Hypoxia induces pluripotency in primordial germ cells by HIF1α stabilization and Oct4 deregulation

Antioxidants and Redox Signaling

Volumn 22, Issue 3, 2015, Pages 205-223

  López Iglesias, Pilar ^a   Alcaina, Yago ^a   Tapia, Natalia ^b   Sabour, Davood ^b   Arauzo Bravo, Marcos J ^b   Sainz De La Maza, Diego ^a   Berra, Edurne ^c   O'Mara, Analia Nunez ^c   Nistal, Manuel ^a   Ortega, Sagrario ^d   Donovan, Peter J ^e,f,g   Schöler, Hans R ^b   De Miguel, Maria P ^a  

^a HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c CIC BIOGUNE   (Spain)

^d Structural Biology and Biocomputing Programme   (Spain)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^g BASQUE FOUNDATION FOR SCIENCE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; HIF1A PROTEIN, MOUSE; POU5F1 PROTEIN, MOUSE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL CULTURE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL METABOLISM; CELL RENEWAL; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; GENE OVEREXPRESSION; GERM LAYER; GLYCOLYSIS; IN VITRO STUDY; IN VIVO STUDY; INNER CELL MASS; METABOLIC REGULATION; MITOCHONDRION; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATIVE PHOSPHORYLATION; PLURIPOTENCY; PLURIPOTENT EMBRYONIC GERM CELL; PLURIPOTENT STEM CELL; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UNIPOTENT PRIMORDIAL GERM CELL; UPREGULATION; ANIMAL; C57BL MOUSE; CELL SURVIVAL; CYTOLOGY; FEMALE; GERM CELL; METABOLISM; PHYSIOLOGY; PROTEIN STABILITY; TRANSGENIC MOUSE;

ANIMALS; BLASTOCYST; CELL DIFFERENTIATION; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; FEMALE; GERM CELLS; GLYCOLYSIS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE, INBRED C57BL; MICE, TRANSGENIC; OCTAMER TRANSCRIPTION FACTOR-3; OXIDATIVE PHOSPHORYLATION; PLURIPOTENT STEM CELLS; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84921064232     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.5871     Document Type: Article

References (83)

1. Abad M, Mosteiro L, Pantoja C, Canamero M, Rayon T, Ors I, Grana O, Megias D, Dominguez O, Martinez D, Manzanares M, Ortega S, and Serrano M. Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502: 340-345, 2013.
2. Aoi T, Yae K, Nakagawa M, Ichisaka T, Okita K, Takahashi K, Chiba T, and Yamanaka S. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 321: 699-702, 2008.
3. Benizri E, Ginouves A, and Berra E. The magic of the hypoxiasignaling cascade. Cell Mol Life Sci 65: 1133-1149, 2008.
4. Boiani M, Eckardt S, Scholer HR, and McLaughlin KJ. Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev 16: 1209-1219, 2002.
5. Brahimi-Horn MC, Chiche J, and Pouyssegur J. Hypoxia signalling controls metabolic demand. Curr Opin Cell Biol 19: 223-229, 2007.
6. Brons IGM, Smithers LE, Trotter MWB, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, and Vallier L. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448: 191-195, 2007.
7. Buganim Y, Faddah DA, Cheng AW, Itskovich E, Markoulaki S, Ganz K, Klemm SL, van Oudenaarden A, and Jaenisch R. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150: 1209-1222, 2012.
8. Corn PG, Ricci MS, Scata KA, Arsham AM, Simon MC, Dicker DT, and El-Deiry WS. Mxi1 is induced by hypoxia in a HIF-1-dependent manner and protects cells from c-Myc-induced apoptosis. Cancer Biol Ther 4: 1285-1294, 2005.
9. Chen H-F, Kuo H-C, Lin S-P, Chien C-L, Chiang M-S, and Ho H-N. Hypoxic culture maintains self-renewal and enhances embryoid body formation of human embryonic stem cells. Tissue Eng Part A 16: 2901-2913, 2010.
10. Chu L-F, Surani MA, Jaenisch R, and Zwaka TP. Blimp1 expression predicts embryonic stem cell development in vitro. Curr Biol 21: 1759-1765, 2011.
11. Dang CV, Kim JW, Gao P, and Yustein J. The interplay between MYC and HIF in cancer. Nat Rev Cancer 8: 51-56, 2008.
12. De Felici M, Farini D, and Dolci S. In or out stemness: comparing growth factor signalling in mouse embryonic stem cells and primordial germ cells. Curr Stem Cell Res Ther 4: 87-97, 2009.
13. De Miguel MP, Cheng L, Holland EC, Federspiel MJ, and Donovan PJ. Dissection of the c-Kit signaling pathway in mouse primordial germ cells by retroviral-mediated gene transfer. Proc Natl Acad Sci USA 99: 10458-10463, 2002.
14. De Miguel MP and Donovan PJ. Isolation and culture of mouse germ cells. Methods Mol Biol 137: 403-408, 2000.
15. Dieguez-Hurtado R, Martin J, Martinez-Corral I, Martinez MD, Megias D, Olmeda D, and Ortega S. A Cre-reporter transgenic mouse expressing the far-red fluorescent protein Katushka. Genesis 49: 36-45, 2011.
16. Donovan PJ, de Miguel M, Cheng L, and Resnick JL. Primordial germ cells, stem cells and testicular cancer. APMIS 106: 134-141, 1998.
17. Donovan PJ and de Miguel MP. Turning germ cells into stem cells. Curr Opin Genet Dev 13: 463-471, 2003.
18. Donovan PJ, De Miguel MP, Hirano MP, Parsons MS, and Lincoln AJ. Germ cell biology-from generation to generation. Int J Dev Biol 45: 523-531, 2001.
19. Donovan PJ, Stott D, Cairns LA, Heasman J, and Wylie CC. Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44: 831-838, 1986.
20. Durcova-Hills G, Tang F, Doody G, Tooze R, and Surani MA. Reprogramming primordial germ cells into pluripotent stem cells. PLoS One 3:e3531, 2008.
21. Edgar R, Domrachev M, and Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210, 2002.
22. Eminli S, Utikal J, Arnold K, Jaenisch R, and Hochedlinger K. Reprogramming of neural progenitor cells into induced pluripotent stem cells in the absence of exogenous Sox2 expression. Stem Cells 26: 2467-2474, 2008.
23. Facucho-Oliveira JM and St. John JC. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 5: 140-158, 2009.
24. Folmes CDL, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ, Dzeja PP, Ikeda Y, Perez-Terzic C, and Terzic A. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 14: 264-271, 2011.
25. Forristal CE, Wright KL, Hanley NA, Oreffo RO, and Houghton FD. Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139: 85-97, 2010.
26. Golipour A, David L, Liu Y, Jayakumaran G, Hirsch CL, Trcka D, and Wrana JL. A late transition in somatic cell reprogramming requires regulators distinct from the pluripotency network. Cell Stem Cell 11: 769-782, 2012.
27. Guo G, Yang J, Nichols J, Hall JS, Eyres I, Mansfield W, and Smith A. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136: 1063-1069, 2009.
28. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, and Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9: 617-628, 2005.
29. Hammachi F, Morrison GM, Sharov AA, Livigni A, Narayan S, Papapetrou EP, O'Malley J, Kaji K, Ko MSH, Ptashne M, and Brickman JM. Transcriptional activation by Oct4 is sufficient for the maintenance and induction of pluripotency. Cell Rep 1: 99-109, 2012.
30. Hanna J, Markoulaki S, Schorderet P, Carey BW, Beard C, Wernig M, Creyghton MP, Steine EJ, Cassady JP, Foreman R, Lengner CJ, Dausman JA, and Jaenisch R. Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 133: 250-264, 2008.
31. Hu CJ, Iyer S, Sataur A, Covello KL, Chodosh LA, and Simon MC. Differential regulation of the transcriptional activities of hypoxia-inducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in stem cells. Mol Cell Biol 26: 3514-3526, 2006.
32. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, and Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15, 2003.
33. Jeong C-H, Lee H-J, Cha J-H, Kim JH, Kim KR, Kim J-H, Yoon D-K, and Kim K-W. Hypoxia-inducible factor-1 alpha inhibits self-renewal of mouse embryonic stem cells in vitro via negative regulation of the leukemia inhibitory factor-STAT3 pathway. J Biol Chem 282: 13672-13679, 2007.
34. Karwacki-Neisius V, Goke J, Osorno R, Halbritter F, Ng JH, Weisse AY, Wong FC, Gagliardi A, Mullin NP, Festuccia N, Colby D, Tomlinson SR, Ng HH, and Chambers I. Reduced Oct4 expression directs a robust pluripotent state with distinct signaling activity and increased enhancer occupancy by Oct4 and Nanog. Cell Stem Cell 12: 531-545, 2013.
35. Kawauchi K, Araki K, Tobiume K, and Tanaka N. p53 regulates glucose metabolism through an IKK-NF-kappaB pathway and inhibits cell transformation. Nat Cell Biol 10: 611-618, 2008.
36. Keith B and Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell 129: 465-472, 2007.
37. Kim JB, Sebastiano V, Wu G, Arauzo-Bravo MJ, Sasse P, Gentile L, Ko K, Ruau D, Ehrich M, van den Boom D, Meyer J, Hubner K, Bernemann C, Ortmeier C, Zenke M, Fleischmann BK, Zaehres H, and Scholer HR. Oct4-induced pluripotency in adult neural stem cells. Cell 136: 411-419, 2009.
38. Kimura T, Tomooka M, Yamano N, Murayama K, Matoba S, Umehara H, Kanai Y, and Nakano T. AKT signaling promotes derivation of embryonic germ cells from primordial germ cells. Development 135: 869-879, 2008.
39. Kishigami S, Wakayama S, Thuan NV, Ohta H, Mizutani E, Hikichi T, Bui H-T, Balbach S, Ogura A, Boiani M, and Wakayama T. Production of cloned mice by somatic cell nuclear transfer. Nat Protoc 1: 125-138, 2006.
40. Kondoh H, Lleonart ME, Gil J, Wang J, Degan P, Peters G, Martinez D, Carnero A, and Beach D. Glycolytic enzymes can modulate cellular life span. Cancer Res 65: 177-185, 2005.
41. Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M, Bernard D, Gil J, and Beach D. A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 9: 293-299, 2007.
42. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC, and Huang LE. HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 23: 1949-1956, 2004.
43. Koshikawa N, Hayashi J, Nakagawara A, and Takenaga K. Reactive oxygen species-generating mitochondrial DNA mutation up-regulates hypoxia-inducible factor-1alpha gene transcription via phosphatidylinositol 3-kinase-Akt/protein kinase C/histone deacetylase pathway. J Biol Chem 284: 33185-33194, 2009.
44. Labosky PA. Embryonic germ cell lines and their derivation from mouse primordial germ cells. Ciba Found Symp 182: 157-168, 1994.
45. Leitch HG, Blair K, Mansfield W, Ayetey H, Humphreys P, Nichols J, Surani MA, and Smith A. Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development 137: 2279-2287, 2010.
46. Li R, Liang J, Ni S, Zhou T, Qing X, Li H, He W, Chen J, Li F, Zhuang Q, Qin B, Xu J, Li W, Yang J, Gan Y, Qin D, Feng S, Song H, Yang D, Zhang B, Zeng L, Lai L, Esteban MA, and Pei D. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 7: 51-63, 2010.
47. Mali P, Ye Z, Hommond HH, Yu X, Lin J, Chen G, Zou J, and Cheng L. Improved efficiency and pace of generating induced pluripotent stem cells from human adult and fetal fibroblasts. Stem Cells 26: 1998-2005, 2008.
48. Mathieu J, Zhang Z, Nelson A, Lamba DA, Reh TA, Ware C, and Ruohola-Baker H. Hypoxia induces re-entry of committed cells into pluripotency. Stem Cells 31: 1737-1748, 2013.
49. Mathieu J, Zhou W, Xing Y, Sperber H, Ferreccio A, Agoston Z, Kuppusamy KT, Moon RT, and Ruohola-Baker H. Hypoxia-inducible factors have distinct and stagespecific roles during reprogramming of human cells to pluripotency. Cell Stem Cell 14: 592-605, 2014.
50. Matsui Y and Okamura D. Mechanisms of germ-cell specification in mouse embryos. Bioessays 27: 136-143, 2005.
51. Matsui Y, Zsebo K, and Hogan BL. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70: 841-847, 1992.
52. Niwa H, Miyazaki J, and Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24: 372-376, 2000.
53. Ohinata Y, Payer B, O'Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, and Surani MA. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436: 207-213, 2005.
54. Oikawa M, Abe M, Kurosawa H, Hida W, Shirato K, and Sato Y. Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem Biophys Res Commun 289: 39-43, 2001.
55. Panopoulos AD, Yanes O, Ruiz S, Kida YS, Diep D, Tautenhahn R, Herrerias A, Batchelder EM, Plongthongkum N, Lutz M, Berggren WT, Zhang K, Evans RM, Siuzdak G, and Izpisua Belmonte JC. The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Res 22: 168-177, 2012.
56. Polo JM, Anderssen E, Walsh RM, Schwarz BA, Nefzger CM, Lim SM, Borkent M, Apostolou E, Alaei S, Cloutier J, Bar-Nur O, Cheloufi S, Stadtfeld M, Figueroa ME, Robinton D, Natesan S, Melnick A, Zhu J, Ramaswamy S, and Hochedlinger K. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 151: 1617-1632, 2012.
57. Prasad SM, Czepiel M, Cetinkaya C, Smigielska K, Weli SC, Lysdahl H, Gabrielsen A, Petersen K, Ehlers N, Fink T, Minger SL, and Zachar V. Continuous hypoxic culturing maintains activation of Notch and allows long-term propagation of human embryonic stem cells without spontaneous differentiation. Cell Prolif 42: 63-74, 2009.
58. Radzisheuskaya A, Le Bin Chia G, Dos Santos RL, Theunissen TW, Castro LF, Nichols J, and Silva JC. A defined Oct4 level governs cell state transitions of pluripotency entry and differentiation into all embryonic lineages. Nat Cell Biol 15: 579-590, 2013.
59. Resnick JL, Bixler LS, Cheng L, and Donovan PJ. Longterm proliferation of mouse primordial germ cells in culture. Nature 359: 550-551, 1992.
60. Sabour D, Arauzo-Bravo MJ, Hubner K, Ko K, Greber B, Gentile L, Stehling M, and Scholer HR. Identification of genes specific to mouse primordial germ cells through dynamic global gene expression. Hum Mol Genet 20: 115-125, 2011.
61. Saitou M, Barton SC, and Surani MA. A molecular programme for the specification of germ cell fate in mice. Nature 418: 293-300, 2002.
62. Samavarchi-Tehrani P, Golipour A, David L, Sung HK, Beyer TA, Datti A, Woltjen K, Nagy A, and Wrana JL. Functional genomics reveals a BMP-driven mesenchymalto-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 7: 64-77, 2010.
63. Scholer HR, Ruppert S, Suzuki N, Chowdhury K, and Gruss P. New type of POU domain in germ line-specific protein Oct-4. Nature 344: 435-439, 1990.
64. Shaw RJ. Glucose metabolism and cancer. Curr Opin Cell Biol 18: 598-608, 2006.
65. Silvan U, Diez-Torre A, Arluzea J, Andrade R, Silio M, and Arechaga J. Hypoxia and pluripotency in embryonic and embryonal carcinoma stem cell biology. Differentiation 78: 159-168, 2009.
66. Stadtfeld M, Brennand K, and Hochedlinger K. Reprogramming of pancreatic beta cells into induced pluripotent stem cells. Curr Biol 18: 890-894, 2008.
67. Szabo PE, Hubner K, Scholer H, and Mann JR. Allelespecific expression of imprinted genes in mouse migratory primordial germ cells. Mech Dev 115: 157-160, 2002.
68. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872, 2007.
69. Takahashi K and Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676, 2006.
70. Taranger CK, Noer A, Sorensen AL, Hakelien A-M, Boquest AC, and Collas P. Induction of dedifferentiation, genomewide transcriptional programming, and epigenetic reprogramming by extracts of carcinoma and embryonic stem cells. Mol Biol Cell 16: 5719-5735, 2005.
71. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, and McKay RDG. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448: 196-199, 2007.
72. West JA, Viswanathan SR, Yabuuchi A, Cunniff K, Takeuchi A, Park I-H, Sero JE, Zhu H, Perez-Atayde A, Frazier AL, Surani MA, and Daley GQ. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460: 909-913, 2009.
73. Wilmut I, Beaujean N, de Sousa PA, Dinnyes A, King TJ, Paterson LA, Wells DN, and Young LE. Somatic cell nuclear transfer. Nature 419: 583-586, 2002.
74. Yabuta Y, Kurimoto K, Ohinata Y, Seki Y, and Saitou M. Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling. Biol Reprod 75: 705-716, 2006.
75. Yamaguchi S, Kimura H, Tada M, Nakatsuji N, and Tada T. Nanog expression in mouse germ cell development. Gene Expr Patterns 5: 639-646, 2005.
76. Yanes O, Clark J, Wong DM, Patti GJ, Sanchez-Ruiz A, Benton HP, Trauger SA, Desponts C, Ding S, and Siuzdak G. Metabolic oxidation regulates embryonic stem cell differentiation. Nat Chem Biol 6: 411-417, 2010.
77. Ying Q-L, Nichols J, Evans EP, and Smith AG. Changing potency by spontaneous fusion. Nature 416: 545-548, 2002.
78. Yoshida Y, Takahashi K, Okita K, Ichisaka T, and Yamanaka S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell 5: 237-241, 2009.
79. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, and Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920, 2007.
80. Zhang J, Nuebel E, Daley GQ, Koehler CM, and Teitell MA. Metabolic regulation in pluripotent stem cells during reprogramming and self-renewal. Cell Stem Cell 11: 589-595, 2012.
81. Zhao Y, Yin X, Qin H, Zhu F, Liu H, Yang W, Zhang Q, Xiang C, Hou P, Song Z, Liu Y, Yong J, Zhang P, Cai J, Liu M, Li H, Li Y, Qu X, Cui K, Zhang W, Xiang T,Wu Y, Zhao Y, Liu C, Yu C, Yuan K, Lou J, Ding M, and Deng H. Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell 3: 475-479, 2008.
82. Zhu S, Li W, Zhou H, Wei W, Ambasudhan R, Lin T, Kim J, Zhang K, and Ding S. Reprogramming of human primary somatic cells by OCT4 and chemical compounds. Cell Stem Cell 7: 651-655, 2010.
83. Zwaka TP and Thomson JA. A germ cell origin of embryonic stem cells Development 132: 227-233, 2005.