Hypoxia and stem cell-based engineering of mesenchymal tissues

Biotechnology Progress

Volumn 25, Issue 1, 2009, Pages 32-42

  Ma, Teng ^a   Grayson, Warren L ^b   Fröhlich, Mirjam ^b,c   Vunjak Novakovic, Gordana ^b  

^a FLORIDA STATE UNIVERSITY   (United States)

^b Columbia University ^*  (United States)

^c Educell doo   (Slovenia)

Author keywords

3D; Adult stem cells; Embryonic stem cells; Hypoxia; Mesenchymal stem cells; Oxygen tension

Indexed keywords

3D; ADULT STEM CELLS; EMBRYONIC STEM CELLS; HYPOXIA; MESENCHYMAL STEM CELLS; OXYGEN TENSION;

CELL CULTURE; HISTOLOGY; MAINTENANCE; OXYGEN; PHYSIOLOGICAL MODELS; TISSUE; TISSUE ENGINEERING;

CELL MEMBRANES;

ANIMAL; BIOLOGICAL MODEL; CELL HYPOXIA; CYTOLOGY; EMBRYONIC STEM CELL; HUMAN; MESENCHYMAL STEM CELL; METABOLISM; METHODOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TISSUE ENGINEERING;

ANIMALS; CELL HYPOXIA; EMBRYONIC STEM CELLS; HUMANS; MESENCHYMAL STEM CELLS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; STEM CELLS; TISSUE ENGINEERING;

EID: 64549084622     PISSN: 87567938     EISSN: None     Source Type: Journal    
DOI: 10.1002/btpr.128     Document Type: Article

References (97)

1. Muschler GE, Nakamoto C, Griffith LG. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am A. 2004;86:1541-1558.
2. Meinel L, Betz O, Fajardo R, Hofmann S, Nazarian A, Cory E, Hilbe M, McCool J, Langer R, Vunjak-Novakovic G, Merkle HP, Rechenberg B, Kaplan DL, Kirker-Head C. Silk based bio-materials to heal critical sized femur defects. Bone. 2006;39: 922-931.
3. Meinel L, Fajardo R, Hofmann S, Langer R, Chen J, Snyder B, Vunjak-Novakovic G, Kaplan D. Silk implants for the healing of critical size bone defects. Bone. 2005;37:688-698.
4. Tuli R, Li WJ, Tuan RS. Current state of cartilage tissue engineering. Arthritis Res Ther. 2003;5:235-238.
5. Mauney JR, Volloch V, Kaplan DL. Matrix-mediated retention of adipogenic differentiation potential by human adult bone marrow-derived mesenchymal stem cells during ex vivo expansion. Biomaterials. 2005;26:6167-6175.
6. Vunjak-Novakovic G, Altman, G, Horan R, Kaplan DL. Tissue engineering of ligaments. Annu Rev Biomed Eng. 2004;6:131-156.
7. Watt FM, Hogan BLM. Out of Eden: stem cells and their niches. Science. 2000;287:1427-1430.
8. Grayson W, Chao PHG, Marolt D, Kaplan D, Vunjak-Nova-kovic G. Engineering custom-designed osteochondral tissue grafts. Trends Biotechnol. 2008;26:181-189.
9. Malda J, Woodfield TBF, van der Vloodt F, Kooy FK, Martens DE, Tramper J, van Blitterswijk CA, Riesle J. The effect of PEGT/PBT scaffold architecture on oxygen gradients in tissue engineered cartilaginous constructs. Biomaterials. 2004;25: 5773-5780.
10. Obradovic B, Carrier RL, Vunjak-Novakovic G, Freed LE. Gas exchange is essential for bioreactor cultivation of tissue engineered cartilage. Biotechnol Bioeng. 1999;63:197-205.
11. Radisic M, Deen W, Langer R, Vunjak-Novakovic G. Mathematical model of oxygen distribution in engineered cardiac tissue with parallel channel array perfused with culture medium containing oxygen carriers. Am J Physiol Heart Circ Physiol. 2005;288:H1278-H1289.
12. Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol. 2006;7:211-224.
13. Malda J, Klein TJ, Upton Z. The roles of hypoxia in the in vitro engineering of tissues. Tissue Eng. 2007;13:2153-2162.
14. Martin I, Wendt D, Heberer M. The role of bioreactors in tissue engineering. Trends Biotechnol. 2004;22:80-86.
15. Toya RE, Barrett JV, Davis ML. Hypoxia induced proliferation of hematopoietic stem-cells in bone-marrow of mice. Radiat Res. 1976;67:591-591.
16. Murphy MJ, Lord BI. Hematopoietic stem-cell regulation. I. Acute effects of hypoxic-hypoxia on cfu kinetics. Blood. 1973;42:81-87.
17. Lord BI, Murphy MJ. Hematopoietic stem-cell regulation. II. Chronic effects of hypoxic-hypoxia on cfu kinetics. Blood. 1973; 42:89-98.
18. Ivanovic Z, Dello Sbarba P, Trimoreau F, Faucher JL, Praloran V. Primitive human HPCs are better maintained and expanded in vitro at 1 percent oxygen than at 20 percent. Transfusion. 2000;40:1482-1488.
19. Cipolleschi MG, Rovida E, Ivanovic Z, Praloran V, Olivotto M, Dello Sbarba P. The expansion of murine bone marrow cells preincubated in hypoxia as an In vitro indicator of their mar-row-repopulating ability. Leukemia. 2000;14:735-739.
20. Ivanovic Z, Bartolozzi B, Bernabei PA, Cipolleschi MG, Rovida E, Milenkovic P, Praloran V, Dello Sbarba P. Incubation of mu-rine bone marrow cells in hypoxia ensures the maintenance of marrow-repopulating ability together with the expansion of committed progenitors. Br J Haematol. 2000;108:424-429.
21. Csete M. Oxygen in the cultivation of stem cells. In Ourednik J, Sakaguchi D, and Nilsen-Hamilton M. Stem Cell Biology: Development and Plasticity, Wiley-Blackwell, 2005:1-8.
22. Ceradini DJ, Gurtner GC. Homing to hypoxia: HIF-1 as a mediator of progenitor cell recruitment to injured tissue. Trends Cardiovasc Med. 2005;15:57-63.
23. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10:858-864.
24. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med. 2003;9:702-712.
25. Potier E, Ferreira E, Andriamanalijaona R, Pujol JP, Oudina K, Logeart-Avramoglou D, Petite H. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone. 2007;40:1078-1087.
26. Sadat S, Gehmert S, Song YH, Yen YS, Bai XW, Gaiser S, Klein H, Alt E. The cardioprotective effect of mesenchymal stem cells is mediated by IGF-1 and VEGF. Biochem Biophys Res Commun. 2007;363:674-679.
27. Xu MF, Uemura R, Dai Y, Wang YG, Pasha Z, Ashraf M. In vitro and in vivo effects of bone marrow stem cells on cardiac structure and function. J Mol Cell Cardiol. 2007;42:441-448.
28. Gnecchi M, He HM, Noiseux N, Liang OD, Zhang LM, Mo-rello F, Mu H, Melo LG, Pratt RE, Ingwall JS, Dzau VJ. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J. 2006;20:661-669.
29. Patel KM, Crisostomo P, Lahm T, Markel T, Herring C, Wang M, Meldrum KK, Lillemoe KD, Meldrum DR. Mesenchymal stem cells attenuate hypoxic pulmonary vasoconstriction by a paracrine mechanism. J Surg Res. 2007;143:281-285.
30. Brunelle JK, Bell EL, Quesada NM, Vercauteren K, Tiranti V, Zeviani M, Scarpulla RC, Chandel NS. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metabol. 2005;1:409-414.
31. Mansfield KD, Guzy RD, Pan Y, Young RM, Cash TP, Schu-macker PT, Simon MC. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metabol. 2005;1:393-399.
32. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell. 2007;129:465-472.
33. Schofield R. Relationship between spleen colony-forming cell and hematopoietic stem-cell-hypothesis. Blood Cell. 1978;4:7-25.
34. Fischer B, Bavister BD. Oxygen-tension in the oviduct and uterus of Rhesus-monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99:673-679.
35. Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early-preganancy. Obstet Gynecol. 1992;80:283-285.
36. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ, Regulation of human placental development by oxygen tension. Science. 1997;277:1669-1672.
37. Weiss L. Hematopoietic microenvironment of bone-marrow-ultrastructural- study of stroma in rats. Anat Rec. 1976;186:161-184.
38. Lord BI. The architecture of bone-marrow cell-populations. Int J Cell Cloning. 1990;8:317-331.
39. Cipolleschi MG, Dellosbarba P, Olivotto M. The role of hypoxia in the maintenance of hematopoietic stem-cells. Blood. 1993;82:2031-2037.
40. 2, and pressure studied in dogs. Acta Orthop Scand. 1985;56:400-403.
41. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA. 2007;104: 5431-5436.
42. 2 distributions in the bone marrow hematopoietic compartment. I. Krogh's model. Biophys J. 2001;81:675-684.
43. Bradley TR, Hodgson GS, Rosendaal M. Effect of oxygen-tension on hematopoietic and fibroblast cell-proliferation in vitro. J Cell Physiol. 1978;97:517-522.
44. Katahira J, Mizoguchi H. Improvement of culture conditions for human megakaryocytic and pluripotent progenitor cells by low oxygen-tension. Int J Cell Cloning. 1987;5:412-420.
45. Koller MR, Bender JG, Miller WM, Papoutsakis ET. Reduced oxygen-tension increases hematopoiesis in long-term culture of human stem and progenitor cells from cord blood and bone-marrow. Exp Hematol. 1992;20:264-270.
46. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211-228.
47. Fraser JK, Wulur I, Alfonso Z, Hedrick MH. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol. 2006;24:150-154.
48. Scherberich A, Galli R, Jaquiery C, Farhadi J, Martin I. Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cell. 2007;25:1823-1829.
49. 2) muscle tissue as determined by in murine fatty and EPR. Magn Reson Med. 2005;54:1530-1535.
50. Ezashi T, Das P, Roberts RM. Low O-2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA. 2005;102:4783-4788.
51. Kurosawa H, Kimura M, Noda T, Amano Y, Effect of oxygen on in vitro differentiation of mouse embryonic stem cells. J Bio-sci Bioeng. 2006;101:26-30.
52. Gassmann M, Fandrey J, Bichet S, Wartenberg M, Marti HH, Bauer C, Wenger RH, Acker H. Oxygen supply and oxygen-dependent gene expression in differentiating embryonic stem cells. Proc Natl Acad Sci USA. 1996;93:2867-2872.
53. Thompson JGE, Simpson AC, Pugh PA, Donnelly PE, Tervit HR. Effect of oxygen concentration on in vitro development of preimplantation sheep and cattle embryos. J Reprod Fertil. 1990;89:573-578.
54. Nakao H, Nakatsuji N. Effects of coculture, medium components and gas-phase on in vitro culture of in vitro matured and in vitro fertilized bovine embryos. Theriogenology. 1990;33: 591-600.
55. Harvey AJ, Kind KL, Pantaleon M, Armstrong DT, Thompson JG. Oxygen-regulated gene expression in bovine blastocysts. Biol Reprod. 2004;71:1108-1119.
56. Li JM, Foote RH. Culture of rabbit zygotes into blastocysts in protein-free medium with one to 20 per cent oxygen. J Reprod Fertil. 1993;98:163-167.
57. Umaoka Y, Noda Y, Narimoto K, Mori T. Effects of oxygen-toxicity on early development of mouse embryos. Mol Reprod Dev. 1992;31:28-33.
58. Catt JW, Henman M. Toxic effects of oxygen on human embryo development. Hum Reprod. 2000;15 (Suppl 2):199-206.
59. Wang FN, Thirumangalathu S, Loeken MR. Establishment of new mouse embryonic stem cell lines is improved by physiological glucose and oxygen. Cloning Stem Cell. 2006;8:108-116.
60. Forsyth NR, Musio A, Vezzoni P, Simpson A, Noble BS, McWhir J. Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities. Cloning Stem Cell. 2006;8:16-23.
61. Grayson WL, Zhao, F, Bunnell B, Ma T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun. 2007;358:948-953.
62. Bauwens C, Yin T, Dang S, Peerani R, Zandstra PW. Development of a perfusion fed bioreactor for embryonic stem cell-derived cardiomyocyte generation: oxygen-mediated enhancement of cardiomyocyte output. Biotechnol Bioeng. 2005;90: 452-461.
63. Lennon DP, Edmison JM, Caplan AI. Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: effects on in vitro and in vivo osteochondrogenesis. J Cell Physiol. 2001;187:345-355.
64. Grayson WL, Zhao F, Izadpanah R, Bunnell B, Ma T. Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J Cell Physiol. 2006;207:331-339.
65. Martin-Rendon E, Hale SJM, Ryan D, Baban D, Forde SP, Rou-belakis M, Sweeney D, Moukayed M, Harris AL, Davies K, Watt SM. Transcriptional profiling of human cord blood CD133(+) and cultured bone marrow mesenchymal stem cells in response to hypoxia. Stem Cell. 2007;25:1003-1012.
66. Ren HY, Cao Y, Zhao QJ, Li J, Zhou CX, Liao LM, Jia MY, Zhao Q, Cai HG, Han ZC, Yang RC, Chen GQ, Zhao RCH. Proliferation and differentiation of bone marrow stromal cells under hypoxic conditions. Biochem Biophys Res Commun. 2006;347:12-21.
67. Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, Gully C, Gassner R, Lepperdinger G. Reduced oxygen tension attenuates differentiation capacity of human mesen-chymal stem cells and prolongs their lifespan. Aging Cell. 2007;6:745-757.
68. Buravkova LB, Anokhina EB. Effect of hypoxia on stromal precursors from rat bone marrow at the early stage of culturing. Bull Exp Biol Med. 2007;143:411-413.
69. D'Ippolito G, Diabira S, Howard GA, Roos BA, Schiller PC. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone. 2006;39:513-522.
70. D'Ippolito G, Diabira S, Howard, GA, Menei P, Roos BA, Schiller PC. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci. 2004;117:2971-2981.
71. Annabi B, Lee YT, Turcotte S, Naud E, Desrosiers RR, Champagne M, Eliopoulos N, Galipeau J, Beliveau R. Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Stem Cell. 2003;21:337-347.
72. Robins JC, Akeno N, Mukherjee A, Dalal RR, Aronow BJ, Koopman P, Clemens TL. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with tran-scriptional activation of Sox9. Bone. 2005;37:313-322.
73. Fink T, Abildtrup L, Fogd K, Abdallah BM, Kassem M, Ebbe-sen P, Zachar V. Induction of adipocyte-like phenotype in human mesenchymal stem cells by hypoxia. Stem Cell. 2004;22: 1346-1355.
74. Wang DW, Fermor B, Gimble JM, Awad HA, Guilak F. Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J Cell Physiol. 2005;204:184-191.
75. Lee JH, Kemp DM. Human adipose-derived stem cells display myogenic potential and perturbed function in hypoxic conditions. Biochem Biophys Res Commun. 2006;341:882-888.
76. Khan WS, Adesida AB, Hardingham TE. Hypoxic conditions increase hypoxia-inducible transcription factor 2 alpha and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res Ther. 2007;9:R55.
77. Betre H, Ong SR, Guilak F, Chilkoti A, Fermor B, Setton LA. Chondrocytic differentiation of human adipose-derived adult stem cells in elastin-like polypeptide. Biomaterials. 2006;27:91-99.
78. Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT. Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol. 2006;290:C1139-C1145.
79. Xu Y, Malladi P, Chiou M, Bekerman E, Giaccia AJ, Longaker MT. In vitro expansion of adipose-derived adult stromal cells in hypoxia enhances early chondrogenesis. Tissue Eng. 2007;13: 2981-2993.
80. Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT. Hypoxia inducible factor-1 alpha deficiency affects chondrogenesis of adipose-derived adult stromal cells. Tissue Eng. 2007;13:1159-1171.
81. Sengers BG, Taylor M, Please CP, Oreffo ROC. Computational modeling of cell spreading and tissue regeneration in porous scaffolds. Biomaterials. 2007;13:1926-1940.
82. Galban CJ, Locke BR. Analysis of cell growth kinetics and substrate diffusion in a polymer scaffold. Biotechnol Bioeng. 1999; 65:121-132.
83. Zhao F, Pathi P, Grayson W, Xing Q, Locke BR, Ma T. Effects of oxygen transport on 3-D human mesenchymal stem cell metabolic activity in perfusion and static cultures: experiments and mathematical model. Biotechnol Prog. 2005;21: 1269-1280.
84. Guaccio A, Borselli C, Oliviero O, Netti PA. Oxygen con sumption of chondrocytes in agarose and collagen gels: a comparative analysis. Biomaterials. 2008;29:1484-1493.
85. Malda J, Rouwkema J, Martens DE, le Comte EP, Kooy FK, Tramper J, van Blitterswijk CA, Riesle J. Oxygen gradients in tissue-engineered PEGT/PBT cartilaginous constructs: measurement and modeling. Biotechnol Bioeng. 2004;86:9-18.
86. Cukierman E, Pankov R, Yamada KM. Cell interactions with three-dimensional matrices. Curr Opin Cell Biol. 2002;14:633-639.
87. Yamada KM, Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell. 2007;130:601-610.
88. Grayson WL, Ma T, Bunnell B. Human mesenchymal stem cells tissue development in 3D PET matrices. Biotechnol Prog. 2004;20:905-912.
89. Kronenberg HM. Developmental regulation of the growth plate. Nature. 2003;423:332-336.
90. Rivron NC, Liu JJ, Rouwkema J, de Boer J, van Blitterswijk CA. Engineering vascularised tissues in vitro. Eur Cell Mater. 2008;15:27-40.
91. Richardson TP, Peters MC, Ennett AB, Mooney DJ. Polymeric system for dual growth factor delivery. Nat Biotechnol. 2001; 19:1029-1034.
92. Hung SC, Pochampally RR Chen SC, Hsu SC, Prockop DJ. Angiogenic effects of human multipotent stromal cell conditioned medium activate the P13K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis. Stem Cell. 2007;25:2363-2370.
93. Cheema U, Brown RA, Alp B, MacRobert AJ. Spatially defined oxygen gradients and vascular endothelial growth factor expression in an engineered 3D cell model. Cell Mol Life Sci. 2008; 65:177-186.
94. Matthews TJW, Smith SR, Peach CA, Rees JL, Urban JPG, Carr AJ. In vivo measurement of tissue metabolism in tendons of the rotator cuff -implications for surgical management. J Bone Joint Surg Br. 2007;89B:633-638.
95. Park J, Bansal T, Pinelis M, Maharbiz MM. A microsystem for sensing and patterning oxidative microgradients during cell culture. Lab on a Chip. 2006;6:611-622.
96. Butt OI, Carruth R, Kutala VK, Kuppusamy P, Moldovan NI. Stimulation of peri-implant vascularization with bone marrow-derived progenitor cells: monitoring by in vivo EPR oximetry. Tissue Eng. 2007;13:2053-2061.
97. King JA, Miller WM. Bioreactor development for stem cell expansion and controlled differentiation. Curr Opin Chem Biol. 2007;11:394-398.