Leucine and arginine regulate trophoblast motility through mTOR-dependent and independent pathways in the preimplantation mouse embryo

Developmental Biology

Volumn 361, Issue 2, 2012, Pages 286-300

  González, Isabel M ^a   Martin, Patrick M ^b   Burdsal, Carol ^c   Sloan, Jennifer L ^d,e   Mager, Sela ^d   Harris, Thurl ^a   Sutherland, Ann E ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b NORTH CAROLINA A AND T STATE UNIVERSITY   (United States)

^c Tulane University   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

Amino acids; Blastocyst activation; Implantation; MTOR

Indexed keywords

ARGININE; INITIATION FACTOR 4E BINDING PROTEIN; LEUCINE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; S6 KINASE;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL MOTILITY; CONTROLLED STUDY; EMBRYO; GESTATIONAL AGE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NIDATION; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TROPHOBLAST;

MAMMALIA;

EID: 84355166527     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.10.021     Document Type: Article

References (118)

1. Barbet N.C., Schneider U., Helliwell S.B., Stansfield I., Tuite M.F., Hall M.N. TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 1996, 7:25-42.
2. Belchetz P.E., Plant T.M., Nakai Y., Keogh E.J., Knobil E. Hypophysial responses to continuous and intermittent delivery of hypopthalamic gonadotropin-releasing hormone. Science 1978, 202:631-633. (New York, N.Y.).
3. Bhatt H., Brunet L.J., Stewart C.L. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:11408-11412.
4. Biggers J.D., Borland R.M., Powers R.D. Transport mechanisms in the preimplantation mammalian embryo. Ciba Foundation symposium 1977, 129-153.
5. Bliss S.P., Navratil A.M., Xie J., Roberson M.S. GnRH signaling, the gonadotrope and endocrine control of fertility. Front. Neuroendocrinol. 2010, 31:322-340.
6. Borland R.M., Tasca R.J. Activation of a Na+-dependent amino acid transport system in preimplantation mouse embryos. Dev. Biol. 1974, 36:169-182.
7. Brown C., Lin Y., Hassid A. Requirement of protein tyrosine phosphatase SHP2 for NO-stimulated vascular smooth muscle cell motility. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H1598-H1605.
8. Brunn G.J., Hudson C.C., Sekulic A., Williams J.M., Hosoi H., Houghton P.J., Lawrence J.C., Abraham R.T. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 1997, 277:99-101. (New York, N.Y.).
9. Carson D.D., Tang J.P., Julian J. Heparan sulfate proteoglycan (perlecan) expression by mouse embryos during acquisition of attachment competence. Dev. Biol. 1993, 155:97-106.
10. Chang Y., Ceacareanu B., Dixit M., Sreejayan N., Hassid A. Nitric oxide-induced motility in aortic smooth muscle cells: role of protein tyrosine phosphatase SHP-2 and GTP-binding protein Rho. Circ. Res. 2002, 91:390-397.
11. Chen J.R., Cheng J.G., Shatzer T., Sewell L., Hernandez L., Stewart C.L. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 2000, 141:4365-4372.
12. Das S.K., Wang X.N., Paria B.C., Damm D., Abraham J.A., Klagsbrun M., Andrews G.K., Dey S.K. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 1994, 120:1071-1083.
13. Das S.K., Wang X.N., Paria B.C., Damm D., Abraham J.A., Klagsbrun M., Andrews G.K., Dey S.K. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 1994, 120:1071-1083. (Cambridge, England).
14. De Benedetti A., Rhoads R.E. Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:8212-8216.
15. Di Como C.J., Arndt K.T. Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 1996, 10:1904-1916.
16. Epstein C.J., Smith S.A. Amino acid uptake and protein synthesis in preimplanatation mouse embryos. Dev. Biol. 1973, 33:171-184.
17. Erbay E., Chen J. The mammalian target of rapamycin regulates C2C12 myogenesis via a kinase-independent mechanism. J. Biol. Chem. 2001, 276:36079-36082.
18. Erbay E., Park I.H., Nuzzi P.D., Schoenherr C.J., Chen J. IGF-II transcription in skeletal myogenesis is controlled by mTOR and nutrients. J. Cell Biol. 2003, 163:931-936.
19. Fadden P., Haystead T.A., Lawrence J.C. Identification of phosphorylation sites in the translational regulator, PHAS-I, that are controlled by insulin and rapamycin in rat adipocytes. J. Biol. Chem. 1997, 272:10240-10247.
20. Flach G., Johnson M.H., Braude P.R., Taylor R.A., Bolton V.N. The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J. 1982, 1:681-686.
21. Flinn R.J., Yan Y., Goswami S., Parker P.J., Backer J.M. The late endosome is essential for mTORC1 signaling. Mol. Biol. Cell 2010, 21:833-841.
22. Fouladi-Nashta A.A., Jones C.J., Nijjar N., Mohamet L., Smith A., Chambers I., Kimber S.J. Characterization of the uterine phenotype during the peri-implantation period for LIF-null, MF1 strain mice. Dev. Biol. 2005, 281:1-21.
23. Franco H.L., Lee K.Y., Broaddus R.R., White L.D., Lanske B., Lydon J.P., Jeong J.W., DeMayo F.J. Ablation of Indian hedgehog in the murine uterus results in decreased cell cycle progression, aberrant epidermal growth factor signaling, and increased estrogen signaling. Biol. Reprod. 2010, 82:783-790.
24. Franco H.L., Dai D., Lee K.Y., Rubel C.A., Roop D., Boerboom D., Jeong J.W., Lydon J.P., Bagchi I.C., Bagchi M.K., DeMayo F.J. WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB J. 2011, 25:1176-1187.
25. Gangloff Y.G., Mueller M., Dann S.G., Svoboda P., Sticker M., Spetz J.F., Um S.H., Brown E.J., Cereghini S., Thomas G., Kozma S.C. Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Mol. Cell. Biol. 2004, 24:9508-9516.
26. Ge Y., Sun Y., Chen J. IGF-II is regulated by microRNA-125b in skeletal myogenesis. J. Cell Biol. 2011, 192:69-81.
27. Gingras A.C., Gygi S.P., Raught B., Polakiewicz R.D., Abraham R.T., Hoekstra M.F., Aebersold R., Sonenberg N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 1999, 13:1422-1437.
28. Glantz, S., 1992. Primer of Biostatistics, in: McGraw-Hill (Ed.), San Francisco, CA, p. 438.
29. Guertin D.A., Stevens D.M., Thoreen C.C., Burds A.A., Kalaany N.Y., Moffat J., Brown M., Fitzgerald K.J., Sabatini D.M. Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1. Dev. Cell 2006, 11:859-871.
30. Gulhati P., Bowen K.A., Liu J., Stevens P.D., Rychahou P.G., Chen M., Lee E.Y., Weiss H.L., O'Connor K.L., Gao T., Evers B.M. mTORC1 and mTORC2 regulate EMT, motility, and metastasis of colorectal cancer via RhoA and Rac1 signaling pathways. Cancer Res. 2011, 71:3246-3256.
31. Gwatkin R.B. Defined media and development of mammalian eggs in vitro. Ann. N. Y. Acad. Sci. 1966, 139:79-90.
32. Hamatani T., Daikoku T., Wang H., Matsumoto H., Carter M.G., Ko M.S., Dey S.K. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10326-10331.
33. Hara K., Maruki Y., Long X., Yoshino K., Oshiro N., Hidayat S., Tokunaga C., Avruch J., Yonezawa K. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 2002, 110:177-189.
34. Harris S.E., Gopichandran N., Picton H.M., Leese H.J., Orsi N.M. Nutrient concentrations in murine follicular fluid and the female reproductive tract. Theriogenology 2005, 64:992-1006.
35. Hernandez-Negrete I., Carretero-Ortega J., Rosenfeldt H., Hernandez-Garcia R., Calderon-Salinas J.V., Reyes-Cruz G., Gutkind J.S., Vazquez-Prado J. P-Rex1 links mammalian target of rapamycin signaling to Rac activation and cell migration. J. Biol. Chem. 2007, 282:23708-23715.
36. Hillman N., Sherman M.I., Graham C. The effect of spatial arrangement on cell determination during mouse development. J. Embryol. Exp. Morphol. 1972, 28:263-278.
37. Kaliman P., Canicio J., Testar X., Palacin M., Zorzano A. Insulin-like growth factor-II, phosphatidylinositol 3-kinase, nuclear factor-kappaB and inducible nitric-oxide synthase define a common myogenic signaling pathway. J. Biol. Chem. 1999, 274:17437-17444.
38. Kanai-Azuma M., Kanai Y., Kurohmaru M., Sakai S., Hayashi Y. Insulin-like growth factor (IGF)-I stimulates proliferation and migration of mouse ectoplacental cone cells, while IGF-II transforms them into trophoblastic giant cells in vitro. Biol. Reprod. 1993, 48:252-261.
39. Kaur K., Yao J., Pan X., Matthews C., Hassid A. NO decreases phosphorylation of focal adhesion proteins via reduction of Ca in rat aortic smooth muscle cells. Am. J. Physiol. 1998, 274:H1613-H1619.
40. Kim D.H., Sarbassov D.D., Ali S.M., King J.E., Latek R.R., Erdjument-Bromage H., Tempst P., Sabatini D.M. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 2002, 110:163-175.
41. Kim J.Y., Burghardt R.C., Wu G., Johnson G.A., Spencer T.E., Bazer F.W. Select nutrients in the ovine uterine lumen. VII. Effects of arginine, leucine, glutamine, and glucose on trophectoderm cell signaling, proliferation, and migration. Biol. Reprod. 2011, 84:62-69.
42. Koromilas A.E., Lazaris-Karatzas A., Sonenberg N. mRNAs containing extensive secondary structure in their 5' non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E. EMBO J. 1992, 11:4153-4158.
43. Kunz J., Henriquez R., Schneider U., Deuter-Reinhard M., Movva N.R., Hall M.N. Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 1993, 73:585-596.
44. Laplante M., Sabatini D.M. An emerging role of mTOR in lipid biosynthesis. Curr. Biol. 2009, 19:R1046-R1052.
45. Laplante M., Sabatini D.M. mTOR signaling at a glance. J. Cell Sci. 2009, 122:3589-3594.
46. Large M.J., Demayo F.J. The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling. Mol. Cell. Endocrinol. 2011, doi:10.1016/j.mce.2011.07.027.
47. Lazaris-Karatzas A., Montine K.S., Sonenberg N. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5' cap. Nature 1990, 345:544-547.
48. Lee J.E., Pintar J., Efstratiadis A. Pattern of the insulin-like growth factor II gene expression during early mouse embryogenesis. Development 1990, 110:151-159. (Cambridge, England).
49. Lee K., Jeong J., Kwak I., Yu C.T., Lanske B., Soegiarto D.W., Toftgard R., Tsai M.J., Tsai S., Lydon J.P., DeMayo F.J. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat. Genet. 2006, 38:1204-1209.
50. Levey I.L., Brinster R.L. Effects of alpha-amanitin on RNA synthesis by mouse embryos in culture. J. Exp. Zool. 1978, 203:351-360.
51. Levine J.E., Ramirez V.D. Luteinizing hormone-releasing hormone release during the rat estrous cycle and after ovariectomy, as estimated with push-pull cannulae. Endocrinology 1982, 111:1439-1448.
52. Levine J.E., Pau K.Y., Ramirez V.D., Jackson G.L. Simultaneous measurement of luteinizing hormone-releasing hormone and luteinizing hormone release in unanesthetized, ovariectomized sheep. Endocrinology 1982, 111:1449-1455.
53. Lin T.A., Kong X., Haystead T.A., Pause A., Belsham G., Sonenberg N., Lawrence J.C. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 1994, 266:653-656. (New York, N.Y.).
54. Lindell T.J., Weinberg F., Morris P.W., Roeder R.G., Rutter W.J. Specific inhibition of nuclear RNA polymerase II by alpha-amanitin. Science 1970, 170:447-449. (New York, N.Y.).
55. Liu L., Li F., Cardelli J.A., Martin K.A., Blenis J., Huang S. Rapamycin inhibits cell motility by suppression of mTOR-mediated S6K1 and 4E-BP1 pathways. Oncogene 2006, 25:7029-7040.
56. Lubahn D.B., Moyer J.S., Golding T.S., Couse J.F., Korach K.S., Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11162-11166.
57. Lydon J.P., DeMayo F.J., Funk C.R., Mani S.K., Hughes A.R., Montgomery C.A., Shyamala G., Conneely O.M., O'Malley B.W. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 1995, 9:2266-2278.
58. Martin P.M., Sutherland A.E. Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway. Dev. Biol. 2001, 240:182-193.
59. Martin P.M., Sutherland A.E., Van Winkle L.J. Amino acid transport regulates blastocyst implantation. Biol. Reprod. 2003, 69:1101-1108.
60. Midgley A.R., Jaffe R.B. Regulation of human gonadotropins. X. Episodic fluctuation of LH during the menstrual cycle. J. Clin. Endocrinol. Metab. 1971, 33:962-969.
61. Mothe-Satney I., Brunn G.J., McMahon L.P., Capaldo C.T., Abraham R.T., Lawrence J.C. Mammalian target of rapamycin-dependent phosphorylation of PHAS-I in four (S/T)P sites detected by phospho-specific antibodies. J. Biol. Chem. 2000, 275:33836-33843.
62. Mothe-Satney I., Yang D., Fadden P., Haystead T.A., Lawrence J.C. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T)P sites that govern translational repression. Mol. Cell. Biol. 2000, 20:3558-3567.
63. Naeslund G. The effect of glucose-, arginine- and leucine-deprivation on mouse blastocyst outgrowth in vitro. Ups. J. Med. Sci. 1979, 84:9-20.
64. Nicklin P., Bergman P., Zhang B., Triantafellow E., Wang H., Nyfeler B., Yang H., Hild M., Kung C., Wilson C., Myer V.E., MacKeigan J.P., Porter J.A., Wang Y.K., Cantley L.C., Finan P.M., Murphy L.O. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 2009, 136:521-534.
65. Nilsson B.O., Ljung L. X-ray micro analyses of cations (Na, K, Ca) and anions (S, P, Cl) in uterine secretions during blastocyst implantation in the rat. J. Exp. Zool. 1985, 234:415-421.
66. Palacin M., Nunes V., Font-Llitjos M., Jimenez-Vidal M., Fort J., Gasol E., Pineda M., Feliubadalo L., Chillaron J., Zorzano A. The genetics of heteromeric amino acid transporters. Physiology 2005, 20:112-124. (Bethesda, Md.).
67. Paria B.C., Das S.K., Andrews G.K., Dey S.K. Expression of the epidermal growth factor receptor gene is regulated in mouse blastocysts during delayed implantation. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:55-59.
68. Paria B.C., Huet-Hudson Y.M., Dey S.K. Blastocyst's state of activity determines the "window" of implantation in the receptive mouse uterus. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:10159-10162.
69. Pause A., Belsham G.J., Gingras A.C., Donze O., Lin T.A., Lawrence J.C., Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5'-cap function. Nature 1994, 371:762-767.
70. Pendeville H., Carpino N., Marine J.C., Takahashi Y., Muller M., Martial J.A., Cleveland J.L. The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol. Cell. Biol. 2001, 21:6549-6558.
71. Psychoyos A. Hormonal control of ovoimplantation. Vitam. Horm. 1973, 31:201-256.
72. Psychoyos A. Endocrine control of egg implantation. Handbook of Physiology 1973, 187-215. American Physiological Society, Washington, D.C. R.O. Greep, E.B. Astwood (Eds.).
73. Raab G., Kover K., Paria B.C., Dey S.K., Ezzell R.M., Klagsbrun M. Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor. Development 1996, 122:637-645. (Cambridge, England).
74. Ramathal C.Y., Bagchi I.C., Taylor R.N., Bagchi M.K. Endometrial decidualization: of mice and men. Semin. Reprod. Med. 2010, 28:17-26.
75. Sancak Y., Peterson T.R., Shaul Y.D., Lindquist R.A., Thoreen C.C., Bar-Peled L., Sabatini D.M. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 2008, 320:1496-1501. (New York, N.Y.).
76. Sancak Y., Bar-Peled L., Zoncu R., Markhard A.L., Nada S., Sabatini D.M. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010, 141:290-303.
77. Santen R.J., Bardin C.W. Episodic luteinizing hormone secretion in man. Pulse analysis, clinical interpretation, physiologic mechanisms. J. Clin. Investig. 1973, 52:2617-2628.
78. Sarbassov D.D., Ali S.M., Kim D.H., Guertin D.A., Latek R.R., Erdjument-Bromage H., Tempst P., Sabatini D.M. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 2004, 14:1296-1302.
79. Schultz J.F., Armant D.R. Beta 1- and beta 3-class integrins mediate fibronectin binding activity at the surface of developing mouse peri-implantation blastocysts. Regulation by ligand-induced mobilization of stored receptor. J. Biol. Chem. 1995, 270:11522-11531.
80. Schultz J.F., Mayernik L., Rout U.K., Armant D.R. Integrin trafficking regulates adhesion to fibronectin during differentiation of mouse peri-implantation blastocysts. Dev. Genet. 1997, 21:31-43.
81. Sengoku K., Takuma N., Horikawa M., Tsuchiya K., Komori H., Sharifa D., Tamate K., Ishikawa M. Requirement of nitric oxide for murine oocyte maturation, embryo development, and trophoblast outgrowth in vitro. Mol. Reprod. Dev. 2001, 58:262-268.
82. Shama S., Meyuhas O. The translational cis-regulatory element of mammalian ribosomal protein mRNAs is recognized by the plant translational apparatus. Eur. J. Biochem. 1996, 236:383-388.
83. Shen M.M., Leder P. Leukemia inhibitory factor is expressed by the preimplantation uterus and selectively blocks primitive ectoderm formation in vitro. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:8240-8244.
84. Sloan J.L. Cloning and Charaterization of the Amino Acid Transporter ATB(0,+), Neurobiology 2002, 193. University of North Carolina at Chapel Hill, Chapel Hill.
85. Sloan J.L., Mager S. Cloning and functional expression of a human Na(+) and Cl(-)-dependent neutral and cationic amino acid transporter B(0+). J. Biol. Chem. 1999, 274:23740-23745.
86. Song H., Lim H., Das S.K., Paria B.C., Dey S.K. Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol. Endocrinol. 2000, 14:1147-1161. (Baltimore, Md.).
87. Song H., Lim H., Paria B.C., Matsumoto H., Swift L.L., Morrow J., Bonventre J.V., Dey S.K. Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development 2002, 129:2879-2889. (Cambridge, England).
88. Spindle A. An improved culture medium for mouse blastocysts. In Vitro 1980, 16:669-674.
89. Spindle A.I., Pedersen R.A. Hatching, attachment, and outgrowth of mouse blastocysts in vitro: fixed nitrogen requirements. J. Exp. Zool. 1973, 186:305-318.
90. Squarize C.H., Castilho R.M., Bugge T.H., Gutkind J.S. Accelerated wound healing by mTOR activation in genetically defined mouse models. PLoS One 2010, 5:e10643.
91. Stephens L.E., Sutherland A.E., Klimanskaya I.V., Andrieux A., Meneses J., Pedersen R.A., Damsky C.H. Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 1995, 9:1883-1895.
92. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Kontgen F., Abbondanzo S.J. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992, 359:76-79.
93. Sutherland A.E., Calarco P.G., Damsky C.H. Developmental regulation of integrin expression at the time of implantation in the mouse embryo. Development 1993, 119:1175-1186. (Cambridge, England).
94. Tarkowski A.K., Wroblewska J. Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J. Embryol. Exp. Morphol. 1967, 18:155-180.
95. Tranguch S., Daikoku T., Guo Y., Wang H., Dey S.K. Molecular complexity in establishing uterine receptivity and implantation. Cell. Mol. Life Sci. 2005, 62:1964-1973.
96. Van Winkle L.J. Activation of amino acid accumulation in delayed implantation mouse blastocysts. J. Exp. Zool. 1981, 218:239-246.
97. Van Winkle L.J. Amino acid transport regulation and early embryo development. Biol. Reprod. 2001, 64:1-12.
98. Van Winkle L.J., Campione A.L., Webster D.P. Sodium ion concentrations in uterine flushings from "implanting" and "delayed implanting" mice. J. Exp. Zool. 1983, 226:321-324.
99. Van Winkle L.J., Christensen H.N., Campione A.L. Na+-dependent transport of basic, zwitterionic, and bicyclic amino acids by a broad-scope system in mouse blastocysts. J. Biol. Chem. 1985, 260:12118-12123.
100. Van Winkle L.J., Haghighat N., Campione A.L., Gorman J.M. Glycine transport in mouse eggs and preimplantation conceptuses. Biochim. Biophys. Acta 1988, 941:241-256.
101. Van Winkle D.M., Matsuki T., Gad N.M., Jordan M.C., Downey J.M. Left ventricular unloading during reperfusion does not limit myocardial infarct size. Circulation 1990, 81:1374-1379.
102. 0,+ in blastocysts by inorganic and organic cations yields insight into the structure of its amino acid receptor site. Biochim. Biophys. Acta 1990, 1025:215-224.
103. 0,+ amino acid transport regulates the penetration stage of blastocyst implantation with possible long-term developmental consequences through adulthood. Hum. Reprod. Updat. 2006, 12:145-157.
104. Wakitani S., Hondo E., Phichitraslip T., Stewart C.L., Kiso Y. Upregulation of Indian hedgehog gene in the uterine epithelium by leukemia inhibitory factor during mouse implantation. J. Reprod. Dev. 2008, 54:113-116.
105. Wang X.N., Das S.K., Damm D., Klagsbrun M., Abraham J.A., Dey S.K. Differential regulation of heparin-binding epidermal growth factor-like growth factor in the adult ovariectomized mouse uterus by progesterone and estrogen. Endocrinology 1994, 135:1264-1271.
106. Wang J., Mayernik L., Schultz J.F., Armant D.R. Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts. Development 2000, 127:33-44. (Cambridge, England).
107. Wang J., Mayernik L., Armant D.R. Integrin signaling regulates blastocyst adhesion to fibronectin at implantation: intracellular calcium transients and vesicle trafficking in primary trophoblast cells. Dev. Biol. 2002, 245:270-279.
108. Wang H., Ma W.G., Tejada L., Zhang H., Morrow J.D., Das S.K., Dey S.K. Rescue of female infertility from the loss of cyclooxygenase-2 by compensatory up-regulation of cyclooxygenase-1 is a function of genetic makeup. J. Biol. Chem. 2004, 279:10649-10658.
109. Wang H., Xie H., Sun X., Tranguch S., Zhang H., Jia X., Wang D., Das S.K., Desvergne B., Wahli W., DuBois R.N., Dey S.K. Stage-specific integration of maternal and embryonic peroxisome proliferator-activated receptor delta signaling is critical to pregnancy success. J. Biol. Chem. 2007, 282:37770-37782.
110. Wilcox A.J., Baird D.D., Weinberg C.R. Time of implantation of the conceptus and loss of pregnancy. N. Engl. J. Med. 1999, 340:1796-1799.
111. Xie H., Tranguch S., Jia X., Zhang H., Das S.K., Dey S.K., Kuo C.J., Wang H. Inactivation of nuclear Wnt-beta-catenin signaling limits blastocyst competency for implantation. Development 2008, 135:717-727. (Cambridge, England).
112. Yang Q., Guan K.L. Expanding mTOR signaling. Cell Res. 2007, 17:666-681.
113. Ye X., Hama K., Contos J.J., Anliker B., Inoue A., Skinner M.K., Suzuki H., Amano T., Kennedy G., Arai H., Aoki J., Chun J. LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature 2005, 435:104-108.
114. Yelian F.D., Yang Y., Hirata J.D., Schultz J.F., Armant D.R. Molecular interactions between fibronectin and integrins during mouse blastocyst outgrowth. Mol. Reprod. Dev. 1995, 41:435-448.
115. Yoshinaga K., Adams C.E. Delayed implantation in the spayed, progesterone treated adult mouse. J. Reprod. Fertil. 1966, 12:593-595.
116. Yoshinaga K., Hawkins R.A., Stocker J.F. Estrogen secretion by the rat ovary in vivo during the estrous cycle and pregnancy. Endocrinology 1969, 85:103-112.
117. Zhao Y.C., Chi Y.J., Yu Y.S., Liu J.L., Su R.W., Ma X.H., Shan C.H., Yang Z.M. Polyamines are essential in embryo implantation: expression and function of polyamine-related genes in mouse uterus during peri-implantation period. Endocrinology 2008, 149:2325-2332.
118. Ziomek C.A., Johnson M.H. Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell 1980, 21:935-942.