Role of hypoxia and growth and differentiation factor-5 on differentiation of human mesenchymal stem cells towards intervertebral nucleus pulposus-like cells

European Cells and Materials

Volumn 21, Issue , 2011, Pages 533-547

  Stoyanov, J V ^a   Gantenbein Ritter, B ^b   Bertolo, A ^a   Aebli, N ^a   Baur, M ^c   Alini, M ^d   Grad, S ^d  

^a SWISS PARAPLEGIC RESEARCH   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c LUZERNER KANTONSSPITAL   (Switzerland)

^d AO RESEARCH INSTITUTE   (Switzerland)

Author keywords

Chondrogenesis; Growth differentiation factor 5; Growth factors; Hypoxia; Intervertebral disc; Nucleus pulposus; Stem cells; Tissue engineering

Indexed keywords

AGGRECAN; ALGINIC ACID; CARBONATE DEHYDRATASE XII; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; CYTOKERATIN 19; FORKHEAD BOX F1 TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR; GLYCOSAMINOGLYCAN; GROWTH DIFFERENTIATION FACTOR 5; MESSENGER RNA; OXYGEN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; ACAN PROTEIN, HUMAN; DIFFERENTIATION ANTIGEN; FIBRILLAR COLLAGEN; FOXF1 PROTEIN, HUMAN; SOX9 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CHONDROGENESIS; COCULTURE; CONTROLLED STUDY; COW; DOWN REGULATION; ENCAPSULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; INTERVERTEBRAL DISK; MESENCHYMAL STEM CELL; NONHUMAN; NUCLEUS PULPOSUS; OXYGEN TENSION; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; CATTLE; CELL HYPOXIA; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHENOTYPE;

AGGRECANS; ANIMALS; ANTIGENS, DIFFERENTIATION; CATTLE; CELL DIFFERENTIATION; CELL HYPOXIA; CELLS, CULTURED; CHONDROGENESIS; COCULTURE TECHNIQUES; FIBRILLAR COLLAGENS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; GROWTH DIFFERENTIATION FACTOR 5; HUMANS; INTERVERTEBRAL DISK; KERATIN-19; MESENCHYMAL STEM CELLS; PHENOTYPE; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 80053157000     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v021a40     Document Type: Article

References (52)

1. Adams MA, Roughley PJ (2006) What is intervertebral disc degeneration, and what causes it? Spine 31: 2151-2161.
2. Bai X, Xiao Z, Pan Y, Hu J, Pohl J, Wen J, Li L (2004) Cartilage-derived morphogenetic protein-1 promotes the differentiation of mesenchymal stem cells into chondrocytes. Biochem Biophys Res Commun 325: 453-460.
3. Baumgartner L, Arnhold S, Brixius K, Addicks K, Bloch W (2010) Human mesenchymal stem cells: Infl uence of oxygen pressure on proliferation and chondrogenic differentiation in fi brin glue in vitro. J Biomed Mater Res A 93: 930-940.
4. Caplan AI. (1991) Mesenchymal stem cells. J OrthopRes 9: 641-650.
5. Chamberlain G, Fox J, Ashton B, Middleton J (2007) Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25: 2739-2749.
6. Chiche J, Ilc K, Laferrière J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC, Pouysségur J (2009) Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res 69: 358-368.
7. Enobakhare BO, Bader DL, Lee DA (1996) Quantifi cation of sulfated glycosaminoglycans in chondrocyte/alginate cultures, by use of 1,9-dimethylmethylene blue. Anal Biochem 243: 189-191.
8. Farndale RW, Buttle DJ, Barrett AJ (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue 1. Biochimica and Biophysica Acta 883: 173-177.
9. Felka T, Schäfer R, Schewe B, Benz K, Aicher WK (2009) Hypoxia reduces the inhibitory effect of IL-1beta on chondrogenic differentiation of FCS-free expanded MSC. Osteoarthritis Cartilage 17: 1368-1376.
10. Feng G, Wan Y, Balian G, Laurencin CT, Li X (2008) Adenovirus-mediated expression of growth and differentiation factor-5 promotes chondrogenesis of adipose stem cells. Growth Factors 26: 132-142.
11. Francis-West PH, Abdelfattah A, Chen P, Allen C, Parish J, Ladher R, Allen S, MacPherson S, Luyten FP, Archer CW (1999) Mechanisms of GDF-5 action during skeletal development. Development 126: 1305-1315.
12. Ganey T, Hutton WC, Moseley T, Hedrick M, Meisel HJ (2009) Intervertebral disc repair using adipose tissuederived stem and regenerative cells: experiments in a canine model. Spine 34: 2297-2304.
13. Gantenbein-Ritter B, Benneker L, Alini M, Grad S (2011) Differential response of Human Bone Marrow Stromal Cells to either TGF-β1 or to rhGDF-5. Eur Spine J 20: 962-971.
14. Grad S, Alini M, Eglin D, Sakai D, Mochida J, Mahor S, Collin E, Dash B, Pandit A (2010) Cells and biomaterials for intervertebral disc regeneration. In: Synthesis lectures on tissue engineering (Athanasiou KA, ed), Morgan and Claypool Publishers, San Francisco, CA, pp 1-94.
15. Ivanov S, Liao SY, Ivanova A, Danilkovitch-Miagkova A, Tarasova N, Weirich G, Merrill MJ, Proescholdt MA, Oldfield EH, Lee J, Zavada J, Waheed A, Sly W, Lerman MI, Stanbridge EJ (2001) Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am J Pathol 158: 905-919.
16. Kim DH, Kim SH, Heo SJ, Shin JW, Lee SW, Park SA, Shin JW (2009) Enhanced differentiation of mesenchymal stem cells into NP-like cells via 3D co-culturing with mechanical stimulation. J Biosci Bioeng 108: 63-67.
17. Lee CR, Sakai D, Nakai T, Toyama K, Mochida J, Alini M, Grad S (2007) A phenotypic comparison of intervertebral disc and articular cartilage cells in the rat. Eur Spine J 16: 2174-2185.
18. Le Maitre CL, Baird P, Freemont AJ, Hoyland JA (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.
19. Leung VY, Chan D, Cheung KM (2006) Regeneration of intervertebral disc by mesenchymal stem cells: potentials, limitations, and future direction. Eur Spine J 15 Suppl 3: S406-S413.
20. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
21. Lu ZF, Zandieh Doulabi B, Wuisman PI, Bank RA, Helder MN (2007) Differentiation of adipose stem cells by nucleus pulposus cells: confi guration effect. Biochem Biophys Res Commun 359: 991-996.
22. Mahlapuu M, Pelto-Huikko M, Aitola M, Enerbäck S, Carlsson P (1998) FREAC-1 contains a cell-type-specifi c transcriptional activation domain and is expressed in epithelial-mesenchymal interfaces. Dev Biol 202: 183-195.
23. Maldonado BA, Oegema TR, (1992) Initial characterisation of the metabolism of intervertebral disc cells encapsulated in microspheres. J Orthop Res 10: 677-690.
24. Malin D, Kim IM, Boetticher E, Kalin TV, Ramakrishna S, Meliton L, Ustiyan V, Zhu X, Kalinichenko VV (2007) Forkhead box F1 is essential for migration of mesenchymal cells and directly induces integrin-beta3 expression. Mol Cell Biol 27: 2486-2498.
25. Markway BD, Tan GK, Brooke G, Hudson JE, Cooper-White JJ, Doran MR (2010) Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant 19: 29-42.
26. Minogue BM, Richardson SM, Zeef LA, Freemont AJ, Hoyland JA (2010) Characterisation of the human nucleus pulposus cell phenotype and evaluation of novel marker gene expression to defi ne adult stem cell differentiation. Arthritis Rheum 62: 3695-3705.
27. Miyamoto T, Muneta T, Tabuchi T, Matsumoto K, Saito H, Tsuji K, Sekiya I (2010) 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 12: R206.
28. Mwale F, Roughley P, Antoniou J (2004) Distinction between the extracellular matrix of the nucleus pulposus and hyaline cartilage: a requisite for tissue engineering of intervertebral disc. Eur Cell Mater 8: 58-63.
29. Paesold G, Nerlich AG, Boos N (2007) Biological treatment strategies for disc degeneration: potentials and shortcomings. Eur Spine J 16: 447-468.
30. Pelttari K, Winter A, Steck E, Goetzke K, Hennig T, Ochs BG, Aigner T, Richter W (2006) Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcifi cation and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 54: 3254-3266.
31. Pelttari K, Steck E, Richter W (2008) The use of mesenchymal stem cells for chondrogenesis. Injury 39 Suppl 1: S58-S65.
32. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143.
33. Richardson SM, Walker RV, Parker S, Rhodes NP, Hunt JA, Freemont AJ, Hoyland JA (2006) Intervertebral disc cell-mediated mesenchymal stem cell differentiation. Stem Cells 24: 707-716.
34. Richardson SM, Hoyland JA, Mobasheri R, Csaki C, Shakibaei M, Mobasheri A (2010) Mesenchymal stem cells in regenerative medicine: opportunities and challenges for articular cartilage and intervertebral disc tissue engineering. J Cell Physiol 222: 23-32.
35. Risbud MV, Albert TJ, Guttapalli A, Vresilovic EJ, Hillibrand AS, Vaccaro AR, Shapiro IM (2004) Differentiation of mesenchymal stem cells towards a nucleus pulposus-like phenotype in vitro: implications for cell-based transplantation therapy. Spine 29: 2627-2632.
36. Risbud MV, Schaer TP, Shapiro IM (2010) Toward an understanding of the role of notochordal cells in the adult intervertebral disc: From discord to accord. Dev Dyn 239: 2141-2148.
37. Rutges J, Creemers LB, Dhert W, Milz S, Sakai D, Mochida J, Alini M, Grad S (2010) Variations in gene and protein expression in human nucleus pulposus in comparison with annulus fi brosus and cartilage cells: potential associations with aging and degeneration. Osteoarthritis Cartilage 18: 416-423.
38. Sakai D (2008) Future perspectives of cell-based therapy for intervertebral disc disease. Eur Spine J 17 Suppl 4: 452-458.
39. Salgado AJ, Oliveira JT, Pedro AJ, Reis RL (2006) Adult stem cells in bone and cartilage tissue engineering. Curr Stem Cell Res Ther 1: 345-364.
40. Sobajima S, Vadala G, Shimer A, Kim JS, Gilbertson LG, Kang JD (2008) Feasibility of a stem cell therapy for intervertebral disc degeneration. Spine J 8: 888-896.
41. Strassburg S, Richardson SM, Freemont AJ, Hoyland JA (2010) Co-culture induces mesenchymal stem cell differentiation and modulation of the degenerate human nucleus pulposus cell phenotype. Regen Med 5: 701-711.
42. Vadalà G, Sobajima S, Lee JY, Huard J, Denaro V, Kang JD, Gilbertson LG (2008) In vitro interaction between muscle-derived stem cells and nucleus pulposus cells. Spine J 8: 804-809.
43. Watanabe T, Sakai D, Yamamoto Y, Iwashina T, Serigano K, Tamura F, Mochida J (2010) Human nucleus pulposus cells signifi cantly enhanced biological properties in a coculture system with direct cell-to-cell contact with autologous mesenchymal stem cells. J Orthop Res 28: 623-630.
44. Weiler C, Nerlich AG, Schaaf R, Bachmeier BE, Wuertz K, Boos N (2010) Immunohistochemical identifi cation of notochordal markers in cells in the aging human lumbar intervertebral disc. Eur Spine J 19: 1761-1770.
45. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL (2000) Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 60: 7075-7083.
46. Yang X, Li X (2009) Nucleus pulposus tissue engineering: a brief review. Eur Spine J 18: 1-9.
47. Yang SH, Wu CC, Shih TT, Sun YH, Lin FH (2008) In vitro study on interaction between human nucleus pulposus cells and mesenchymal stem cells through paracrine stimulation. Spine 33: 1951-1957.
48. Yang F, Leung VY, Luk KD, Chan D, Cheung KM (2009) Mesenchymal stem cells arrest intervertebral disc degeneration through chondrocytic differentiation and stimulation of endogenous cells. Mol Ther 17: 1959-1966.
49. Bartels EM, Fairbank JC, Winlove CP, Urban JP (1998) Oxygen and lactate concentrations measured in vivo in the intervertebral discs of patients with scoliosis and back pain. Spine 23: 1-7.
50. Ejeskär A, Holm S (1979) Oxygen tension measurements in the intervertebral disc. A methodological and experimental study. Ups J Med Sci 84: 83-93.
51. Holm S, Maroudas A, Urban JP, Selstam G, Nachemson A (1981) Nutrition of the intervertebral disc: solute transport and metabolism. Connect Tissue Res 8: 101-119.
52. Lee DC, Adams CS, Albert TJ, Shapiro IM, Evans SM, Koch CJ (2007) In situ oxygen utilization in the rat intervertebral disc. J Anat 210: 294-303.