TEAD4 establishes the energy homeostasis essential for blastocoel formation

Development (Cambridge)

Volumn 140, Issue 17, 2013, Pages 3680-3690

  Kaneko, Kotaro J ^a   De Pamphilis, Melvin L ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Anti oxidant; Blastocoel; Blastocyst; Mouse; Oxidative stress; Tead4; Trophectoderm

Indexed keywords

REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TEAD4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO CELL; EMBRYO CULTURE; FEMALE; FIBROBLAST; HOMEOSTASIS; IMMUNOCYTOCHEMISTRY; MITOCHONDRIAL MEMBRANE POTENTIAL; MORULA; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; TROPHOBLAST;

ANTI-OXIDANT; BLASTOCOEL; BLASTOCYST; MOUSE; OXIDATIVE STRESS; TEAD4; TROPHECTODERM;

ANIMALS; BLASTOCYST; DNA-BINDING PROTEINS; EMBRYONIC DEVELOPMENT; ENERGY METABOLISM; FIBROBLASTS; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MUSCLE PROTEINS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84881572567     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.093799     Document Type: Article

References (90)

1. Adelman, R., Saul, R. L. and Ames, B. N. (1988). Oxidative damage to DNA: relation to species metabolic rate and life span. Proc. Natl. Acad. Sci. USA 85, 2706-2708.
2. Arman, E., Haffner-Krausz, R., Chen, Y., Heath, J. K. and Lonai, P. (1998). Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. USA 95, 5082-5087.
3. Armant, D. R. (2006). Blastocyst culture. Methods Mol. Med. 121, 35-56.
4. Benos, D. J. and Balaban, R. S. (1983). Energy metabolism of preimplantation mammalian blastocysts. Am. J. Physiol. 245, C40-C45.
5. Betts, D. H. and Madan, P. (2008). Permanent embryo arrest: molecular and cellular concepts. Mol. Hum. Reprod. 14, 445-453.
6. Blij, S., Frum, T., Akyol, A., Fearon, E. and Ralston, A. (2012). Maternal Cdx2 is dispensable for mouse development. Development 139, 3969-3972.
7. Brandt, R. and Keston, A. S. (1965). Synthesis of Diacetyldichlorofluorescin: A Stable Reagent for Fluorometric Analysis. Anal. Biochem. 11, 6-9.
8. Burton, G. J., Hempstock, J. and Jauniaux, E. (2003). Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod. Biomed. Online 6, 84-96.
9. Conner, D. A. (2001). Mouse embryo fibroblast (MEF) feeder cell preparation. Curr. Protoc. Mol. Biol. Chapter 23, Unit 23 22.
10. DePamphilis, M. L., Herman, S. A., Martínez-Salas, E., Chalifour, L. E., Wirak, D. O., Cupo, D. Y. and Miranda, M. (1988). Microinjecting DNA into mouse ova to study DNA replication and gene expression and to produce transgenic animals. Biotechniques 6, 662-680.
11. Dey, S. K., Lim, H., Das, S. K., Reese, J., Paria, B. C., Daikoku, T. and Wang, H. (2004). Molecular cues to implantation. Endocr. Rev. 25, 341-373.
12. Dumollard, R., Ward, Z., Carroll, J. and Duchen, M. R. (2007). Regulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455-465.
13. Dumollard, R., Carroll, J., Duchen, M. R., Campbell, K. and Swann, K. (2009). Mitochondrial function and redox state in mammalian embryos. Semin. Cell Dev. Biol. 20, 346-353.
14. Erbach, G. T., Lawitts, J. A., Papaioannou, V. E. and Biggers, J. D. (1994). Differential growth of the mouse preimplantation embryo in chemically defined media. Biol. Reprod. 50, 1027-1033.
15. Favetta, L. A., Madan, P., Mastromonaco, G. F., St John, E. J., King, W. A. and Betts, D. H. (2007). The oxidative stress adaptor p66Shc is required for permanent embryo arrest in vitro. BMC Dev. Biol. 7, 132.
16. Finkel, T. and Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247.
17. Gardner, D. K. (1998). Changes in requirements and utilization of nutrients during mammalian preimplantation embryo development and their significance in embryo culture. Theriogenology 49, 83-102.
18. Gardner, D. K. (2008). Dissection of culture media for embryos: the most important and less important components and characteristics. Reprod. Fertil. Dev. 20, 9-18.
19. Gardner, D. K. and Leese, H. J. (1990). Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J. Reprod. Fertil. 88, 361-368.
20. Gopichandran, N. and Leese, H. J. (2003). Metabolic characterization of the bovine blastocyst, inner cell mass, trophectoderm and blastocoel fluid. Reproduction 126, 299-308.
21. Gough, D. J., Corlett, A., Schlessinger, K., Wegrzyn, J., Larner, A. C. and Levy, D. E. (2009). Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 324, 1713-1716.
22. Guérin, P., El Mouatassim, S. and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175-189.
23. Harvey, A. J., Kind, K. L. and Thompson, J. G. (2002). REDOX regulation of early embryo development. Reproduction 123, 479-486.
24. Hayashi, S. and McMahon, A. P. (2002). Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244, 305-318.
25. Hewitson, L. C., Martin, K. L. and Leese, H. J. (1996). Effects of metabolic inhibitors on mouse preimplantation embryo development and the energy metabolism of isolated inner cell masses. Mol. Reprod. Dev. 43, 323-330.
26. Himeno, E., Tanaka, S. and Kunath, T. (2008). Isolation and manipulation of mouse trophoblast stem cells. Curr. Protoc. Stem Cell Biol. Chapter 1, Unit 1E 4.
27. Hirate, Y., Cockburn, K., Rossant, J. and Sasaki, H. (2012). Tead4 is constitutively nuclear, while nuclear vs. cytoplasmic Yap distribution is regulated in preimplantation mouse embryos. Proc. Natl. Acad. Sci. USA 109, E3389-E3390, author reply E3391-E3392.
28. Ho, Y., Wigglesworth, K., Eppig, J. J. and Schultz, R. M. (1995). Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol. Reprod. Dev. 41, 232-238.
29. Home, P., Ray, S., Dutta, D., Bronshteyn, I., Larson, M. and Paul, S. (2009). GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J. Biol. Chem. 284, 28729-28737.
30. Home, P., Saha, B., Ray, S., Dutta, D., Gunewardena, S., Yoo, B., Pal, A., Vivian, J. L., Larson, M., Petroff, M. et al. (2012). Altered subcellular localization of transcription factor TEAD4 regulates first mammalian cell lineage commitment. Proc. Natl. Acad. Sci. USA 109, 7362-7367.
31. Houghton, F. D. (2006). Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation 74, 11-18.
32. Houghton, F. D., Thompson, J. G., Kennedy, C. J. and Leese, H. J. (1996). Oxygen consumption and energy metabolism of the early mouse embryo. Mol. Reprod. Dev. 44, 476-485.
33. Houghton, F. D., Humpherson, P. G., Hawkhead, J. A., Hall, C. J. and Leese, H. J. (2003). Na+, K+, ATPase activity in the human and bovine preimplantation embryo. Dev. Biol. 263, 360-366.
34. Huang, T. T., Naeemuddin, M., Elchuri, S., Yamaguchi, M., Kozy, H. M., Carlson, E. J. and Epstein, C. J. (2006). Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum. Mol. Genet. 15, 1187-1194.
35. Jacquemin, P., Hwang, J. J., Martial, J. A., Dollé, P. and Davidson, I. (1996). A novel family of developmentally regulated mammalian transcription factors containing the TEA/ATTS DNA binding domain. J. Biol. Chem. 271, 21775-21785.
36. Jacquemin, P., Sapin, V., Alsat, E., Evain-Brion, D., Dollé, P. and Davidson, I. (1998). Differential expression of the TEF family of transcription factors in the murine placenta and during differentiation of primary human trophoblasts in vitro. Dev. Dyn. 212, 423-436.
37. Jansen, S., Cashman, K., Thompson, J. G., Pantaleon, M. and Kaye, P. L. (2009). Glucose deprivation, oxidative stress and peroxisome proliferator-activated receptor-alpha (PPARA) cause peroxisome proliferation in preimplantation mouse embryos. Reproduction 138, 493-505.
38. Jedrusik, A., Bruce, A. W., Tan, M. H., Leong, D. E., Skamagki, M., Yao, M. and Zernicka-Goetz, M. (2010). Maternally and zygotically provided Cdx2 have novel and critical roles for early development of the mouse embryo. Dev. Biol. 344, 66-78.
39. Johnson, M. H. and Nasr-Esfahani, M. H. (1994). Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? BioEssays 16, 31-38.
40. Johnson, M. T., Mahmood, S. and Patel, M. S. (2003). Intermediary metabolism and energetics during murine early embryogenesis. J. Biol. Chem. 278, 31457-31460.
41. Kaneko, K. J. and DePamphilis, M. L. (1998). Regulation of gene expression at the beginning of mammalian development and the TEAD family of transcription factors. Dev. Genet. 22, 43-55.
42. Kaneko, K. J., Cullinan, E. B., Latham, K. E. and DePamphilis, M. L. (1997). Transcription factor mTEAD-2 is selectively expressed at the beginning of zygotic gene expression in the mouse. Development 124, 1963-1973.
43. Kaneko, K. J., Rein, T., Guo, Z. S., Latham, K. and DePamphilis, M. L. (2004). DNA methylation may restrict but does not determine differential gene expression at the Sgy/Tead2 locus during mouse development. Mol. Cell. Biol. 24, 1968-1982.
44. Kaneko, K. J., Kohn, M. J., Liu, C. and DePamphilis, M. L. (2007). Transcription factor TEAD2 is involved in neural tube closure. Genesis 45, 577-587.
45. Kawamura, Y., Uchijima, Y., Horike, N., Tonami, K., Nishiyama, K., Amano, T., Asano, T., Kurihara, Y. and Kurihara, H. (2010). Sirt3 protects in vitrofertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest. J. Clin. Invest. 120, 2817-2828.
46. Kohn, M. J., Kaneko, K. J. and DePamphilis, M. L. (2011). Regulation of gene expression at the beginning of mammalian development. In Encyclopedia of Molecular Cell Biology and Molecular Medicine, 2nd edn (ed. R. A. Meyers). Weinheim: Wiley.
47. Korbie, D. J. and Mattick, J. S. (2008). Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat. Protoc. 3, 1452-1456.
48. Lane, M. and Gardner, D. K. (1996). Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum. Reprod. 11, 1975-1978.
49. Lane, M. and Gardner, D. K. (1997). Differential regulation of mouse embryo development and viability by amino acids. J. Reprod. Fertil. 109, 153-164.
50. Lane, M. and Gardner, D. K. (1998). Amino acids and vitamins prevent cultureinduced metabolic perturbations and associated loss of viability of mouse blastocysts. Hum. Reprod. 13, 991-997.
51. Lawitts, J. A. and Biggers, J. D. (1993). Culture of preimplantation embryos. Methods Enzymol. 225, 153-164.
52. Leese, H. J., Baumann, C. G., Brison, D. R., McEvoy, T. G. and Sturmey, R. G. (2008). Metabolism of the viable mammalian embryo: quietness revisited. Mol. Hum. Reprod. 14, 667-672.
53. Lewandoski, M., Wassarman, K. M. and Martin, G. R. (1997). Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line. Curr. Biol. 7, 148-151.
54. Macho, A., Decaudin, D., Castedo, M., Hirsch, T., Susin, S. A., Zamzami, N. and Kroemer, G. (1996). Chloromethyl-X-Rosamine is an aldehyde-fixable potential-sensitive fluorochrome for the detection of early apoptosis. Cytometry 25, 333-340.
55. Madan, P., Rose, K. and Watson, A. J. (2007). Na/K-ATPase beta1 subunit expression is required for blastocyst formation and normal assembly of trophectoderm tight junction-associated proteins. J. Biol. Chem. 282, 12127-12134.
56. Mathur, A., Hong, Y., Kemp, B. K., Barrientos, A. A. and Erusalimsky, J. D. (2000). Evaluation of fluorescent dyes for the detection of mitochondrial membrane potential changes in cultured cardiomyocytes. Cardiovasc. Res. 46, 126-138.
57. Nagaraj, R., Gururaja-Rao, S., Jones, K. T., Slattery, M., Negre, N., Braas, D., Christofk, H., White, K. P., Mann, R. and Banerjee, U. (2012). Control of mitochondrial structure and function by the Yorkie/YAP oncogenic pathway. Genes Dev. 26, 2027-2037.
58. Nagy, A., Gertsenstein, M., Vintersten, K. and Behringer, R. (2003). Summary of mouse development. In Manipulating the Mouse Embryo, pp. 31-139. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
59. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Schöler, H. and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391.
60. Nicklin, P., Bergman, P., Zhang, B., Triantafellow, E., Wang, H., Nyfeler, B., Yang, H., Hild, M., Kung, C., Wilson, C. et al. (2009). Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 136, 521-534.
61. Nishioka, N., Yamamoto, S., Kiyonari, H., Sato, H., Sawada, A., Ota, M., Nakao, K. and Sasaki, H. (2008). Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech. Dev. 125, 270-283.
62. Nishioka, N., Inoue, K., Adachi, K., Kiyonari, H., Ota, M., Ralston, A., Yabuta, N., Hirahara, S., Stephenson, R. O., Ogonuki, N. et al. (2009). The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398-410.
63. Orsi, N. M. and Leese, H. J. (2001). Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol. Reprod. Dev. 59, 44-53.
64. Pandolfi, P. P., Roth, M. E., Karis, A., Leonard, M. W., Dzierzak, E., Grosveld, F. G., Engel, J. D. and Lindenbaum, M. H. (1995). Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat. Genet. 11, 40-44.
65. Pérez-Crespo, M., Ramírez, M. A., Fernández-González, R., Rizos, D., Lonergan, P., Pintado, B. and Gutiérrez-Adán, A. (2005). Differential sensitivity of male and female mouse embryos to oxidative induced heatstress is mediated by glucose-6-phosphate dehydrogenase gene expression. Mol. Reprod. Dev. 72, 502-510.
66. Ralston, A. and Rossant, J. (2008). Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev. Biol. 313, 614-629.
67. Ralston, A., Cox, B. J., Nishioka, N., Sasaki, H., Chea, E., Rugg-Gunn, P., Guo, G., Robson, P., Draper, J. S. and Rossant, J. (2010). Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137, 395-403.
68. Reers, M., Smiley, S. T., Mottola-Hartshorn, C., Chen, A., Lin, M. and Chen, L. B. (1995). Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 260, 406-417.
69. Russ, A. P., Wattler, S., Colledge, W. H., Aparicio, S. A., Carlton, M. B., Pearce, J. J., Barton, S. C., Surani, M. A., Ryan, K., Nehls, M. C. et al. (2000). Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404, 95-99.
70. Saha, B., Home, P. and Paul, S. (2012). Reply to Sasaki et al.: TEAD4 is predominantly cytoplasmic in the inner cell mass of mouse blastocysts. Proc. Natl. Acad. Sci. USA 109, E3391-E3392.
71. Sengupta, S., Peterson, T. R. and Sabatini, D. M. (2010). Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40, 310-322.
72. Stern, S., Biggers, J. D. and Anderson, E. (1971). Mitochondria and early development of the mouse. J. Exp. Zool. 176, 179-191.
73. Strumpf, D., Mao, C. A., Yamanaka, Y., Ralston, A., Chawengsaksophak, K., Beck, F. and Rossant, J. (2005). Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093-2102.
74. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. and Rossant, J. (1998). Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075.
75. Thomson, J. L. (1967). Effect of inhibitors of carbohydrate metabolism on the development of preimplantation mouse embryos. Exp. Cell Res. 46, 252-262.
76. Turrens, J. F. (1997). Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 17, 3-8.
77. Ullah, Z., Kohn, M. J., Yagi, R., Vassilev, L. T. and DePamphilis, M. L. (2008). Differentiation of trophoblast stem cells into giant cells is triggered by p57/Kip2 inhibition of CDK1 activity. Genes Dev. 22, 3024-3036.
78. Van Blerkom, J. (2009). Mitochondria in early mammalian development. Semin. Cell Dev. Biol. 20, 354-364.
79. Vander Heiden, M. G., Cantley, L. C. and Thompson, C. B. (2009). Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033.
80. Vassilev, A., Kaneko, K. J., Shu, H., Zhao, Y. and DePamphilis, M. L. (2001). TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev. 15, 1229-1241.
81. Wale, P. L. and Gardner, D. K. (2012). Oxygen regulates amino acid turnover and carbohydrate uptake during the preimplantation period of mouse embryo development. Biol. Reprod. 87, 24, 1-8.
82. Wang, K., Degerny, C., Xu, M. and Yang, X. J. (2009). YAP, TAZ, and Yorkie: a conserved family of signal-responsive transcriptional coregulators in animal development and human disease. Biochem. Cell Biol. 87, 77-91.
83. Watson, A. J. and Barcroft, L. C. (2001). Regulation of blastocyst formation. Front. Biosci. 6, d708-d730.
84. Wise, D. R. and Thompson, C. B. (2010). Glutamine addiction: a new therapeutic target in cancer. Trends Biochem. Sci. 35, 427-433.
85. Wu, S., Liu, Y., Zheng, Y., Dong, J. and Pan, D. (2008). The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growthregulatory pathway. Dev. Cell 14, 388-398.
86. Wu, G., Gentile, L., Fuchikami, T., Sutter, J., Psathaki, K., Esteves, T. C., Araúzo-Bravo, M. J., Ortmeier, C., Verberk, G., Abe, K. et al. (2010). Initiation of trophectoderm lineage specification in mouse embryos is independent of Cdx2. Development 137, 4159-4169.
87. Yagi, R., Kohn, M. J., Karavanova, I., Kaneko, K. J., Vullhorst, D., DePamphilis, M. L. and Buonanno, A. (2007). Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134, 3827-3836.
88. Yang, S. H., Liu, R., Perez, E. J., Wen, Y., Stevens, S. M., Jr, Valencia, T., Brun-Zinkernagel, A. M., Prokai, L., Will, Y., Dykens, J. et al. (2004). Mitochondrial localization of estrogen receptor beta. Proc. Natl. Acad. Sci. USA 101, 4130-4135.
89. Zhang, C., Liu, C., Li, D., Yao, N., Yuan, X., Yu, A., Lu, C. and Ma, X. (2010). Intracellular redox imbalance and extracellular amino acid metabolic abnormality contribute to arsenic-induced developmental retardation in mouse preimplantation embryos. J. Cell. Physiol. 222, 444-455.
90. Zhang, F., Lau, S. S. and Monks, T. J. (2011). The cytoprotective effect of Nacetyl-L-cysteine against ROS-induced cytotoxicity is independent of its ability to enhance glutathione synthesis. Toxicol. Sci. 120, 87-97.