Oxygen tension differentially influences osteogenic differentiation of human adipose stem cells in 2D and 3D cultures

Journal of Cellular Biochemistry

Volumn 110, Issue 1, 2010, Pages 87-96

  He, Jiawei ^a   Genetos, Damian C ^b   Yellowley, Clare E ^c   Kent Leach, J ^a  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

3D culture; Adipose stem cells; Hypoxia; Osteogenesis; Oxygen

Indexed keywords

ALKALINE PHOSPHATASE; CALCIUM; CELL MARKER; VASCULOTROPIN;

ADIPOSE STEM CELL; ADULT; ANGIOGENESIS; ARTICLE; BONE DEVELOPMENT; CALCIFICATION; CELL DIFFERENTIATION; CONTROLLED STUDY; CULTURE TECHNIQUE; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; OSTEOBLAST; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; STEM CELL; THREE DIMENSIONAL CULTURE; TWO DIMENSIONAL CELL CULTURE;

ADIPOSE TISSUE; ADULT; ALKALINE PHOSPHATASE; APOPTOSIS; CALCIUM; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DNA; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOGENESIS; OXYGEN; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77951732961     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22514     Document Type: Article

References (47)

1. Anderson HC. 1989. Biology of disease. Mechanism of mineral formation in bone. Lab Invest 60:320-323.
2. Barralet JE, Wang L, Lawson M, Triffitt JT, Cooper PR, Shelton RM. 2005. Comparison of bone marrow cell growth on 2D and 3D alginate hydrogels. J Mater Sci Mater Med 16:515-519. (Pubitemid 40884243)
3. Brighton CT, Krebs AG. 1972. Oxygen tension of healing fractures in the rabbit. J Bone Joint Surg Am 54:323-332.
4. Caplan AI. 2009. Why are MSCs therapeutic? New data: New insight. J Pathol 217:318-324.
5. Caplan AI, Dennis JE. 2006. Mesenchymal stem cells as trophic mediators. J Cell Biochem 98:1076-1084. (Pubitemid 44128350)
6. Davis HE, Rao RR, He J, Leach JK. 2009. Biomimetic scaffolds fabricated from apatite-coated polymer microspheres. J Biomed Mater Res Part A 90:1021-1031.
7. D'Ippolito G, Schiller PC, Ricordi C, Roos BA, Howard GA. 1999. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 14:1115-1122. (Pubitemid 29314054)
8. D'Ippolito G, Diabira S, Howard GA, Roos BA, Schiller PC. 2006. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 39:513-522. (Pubitemid 44149268)
9. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. 1997. Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89:747-754. (Pubitemid 27516177)
10. Ferrara N, Gerber HP. 2001. The role of vascular endothelial growth factor in angiogenesis. Acta Haematol 106:148-156. (Pubitemid 34124153)
11. Gimble J, Guilak F. 2003. Adipose-derived adult stem cells: Isolation, characterization, and differentiation potential. Cytotherapy 5:362-369. (Pubitemid 37369023)
12. He J, Genetos DC, Leach JK. 2010. Osteogenesis and trophic factor secretion are enhanced with hydroxyapatite/poly(lactide-co-glycolide) composite scaffolds and human mesenchymal stem cells. Tissue Eng Part A 16:127-137.
13. Jarrahy R, Huang W, Rudkin GH, Lee JM, Ishida K, Berry MD, Sukkarieh M, Wu BM, Yamaguchi DT, Miller TA. 2005. Osteogenic differentiation is inhibited and angiogenic expression is enhanced in MC3T3-E1 cells cultured on three-dimensional scaffolds. Am J Physiol Cell Physiol 289:C408-C414. (Pubitemid 41008887)
14. Jeon O, Rhie JW, Kwon IK, Kim JH, Kim BS, Lee SH. 2008. In vivo bone formation following transplantation of human adipose-derived stromal cells that are not differentiated osteogenically. Tissue Eng Part A 14:1285-1294.
15. Kärner E, Karlström E, Ährlund-Richter L, Wendel M, Sugars RV. 2008. Osteogenic-differentiation of human embryonic stem cells: 2D vs. 3D culture-conditions. J Dent Res 87:96.
16. Kassem M, Kristiansen M, Abdallah BM. 2004. Mesenchymal stem cells: Cell biology and potential use in therapy. Basic Clin Pharmacol Toxicol 95:209-214. (Pubitemid 39564237)
17. Kim Y, Kim H, Cho H, Bae Y, Suh K, Jung J. 2007. Direct comparison of human mesenchymal stem cells derived from adipose tissues and bone marrow in mediating neovascularization in response to vascular ischemia. Cell Physiol Biochem 20:867-876. (Pubitemid 350059730)
18. Kocher MS, Shapiro F. 1998. Osteogenesis imperfecta. J Am Acad Orthop Surg 6:225-236.
19. Komatsu DE, Hadjiargyrou M. 2004. Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair. Bone 34:680-688. (Pubitemid 38393804)
20. Lennon DP, Edmison JM, Caplan AI. 2001. Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: Effects on in vitro and in vivo osteochondrogenesis. J Cell Physiol 187:345-355.
21. Logeart-Avramoglou D, Anagnostou F, Bizios R, Petite H. 2005. Engineering bone: Challenges and obstacles. J Cell Mol Med 9:72-84.
22. Lund P, Pilgaard L, Duroux M, Fink T, Zachar V. 2009. Effect of growth media and serum replacements on the proliferation and differentiation of adipose-derived stem cells. Cytotherapy 11:189-197.
23. Malda J, Klein TJ, Upton Z. 2007. The roles of hypoxia in the in vitro engineering of tissues. Tissue Eng 13:2153-2162. (Pubitemid 47404431)
24. Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT. 2006. Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol 290:C1139-C1146.
25. Mayr-Wohlfart U, Waltenberger J, Hausser H, Kessler S, Gunther KP, Dehio C, Puhl W, Brenner RE. 2002. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 30:472-477. (Pubitemid 34204121)
26. Mizuno H. 2009. Adipose-derived stem cells for tissue repair and regeneration: Ten years of research and a literature review. J Nippon Med Sch 76:56-66.
27. Nacamuli RP, Fong KD, Warren SM, Fang TD, Song HM, Helms JA, Longaker MT. 2003. Markers of osteoblast differentiation in fusing and nonfusing cranial sutures. Plast Reconstr Surg 112:1328-1335.
28. Peroni D, Scambi I, Pasini A, Lisi V, Bifari F, Krampera M, Rigotti G, Sbarbati A, Galie M. 2008. Stem molecular signature of adipose-derived stromal cells. Exp Cell Res 314:603-615.
29. Piattelli A, Piattelli M, Scarano A. 1997. Simultaneous demonstration of alkaline and acid phosphatase activity in bone, at bone-implant interfaces and at the epiphyseal growth plate in plastic-embedded undemineralized tissues. Biomaterials 18:545-549. (Pubitemid 27156268)
30. Raheja LF, Genetos DC, Yellowley CE. 2008. Hypoxic osteocytes recruit human MSCs through an OPN/CD44-mediated pathway. Biochem Biophys Res Commun 366:1061-1066.
31. Raheja LF, Genetos DC, Yellowley CE. 2009. The effect of oxygen tension on the long-term osteogenic differentiation and MMP/TIMP expression of human mesenchymal stem cells. Cells Tissues Organs (in press).
32. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL. 2004. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292-1298. (Pubitemid 38372789)
33. Riddle RC, Khatri R, Schipani E, Clemens TL. 2009. Role of hypoxia-inducible factor-1alpha in angiogenic-osteogenic coupling. J Mol Med 86:583-590.
34. Rubina K, Kalinina N, Efimenko A, Lopatina T, Melikhova V, Tsokolaeva Z, Sysoeva V, Tkachuk V, Parfyonova Y. 2009. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng Part A 15:2039-2050.
35. Ruiz SA, Chen CS. 2008. Emergence of patterned stem cell differentiation within multicellular structures. Stem Cells 26:2921-2927.
36. Salim A, Nacamuli RP, Morgan EF, Giaccia AJ, Longaker MT. 2004. Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts. J Biol Chem 279:40007-40016. (Pubitemid 39258275)
37. Schleier P, Hyckel P, Fried W, Beinemann J, Wurdinger J, Hinz M, Steen M, Schumann D. 2006. Vertical distraction of fibula transplant in a case of mandibular defect caused by shotgun injury. Int J Oral Maxillofac Surg 35:861-864. (Pubitemid 44070645)
38. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108. (Pubitemid 351818697)
39. Shea LD, Wang D, Franceschi RT, Mooney DJ. 2000. Engineered bone development from a pre-osteoblast cell line on three-dimensional scaffolds. Tissue Eng 6:605-617.
40. Stanford CM, Jacobson PA, Eanes ED, Lembke LA, Midura RJ. 1995. Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106-01 BSP). J Biol Chem 270:9420-9428.
41. Sterodimas A, De Faria J, Correa WE, Pitanguy I. 2009. Tissue engineering in plastic surgery: An up-to-date review of the current literature. Ann Plast Surg 62:97-103.
42. Stolzing A, Jones E, McGonagle D, Scutt A. 2008. Age-related changes in human bone marrow-derived mesenchymal stem cells: Consequences for cell therapies. Mech Ageing Dev 129:163-173.
43. Utting JC, Robins SP, Brandao-Burch A, Orriss IR, Behar J, Arnett TR. 2006. Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Exp Cell Res 312:1693-1702. (Pubitemid 43776006)
44. Wang Y,Wan C, Deng L, Liu X, Cao X, Gilbert SR, Bouxsein ML, Faugere MC, Guldberg RE, Gerstenfeld LC, Haase VH, Johnson RS, Schipani E, Clemens TL. 2007. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 117:1616-1626. (Pubitemid 46871346)
45. Weinreb M, Shinar D, Rodan GA. 1990. Different pattern of alkaline phosphatase, osteopontin, and osteocalcin expression in developing rat bone visualized by in situ hybridization. J Bone Miner Res 5:831-842. (Pubitemid 20294767)
46. Yefang Z, Hutmacher DW, Varawan SL, Meng LT. 2007. Comparison of human alveolar osteoblasts cultured on polymer-ceramic composite scaffolds and tissue culture plates. Int J Oral Maxillofac Surg 36:137-145. (Pubitemid 46179151)
47. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. 2002. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295. (Pubitemid 35471185)