Hypoxic priming of mESCs accelerates vascular-lineage differentiation through HIF1-mediated inverse regulation of Oct4 and VEGF

EMBO Molecular Medicine

Volumn 4, Issue 9, 2012, Pages 924-938

  Lee, Sae Won ^a   Jeong, Han Kyul ^a   Lee, Ji Young ^a   Yang, Jimin ^a   Lee, Eun Ju ^a   Kim, Su Yeon ^a   Youn, Seock Won ^a   Lee, Jaewon ^a   Kim, Woo Jean ^b   Kim, Kyu Won ^c   Lim, Jeong Mook ^d   Park, Jong Wan ^e   Park, Young Bae ^a   Kim, Hyo Soo ^a,c  

^a Seoul National University Hospital   (South Korea)

^b Inha University School of Medicine   (South Korea)

^c Seoul National University   (South Korea)

^d Seoul National University   (South Korea)

^e Seoul National University College of Medicine   (South Korea)

Author keywords

Embryoid bodies; Endothelial cells; Mesoderm differentiation; Mouse embryonic stem cells; Niche

Indexed keywords

CADHERIN; HYPOXIA INDUCIBLE FACTOR 1; LECTIN; OCTAMER TRANSCRIPTION FACTOR 4; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; ENDODERM; ENDOTHELIUM CELL; IN VIVO STUDY; LIMB ISCHEMIA; MALE; MESODERM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SMOOTH MUSCLE FIBER; SPHEROID CELL; STEM CELL TRANSPLANTATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; ANOXIA; BASE SEQUENCE; CELL DIFFERENTIATION; DOWN-REGULATION; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; OCTAMER TRANSCRIPTION FACTOR-3; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84865798238     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201101107     Document Type: Article

References (50)

1. Acker T, Diez-Juan A, Aragones J, Tjwa M, Brusselmans K, Moons L, Fukumura D, Moreno-Murciano MP, Herbert JM, Burger A, et al (2005) Genetic evidence for a tumor suppressor role of HIF-2alpha. Cancer Cell 8: 131-141.
2. Arteel GE, Thurman RG, Yates JM, Raleigh JA (1995) Evidence that hypoxia markers detect oxygen gradients in liver: pimonidazole and retrograde perfusion of rat liver. Br J Cancer 72: 889-895.
3. Ateghang B, Wartenberg M, Gassmann M, Sauer H (2006) Regulation of cardiotrophin-1 expression in mouse embryonic stem cells by HIF-1alpha and intracellular reactive oxygen species. J Cell Sci 119: 1043-1052.
4. Berthelemy N, Kerdjoudj H, Schaaf P, Prin-Mathieu C, Lacolley P, Stoltz JF, Voegel JC, Menu P (2009) O2 level controls hematopoietic circulating progenitor cells differentiation into endothelial or smooth muscle cells. PLoS One 4: e5514.
5. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
6. Bussolati B, Grange C, Sapino A, Camussi G (2009) Endothelial cell differentiation of human breast tumour stem/progenitor cells. J Cell Mol Med 13: 309-319.
7. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, et al (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.
8. Cascio S, Bartella V, Auriemma A, Johannes GJ, Russo A, Giordano A, Surmacz E (2008) Mechanism of leptin expression in breast cancer cells: role of hypoxia-inducible factor-1alpha. Oncogene 27: 540-547.
9. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ, Labosky PA, Simon MC, Keith B (2006) HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20: 557-570.
10. Davy P, Allsopp R (2011) Hypoxia: are stem cells in it for the long run? Cell Cycle 10: 206-211.
11. Ezashi T, Das P, Roberts RM (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 102: 4783-4788.
12. Francis KR, Wei L (2010) Human embryonic stem cell neural differentiation and enhanced cell survival promoted by hypoxic preconditioning. Cell Death Dis 1: e22.
13. Gidekel S, Pizov G, Bergman Y, Pikarsky E (2003) Oct-3/4 is a dose-dependent oncogenic fate determinant. Cancer Cell 4: 361-370.
14. Heddleston JM, Li Z, McLendon RE, Hjelmeland AB, Rich JN (2009) The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 8: 3274-3284.
15. Hochedlinger K, Yamada Y, Beard C, Jaenisch R (2005) Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121: 465-477.
16. Itskovitz-Eldor J, Schuldiner M, Karsenti D, Eden A, Yanuka O, Amit M, Soreq H, Benvenisty N (2000) Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med 6: 88-95.
17. Jogi A, Ora I, Nilsson H, Lindeheim A, Makino Y, Poellinger L, Axelson H, Pahlman S (2002) Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc Natl Acad Sci USA 99: 7021-7026.
18. Keith B, Simon MC (2007) Hypoxia-inducible factors, stem cells, and cancer. Cell 129: 465-472.
19. Koay EJ, Athanasiou KA (2008) Hypoxic chondrogenic differentiation of human embryonic stem cells enhances cartilage protein synthesis and biomechanical functionality. Osteoarthritis Cartilage 16: 1450-1456.
20. Kouskoff V, Lacaud G, Schwantz S, Fehling HJ, Keller G (2005) Sequential development of hematopoietic and cardiac mesoderm during embryonic stem cell differentiation. Proc Natl Acad Sci USA 102: 13170-13175.
21. Lee SW, Kim WJ, Choi YK, Song HS, Son MJ, Gelman IH, Kim YJ, Kim KW (2003) SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat Med 9: 900-906.
22. Lee SW, Youn SW, Kim TY, Suh JW, Koh GY, Kwon YW, Chae IH, Park YB, Kim HS (2009) Angiopoietin-1 protects endothelial cells from hypoxia-induced apoptosis via inhibition of phosphatase and tensin homologue deleted from chromosome ten. Korean Circ J 39: 57-65.
23. Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC (1997) Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386: 403-407.
24. Maltepe E, Simon MC (1998) Oxygen, genes, and development: an analysis of the role of hypoxic gene regulation during murine vascular development. J Mol Med 76: 391-401.
25. Mazure NM, Chauvet C, Bois-Joyeux B, Bernard MA, Nacer-Cherif H, Danan JL (2002) Repression of alpha-fetoprotein gene expression under hypoxic conditions in human hepatoma cells: characterization of a negative hypoxia response element that mediates opposite effects of hypoxia inducible factor-1 and c-Myc. Cancer Res 62: 1158-1165.
26. Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7: 150-161.
27. Narravula S, Colgan SP (2001) Hypoxia-inducible factor 1-mediated inhibition of peroxisome proliferator-activated receptor alpha expression during hypoxia. J Immunol 166: 7543-7548.
28. Ng KM, Lee YK, Chan YC, Lai WH, Fung ML, Li RA, Siu CW, Tse HF (2010) Exogenous expression of HIF-1 alpha promotes cardiac differentiation of embryonic stem cells. J Mol Cell Cardiol 48: 1129-1137.
29. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379-391.
30. Niebruegge S, Bauwens CL, Peerani R, Thavandiran N, Masse S, Sevaptisidis E, Nanthakumar K, Woodhouse K, Husain M, Kumacheva E, et al (2009) Generation of human embryonic stem cell-derived mesoderm and cardiac cells using size-specified aggregates in an oxygen-controlled bioreactor. Biotechnol Bioeng 102: 493-507.
31. Niwa H, Miyazaki J, Smith AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24: 372-376.
32. Nordhoff V, Hubner K, Bauer A, Orlova I, Malapetsa A, Scholer HR (2001) Comparative analysis of human, bovine, and murine Oct-4 upstream promoter sequences. Mamm Genome 12: 309-317.
33. Nourse MB, Halpin DE, Scatena M, Mortisen DJ, Tulloch NL, Hauch KD, Torok-Storb B, Ratner BD, Pabon L, Murry CE (2010) VEGF induces differentiation of functional endothelium from human embryonic stem cells: implications for tissue engineering. Arterioscler Thromb Vasc Biol 30: 80-89.
34. Ohlstein B, Kai T, Decotto E, Spradling A (2004) The stem cell niche: theme and variations. Curr Opin Cell Biol 16: 693-699.
35. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling-in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371.
36. Ong LL, Li W, Oldigs JK, Kaminski A, Gerstmayer B, Piechaczek C, Wagner W, Li RK, Ma N, Steinhoff G (2010) Hypoxic/normoxic preconditioning increases endothelial differentiation potential of human bone marrow CD133+ cells. Tissue Eng Part C Methods 16: 1069-1081.
37. Powers DE, Millman JR, Huang RB, Colton CK (2008) Effects of oxygen on mouse embryonic stem cell growth, phenotype retention, and cellular energetics. Biotechnol Bioeng 101: 241-254.
38. Purpura KA, George SH, Dang SM, Choi K, Nagy A, Zandstra PW (2008) Soluble Flt-1 regulates Flk-1 activation to control hematopoietic and endothelial development in an oxygen-responsive manner. Stem Cells 26: 2832-2842.
39. Ramirez-Bergeron DL, Runge A, Dahl KD, Fehling HJ, Keller G, Simon MC (2004) Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development 131: 4623-4634.
40. Ryan HE, Lo J, Johnson RS (1998) HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 17: 3005-3015.
41. Semenza GL (1999) Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15: 551-578.
42. Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
43. Tomita S, Ueno M, Sakamoto M, Kitahama Y, Ueki M, Maekawa N, Sakamoto H, Gassmann M, Kageyama R, Ueda N, et al (2003) Defective brain development in mice lacking the Hif-1alpha gene in neural cells. Mol Cell Biol 23: 6739-6749.
44. van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K, Demmers J, Chambers I, Poot RA (2010) An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6: 369-381.
45. Vittet D, Prandini MH, Berthier R, Schweitzer A, Martin-Sisteron H, Uzan G, Dejana E (1996) Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood 88: 3424-3431.
46. Wang M, Su Y, Sun H, Wang T, Yan G, Ran X, Wang F, Cheng T, Zou Z (2010) Induced endothelial differentiation of cells from a murine embryonic mesenchymal cell line C3H/10T1/2 by angiogenic factors in vitro. Differentiation 79: 21-30.
47. Warnecke C, Zaborowska Z, Kurreck J, Erdmann VA, Frei U, Wiesener M, Eckardt KU (2004) Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J 18: 1462-1464.
48. Yeo EJ, Chun YS, Cho YS, Kim J, Lee JC, Kim MS, Park JW (2003) YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1. J Natl Cancer Inst 95: 516-525.
49. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A (2008) The ground state of embryonic stem cell self-renewal. Nature 453: 519-523.
50. Yoshida Y, Takahashi K, Okita K, Ichisaka T, Yamanaka S (2009) Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell 5: 237-241.