Molecular biology of the stress response in the early embryo and its stem cells

Advances in Experimental Medicine and Biology

Volumn 843, Issue , 2015, Pages 77-128

  Puscheck, Elizabeth E ^a   Awonuga, Awoniyi O ^a   Yang, Yu ^a,b   Jiang, Zhongliang ^a,b   Rappolee, Daniel A ^a,b,c,d  

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

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

^c Detroit Department of Health and Wellness Promotion   (United States)

^d UNIVERSITY OF WINDSOR   (Canada)

Author keywords

Blastocyst; Differentiation; Embryonic stem cells; Null lethal; Oocyte; Potency; Stress; Stress enzymes; Transcription factors; Trophoblast stem cells

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ADENYLATE KINASE; ADRENALIN; BENZO[A]PYRENE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIOXIN; HYDROCORTISONE; INITIATION FACTOR 2 ALPHA KINASE 3; LEPTIN; MESSENGER RNA; METAL; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE P38; OCTAMER TRANSCRIPTION FACTOR 1; OCTAMER TRANSCRIPTION FACTOR 4; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR JUNB; TRANSCRIPTION FACTOR JUNC; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL LINEAGE; CELL MANIPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CRYOPRESERVATION; CULTURE MEDIUM; CYTOSOL; DEHYDRATION; DIABETES MELLITUS; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE CONTROL; HEAT STRESS; HOMEOSTASIS; HUMAN; HYPEROSMOTIC STRESS; HYPOXIA; IN VITRO STUDY; INFECTION; INFLAMMATION; MATERNAL NUTRITION; MITOCHONDRION; MOLECULAR BIOLOGY; NIDATION; NUTRITIONAL STATUS; PLACENTA; PRIORITY JOURNAL; PROCESS MODEL; PROTEIN FUNCTION; PROTEIN INTERACTION; SHEAR STRESS; SIGNAL TRANSDUCTION; STEM CELL; ZYGOTE; ANIMAL; CYTOLOGY; EMBRYONIC STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PREGNANCY; TROPHOBLAST;

ANIMALS; CELL DIFFERENTIATION; EMBRYO IMPLANTATION; EMBRYONIC STEM CELLS; EPINEPHRINE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYDROCORTISONE; LEPTIN; PREGNANCY; PROGESTERONE; PROTEIN KINASES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84929180104     PISSN: 00652598     EISSN: 22148019     Source Type: Book Series    
DOI: 10.1007/978-1-4939-2480-6_4     Document Type: Article

References (201)

1. Abdallah M, Xie Y, Puscheck EE, Rappolee DA, Awonuga AO. Benzopyrene activates SAPK and induces HAND1 that favors differentiation of trophoblast stem cells. Fertil Steril 2009;92(3):S136–7.
2. Abecia JA, Forcada F, Palacin I, Sanchez-Prieto L, Sosa C, Fernandez-Foren A, Meikle A. Undernutrition affects embryo quality of superovulated ewes. Zygote. 2013;91(10):4832–40
3. Abell AN, Granger DA, Johnson NL, Vincent-Jordan N, Dibble CF, Johnson GL. Trophoblast stem cell maintenance by fibroblast growth factor 4 requires MEKK4 activation of Jun N-terminal kinase. Mol Cell Biol. 2009;29:2748–61.
4. Abraham T, Pin CL, Watson AJ. Embryo collection induces transient activation of XBP1 arm of the ER stress response while embryo vitrification does not. Mol Hum Reprod. 2011;18(5):229–42
5. Adachi K, Nikaido I, Ohta H, Ohtsuka S, Ura H, Kadota M, Wakayama T, Ueda HR, Niwa H. Context-dependent wiring of Sox2 regulatory networks for self-renewal of embryonic and trophoblast stem cells. Mol Cell. 2013;52:380–92.
6. Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 2000;14:3191–203.
7. Ain R, Dai G, Dunmore JH, Godwin AR, Soares MJ. A prolactin family paralog regulates reproductive adaptations to a physiological stressor. Proc Natl Acad Sci U S A. 2004;101:16543–8.
8. Anderson P, Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem Sci. 2008;33:141–50.
9. Armant DR. Blastocysts don’t go it alone. Extrinsic signals fine-tune the intrinsic developmental program of trophoblast cells. Dev Biol. 2005;280:260–80.
10. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on Sox2 function. Genes Dev. 2003;17:126–40.
11. Awonuga AO, Zhong W, Abdallah ME, Slater JA, Zhou SC, Xie YF, Puscheck EE, Rappolee DA. Eomesodermin, HAND1, and CSH1 proteins are induced by cellular stress in a stress-activated protein kinase-dependent manner. Mol Reprod Dev. 2011;78:519–28.
12. Awonuga AO, Yang Y, Rappolee DA. When stresses collide. Biol Reprod. 2013;89:74.
13. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell. 1999;4:585–95.
14. Barcroft LC, Offenberg H, Thomsen P, Watson AJ. Aquaporin proteins in murine trophectoderm mediate transepithelial water movements during cavitation. Dev Biol. 2003;256:342–54.
15. Batten BE, Albertini DF, Ducibella T. Patterns of organelle distribution in mouse embryos during preimplantation development. Am J Anat. 1987;178:204–13.
16. Baumann CG, Morris DG, Sreenan JM, Leese HJ. The quiet embryo hypothesis: Molecular characteristics favoring viability. Mol Reprod Dev. 2007;74:1345–53.
17. Bell CE, Lariviere NM, Watson PH, Watson AJ. Mitogen-activated protein kinase (MAPK) pathways mediate embryonic responses to culture medium osmolarity by regulating Aquaporin 3 and 9 expression and localization, as well as embryonic apoptosis. Hum Reprod. 2009;24:1373–86.
18. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature. 2006;441:349–53.
19. Brison DR, Leese HJ. Energy metabolism in late preimplantation rat embryos. J Reprod Fertil. 1991;93:245–51.
20. Brison DR, Leese HJ. The role of exogenous energy substrates in blastocoele fluid accumulation in the rat. Zygote. 1994;2:69–77.
21. Brison DR, Schultz RM. Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol Reprod. 1997;56:1088–96.
22. Burton GJ. Oxygen, the Janus gas; its effects on human placental development and function. J Anat. 2009;215:27–35.
23. Burton PJ, Waddell BJ. Dual function of 11beta-hydroxysteroid dehydrogenase in placenta: modulating placental glucocorticoid passage and local steroid action. Biol Reprod. 1999;60:234–40.
24. Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniaux E. Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab. 2002;87:2954–9.
25. Burton GJ, Jauniaux E, Charnock-Jones DS. The influence of the intrauterine environment on human placental development. Int J Dev Biol. 2010;54:303–12.
26. Butcher L, Coates A, Martin KL, Rutherford AJ, Leese HJ. Metabolism of pyruvate by the early human embryo. Biol Reprod. 1998;58:1054–6.
27. Carling D. The AMP-activated protein kinase cascade—a unifying system for energy control. Trends Biochem Sci. 2004;29:18–24.
28. Cikos S, Vesela J, Ilʼkova G, Rehak P, Czikkova S, Koppel J. Expression of beta adrenergic receptors in mouse oocytes and preimplantation embryos. Mol Reprod Dev. 2005;71:145–53.
29. Cikos S, Rehak P, Czikkova S, Vesela J, Koppel J. Expression of adrenergic receptors in mouse preimplantation embryos and ovulated oocytes. Reproduction. 2007;133:1139–47.
30. Chae HD, Lee MR, Broxmeyer HE. 5-Aminoimidazole-4-carboxyamide ribonucleoside induces G(1)/S arrest and Nanog downregulation via p53 and enhances erythroid differentiation. Stem Cells. 2012;30:140–9.
31. Chai N, Patel Y, Jacobson K, McMahon J, McMahon A, Rappolee DA. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev Biol. 1998;198:105–15.
32. Chamberlain SJ, Yee D, Magnuson T. Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells. 2008;26:1496–505.
33. Chandler KJ, Barrier M, Jeffay S, Nichols HP, Kleinstreuer NC, Singh AV, Reif DM, Sipes NS, Judson RS, Dix DJ, Kavlock R, Hunter ES, 3rd, et al. Evaluation of 309 environmental chemicals using a mouse embryonic stem cell adherent cell differentiation and cytotoxicity assay. PLoS One. 2011;6:e18540.
34. Chandrakanthan V, Li A, Chami O, OʼNeill C. Effects of in vitro fertilization and embryo culture on TRP53 and Bax expression in B6 mouse embryos. Reprod Biol Endocrinol. 2006;4:61.
35. Chawengsaksophak K, James R, Hammond VE, Kontgen F, Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature. 1997;386:84–7.
36. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol. 2003;160:189–200.
37. Chen J, Hudson E, Chi MM, Chang AS, Moley KH, Hardie DG, Downs SM. AMPK regulation of mouse oocyte meiotic resumption in vitro. Dev Biol. 2006;291:227–38.
38. Christofk HR, Vander Heiden MG, Wu N, Asara JM, Cantley LC. Pyruvate kinase M2 is a phosphotyrosine- binding protein. Nature. 2008;452:181–6.
39. Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med. 2007;4(Suppl. 1):S60–7.
40. Coan PM, Ferguson-Smith AC, Burton GJ. Ultrastructural changes in the interhaemal membrane and junctional zone of the murine chorioallantoic placenta across gestation. J Anat. 2005;207:783–96.
41. Corson LB, Yamanaka Y, Lai KM, Rossant J. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development. 2003;130:4527–37.
42. Cowden Dahl KD, Fryer BH, Mack FA, Compernolle V, Maltepe E, Adelman DM, Carmeliet P, Simon MC. Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol Cell Biol. 2005;25:10479–91.
43. Dawson KM, Collins JL, Baltz JM. Osmolarity-dependent glycine accumulation indicates a role for glycine as an organic osmolyte in early preimplantation mouse embryos. Biol Reprod. 1998;59:225–32.
44. de Nadal E Ammerer G Posas F. Controlling gene expression in response to stress. Nat Rev Genet. 2011;12:833–45.
45. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod. 2000;62:1526–35.
46. Donnay I, Leese HJ. Embryo metabolism during the expansion of the bovine blastocyst. Mol Reprod Dev. 1999;53:171–8.
47. Drake AJ, McPherson RC, Godfrey KM, Cooper C, Lillycrop KA, Hanson MA, Meehan RR, Seckl JR, Reynolds RM. An unbalanced maternal diet in pregnancy associates with offspring epigenetic changes in genes controlling glucocorticoid action and foetal growth. Clin Endocrinol (Oxf). 2012;77:808–15.
48. Dzeja PP, Chung S, Faustino RS, Behfar A, Terzic A. Developmental enhancement of adenylate kinase-AMPK metabolic signaling axis supports stem cell cardiac differentiation. PLoS One. 2011;6:e19300.
49. Eng GS, Sheridan RA, Wyman A, Chi MM, Bibee KP, Jungheim ES, Moley KH. AMP kinase activation increases glucose uptake, decreases apoptosis, and improves pregnancy outcome in embryos exposed to high IGF-I concentrations. Diabetes. 2007;56:2228–34.
50. Entringer S, Buss C, Andersen J, Chicz-DeMet A, Wadhwa PD. Ecological momentary assessment of maternal cortisol profiles over a multiple-day period predicts the length of human gestation. Psychosom Med. 2011;73:469–74.
51. Entringer S, Buss C, Wadhwa PD. Prenatal stress, telomere biology, and fetal programming of health and disease risk. Sci Signal. 2012;5:pt12.
52. Entringer S, Epel ES, Lin J, Buss C, Shahbaba B, Blackburn EH, Simhan HN, Wadhwa PD. Maternal psychosocial stress during pregnancy is associated with newborn leukocyte telomere length. Am J Obstet Gynecol. 2013;208:134 e131–7.
53. Erbach GT, Lawitts JA, Papaioannou VE, Biggers JD. Differential growth of the mouse preimplantation embryo in chemically defined media. Biol Reprod. 1994;50:1027–33.
54. Farny NG, Kedersha NL, Silver PA. Metazoan stress granule assembly is mediated by P-eIF2alpha- dependent and -independent mechanisms. RNA. 2009;15:1814–21.
55. Feil D, Lane M, Roberts CT, Kelley RL, Edwards LJ, Thompson JG, Kind KL. Effect of culturing mouse embryos under different oxygen concentrations on subsequent fetal and placental development. J Physiol. 2006;572:87–96.
56. Ferdous A, Morris J, Abedin MJ, Collins S, Richardson JA, Hill JA. Forkhead factor FoxO1 is essential for placental morphogenesis in the developing embryo. Proc Natl Acad Sci U S A. 2011;108:16307–12.
57. Fernandes R, Tsuda C, Perumalsamy AL, Naranian T, Chong J, Acton BM, Tong ZB, Nelson LM, Jurisicova A. NLRP5 mediates mitochondrial function in mouse oocytes and embryos. Biol Reprod. 2012;86:138, 131–10.
58. Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99:673–9.
59. Folmes CD, Dzeja PP, Nelson TJ, Terzic A. Mitochondria in control of cell fate. Circ Res. 2012;110:526–9.
60. Fong B, Watson PH, Watson AJ. Mouse preimplantation embryo responses to culture medium osmolarity include increased expression of CCM2 and p38 MAPK activation. BMC Dev Biol. 2007;7:2.
61. Frankenberg S, Gerbe F, Bessonnard S, Belville C, Pouchin P, Bardot O, Chazaud C. Primitive Endoderm differentiates via a three-step mechanism involving nanog and RTK signaling. Dev Cell 2011;21:1005–13.
62. Gardner DK. Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology. 1998;49:83–102.
63. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science. 1997;277:1669–72.
64. Gerbe F, Cox B, Rossant J, Chazaud C. Dynamic expression of Lrp2 pathway members reveals progressive epithelial differentiation of primitive endoderm in mouse blastocyst. Dev Biol. 2008;313:594–602.
65. Giroux S, Tremblay M, Bernard D, Cardin-Girard JF, Aubry S, Larouche L, Rousseau S, Huot J, Landry J, Jeannotte L, Charron J. Embryonic death of Mek1-deficient mice reveals a role for this kinase in angiogenesis in the labyrinthine region of the placenta. Curr Biol. 1999;9:369–72.
66. Gonzalez RR, Simon C, Caballero-Campo P, Norman R, Chardonnens D, Devoto L, Bischof P. Leptin and reproduction. Hum Reprod Update. 2000a;6:290–300.
67. Gonzalez RR, Caballero-Campo P, Jasper M, Mercader A, Devoto L, Pellicer A, Simon C. Leptin and leptin receptor are expressed in the human endometrium and endometrial leptin secretion is regulated by the human blastocyst. J Clin Endocrinol Metab. 2000b;85:4883–8.
68. Gosden R, Trasler J, Lucifero D, Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet. 2003;361:1975–7.
69. Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell. 2004;6:117–31.
70. Hammer MA, Baltz JM. Betaine is a highly effective organic osmolyte but does not appear to be transported by established organic osmolyte transporters in mouse embryos. Mol Reprod Dev. 2002;62:195–202.
71. Hanahan D. Signaling vascular morphogenesis and maintenance. Science. 1997;277:48–50.
72. Hansen PJ, Drost M, Rivera RM, Paula-Lopes FF, al-Katanani YM, Krininger CE, 3rd, Chase CC, Jr. Adverse impact of heat stress on embryo production: causes and strategies for mitigation. Theriogenology. 2001;55:91–103.
73. Hardie DG. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology. 2003;144:5179–83.
74. Harding HP, Zhang Y, Scheuner D, Chen JJ, Kaufman RJ, Ron D. Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2alpha) dephosphorylation in mammalian development. Proc Natl Acad Sci U S A. 2009;106:1832–7.
75. He Y, Hakvoort TB, Vermeulen JL, Lamers WH, Van Roon MA. Glutamine synthetase is essential in early mouse embryogenesis. Dev Dyn. 2007;236:1865–75.
76. Heo YS, Cabrera LM, Bormann CL, Shah CT, Takayama S, Smith GD. Dynamic microfunnel culture enhances mouse embryo development and pregnancy rates. Hum Reprod. 2010;25:613–22.
77. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K, Dong S, Lonial S, Wang X, Chen GZ, Xie J, Gu TL, et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal. 2009;2:ra73.
78. Houghton FD, Thompson JG, Kennedy CJ, Leese HJ. Oxygen consumption and energy metabolism of the early mouse embryo. Mol Reprod Dev. 1996;44:476–85.
79. Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension. 2008;51:970–5.
80. Hur YS, Park JH, Ryu EK, Park SJ, Lee JH, Lee SH, Yoon J, Yoon SH, Hur CY, Lee WD, Lim JH. Effect of micro-vibration culture system on embryo development. J Assist Reprod Genet. 2013;30:835–41.
81. Hyslop L, Stojkovic M, Armstrong L, Walter T, Stojkovic P, Przyborski S, Herbert M, Murdoch A, Strachan T, Lako M. Downregulation of NANOG induces differentiation of human embryonic stem cells to extraembryonic lineages. Stem Cells. 2005;23:1035–43.
82. Iwawaki T, Akai R, Yamanaka S, Kohno K. Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability. Proc Natl Acad Sci U S A. 2009;106:16657–62.
83. Jin XL, Chandrakanthan V, Morgan HD, O’Neill C. Preimplantation embryo development in the mouse requires the latency of TRP53 expression, which is induced by a ligand-activated PI3 kinase/AKT/MDM2-mediated signaling pathway. Biol Reprod. 2009;81:234–42.
84. Kaijser M, Bonamy AK, Akre O, Cnattingius S, Granath F, Norman M, Ekbom A. Perinatal risk factors for diabetes in later life. Diabetes. 2009;58:523–6.
85. Kang J, Shakya A, Tantin D. Stem cells, stress, metabolism and cancer: a drama in two Octs. Trends Biochem Sci. 2009a;34:491–9.
86. Kang J, Gemberling M, Nakamura M, Whitby FG, Handa H, Fairbrother WG, Tantin D. A general mechanism for transcription regulation by Oct1 and Oct4 in response to genotoxic and oxidative stress. Genes Dev. 2009b;23:208–22.
87. Katsanou V, Milatos S, Yiakouvaki A, Sgantzis N, Kotsoni A, Alexiou M, Harokopos V, Aidinis V, Hemberger M, Kontoyiannis DL. The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol Cell Biol. 2009;29:2762–76.
88. Kawamura K, Sato N, Fukuda J, Kodama H, Kumagai J, Tanikawa H, Murata M, Tanaka T. The role of leptin during the development of mouse preimplantation embryos. Mol Cell Endocrinol. 2003;202:185–9.
89. Keim AL, Chi MM, Moley KH. Hyperglycemia-induced apoptotic cell death in the mouse blastocyst is dependent on expression of p53. Mol Reprod Dev. 2001;60:214–24.
90. Kleinhaus K, Harlap S, Perrin M, Manor O, Margalit-Calderon R, Opler M, Friedlander Y, Malaspina D. Prenatal stress and affective disorders in a population birth cohort. Bipolar Disord. 2013;15:92–9.
91. Knobil E, Neill JD. Knobil and Neill’s physiology of reproduction. Amsterdam: Elsevier; 2006.
92. Kolahi KS, Donjacour A, Liu X, Lin W, Simbulan RK, Bloise E, Maltepe E, Rinaudo P. Effect of substrate stiffness on early mouse embryo development. PLoS One. 2012;7:e41717.
93. Krininger CE, 3rd, Stephens SH, Hansen PJ. Developmental changes in inhibitory effects of arsenic and heat shock on growth of pre-implantation bovine embryos. Mol Reprod Dev. 2002;63:335–40.
94. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127:4195–202.
95. Kwong WY, Osmond C, Fleming TP. Support for Barker hypothesis upheld in rat model of maternal undernutrition during the preimplantation period: application of integrated ʻrandom effectsʼ statistical model. Reprod Biomed Online. 2004;8:574–6.
96. LaRosa C, Downs SM. Stress stimulates AMP-activated protein kinase and meiotic resumption in mouse oocytes. Biol Reprod. 2006;74:585–92.
97. Larosa C, Downs SM. Meiotic induction by heat stress in mouse oocytes: involvement of AMPactivated protein kinase and MAPK family members. Biol Reprod. 2007;76:476–86.
98. Lee N, Maurange C, Ringrose L, Paro R. Suppression of Polycomb group proteins by JNK signalling induces transdetermination in Drosophila imaginal discs. Nature. 2005;438:234–7.
99. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell. 2006;125:301–13.
100. Leese HJ. Human assisted conception: a cautionary tale. Lessons from domestic animals. Hum Reprod (Oxf). 1998;13(Suppl. 4):184–202.
101. Leese HJ. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays. 2002;24:845–9.
102. Leese HJ. Metabolism of the preimplantation embryo: 40 years on. Reproduction. 2012;143:417–27.
103. Leese HJ, Baumann CG, Brison DR, McEvoy TG, Sturmey RG. Metabolism of the viable mammalian embryo: quietness revisited. Mol Hum Reprod. 2008;14:667–72.
104. Le Masson F, Christians E. HSFs and regulation of Hsp70.1 (Hspa1b) in oocytes and preimplantation embryos: new insights brought by transgenic and knockout mouse models. Cell Stress Chaperones. 2011;16:275–85.
105. Li A, Chandrakanthan V, Chami O, OʼNeill C. Culture of zygotes increases TRP53 [corrected] expression in B6 mouse embryos, which reduces embryo viability. Biol Reprod. 2007;76:362–7.
106. Liu L, Cash TP, Jones RG, Keith B, Thompson CB, Simon MC. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell. 2006;21:521–31.
107. Liu J, Xu W, Sun T, Wang F, Puscheck E, Brigstock D, Wang QT, Davis R, Rappolee DA. Hyperosmolar stress induces global mRNA responses in placental trophoblast stem cells that emulate early post-implantation differentiation. Placenta. 2009;30:66–73.
108. Louden E, Chi MM, Moley KH. Crosstalk between the AMP-activated kinase and insulin signalling pathways rescues murine blastocyst cells from insulin resistance. Reproduction. 2008;136:335–44.
109. Lu DP, Chandrakanthan V, Cahana A, Ishii S, OʼNeill C. Trophic signals acting via phosphatidylinositol- 3 kinase are required for normal pre-implantation mouse embryo development. J Cell Sci. 2004;117:1567–76.
110. Madan P, Calder MD, Watson AJ. Mitogen-activated protein kinase (MAPK) blockade of bovine preimplantation embryogenesis requires inhibition of both p38 and extracellular signal-regulated kinase (ERK) pathways. Reproduction. 2005;130:41–51.
111. Maltepe E, Krampitz GW, Okazaki KM, Red-Horse K, Mak W, Simon MC, Fisher SJ. Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development. 2005;132:3393–403.
112. Mandl M, Ghaffari-Tabrizi N, Haas J, Nohammer G, Desoye G. Differential glucocorticoid effects on proliferation and invasion of human trophoblast cell lines. Reproduction. 2006;132:159–67.
113. Mansouri L, Xie Y, Rappolee D. Adaptive and pathogenic responses to stress by stem cells during development. Cells. 2012;1:1197–224.
114. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell. 2008;134:521–33.
115. Martindill DM, Risebro CA, Smart N, Franco-Viseras Mdel M, Rosario CO, Swallow CJ, Dennis JW, Riley PR. Nucleolar release of Hand1 acts as a molecular switch to determine cell fate. Nat Cell Biol. 2007;9:1131–41.
116. Mezger V, Rallu M, Morimoto RI, Morange M, Renard JP. Heat shock factor 2-like activity in mouse blastocysts. Dev Biol. 1994;166:819–22.
117. McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A, Chen JJ, Anderson P, Kaufman RJ. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem. 2005;280:16925–33.
118. McLaren A. Embryo growth during the immediate postimplantation period. in Embryogenesis in mammals. Amsterdam: Elsevier; 1976. pp. 53–66.
119. McMillan DR, Christians E, Forster M, Xiao X, Connell P, Plumier JC, Zuo X, Richardson J, Morgan S, Benjamin IJ. Heat shock transcription factor 2 is not essential for embryonic development, fertility, or adult cognitive and psychomotor function in mice. Mol Cell Biol. 2002;22:8005–14.
120. Monk C, Spicer J, Champagne FA. Linking prenatal maternal adversity to developmental outcomes in infants: the role of epigenetic pathways. Dev Psychopathol. 2012;24:1361–76.
121. Mudgett JS, Ding J, Guh-Siesel L, Chartrain NA, Yang L, Gopal S, Shen MM. Essential role for p38alpha mitogen-activated protein kinase in placental angiogenesis. Proc Natl Acad Sci U S A. 2000;97:10454–9.
122. Natale DR, Paliga AJ, Beier F, DʼSouza SJ, Watson AJ. p38 MAPK signaling during murine preimplantation development. Dev Biol. 2004;268:76–88.
123. National Research Council (U.S.). Committee on Toxicity Testing and Assessment of Environmental Agents. Toxicity testing in the 21st century: a vision and a strategy. Washington, DC: National Academies Press; 2007.
124. Neugebauer R, Hoek HW, Susser E. Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. JAMA. 1999;282:455–62.
125. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 2008;3:97–106.
126. OʼNeill C. Evidence for the requirement of autocrine growth factors for development of mouse preimplantation embryos in vitro. Biol Reprod. 1997;56:229–37.
127. Owusu-Ansah E, Banerjee U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature. 2009;461:537–41.
128. Paliga AJ, Natale DR, Watson AJ. p38 mitogen-activated protein kinase (MAPK) first regulates filamentous actin at the 8–16-cell stage during preimplantation development. Biol Cell. 2005;97:629–40.
129. Patel Y, Kim H, Rappolee DA. A role for hepatocyte growth factor during early postimplantation growth of the placental lineage in mice. Biol Reprod. 2000;62:904–12.
130. Pribenszky C, Vajta G, Molnar M, Du Y, Lin L, Bolund L, Yovich J. Stress for stress tolerance? A fundamentally new approach in mammalian embryology. Biol Reprod. 2010;83:690–7.
131. Proud CG. eIF2 and the control of cell physiology. Semin Cell Dev Biol. 2005;16:3–12.
132. Qin J, Diaz-Cueto L, Schwarze JE, Takahashi Y, Imai M, Isuzugawa K, Yamamoto S, Chang KT, Gerton GL, Imakawa K. Effects of progranulin on blastocyst hatching and subsequent adhesion and outgrowth in the mouse. Biol Reprod. 2005;73:434–42.
133. Rappolee DA. Itʼs not just babyʼs babble/Babel: recent progress in understanding the language of early mammalian development: a minireview. Mol Reprod Dev. 1999;52:234–40.
134. Rappolee DA. Impact of transient stress and stress enzymes on development. Dev Biol. 2007;304:1–8.
135. Rappolee DA, Sturm KS, Behrendtsen O, Schultz GA, Pedersen RA, Werb Z. Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev. 1992;6:939–52.
136. Rappolee DA, Basilico C, Patel Y, Werb Z. Expression and function of FGF-4 in peri-implantation development in mouse embryos. Development. 1994;120:2259–69.
137. Rappolee DA, Awonuga AO, Puscheck EE, Zhou S, Xie Y. Benzopyrene and experimental stressors cause compensatory differentiation in placental trophoblast stem cells. Syst Biol Reprod Med. 2010;56:168–83.
138. Rappolee DA, Xie YF, Zhou SC, Huttemann M, Lee IS, Puscheck EE. Hypoxia induces maximal preparation for, but incomplete differentiation of stem cells that is associated with decreased mitochondrial function and increased expression of two potency factors. Fertil Steril. 2011a;96:S169.
139. Rappolee DA, Xie YF, Zhou SC, Slater J, Puscheck EE. Cellular and toxicological stress cause adaptive “Prioritized” and “Compensatory” differentiation of embryonic and placental stem cells of the implanting blastocyst. Fertil Steril. 2011b;96:S171.
140. Rappolee DA, Xie Y, Slater JA, Zhou S, Puscheck EE. 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.
141. Rappolee DA, Zhou S, Puscheck EE, Xie Y. Stress responses at the endometrial-placental interface regulate labyrinthine placental differentiation from trophoblast stem cells. Reproduction. 2013;145:R139–55.
142. Rassoulzadegan M, Rosen BS, Gillot I, Cuzin F. Phagocytosis reveals a reversible differentiated state early in the development of the mouse embryo. Embo J. 2000;19:3295–303.
143. Ratchford AM, Chang AS, Chi MM, Sheridan R, Moley KH. Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes. Am J Physiol Endocrinol Metab. 2007;293:E1198–206.
144. Redman CW. Current topic: pre-eclampsia and the placenta. Placenta. 1991;12:301–08.
145. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005;308:1592–4.
146. Reynolds RM. Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis–2012 Curt Richter Award Winner. Psychoneuroendocrinology. 2013;38:1–11.
147. Richards T, Wang F, Liu L, Baltz JM. Rescue of postcompaction-stage mouse embryo development from hypertonicity by amino acid transporter substrates that may function as organic osmolytes. Biol Reprod. 2010; 82:769–77.
148. Rinaudo PF, Giritharan G, Talbi S, Dobson AT, Schultz RM. Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril. 2006;86:1252–65, 1265 e1251–36.
149. Rivera RM, Rinaudo P. Bovine preimplantation embryo development is affected by the stiffness of the culture substrate. Mol Reprod Dev. 2013;80:184.
150. Rivera RM, Stein P, Weaver JR, Mager J, Schultz RM, Bartolomei MS. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet. 2008;17:1–14.
151. Robertson SA, Sjoblom C, Jasper MJ, Norman RJ, Seamark RF. Granulocyte-macrophage colonystimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos. Biol Reprod. 2001;64:1206–15.
152. Salameh W, Helliwell JP, Han G, McPhaul L, Khorram O. Expression of endometrial glycogen synthase kinase-3beta protein throughout the menstrual cycle and its regulation by progesterone. Mol Hum Reprod. 2006;12:543–9.
153. Samavati L, Lee I, Mathes I, Lottspeich F, Huttemann M. Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J Biol Chem. 2008;283:21134–44.
154. Schorpp-Kistner M, Wang ZQ, Angel P, Wagner EF. JunB is essential for mammalian placentation. Embo J. 1999;18:934–48.
155. Sebastiano V, Dalvai M, Gentile L, Schubart K, Sutter J, Wu GM, Tapia N, Esch D, Ju JY, Hubner K, Bravo MJ, Scholer HR, et al. Oct1 regulates trophoblast development during early mouse embryogenesis. Development. 2010;137:3551–60.
156. Seckl JR, Holmes MC. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ʻprogramming’ of adult pathophysiology. Nat Clin Pract Endocrinol Metab. 2007;3:479–88.
157. Seval Y, Cakmak H, Kayisli UA, Arici A. Estrogen-mediated regulation of p38 mitogen-activated protein kinase in human endometrium. J Clin Endocrinol Metab. 2006;91:2349–57.
158. Shapiro SS, Dyer SD, Colas AE. Progesterone-induced glycogen accumulation in human endometrium during organ culture. Am J Obstet Gynecol. 1980;136:419–25.
159. Simmons SO, Fan CY, Ramabhadran R. Cellular stress response pathway system as a sentinel ensemble in toxicological screening. Toxicol Sci. 2009;111:202–25.
160. Slater JA, Zhou S, Puscheck E, Rappolee D. Stress-induced enzyme activation primes murine embryonic stem cells to differentiate toward the first extraembryonic lineage. Stem Cells Dev. 2014;22:3049–64. (In Press).
161. Steeves CL, Baltz JM. Regulation of intracellular glycine as an organic osmolyte in early preimplantation mouse embryos. J Cell Physiol. 2005;204:273–9.
162. Stein SC, Woods A, Jones NA, Davison MD, Carling D. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J. 2000;345(Pt 3):437–43.
163. Stojkovic M, Westesen K, Zakhartchenko V, Stojkovic P, Boxhammer K, Wolf E. Coenzyme Q(10) in submicron-sized dispersion improves development, hatching, cell proliferation, and adenosine triphosphate content of in vitro-produced bovine embryos. Biol Reprod. 1999;61:541–7.
164. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development. 2005;132:2093–102.
165. Stumpo DJ, Byrd NA, Phillips RS, Ghosh S, Maronpot RR, Castranio T, Meyers EN, Mishina Y, Blackshear PJ. Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc finger protein of the Tristetraprolin family. Mol Cell Biol. 2004;24:6445–55.
166. Summers MC, Biggers JD. Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues. Hum Reprod Update. 2003;9: 557–82.
167. Tantin D, Schild-Poulter C, Wang V, Hache RJ, Sharp PA. The octamer binding transcription factor Oct-1 is a stress sensor. Cancer Res. 2005;65:10750–8.
168. Thompson JG, Kind KL, Roberts CT, Robertson SA, Robinson JS. Epigenetic risks related to assisted reproductive technologies: short- and long-term consequences for the health of children conceived through assisted reproduction technology: more reason for caution? Hum Reprod. 2002;17:2783–6.
169. Tong S, Wallace EM, Rombauts L. Association between low day 16 hCG and miscarriage after proven cardiac activity. Obstet Gynecol. 2006;107:300–4.
170. Van Blerkom J Cox H Davis P. Regulatory roles for mitochondria in the peri-implantation mouse blastocyst: possible origins and developmental significance of differential DeltaPsim. Reproduction. 2006;131:961–76.
171. Vazquez-Martin A, Vellon L, Quiros PM, Cufi S, Ruiz de Galarreta E, Oliveras-Ferraros C, Martin AG, Martin-Castillo B, Lopez-Otin C, Menendez JA. Activation of AMP-activated protein kinase (AMPK) provides a metabolic barrier to reprogramming somatic cells into stem cells. Cell Cycle. 2012;11:974–89.
172. Voss AK, Thomas T, Gruss P. Mice lacking HSP90beta fail to develop a placental labyrinth. Development. 2000;127:1–11.
173. Wale PL, Gardner DK. Oxygen affects the ability of mouse blastocysts to regulate ammonium. Biol Reprod. 2013;89:75.
174. Wallace JM, Bourke DA, Aitken RP, Cruickshank MA. Switching maternal dietary intake at the end of the first trimester has profound effects on placental development and fetal growth in adolescent ewes carrying singleton fetuses. Biol Reprod. 1999;61:101–10.
175. Wallace J, Bourke D, Da Silva P, Aitken R. Nutrient partitioning during adolescent pregnancy. Reproduction. 2001;122:347–57.
176. Wallace JM, Bourke DA, Da Silva P, Aitken RP. Influence of progesterone supplementation during the first third of pregnancy on fetal and placental growth in overnourished adolescent ewes. Reproduction. 2003;126:481–7.
177. Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, Davis RW, Zernicka-Goetz M. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell. 2004;6:133–44.
178. Wang Y, Puscheck EE, Lewis JJ, Trostinskaia AB, Wang F, Rappolee DA. Increases in phosphorylation of SAPK/JNK and p38MAPK correlate negatively with mouse embryo development after culture in different media. Fertil Steril. 2005;83(Suppl. 1):1144–54.
179. Wek RC, Jiang HY, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans. 2006;34:7–11.
180. Wilcox AJ, Weinberg CR, OʼConnor JF, Baird DD, Schlatterer JP, Canfield RE, Armstrong EG, Nisula BC. Incidence of early loss of pregnancy. N Engl J Med. 1988;319:189–94.
181. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol. 2003;13:2004–8.
182. Wu G, Gentile L, Fuchikami T, Sutter J, Psathaki K, Esteves TC, Arauzo-Bravo MJ, Ortmeier C, Verberk G, Abe K, Scholer HR. Initiation of trophectoderm lineage specification in mouse embryos is independent of Cdx2. Development. 2010;137:4159–69.
183. Xie Y, Puscheck EE, Rappolee DA. Effects of SAPK/JNK inhibitors on preimplantation mouse embryo development are influenced greatly by the amount of stress induced by the media. Mol Hum Reprod. 2006a;12:217–24.
184. Xie Y, Wang F, Zhong W, Puscheck E, Shen H, Rappolee DA. Shear stress induces preimplantation embryo death that is delayed by the zona pellucida and associated with stress-activated protein kinase-mediated apoptosis. Biol Reprod 2006b;75:45–5.
185. Xie Y, Wang F, Puscheck EE, Rappolee DA. Pipetting causes shear stress and elevation of phosphorylated stress-activated protein kinase/jun kinase in preimplantation embryos. Mol Reprod Dev. 2007a;74:1287–94.
186. Xie Y, Zhong W, Wang Y, Trostinskaia A, Wang F, Puscheck EE, Rappolee DA. Using hyperosmolar stress to measure biologic and stress-activated protein kinase responses in preimplantation embryos. Mol Hum Reprod. 2007b;13:473–81.
187. Xie Z, Zhang J, Wu J, Viollet B, Zou MH. Upregulation of mitochondrial uncoupling protein-2 by the AMP-activated protein kinase in endothelial cells attenuates oxidative stress in diabetes. Diabetes. 2008a;57:3222–30.
188. Xie Y, Liu J, Proteasa S, Proteasa G, Zhong W, Wang Y, Wang F, Puscheck EE, Rappolee DA. Transient stress and stress enzyme responses have practical impacts on parameters of embryo development, from IVF to directed differentiation of stem cells. Mol Reprod Dev. 2008b;75:689–97.
189. Xie Y, Abdallah ME, Awonuga AO, Slater JA, Puscheck EE, Rappolee DA. Benzo(a)pyrene causes PRKAA1/2-dependent ID2 loss in trophoblast stem cells. Mol Reprod Dev. 2010;77:533–9.
190. Xie Y, Awonuga AO, Zhou S, Puscheck EE, Rappolee DA. Interpreting the stress response of early mammalian embryos and their stem cells. Int Rev Cell Mol Biol. 2011;287:43–95.
191. Xie Y, Awonuga A, Liu J, Rings E, Puscheck EE, Rappolee DA. Stress induces AMPK-dependent loss of potency factors Id2 and Cdx2 in early embryos and stem cells. Stem Cells Dev. 2013a;22:1564–75.
192. Xie Y, Zhou S, Jiang Z, Dai J, Puscheck EE, Lee I, Parker G, Huttemann M, Rappolee DA. Hypoxic stress induces, but cannot sustain trophoblast stem cell differentiation to labyrinthine placenta due to mitochondrial insufficiency. Stem Cell Res. 2014;13:478–491.
193. Xie Y, Awonuga A, Liu J, Rings E, Puscheck EE, Rappolee DA. Stress induces AMP-dependent loss of potency factors Id2 and Cdx2 in early embryos and stem cells. Stem Cells Dev. 2013c;22:1564–75.
194. Xie Y, Zhou S, Jiang Z, Puscheck E, Lee I, Parker GC, Huttemann M, Rappolee D. Hypoxic stress induces SAPK-dependent, imbalanced trophoblast stem cell differentiation but does not sustain it due to mitochondrial insufficiency. Stem Cell Res. 2014; In Press.
195. Xu P, Davis RJ. c-Jun NH2-terminal kinase is required for lineage-specific differentiation but not stem cell self-renewal. Mol Cell Biol. 2010;30:1329–40.
196. Yang Y, Ding C, Khoudja R, Lin M, Dai J, Puscheck E, Awonuga A, Rappolee D, Zhou C. Comparison of 2%, 5% and 20% O2 on the development of cryopreserved human embryos from day 3 through blastocyst. Hum Reprod. 2014a; To be submitted.
197. Yang Y, Jiang Z, Bolnick A, Dai J, Puscheck EE, Rappolee DA. Determining the utility of SAPK and AMPK activities as biomarkers for measuring stressful O2 levels in stem cells of the blastocyst. Fertil Steril. submitted 2014b.
198. Yaron Y, Ochshorn Y, Heifetz S, Lehavi O, Sapir Y, Orr-Urtreger A. First trimester maternal serum free human chorionic gonadotropin as a predictor of adverse pregnancy outcome. Fetal Diagn Ther. 2002;17:352–6.
199. Zhong W, Xie Y, Wang Y, Lewis J, Trostinskaia A, Wang F, Puscheck EE, Rappolee DA. 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;14:534–47.
200. Zhong W, Xie Y, Abdallah M, Awonuga AO, Slater JA, Sipahi L, Puscheck EE, Rappolee DA. Cellular stress causes reversible, PRKAA1/2-, and proteasome-dependent ID2 protein loss in trophoblast stem cells. Reproduction. 2010;140:921–30.
201. Zhou S, Xie Y, Puscheck EE, Rappolee DA. Oxygen levels that optimize TSC culture are identified by maximizing growth rates and minimizing stress. Placenta. 2011;32:475–81.