Hypoxic stress induces, but cannot sustain trophoblast stem cell differentiation to labyrinthine placenta due to mitochondrial insufficiency

Stem Cell Research

Volumn 13, Issue 3, 2014, Pages 478-491

  Xie, Yufen ^a   Zhou, Sichang ^a,b,e   Jiang, Zhongliang ^a   Dai, Jing ^a   Puscheck, Elizabeth E ^a,b   Lee, Icksoo ^c   Parker, Graham ^b   Hüttemann, Maik ^b   Rappolee, Daniel A ^a,b,d  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Dankook University   (South Korea)

^d UNIVERSITY OF WINDSOR   (Canada)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; FIBROBLAST GROWTH FACTOR 4; INHIBITOR OF DIFFERENTIATION 2; OXYGEN; PYRUVATE KINASE; PYRUVATE KINASE M2; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR CDX2; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GCM1 PROTEIN, MOUSE; HAND1 PROTEIN, MOUSE; NEUROPEPTIDE; PLACENTA PROTEIN; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE 1; TPBPA PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINEAGE; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT; GLYCOLYSIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PLACENTA; PROTEIN EXPRESSION; RESPIRATORY CHAIN; STEM CELL; SYNCYTIOTROPHOBLAST; TROPHOBLAST; TROPHOBLAST STEM CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; METABOLISM; MITOCHONDRION; PREGNANCY;

ADENOSINE TRIPHOSPHATE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; ELECTRON TRANSPORT COMPLEX IV; FEMALE; FIBROBLAST GROWTH FACTOR 4; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 8; NEUROPEPTIDES; PLACENTA; PREGNANCY; PREGNANCY PROTEINS; PYRUVATE KINASE; REACTIVE OXYGEN SPECIES; STEM CELLS; TROPHOBLASTS;

EID: 84919399072     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2014.07.007     Document Type: Article

References (85)

1. Ahmed A., Singh J., Khan Y., et al. A new mouse model to explore therapies for preeclampsia. PLoS One 2010, 5:e13663.
2. Ain R., Dai G., Dunmore J.H., et al. A prolactin family paralog regulates reproductive adaptations to a physiological stressor. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16543-16548.
3. Alam S.M., Konno T., Dai G., et al. A uterine decidual cell cytokine ensures pregnancy-dependent adaptations to a physiological stressor. Development 2007, 134:407-415.
4. Anson-Cartwright L., Dawson K., Holmyard D., et al. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 2000, 25:311-314.
5. Awonuga A.O., Zhong W., Abdallah M.E., et al. Eomesodermin, HAND1, and CSH1 proteins are induced by cellular stress in a stress-activated protein kinase-dependent manner. Mol. Reprod. Dev. 2011, 78:519-528.
6. Baczyk D., Drewlo S., Proctor L., et al. Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ. 2009, 16:719-727.
7. Burton G.J. Oxygen, the Janus gas; its effects on human placental development and function. J. Anat. 2009, 215:27-35.
8. Burton G.J., Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J. Soc. Gynecol. Investig. 2004, 11:342-352.
9. Burton G.J., Jauniaux E., Charnock-Jones D.S. The influence of the intrauterine environment on human placental development. Int. J. Dev. Biol. 2010, 54:303-312.
10. Byatt-Smith J.G., Leese H.J., Gosden R.G. An investigation by mathematical modelling of whether mouse and human preimplantation embryos in static culture can satisfy their demands for oxygen by diffusion. Hum. Reprod. 1991, 6:52-57.
11. Caniggia I., Winter J., Lye S.J., et al. Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia. Placenta 2000, 21(Suppl. A):S25-S30.
12. Chai N., Patel Y., Jacobson K., et al. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev. Biol. 1998, 198:105-115.
13. Chakraborty D., Rumi M.A., Soares M.J. NK cells, hypoxia and trophoblast cell differentiation. Cell Cycle 2012, 11:2427-2430.
14. Chawengsaksophak K., James R., Hammond V.E., et al. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 1997, 386:84-87.
15. Chiang M.H., Liang F.Y., Chen C.P., et al. Mechanism of hypoxia-induced GCM1 degradation: implications for the pathogenesis of preeclampsia. J. Biol. Chem. 2009, 284:17411-17419.
16. Christofk H.R., Vander Heiden M.G., Wu N., et al. Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 2008, 452:181-186.
17. Corson L.B., Yamanaka Y., Lai K.M., et al. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 2003, 130:4527-4537.
18. Cox B., Kotlyar M., Evangelou A.I., et al. Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol. Syst. Biol. 2009, 5:279.
19. Cross J.C., Werb Z., Fisher S.J. Implantation and the placenta: key pieces of the development puzzle. Science 1994, 266:1508-1518.
20. Drewlo S., Baczyk D., Dunk C., et al. Fusion assays and models for the trophoblast. Methods Mol. Biol. 2008, 475:363-382.
21. Enders A.C. Trophoblast differentiation during the transition from trophoblastic plate to lacunar stage of implantation in the rhesus monkey and human. Am. J. Anat. 1989, 186:85-98.
22. Enders A.C., Lantz K.C., Peterson P.E., et al. From blastocyst to placenta: the morphology of implantation in the baboon. Hum. Reprod. Update 1997, 3:561-573.
23. Fischer B., Bavister B.D. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J. Reprod. Fertil. 1993, 99:673-679.
24. Genbacev O., Zhou Y., Ludlow J.W., et al. Regulation of human placental development by oxygen tension. Science 1997, 277:1669-1672.
25. Harvey A.J., Kind K.L., Thompson J.G. REDOX regulation of early embryo development. Reproduction 2002, 123:479-486.
26. Hewitson L.C., Leese H.J. Energy metabolism of the trophectoderm and inner cell mass of the mouse blastocyst. J. Exp. Zool. 1993, 267:337-343.
27. Hitosugi T., Kang S., Vander Heiden M.G., et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci. Signal. 2009, 2:ra73.
28. Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension 2008, 51:970-975.
29. Janatpour M.J., McMaster M.T., Genbacev O., et al. Id-2 regulates critical aspects of human cytotrophoblast differentiation, invasion and migration. Development 2000, 127:549-558.
30. Ji A.R., Ku S.Y., Cho M.S., et al. Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp. Mol. Med. 2010, 42:175-186.
31. Johnson K.L., Tao K., Stroh H., et al. Increased fetal cell trafficking in murine lung following complete pregnancy loss from exposure to lipopolysaccharide. Fertil. Steril. 2010, 93:1718-1721. (e1712).
32. Kaufman D.L., Mitchell J.A. Alterations in intrauterine oxygen tension during the estrous cycle in the rat and hamster and its regulation by ovarian steroid hormones: a comparative study. Adv. Exp. Med. Biol. 1990, 277:745-750.
33. Knofler M. Critical growth factors and signalling pathways controlling human trophoblast invasion. Int. J. Dev. Biol. 2010, 54:269-280.
34. Kumasawa K., Ikawa M., Kidoya H., et al. Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1451-1455.
35. Lee I., Salomon A.R., Ficarro S., et al. cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J. Biol. Chem. 2005, 280:6094-6100.
36. Li Q., Sanchez-Rodriguez E., Gomez-Lopez N., et al. Rapid Development and Validation of Double Viable Potency Factor Activity Reporter Embryonic Stem Cells. Biotechniques 2014, (in preparation).
37. Liu J., Xu W., Sun T., et al. Hyperosmolar stress induces global mRNA responses in placental trophoblast stem cells that emulate early post-implantation differentiation. Placenta 2009, 30:66-73.
38. Longtine M.S., Chen B., Odibo A.O., et al. Villous trophoblast apoptosis is elevated and restricted to cytotrophoblasts in pregnancies complicated by preeclampsia, IUGR, or preeclampsia with IUGR. Placenta 2012, 33:352-359.
39. Luo J., Sladek R., Bader J.A., et al. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature 1997, 388:778-782.
40. Luo W., Hu H., Chang R., et al. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 2011, 145:732-744.
41. Martindill D.M., Riley P.R. Cell cycle switch to endocycle: the nucleolus lends a hand. Cell Cycle 2008, 7:17-23.
42. Mitchell J.A., Van Kainen B.R. Effects of alcohol on intrauterine oxygen tension in the rat. Alcohol. Clin. Exp. Res. 1992, 16:308-310.
43. Myatt L. Review: reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta 2010, 31:S66-S69. (Suppl.).
44. Nagata Y., Shoji W., Obinata M., et al. Phosphorylation of helix-loop-helix proteins ID1, ID2 and ID3. Biochem. Biophys. Res. Commun. 1995, 207:916-926.
45. Niwa H., Toyooka Y., Shimosato D., et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005, 123:917-929.
46. Pacelli C., Latorre D., Cocco T., et al. Tight control of mitochondrial membrane potential by cytochrome c oxidase. Mitochondrion 2011, 11:334-341.
47. Puscheck E.E., Awonuga A.O., Yang Y., et al. Molecular biology of the stress response in the early embryo and its stem cells. Cell Signaling During Mammalian Early Embryo Development 2014, Springer. L. Henry, B. Daniel (Eds.).
48. Qing G., Skuli N., Mayes P.A., et al. Combinatorial regulation of neuroblastoma tumor progression by N-Myc and hypoxia inducible factor HIF-1alpha. Cancer Res. 2010, 70:10351-10361.
49. Rappolee D.A., Xie Y., Slater J.A., et al. Toxic stress prioritizes and imbalances stem cell differentiation: implications for new biomarkers and in vitro toxicology tests. Syst. Biol. Reprod. Med. 2012, 58:33-40.
50. Rappolee D.A., Zhou S., Puscheck E.E., et al. Stress responses at the endometrial-placental interface regulate labyrinthine placental differentiation from trophoblast stem cells. Reproduction 2013, 145:R139-R155.
51. Redman C.W. Current topic: pre-eclampsia and the placenta. Placenta 1991, 12:301-308.
52. Redman C.W., Sargent I.L. Latest advances in understanding preeclampsia. Science 2005, 308:1592-1594.
53. Rehman J. Empowering self-renewal and differentiation: the role of mitochondria in stem cells. J. Mol. Med. 2010, 88:981-986.
54. Riley P., Anson-Cartwright L., Cross J.C. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat. Genet. 1998, 18:271-275.
55. Roberts J.M., Hubel C.A. The two stage model of preeclampsia: variations on the theme. Placenta 2009, 30(Suppl. A):S32-S37.
56. Robins J.C., Heizer A., Hardiman A., et al. Oxygen tension directs the differentiation pathway of human cytotrophoblast cells. Placenta 2007, 28:1141-1146.
57. Rosario G.X., Konno T., Soares M.J. Maternal hypoxia activates endovascular trophoblast cell invasion. Dev. Biol. 2008, 314:362-375.
58. Samavati L., Lee I., Mathes I., et al. Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J. Biol. Chem. 2008, 283:21134-21144.
59. Semenza G.L. Regulation of metabolism by hypoxia-inducible factor 1. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:347-353.
60. Simmons D.G., Fortier A.L., Cross J.C. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 2007, 304:567-578.
61. Simmons D.G., Natale D.R., Begay V., et al. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 2008, 135:2083-2091.
62. Simmons D.G., Rawn S., Davies A., et al. Spatial and temporal expression of the 23 murine prolactin/placental lactogen-related genes is not associated with their position in the locus. BMC Genomics 2008, 9:352.
63. Simon M.C., Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat. Rev. Mol. Cell Biol. 2008, 9:285-296.
64. Slater J.A., Zhou S., Puscheck E.E., et al. Stress-induced enzyme activation primes murine embryonic stem cells to differentiate toward extraembryonic lineages. Stem Cells Dev. 2014, (In press).
65. Soares M.J., Konno T., Alam S.M. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol. Metab. 2007, 18:114-121.
66. Soleymanlou N., Jurisicova A., Wu Y., et al. Hypoxic switch in mitochondrial myeloid cell leukemia factor-1/Mtd apoptotic rheostat contributes to human trophoblast cell death in preeclampsia. Am. J. Pathol. 2007, 171:496-506.
67. Sun X.H., Copeland N.G., Jenkins N.A., et al. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 1991, 11:5603-5611.
68. Tache V., Ciric A., Moretto-Zita M., et al. Hypoxia and trophoblast differentiation: a key role for PPARgamma. Stem Cells Dev. 2013, 22:2815-2824.
69. Tanaka S., Kunath T., Hadjantonakis A.K., et al. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998, 282:2072-2075.
70. Tremblay G.B., Kunath T., Bergeron D., et al. Diethylstilbestrol regulates trophoblast stem cell differentiation as a ligand of orphan nuclear receptor ERR beta. Genes Dev. 2001, 15:833-838.
71. Ullah Z., Kohn M.J., Yagi R., et al. Differentiation of trophoblast stem cells into giant cells is triggered by p57/Kip2 inhibition of CDK1 activity. Genes Dev. 2008, 22:3024-3036.
72. Vander Heiden M.G., Lunt S.Y., Dayton T.L., et al. Metabolic pathway alterations that support cell proliferation. Cold Spring Harb. Symp. Quant. Biol. 2012, 76:325-334.
73. Villani G., Greco M., Papa S., et al. Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J. Biol. Chem. 1998, 273:31829-31836.
74. Vogt E., Ng A.K., Rote N.S. A model for the antiphospholipid antibody syndrome: monoclonal antiphosphatidylserine antibody induces intrauterine growth restriction in mice. Am. J. Obstet. Gynecol. 1996, 174:700-707.
75. Wich C., Kausler S., Dotsch J., et al. Syncytin-1 and glial cells missing a: hypoxia-induced deregulated gene expression along with disordered cell fusion in primary term human trophoblasts. Gynecol. Obstet. Invest. 2009, 68:9-18.
76. Winn V.D., Gormley M., Paquet A.C., et al. Severe preeclampsia-related changes in gene expression at the maternal-fetal interface include sialic acid-binding immunoglobulin-like lectin-6 and pappalysin-2. Endocrinology 2009, 150:452-462.
77. Xie Y., Zhong W., Wang Y., et al. Using hyperosmolar stress to measure biologic and stress-activated protein kinase responses in preimplantation embryos. Mol. Hum. Reprod. 2007, 13:473-481.
78. Xie Y., Abdallah M.E., Awonuga A.O., et al. Benzo(a)pyrene causes PRKAA1/2-dependent ID2 loss in trophoblast stem cells. Mol. Reprod. Dev. 2010, 77:533-539.
79. Xie Y., Awonuga A.O., Zhou S., et al. Interpreting the stress response of early mammalian embryos and their stem cells. Int. Rev. Cell Mol. Biol. 2011, 287:43-95.
80. Xu Z., Zhao J., Zhang H., et al. Spontaneous miscarriages are explained by the stress/glucocorticoid/lipoxin A4 axis. J. Immunol. 2013, 190:6051-6058.
81. Yedwab G.A., Paz G., Homonnai T.Z., et al. The temperature, pH, and partial pressure of oxygen in the cervix and uterus of women and uterus of rats during the cycle. Fertil. Steril. 1976, 27:304-309.
82. Zhong W., Sun T., Wang Q.T., et al. SAPKgamma/JNK1 and SAPKalpha/JNK2 mRNA transcripts are expressed in early gestation human placenta and mouse eggs, preimplantation embryos, and trophoblast stem cells. Fertil. Steril. 2004, 82(Suppl. 3):1140-1148.
83. Zhong W., Xie Y., Wang Y., et al. Use of hyperosmolar stress to measure stress-activated protein kinase activation and function in human HTR cells and mouse trophoblast stem cells. Reprod. Sci. 2007, 14:534-547.
84. Zhong W., Xie Y., Abdallah M., et al. Cellular stress causes reversible, PRKAA1/2-, and proteasome-dependent ID2 protein loss in trophoblast stem cells. Reproduction 2010, 140:921-930.
85. Zhou S., Xie Y., Puscheck E.E., et al. Oxygen levels that optimize TSC culture are identified by maximizing growth rates and minimizing stress. Placenta 2011, 32:475-481.