Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs

Journal of Cellular Physiology

Volumn 207, Issue 2, 2006, Pages 331-339

  Grayson, Warren L ^a   Zhao, Feng ^a   Izadpanah, Reza ^b   Bunnell, Bruce ^b,c   Ma, Teng ^a  

^a FAMU FSU COLLEGE OF ENGINEERING   (United States)

^b TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; OXYGEN;

ACCLIMATIZATION; ADIPOCYTE; ARTICLE; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL MATURATION; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; MICROENVIRONMENT; OSTEOBLAST; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE ENGINEERING;

ADULT; CARRIER PROTEINS; CELL CULTURE TECHNIQUES; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL HYPOXIA; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; DNA; FIBRONECTINS; GENE EXPRESSION; GLUCOSE; HSP47 HEAT-SHOCK PROTEINS; HUMANS; LACTIC ACID; MESENCHYMAL STEM CELLS; MICROSCOPY, ELECTRON, SCANNING; MIDDLE AGED; OCTAMER TRANSCRIPTION FACTOR-3; OSTEOBLASTS; OXYGEN; TISSUE ENGINEERING;

EID: 31744442047     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20571     Document Type: Article

References (50)

1. Abbott A. 2003. Cell culture: Biology's new dimension. Nature 424:870-872.
2. Annabi B, Lee Y, Turcotte S, Naud E, Desrosiers RR, Champagne M, Eliopoulos N, Galipeau J, Béliveau R. 2003. Hypoxia promotes murine bone marrow-derived stromal cell migration and tube formation. Stem Cells 21:337-347.
3. 2 in muscle cells in culture. Am J Phys 262:C682-C690.
4. Bruder SP, Jaiswal N, Haynesworth SE. 1997. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 64:278-294.
5. Bunting KD, Hawley RG. 2003. Integrative molecular and developmental biology of adult stem cells. Biol Cell 95:563-078.
6. Carmeliet P, Dor Y, Herbert J, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshet E. 1998. Role of HIF-1 in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis. Nature 394:485-490.
7. Cipolleschi MG, Sbarba PD, Olivotto M. 1993. The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 82:2031-2037.
8. Cukierman E, Pankov R, Stevens DR, Yamada KM. 2001. Taking cell-matrix adhesions to the third dimension. Science 294:1708-1712.
9. Derubeis AR, Cancedda R. 2004. Bone marrow stromal cells (BMSCs) in bone engineering: Limitations and recent advances. Ann Biomed Eng 32:160-165.
10. DiGirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ. 1999. Propagation and senescence of human marrow stromal cells in culture: A simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Hemat 107:275-281.
11. Downard J. 2003. Metabolism meets death. Nature 424:896-897.
12. 2 tensions and the prevention of differentiation on hES cells. Proc Natl Acad Sci 102:4783-4788.
13. Faller DV. 1999. Endothelial cell responses to hypoxic stress. Clin Exp Pharm Phys 26:74-84.
14. Firth JD, Ebert BL, Pugh CW, Ratcliffe PJ. 1994. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: Similarities with the erythropoietin 3' enhancer. Proc Natl Acad Sci 91:6496-6500.
15. Fischer B, Bavista BD. 1993. Oxygen-tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 99:673-679.
16. 1/S transition through regulation of p27 expression. J Biol Chem 276:7919-7926.
17. Grayson WL, Ma T, Bunnell B. 2004. Human mesenchymal stem cell tissue development in 3D PET matrices. Biotechnol Prog 20:905-912.
18. Greenspan P, Mayer EP, Fowler SD. 1985. Nile red: A selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100:965-973.
19. Guillemin K, Krasnow MA. 1997. The hypoxic response: Huffing and HIFing. Cell 89:9-12.
20. Hevehan DL, Papoutsakis T, Miller WM. 2000. Physiologically significant effects of pH and oxygen tension on granulopoiesis. Exp Hemat 28:267-275.
21. Holtorf H, Jansen JA, Mikos AG. 2005. Flow perfusion culture induces the osteoblastic differentiation of marrow stromal cell-scaffold constructs in the absence of dexamethasone. J Biomed Mat Res A 72A:326-334.
22. Horino Y, Takahashi S, Miura T, Takahashi Y. 2002. Prolonged hypoxia accelerates the post-transcriptional process of collagen synthesis in cultured fibroblasts. Life Sci 71:3031-3045.
23. Iida T, Mine S, Fujimoto H, Suzuki K, Minami Y, Tanaka Y. 2002. Hypoxia-inducible factor-1α induces cell cycle arrest of endothelial cells. Genes Cells 7:143-149.
24. Ivanovic Z, Sbarba PD, Trimoreau F, Faucher J, Praloran V. 2000. Primitive human HPCs are better maintained and expanded in vitro at 1 percent oxygen than at 20 percent. Transfusion 40:1482-1488.
25. Ivanovic Z, Belloc F, Faucher J, Cipolleschi MG, Praloran V, Sbarba PD. 2002. Hypoxia maintains and interleukin-3 reduces the pre-colony forming cell potential of dividing CD34+ murine bone marrow cells. Exp Hematol 30:67-73.
26. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. 2001. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac functions. Nat Med 7:430-436.
27. Krishnamurthy P, Ross DD, Nakanishi T, Bailey-Dell K, Zhou S, Mercer KE, Sarkadi B, Sorrentino BP, Schuetz JD. 2004. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 279:24218-24225.
28. Lash GE, Fitzpatrick TE, Graham CH. 2001. Effect of hypoxia on cellular adhesion to vitronectin and fibronectin. Biochem Biophys Res Commun 287:622-629.
29. 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 Phys 187:345-355.
30. Levenberg S, Huang NF, Lavik E, Rogers AB, Itskovitz-Eldor J, Langer R. 2003. Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc Natl Acad Sci 100:12741-12746.
31. Li Y, Ma T, Kniss DA, Lasky LC, Yang ST. 2001. Effects of nitration seeding on cell density, spatial distribution, and proliferation in nonwoven fibrous matrices. Biotechnol Prog 17:935-944.
32. Lin Z, Weinberg JM, Malhorta R, Merritt SE, Holzman LB, Brosius FC III. 2000. GLUT-1 reduces hypoxia-induced apoptosis and JNK pathway activation. Am J Phys 278:E958-E966.
33. Loike JD, Cao L, Brett J, Ogawa S, Silverstein SC, Stern D. 1992. Hypoxia induces glucose transporter expression in endothelial cells. Am J Phys 263:C326-C333.
34. Ma T, Li Y, Yang ST, Kniss DA. 2000. Effects of pore size in 3-D fibrous matrix on human trophoblast tissue development. Biotechnol Bioeng 70:606-618.
35. Malhorta R, Brosius FC III. 1999. Glucose uptake and glycolysis reduce hypoxia-induced apoptosis in cultured neonatal rat cardiac myocytes. J Cell Biol 274:12567-12575.
36. Minchenko A, Salceda S, Bauer T, Caro J. 1994. Hypoxia regulatory elements of the human vascular endothelial growth factor Gene. Cell Mol Biol Res 40:35-39.
37. Morrison SJ, Csete M, Groves AK, Melega W, Wold B, Anderson DJ. 2000. Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. J Neurosci 20:7370-7376.
38. Mostafa SS, Miller WM, Papoutsakis ET. 2000. Oxygen tension influences the differentiation, maturation and apoptosis of human megakaryocytes. Br J Haematol 111:879-889.
39. Munoz-Elias G, Woodbury B, Black IB. 2003. Marrow stromal cells, mitosis, and neuronal differentiation: Stem cell and precursor functions. Stem Cells 21:437-448.
40. Nagata K. 1998. Expression and function of heat shock protein 47: A collagen-specific molecular chaperone in the endoplasmic reticulum. Matrix Biol 16:379-386.
41. Packer L, Fuehr K. 1977. Low oxygen concentrations extends the lifespan of cultured human diploid cells. Nature 267:423-425.
42. Plas DR, Thompson CB. 2002. Cell metabolism in the regulation of programmed cell death. Trends Endocrinol Metabol 13:74-77.
43. Salim A, Giaccia AJ, Longaker MT. 2004. Stem cell differentiation. Nat Biotechnol 22:804-805.
44. Sekiya I, Larson BL, Smith JR, Pochampally R, Cui J, Prockop DJ. 2002a. Expansion of human adult stem cells from bone marrow stroma: Conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20:530-541.
45. Sekiya I, Vuoristo JT, Larson BL, Prockop DJ. 2002b. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci 99:4397-4402.
46. Shur I, Marom R, Lokiec F, Socher R, Benayahu D. 2002. Identification of progenitor cells from human marrow stroma. J Cell Biochem 87:51-57.
47. Steinbrech DS, Longaker MT, Mehrar BJ, Saadeh PB, Chin GS, Gerrets RP, Chau DC, Rowe NM, Gittes GK. 1999. Fibroblast response to hypoxia: The relationship between angiogenesis and matrix regulation. J Surg Res 84:127-133.
48. Studer L, Csete M, Lee SH, Kabbani N, Walikonis J, Wold B, McKay R. 2000. Enhanced proliferation, survival and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 20:7377-7383.
49. Wang DW, Fermor B, Gimble JM, Awad HA, Guilak F. 2005. Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J Cell Phys 204:184-191.
50. Zhu LL, Wu LY, Yew DT, Fan M. 2005. Effects of Hypoxia on the proliferation and differentiation of NSCs, Mol Neurobio 31:231-242.