Hypoxic conditions during expansion culture prime human mesenchymal stromal precursor cells for chondrogenic differentiation in three-dimensional cultures

Cell Transplantation

Volumn 20, Issue 10, 2011, Pages 1589-1602

  Müller, Jana ^a   Benz, Karin ^a   Ahlers, Michael ^b   Gaissmaier, Christoph ^c   Mollenhauer, Jürgen ^a,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Gelita AG   (Germany)

^c Tissue Engineering Technologies   (Germany)

Author keywords

Chondrogenic differentiation; Gelatin hydrogel; Hypoxia; Intervertebral disc; Mesenchymal stromal precursor cell

Indexed keywords

AGGRECAN; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; GELATIN; MESSENGER RNA; MIANSERIN; TRANSCRIPTION FACTOR SOX9;

ADULT; AGED; ARTICLE; BIOCHEMISTRY; CELL ANCHORAGE; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CELL HYPOXIA; CHONDROGENESIS; CLINICAL ARTICLE; CLINICAL EXAMINATION; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROGEL; HYPOXIA; IN VITRO STUDY; INTERVERTEBRAL DISK; MALE; MESENCHYMAL STROMA CELL; NUTRITION; OXYGEN TENSION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; THREE DIMENSIONAL ECHOCARDIOGRAPHY;

EID: 84856036173     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X564094     Document Type: Article

References (54)

1. Altschul, S. F.; Madden, T. L.; Schaffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25(17):3389-3402; 1997.
2. Boos, N.; Weissbach, S.; Rohrbach, H.; Weiler, C.; Spratt, K. F.; Nerlich, A. G. Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic science. Spine 27(23):2631-2644; 2002.
3. Buckwalter, J. A. Aging and degeneration of the human intervertebral disc. Spine 20(11):1307-1314; 1995.
4. Carragee, E. J.; Don, A. S.; Hurwitz, E. L.; Cuellar, J. M.; Carrino, J.; Herzog, R. 2009 ISSLS Prize Winner: Does discography cause accelerated progression of degeneration changes in the lumbar disc: A ten-year matched cohort study. Spine 34(21):2338-2345; 2009.
5. Crevensten, G.; Walsh, A. J.; Ananthakrishnan, D.; Page, P.; Wahba, G. M.; Lotz, J. C.; Berven, S. Intervertebral disc cell therapy for regeneration: Mesenchymal stem cell implantation in rat intervertebral discs. Ann. Biomed. Eng. 32(3):430-434; 2004.
6. Felka, T.; Schafer, R.; Schewe, B.; Benz, K.; Aicher, W. K. Hypoxia reduces the inhibitory effect of IL-1beta on chondrogenic differentiation of FCS-free expanded MSC. Osteoarthritis Cartilage 17(10):1368-1376; 2009.
7. Fink, T.; Lund, P.; Pilgaard, L.; Rasmussen, J. G.; Duroux, M.; Zachar, V. Instability of standard PCR reference genes in adipose-derived stem cells during propagation, differentiation and hypoxic exposure. BMC Mol. Biol. 9:98; 2008.
8. Ganey, T.; Hutton, W. C.; Moseley, T.; Hedrick, M.; Meisel, H. J. Intervertebral disc repair using adipose tissue-derived stem and regenerative cells: Experiments in a canine model. Spine 34(21):2297-2304; 2009.
9. Girkontaite, I.; Frischholz, S.; Lammi, P.; Wagner, K.; Swoboda, B.; Aigner, T.; Von der Mark, K. Immunolocalization of type X collagen in normal fetal and adult osteoarthritic cartilage with monoclonal antibodies. Matrix Biol. 15(4):231-238; 1996.
10. Granero-Molto, F.; Weis, J. A.; Miga, M. I.; Landis, B.; Myers, T. J.; O'Rear, L.; Longobardi, L.; Jansen, E. D.; Mortlock, D. P.; Spagnoli, A. Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells 27(8):1887-1898; 2009.
11. Grayson, W. L.; Zhao, F.; Bunnell, B.; Ma, T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem. Biophys. Res. Commun. 358(3):948-953; 2007.
12. Hardingham, T. E.; Oldershaw, R. A.; Tew, S. R. Cartilage, SOX9 and Notch signals in chondrogenesis. J. Anat. 209(4):469-480; 2006.
13. Hennig, T.; Lorenz, H.; Thiel, A.; Goetzke, K.; Dickhut, A.; Geiger, F.; Richter, W. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profile and is over- come by BMP-6. J. Cell. Physiol. 211(3):682-691; 2007.
14. Henriksson, H. B.; Svanvik, T.; Jonsson, M.; Hagman, M.; Horn, M.; Lindahl, A.; Brisby, H. Transplantation of human mesenchymal stems cells into intervertebral discs in a xenogeneic porcine model. Spine 34(2):141-148; 2009.
15. Hohaus, C.; Ganey, T. M.; Minkus, Y.; Meisel, H. J. Cell transplantation in lumbar spine disc degeneration disease. Eur. Spine J. 17(Suppl. 4):492-503; 2008.
16. Holzwarth, C.; Vaegler, M.; Gieseke, F.; Pfister, S. M.; Handgretinger, R.; Kerst, G.; Muller, I. Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biol. 11:11; 2010.
17. Johnstone, B.; Hering, T. M.; Caplan, A. I.; Goldberg, V. M.; Yoo, J. U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 238(1):265-272; 1998.
18. Jung, M.; Kaszap, B.; Redohl, A.; Steck, E.; Breusch, S.; Richter, W.; Gotterbarm, T. Enhanced early tissue regeneration after matrix-assisted autologous mesenchymal stem cell transplantation in full thickness chondral defects in a minipig model. Cell Transplant. 18(8):923-932; 2009.
19. Kanichai, M.; Ferguson, D.; Prendergast, P. J.; Campbell, V. A. Hypoxia promotes chondrogenesis in rat mesenchymal stem cells: A role for AKT and hypoxia-inducible factor (HIF)-1alpha. J. Cell. Physiol. 216(3):708-715; 2008.
20. Kim, H. J.; Kim, Y. J.; Im, G. I. Is continuous treatment with transforming growth factor-beta necessary to induce chondrogenic differentiation in mesenchymal stem cells? Cells Tissues Organs 190(1):1-10; 2009.
21. Koga, H.; Engebretsen, L.; Brinchmann, J. E.; Muneta, T.; Sekiya, I. Mesenchymal stem cell-based therapy for cartilage repair: A review. Knee Surg. Sports Traumatol. Arthrosc. 17(11):1289-1297; 2009.
22. Lefebvre, V.; de Crombrugghe, B. Toward understanding SOX9 function in chondrocyte differentiation. Matrix Biol. 16(9):529-540; 1998.
23. Le Maitre, C. L.; Baird, P.; Freemont, A. J.; Hoyland, J. A. An in vitro study investigating the survival and phenotype of mesenchymal stem cells following injection into nucleus pulposus tissue. Arthritis Res. Ther. 11(1):R20; 2009.
24. Liebscher, T.; Haefeli, M.; Wuertz, K.; Nerlich, A. G.; Boos, N. Age-related variation in cell density of human lumbar intervertebral disc. Spine 36(2):153-159; 2011.
25. Linsenmayer, T. F.; Hendrix, M. J. Monoclonal antibodies to connective tissue macromolecules: Type II collagen. Biochem. Biophys. Res. Commun. 92(2):440-446; 1980.
26. Ma, T.; Grayson, W. L.; Frohlich, M.; Vunjak-Novakovic, G. Hypoxia and stem cell-based engineering of mesenchymal tissues. Biotechnol. Prog. 25(1):32-42; 2009.
27. Majumdar, M. K.; Wang, E.; Morris, E. A. BMP-2 and BMP-9 promotes chondrogenic differentiation of human multipotential mesenchymal cells and overcomes the inhibitory effect of IL-1. J. Cell. Physiol. 189(3):275-284; 2001.
28. Malladi, P.; Xu, Y.; Chiou, M.; Giaccia, A. J.; Longaker, M. T. Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am. J. Physiol. Cell Physiol. 290(4):C1139-1146; 2006.
29. Malladi, P.; Xu, Y.; Chiou, M.; Giaccia, A. J.; Longaker, M. T. Hypoxia inducible factor-1alpha deficiency affects chondrogenesis of adipose-derived adult stromal cells. Tissue Eng. 13(6):1159-1171; 2007.
30. Markway, B. D.; Tan, G. K.; Brooke, G.; Hudson, J. E.; Cooper-White, J. J.; Doran, M. R. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchy- mal stem cells in low oxygen environment micropellet cultures. Cell Transplant. 19(1):29-42; 2010
31. Maroudas, A.; Stockwell, R. A.; Nachemson, A.; Urban, J. Factors involved in the nutrition of the human lumbar intervertebral disc: Cellularity and diffusion of glucose in vitro. J. Anat. 120(1):113-130; 1975.
32. Meisel, H. J.; Siodla, V.; Ganey, T.; Minkus, Y.; Hutton, W. C.; Alasevic, O. J. Clinical experience in cell-based therapeutics: Disc chondrocyte transplantation A treatment for degenerated or damaged intervertebral disc. Bio-mol. Eng. 24(1):5-21; 2007.
33. Noth, U.; Rackwitz, L.; Heymer, A.; Weber, M.; Baumann, B.; Steinert, A.; Schutze, N.; Jakob, F.; Eulert, J. Chondrogenic differentiation of human mesenchymal stem cells in collagen type I hydrogels. J. Biomed. Mater. Res. A. 83(3):626-635; 2007.
34. Oegema, Jr., T. R. Biochemistry of the intervertebral disc. Clin. Sports Med. 12(3):419-439; 1993.
35. Panetta, N. J.; Gupta, D. M.; Quarto, N.; Longaker, M. T. Mesenchymal cells for skeletal tissue engineering. Panminerva Med. 51(1):25-41; 2009.
36. Pelttari, K.; Winter, A.; Steck, E.; Goetzke, K.; Hennig, T.; Ochs, B. G.; Aigner, T.; Richter, W. Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum. 54(10):3254-3266; 2006.
37. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jauswal, R. K.; Douglas, R.; Mosca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage potential of adult human mesechymal stem cells. Science 284(5411):143-147; 1999.
38. Presti, D.; Scott, J. E. Hyaluronan-mediated protective ef- fect against cell damage caused by enzymatically produced hydroxyl (OH•) radicals is dependent on hyaluronan molecular mass. Cell Biochem. Funct. 12(4):281-288; 1994.
39. Risbud, M. V.; Albert, T. J.; Guttapalli, A.; Vresilovic, E. J.; Hillibrand, A. S.; Vaccaro, A. R.; Shapiro, I. M. Differentiation of mesenchymal stem cells towards a nucleus pulposus-like phenotype in vitro: Implications for cell-based transplantation therapy. Spine 29(23):2627-2632; 2004.
40. Sakai, D.; Mochida, J.; Iwashina, T.; Hiyama, A.; Omi, H.; Imai, M.; Nakai, T.; Ando, K.; Hotta, T. Regenerative effects of transplanting mesenchymal stem cells embedded in atelocollagen to the degenerated intervertebral disc. Biomaterials 27(3):335-345; 2006.
41. Sakai, D.; Mochida, J.; Yamamoto, Y.; Nomura, T.; Okuma, M.; Nishimura, K.; Nakai, T.; Ando, K.; Hotta, T. Transplantation of mesenchymal stem cells embedded in Atelocollagen gel to the intervertebral disc: A potential therapeutic model for disc degeneration. Biomaterials 24(20):3531-3541; 2003.
42. Scharstuhl, A.; Schewe, B.; Benz, K.; Gaissmaier, C.; Buhring, H. J.; Stoop, R. Chondrogenic potential of human adult mesenchymal stem cells is independent of age or osteoarthritis etiology. Stem Cells 25(12):3244-3251; 2007.
43. Scott, D.; Coleman, P. J.; Mason, R. M.; Levick, J. R. Concentration dependence of interstitial flow buffering by hyaluronan in synovial joints. Microvasc. Res. 59(3):345-353; 2000.
44. Scott, J. E.; Dorling, J. Differential staining of acid glyco-saminoglycans (mucopolysaccharides) by alcian blue in salt solutions. Histochemie 5(3):221-233; 1965.
45. Sobajima, S.; Vadala, G.; Shimer, A.; Kim, J. S.; Gilbertson, L. G.; Kang, J. D. Feasibility of a stem cell therapy for intervertebral disc degeneration. Spine 8(6):888-896; 2008.
46. Steck, E.; Bertram, H.; Abel, R.; Chen, B.; Winter, A.; Richter, W. Induction of intervertebral disc-like cells from adult mesenchymal stem cells. Stem Cells 23(3):403-411; 2005.
47. Steck, E.; Fischer, J.; Lorenz, H.; Gotterbarm, T.; Jung, M.; Richter, W. Mesenchymal stem cell differentiation in an experimental cartilage defect: Restriction of hypertrophy to bone-close neocartilage. Stem Cells Dev. 18(7): 969-978; 2009.
48. Trout, J. J.; Buckwalter, J. A.; Moore, K. C. Ultrastructure of the human intervertebral disc: II. Cells of the nucleus pulposus. Anat. Rec. 204(4):307-314; 1982.
49. Urban, J. P.; Smith, S.; Fairbank, J. C. Nutrition of the intervertebral disc. Spine 29(23):2700-2709; 2004.
50. Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3(7):RESEARCH0034; 2002.
51. Wenig, C. M.; Schmidt, C. O.; Kohlmann, T.; Schweikert, B. Costs of back pain in Germany. Eur. J. Pain 13(3): 280-286; 2009.
52. Xu, Y.; Malladi, P.; Chiou, M.; Bekerman, E.; Giaccia, A. J.; Longaker, M. T. In vitro expansion of adipose-derived adult stromal cells in hypoxia enhances early chondrogenesis. Tissue Eng. 13(12):2981-2993; 2007.
53. Zhang, L.; Su, P.; Xu, C.; Yang, J.; Yu, W.; Huang, D. Chondrogenic differentiation of human mesenchymal stem cells: A comparison between micromass and pellet culture systems. Biotechnol. Lett. 32(9):1339-1346; 2010.
54. Zscharnack, M.; Poesel, C.; Galle, J.; Bader, A. Low oxy- gen expansion improves subsequent chondrogenesis of ovine bone-marrow-derived mesenchymal stem cells in collagen type I hydrogel. Cells Tissues Organs 190(2):81-93; 2009.