Low-oxygen culture conditions extend the multipotent properties of human retinal progenitor cells

Tissue Engineering - Part A

Volumn 20, Issue 9-10, 2014, Pages 1465-1475

  Baranov, Petr Y ^a   Tucker, Budd A ^a,b   Young, Michael J ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; OPHTHALMOLOGY;

CELL-BASED THERAPY; CULTURE CONDITIONS; DIFFERENTIATION MARKERS; FIELD DEVELOPMENT; POTENTIAL SOURCES; PROLIFERATION AND APOPTOSIS; PROLIFERATION RATE; TELOMERASE ACTIVITY;

OXYGEN;

CYCLIN D1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; KI 67 ANTIGEN; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; OXYGEN; PROTEIN P53; RECOVERIN; TELOMERASE; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL METABOLISM; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; ENZYME ACTIVITY; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; NERVE CELL; OXYGEN TENSION; PHOTORECEPTOR; PHOTORECEPTOR OUTER SEGMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; RETINA CELL; RETINA NEUROEPITHELIAL LAYER; STEM CELL; UPREGULATION; BATCH CELL CULTURE; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; METABOLISM; MULTIPOTENT STEM CELL; PHYSIOLOGY; PROCEDURES; RETINA NERVE CELL; TISSUE ENGINEERING;

BATCH CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; HUMANS; MULTIPOTENT STEM CELLS; OXYGEN; RETINAL NEURONS; TISSUE ENGINEERING;

EID: 84899837855     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0361     Document Type: Article

References (80)

1. Schmitt, S.G., Aftab, U., Jiang, C., et al. Molecular characterization of human retinal progenitor cells. Invest Ophthalmol Vis Sci 50, 5901, 2009.
2. Aftab, U., Jiang, C., Tucker, B., et al. Growth kinetics and transplantation of human retinal progenitor cells. Exp Eye Res 89, 301, 2009.
3. Hasan, S.M., Vugler, A.A., Miljan, E.A., et al. Immortalised human foetal retinal cells retain progenitor characteristics and represent a potential source for the treatment of retinal degenerative disease. Cell Transplant 19, 1291, 2010.
4. Otteson, D.C., and Phillips, M.J. A conditional immortalized mouse Muller glial cell line expressing glial and retinal stem-cell genes. Invest Ophthalmol Vis Sci 51, 5991, 2010.
5. Marx, M., Lebuhotel, C., Laugier, D., et al. Down regulation of pRb in cultures of avian neuroretina cells promotes proliferation of reactive Muller-like cells and emergence of retinal stem/progenitors. Exp Eye Res 90, 791, 2010.
6. Santilli, G., Lamorte, G., Carlessi, L., et al. Mild hypoxia enhances proliferation and multipotency of human neural stem cells. PLoS One 5, e8575, 2010.
7. Xiong, L., Zhao, T., Huang, X., et al. Heat shock protein 90 is involved in regulation of hypoxia-driven proliferation of embryonic neural stem/progenitor cells. Cell Stress Chaperones 14, 183, 2009.
8. Sims, J.R., Lee, S.W., Topalkara, K., et al. Sonic hedgehog regulates ischemia/hypoxia-induced neural progenitor proliferation. Stroke 40, 3618, 2009.
9. Clarke, L., and van der Kooy, D. Low oxygen enhances primitive and definitive neural stem cell colony formation by inhibiting distinct cell death pathways. Stem Cells 27, 1879, 2009.
10. Zhao, T., Zhang, C.P., Liu, Z.H., et al. Hypoxia-driven proliferation of embryonic neural stem/progenitor cells-role of hypoxia-inducible transcription factor-1alpha. FEBS J 275, 1824, 2008.
11. Horie, N., So, K., Moriya, T., et al. Effects of oxygen concentration on the proliferation and differentiation of mouse neural stem cells in vitro. Cell Mol Neurobiol 28, 833, 2008.
12. Zhang, C.P., Zhu, L.L., Zhao, T., et al. Characteristics of neural stem cells expanded in lowered oxygen and the potential role of hypoxia-inducible factor-1Alpha. Neurosignals 15, 259, 2006.
13. Zhu, L.L., Wu, L.Y., Yew, D.T., et al. Effects of hypoxia on the proliferation and differentiation of NSCs. Mol Neurobiol 31, 231, 2005.
14. Studer, L., Csete, M., Lee, S.H., et al. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 20, 7377, 2000.
15. Panchision, D.M. The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 220, 562, 2009.
16. D'Ippolito, G., Diabira, S., Howard, G.A., et al. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 39, 513, 2006.
17. Lennon, D.P., Edmison, J.M., and Caplan, A.I. 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, 2001.
18. Ivanovic, Z., Bartolozzi, B., Bernabei, P.A., et al. Incubation of murine bone marrow cells in hypoxia ensures the maintenance of marrow-repopulating ability together with the expansion of committed progenitors. Br J Haematol 108, 424, 2000.
19. Miyashita, H., Higa, K., Kato, N., et al. Hypoxia enhances the expansion of human limbal epithelial progenitor cells in vitro. Invest Ophthalmol Vis Sci 48, 3586, 2007.
20. Forristal, C.E., Wright, K.L., Hanley, N.A., et al. Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139, 85, 2010.
21. Silvan, U., Diez-Torre, A., Arluzea, J., et al. Hypoxia and pluripotency in embryonic and embryonal carcinoma stem cell biology. Differentiation 78, 159, 2009.
22. Theus, M.H., Wei, L., Cui, L., et al. In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp Neurol 210, 656, 2008.
23. Prasad, S.M., Czepiel, M., Cetinkaya, C., et al. Continuous hypoxic culturing maintains activation of Notch and allows long-term propagation of human embryonic stem cells without spontaneous differentiation. Cell Prolif 42, 63, 2009.
24. Meininger, C.J., Schelling, M.E., and Granger, H.J. Adenosine and hypoxia stimulate proliferation and migration of endothelial cells. Am J Physiol 255, H554, 1988.
25. Yu, D.Y., and Cringle, S.J. Oxygen distribution in the mouse retina. Invest Ophthalmol Vis Sci 47, 1109, 2006.
26. Cringle, S.J., Yu, P.K., Su, E.N., et al. Oxygen distribution and consumption in the developing rat retina. Invest Ophthalmol Vis Sci 47, 4072, 2006.
27. Kelley, M.W., Turner, J.K., and Reh, T.A. Regulation of proliferation and photoreceptor differentiation in fetal human retinal cell cultures. Invest Ophthalmol Vis Sci 36, 1280, 1995.
28. Wiesener, M.S., Jurgensen, J.S., Rosenberger, C., et al. Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J 17, 271, 2003.
29. Hu, C.J., Wang, L.Y., Chodosh, L.A., et al. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 23, 9361, 2003.
30. Erler, J.T., Bennewith, K.L., Nicolau, M., et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440, 1222, 2006.
31. Wang, V., Davis, D.A., Haque, M., et al. Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res 65, 3299, 2005.
32. Klassen, H.J., Ng, T.F., Kurimoto, Y., et al. Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Invest Ophthalmol Vis Sci 45, 4167, 2004.
33. Klassen, H., Ziaeian, B., Kirov, II, et al. Isolation of retinal progenitor cells from post-mortem human tissue and comparison with autologous brain progenitors. J Neurosci Res 77, 334, 2004.
34. Klassen, H., Kiilgaard, J.F., Zahir, T., et al. Progenitor cells from the porcine neural retina express photoreceptor markers after transplantation to the subretinal space of allorecipients. Stem Cells 25, 1222, 2007.
35. Yang, P., Seiler, M.J., Aramant, R.B., et al. In vitro isolation and expansion of human retinal progenitor cells. Exp Neurol 177, 326, 2002.
36. Bozanic, D., and Saraga-Babic, M. Cell proliferation during the early stages of human eye development. Anat Embryol (Berl) 208, 381, 2004.
37. Smirnov, E.B., and Puchkov, V.F. Characteristics of cellular proliferation in the developing human retina. Neurosci Behav Physiol 34, 643, 2004.
38. Esteban, M.A., Tran, M.G., Harten, S.K., et al. Regulation of E-cadherin expression by VHL and hypoxia-inducible factor. Cancer Res 66, 3567, 2006.
39. Lash, G.E., Fitzpatrick, T.E., and Graham, C.H. Effect of hypoxia on cellular adhesion to vitronectin and fibronectin. Biochem Biophys Res Commun 287, 622, 2001.
40. Moreno-Manzano, V., Rodriguez-Jimenez, F.J., Acena-Bonilla, J.L., et al. FM19G11, a new hypoxia-inducible factor (HIF) modulator, affects stem cell differentiation status. J Biol Chem 285, 1333, 2010.
41. Covello, K.L., Kehler, J., Yu, H., et al. HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20, 557, 2006.
42. Revoltella, R.P., Papini, S., Rosellini, A., et al. Epithelial stem cells of the eye surface. Cell Prolif 40, 445, 2007.
43. Barbaro, V., Testa, A., Di Iorio, E., et al. C/EBPdelta regulates cell cycle and self-renewal of human limbal stem cells. J Cell Biol 177, 1037, 2007.
44. Joyce, N.C., Meklir, B., Joyce, S.J., et al. Cell cycle protein expression and proliferative status in human corneal cells. Invest Ophthalmol Vis Sci 37, 645, 1996.
45. Chen, D., Li, M., Luo, J., et al. Direct interactions between HIF-1 alpha and Mdm2 modulate p53 function. J Biol Chem 278, 13595, 2003.
46. An, W.G., Kanekal, M., Simon, M.C., et al. Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature 392, 405, 1998.
47. Fels, D.R., and Koumenis, C. HIF-1alpha and p53: the ODD couple? Trends Biochem Sci 30, 426, 2005.
48. Goda, N., Ryan, H.E., Khadivi, B., et al. Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol Cell Biol 23, 359, 2003.
49. Gardner, L.B., Li, Q., Park, M.S., et al. Hypoxia inhibits G1/S transition through regulation of p27 expression. J Biol Chem 276, 7919, 2001.
50. Carmeliet, P., Dor, Y., Herbert, J.M., et al. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394, 485, 1998.
51. Regatieri, C.V., Baranov, P., Carvalho, A., et al. Pre differentiated human retinal progenitor cells integrate and express mature markers on the host retina. ARVO. FT Lauderdale, Florida, 2012:1128/A1593.
52. Siren, A.L., Fratelli, M., Brines, M., et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci USA 98, 4044, 2001.
53. Siren, A.L., and Ehrenreich, H. Erythropoietin-a novel concept for neuroprotection. Eur Arch Psychiatry Clin Neurosci 251, 179, 2001.
54. Siren, A.L., Knerlich, F., Poser, W., et al. Erythropoietin and erythropoietin receptor in human ischemic/hypoxic brain. Acta Neuropathol 101, 271, 2001.
55. Dai, T., Zheng, H., and Fu, G.S. Hypoxia confers protection against apoptosis via the PI3K/Akt pathway in endothelial progenitor cells. Acta Pharmacol Sin 29, 1425, 2008.
56. Tong, Q., Zheng, L., Li, B., et al. Hypoxia-induced mitogenic factor enhances angiogenesis by promoting proliferation and migration of endothelial cells. Exp Cell Res 312, 3559, 2006.
57. Oki, M., and Ando, K. [Hematopoietic growth factors, cytokines, and bone-marrow microenvironment]. Nippon Rinsho 66, 444, 2008.
58. Pedersen, M., Lofstedt, T., Sun, J., et al. Stem cell factor induces HIF-1alpha at normoxia in hematopoietic cells. Biochem Biophys Res Commun 377, 98, 2008.
59. Han, Z.B., Ren, H., Zhao, H., et al. Hypoxia-inducible factor (HIF)-1 alpha directly enhances the transcriptional activity of stem cell factor (SCF) in response to hypoxia and epidermal growth factor (EGF). Carcinogenesis 29, 1853, 2008.
60. Comerford, K.M., Wallace, T.J., Karhausen, J., et al. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res 62, 3387, 2002.
61. Krishnamurthy, P., Ross, D.D., Nakanishi, T., et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 279, 24218, 2004.
62. Martin, C.M., Ferdous, A., Gallardo, T., et al. Hypoxiainducible factor-2alpha transactivates Abcg2 and promotes cytoprotection in cardiac side population cells. Circ Res 102, 1075, 2008.
63. Semenza, G.L. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15, 551, 1999.
64. Grimm, C., Wenzel, A., Groszer, M., et al. HIF-1-induced erythropoietin in the hypoxic retina protects against lightinduced retinal degeneration. Nat Med 8, 718, 2002.
65. Grimm, C., Hermann, D.M., Bogdanova, A., et al. Neuroprotection by hypoxic preconditioning: HIF-1 and erythropoietin protect from retinal degeneration. Semin Cell Dev Biol 16, 531, 2005.
66. Grimm, C., Wenzel, A., Acar, N., et al. Hypoxic preconditioning and erythropoietin protect retinal neurons from degeneration. Adv Exp Med Biol 588, 119, 2006.
67. Nishi, H., Nakada, T., Kyo, S., et al. Hypoxia-inducible factor 1 mediates upregulation of telomerase (hTERT). Mol Cell Biol 24, 6076, 2004.
68. Pugh, C.W., Tan, C.C., Jones, R.W., et al. Functional analysis of an oxygen-regulated transcriptional enhancer lying 3¢ to the mouse erythropoietin gene. Proc Natl Acad Sci USA 88, 10553, 1991.
69. Westfall, S.D., Sachdev, S., Das, P., et al. Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells. Stem Cells Dev 17, 869, 2008.
70. Prado-Lopez, S., Conesa, A., Arminan, A., et al. Hypoxia promotes efficient differentiation of human embryonic stem cells to functional endothelium. Stem Cells 28, 407, 2010.
71. Forristal, C.E., Wright, K.L., Hanley, N.A., et al. Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139, 85, 2010.
72. Millman, J.R., Tan, J.H., and Colton, C.K. The effects of low oxygen on self-renewal and differentiation of embryonic stem cells. Curr Opin Organ Transplant 14, 694, 2009.
73. Gordan, J.D., Thompson, C.B., and Simon, M.C. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 12, 108, 2007.
74. Gordan, J.D., Bertout, J.A., Hu, C.J., et al. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 11, 335, 2007.
75. Wu, L.Y., Wang, Y., Jin, B., et al. The role of hypoxia in the differentiation of P19 embryonal carcinoma cells into dopaminergic neurons. Neurochem Res 33, 2118, 2008.
76. Ezashi, T., Das, P., and Roberts, R.M. Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 102, 4783, 2005.
77. Jiang, M., Wang, C.Q., Wang, B.Y., et al. [Inhibitory effect of siRNA targeting HIF-1alpha on differentiation of peripheral blood endothelial progenitor cells]. Ai Zheng 24, 1293, 2005.
78. Gustafsson, M.V., Zheng, X., Pereira, T., et al. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9, 617, 2005.
79. Cejudo-Martin, P., and Johnson, R.S. A new notch in the HIF belt: how hypoxia impacts differentiation. Dev Cell 9, 575, 2005.
80. Khan, W.S., Adesida, A.B., and Hardingham, T.E. Hypoxic conditions increase hypoxia-inducible transcription factor 2alpha and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res Ther 9, R55, 2007.