslike phenotype in vitro: implications for cellbased transplantation therapy. Spine (Phila Pa 1976) 29: 2627-2632. (Pubitemid 40353248)
26. Roughley, P.J. (2004) Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine (Phila Pa 1976) 29: 2691-2699. (Pubitemid 40353255)
27. Rudert, M., B. Tillmann (1993) Lymph and blood supply of the human intervertebral disc. Cadaver study of correlations to discitis. Acta Orthop Scand 64: 37-40. (Pubitemid 23092299)
28. Sakai, D. (2008) Future perspectives of cell-based therapy for intervertebral disc disease. Eur Spine J 17: 452-458.
29. Sakai, D., J. Mochida, T. Iwashina, A. Hiyama, H. Omi, M. Imai, T. Nakai, K. Ando, T. Hotta (2006) Regenerative effects of transplanting mesenchymal stem cells embedded in atelocollagen to the degenerated intervertebral disc. Biomaterials 27: 335-345. (Pubitemid 41457236)
30. Semenza, G.L. (2000) HIF-1 and human disease: one highly involved factor. Genes Dev 14: 1983-1991. (Pubitemid 30637348)
31. Semenza, G.L. (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148: 399-408.
32. Steck, E., H. Bertram, R. Abel, B. Chen, A. Winter, W. Richter (2005) Induction of intervertebral disc-like cells from adult mesenchymal stem cells. Stem Cells 23: 403-411. (Pubitemid 40404459)
33. Stubbs, S.L., S.T. Hsiao, H.M. Peshavariya, S.Y. Lim, G.J. Dusting, R.J. Dilley (2012) Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro. Stem Cells Dev 21: 1887-1896.
34. Tapp, H., R. Deepe, J.A. Ingram, M. Kuremsky, E.N. Hanley, Jr., H.E. Gruber (2008) Adiposederived mesenchymal stem cells from the sand rat: transforming growth factor beta and 3D co-culture with human disc cells stimulate proteoglycan and collagen type I rich extracellular matrix. Arthritis Res Ther 10: R89.
35. Wang, D.W., B. Fermor, J.M. Gimble, H.A. Awad, F. Guilak (2005) Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J Cell Physiol 204: 184-191. (Pubitemid 40776821)
36. Wang, L., R.R. Rao, J.P. Stegemann (2013) Delivery of mesenchymal stem cells in chitosan/collagen microbeads for orthopedic tissue repair. Cells Tissues Organs 197: 333-343.
37. Wang, Y.T., X.T. Wu, F. Wang (2010) Regeneration potential and mechanism of bone marrow mesenchymal stem cell transplantation for treating intervertebral disc degeneration. J Orthop Sci 15: 707-719.
38. Xue, K., L. Qi, G. Zhou, K. Liu (2013) A two-step method of constructing mature cartilage using bone marrow-derived mesenchymal stem cells. Cells Tissues Organs 197: 484-495.
39. Yang, F., V.Y. Leung, K.D. Luk, D. Chan, K.M. Cheung (2009) Mesenchymal stem cells arrest intervertebral disc degeneration through chondrocytic differentiation and stimulation of endogenous cells. Mol Ther 17: 1959-1966.
40. Zhang, Y.G., X. Guo, P. Xu, L.L. Kang, J. Li (2005) Bone mesenchymal stem cells transplanted into rabbit intervertebral discs can increase proteoglycans. Clin Orthop Relat Res 430: 219-226. (Pubitemid 40096155)