Involvement of the STAT5 signaling pathway in the regulation of mouse preimplantation development

Biology of Reproduction

Volumn 75, Issue 4, 2006, Pages 508-517

  Nakasato, Makoto ^a   Shirakura, Yoshiyuki ^a   Ooga, Masatoshi ^a   Iwatsuki, Masato ^a   Ito, Masahiko ^a   Kageyama, Shun Ichiro ^a   Sakai, Senkiti ^b   Nagata, Masao ^a   Aoki, Fugaku ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Developmental biology; Early development; Embryo; Growth factors; Signal transduction

Indexed keywords

CYTOKINE; JANUS KINASE; PROTEIN TYROSINE KINASE; STAT5 PROTEIN; STAT5A PROTEIN; STAT5B PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; GENE EXPRESSION REGULATION; GROWTH REGULATION; HORMONAL REGULATION; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NONHUMAN; NUCLEAR IMPORT; NUCLEOTIDE SEQUENCE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BLASTOCYST; EMBRYONIC DEVELOPMENT; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INDOLES; MALE; MICE; MICE, INBRED ICR; MICE, INBRED STRAINS; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; STAT5 TRANSCRIPTION FACTOR; SULFONAMIDES; TYRPHOSTINS;

MAMMALIA;

EID: 33749044834     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.105.047860     Document Type: Article

References (59)

1. Markham KE, Kaye PL. Growth hormone, insulin-like growth factor I and cell proliferation in the mouse blastocyst. Reproduction 2003; 125:327-336.
2. Robertson SA, Sjoblom C, Jasper MJ, Norman RJ, Seamark RF. Granulocyte-macrophage colony-stimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos. Biol Reprod 2001; 64:1206-1215.
3. Binart N, Melaine N, Pineau C, Kercret H, Touzalin AM, Bollore PI, Kelly PA. Male reproductive function is not affected in prolactin receptor-deficient mice. Endocrinology 2003; 144:3779-3782.
4. Gouilleux F, Wakao H, Mundt M, Groner B. Prolactin induces phosphorylation of Tyr694 of Stat5 (MGF), a prerequisite for DNA binding and induction of transcription. EMBO J 1994; 13:4361-4369.
5. Groner B, Gouilleux F. Prolactin-mediated gene activation in mammary epithelial cells. Curr Opin Genet Dev 1995; 5:587-594.
6. Groner B. Transcription factor regulation in mammary epithelial cells. Domest Anim Endocrinol 2002; 23:25-32.
7. Liu X, Robinson GW, Gouilleux F, Groner B, Hennighausen L. Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue. Proc Natl Acad Sci U S A 1995; 92:8831-8835.
8. Cella N, Groner B, Hynes NE. Characterization of Stat5a and Stat5b homodimers and heterodimers and their association with the glucocortiocoid receptor in mammary cells. Mol Cell Biol 1998; 18:1783-1792.
9. Pless M, Norga K, Carroll M, Heim MH, D'Andrea AD, Mathey-Prevot B. Receptors that induce erythroid differentiation of Ba/F3 cells: structural requirements and effect on STAT5 binding. Blood 1997; 89:3175-3185.
10. Woldman I, Mellitzer G, Kieslinger M, Buchhart D, Meinke A, Beug H, Decker T. STAT5 involvement in the differentiation response of primary chicken myeloid progenitor cells to chicken myelomonocytic growth factor. J Immunol 1997; 159:877-886.
11. Friedrichsen BN, Richter HE, Hansen JA, Rhodes CJ, Nielsen JH, Billestrup N, Moldrup A. Signal transducer and activator of transcription 5 activation is sufficient to drive transcriptional induction of cyclin D2 gene and proliferation of rat pancreatic beta-cells. Mol Endocrinol 2003; 17:945-958.
12. Shelburne CP, McCoy ME, Piekorz R, Sexl V, Roh KH, Jacobs-Helber SM, Gillespie SR, Bailey DP, Mirmonsef P, Mann MN, Kashyap M, Wright HV, et al. Stat5 expression is critical for mast cell development and survival. Blood 2003; 102:1290-1297.
13. Baskiewicz-Masiuk M, Machalinski B. The role of the STAT5 proteins in the proliferation and apoptosis of the CML and AML cells. Eur J Haematol 2004; 72:420-429.
14. Teglund S, McKay C, Schuetz E, van Deursen JM, Stravopodis D, Wang D, Brown M, Bodner S, Grosveld G, Ihle JN. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 1998; 93:841-850.
15. Darnell JE Jr. STATs and Gene Regulation. Science 1997; 277:1630-1635.
16. Finbloom DS, Larner AC. Regulation of the Jak/STAT signalling pathway. Cell Signal 1995; 7:739-745.
17. IhIe JN, Kerr IM. Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet 1995; 11:69-74.
18. Sattler M, Durstin MA, Frank DA, Okuda K, Kaushansky K, Salgia R, Griffin JD. The thrombopoietin receptor c-MPL activates JAK2 and TYK2 tyrosine kinases. Exp Hematol 1995; 23:1040-1048.
19. Okutani Y, Kitanaka A, Tanaka T, Kamano H, Ohnishi H, Kubota Y, Ishida T, Takahara J. Src directly tyrosine-phosphorylates STAT5 on its activation site and is involved in erythropoietin-induced signaling pathway. Oncogene 2001; 20:6643-6650.
20. Xi S, Zhang Q, Dyer KF, Lerner EC, Smithgall TE, Gooding WE, Kamens J, Grandis JR. Src kinases mediate STAT growth pathways in squamous cell carcinoma of the head and neck. J Biol Chem 2003; 278:31574-31583.
21. Silva CM. Role of STATs as downstream signal transducers in Src family kinase-mediated tumorigenesis. Oncogene 2004; 23:8017-8023.
22. Whitten WK. Nutrient requirements for the culture of preimplantation embryos in vitro. In: Raspé G, (ed.), Advances in the Biosciences, vol. 6. Oxford, UK: Pergamon Press; 1971:129-141.
23. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 1989; 86:679-688.
24. Evans JP, Schultz RM, Kopf GS. Identification and localization of integrin subunits in oocytes and eggs of the mouse. Mol Reprod Dev 1995; 40: 211-220.
25. Kim J-M, Ogura A, Nagata M, Aoki F. Analysis of the chromatin remodeling in the embryos reconstructed by somatic nuclear transfer. Biol Reprod 2002; 67:760-766.
26. Schultz RM. Regulation of zygotic gene activation in the mouse. Bioessays 1993; 15:531-538.
27. Liu X, Robinson GW, Hennighausen L. Activation of Stat5a and Stat5b by tyrosine phosphorylation is tightly linked to mammary gland differentiation. Mol Endocrinol 1996; 10:1496-1506.
28. Lu L, Zhu J, Zheng Z, Yan M, Xu W, Sun L, Theze J, Liu X. Jak-STAT pathway is involved in the induction of TNF-beta gene during stimulation by IL-2. Eur J Immunol 1998; 28:805-810.
29. Nosaka T, Kawashima T, Misawa K, Ikuta K, Mui AL, Kitamura T. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J 1999; 18:4754-4765.
30. Takahashi S, Harigae H, Kaku M, Sasaki T, Licht JD. Flt3 mutation activates p21WAF1/CIP1 gene expression through the action of STAT5. Biochem Biophys Res Commun 2004; 316:85-92.
31. Wakao H, Gouilleux F, Groner B. Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 1994; 13:2182-2191.
32. Yoshimura A, Ichihara M, Kinjyo I, Moriyama M, Copeland NG, Gilbert DJ, Jenkins NA, Hara T, Miyajima A. Mouse oncostatin M: an immediate early gene induced by multiple cytokines through the JAK-STAT5 pathway. EMBO J 1996; 15:1055-1063.
33. Hamatani T, Daikoku T, Wang H, Matsumoto H, Carter MG, Ko MS, Dey SK. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci USA 2004; 101:10326-10331.
34. 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; 6:133-144.
35. Zeng F, Baldwin DA, Schultz RM. Transcript profiling during preimplantation mouse development. Dev Biol 2004; 272:483-496.
36. Piko L, Clegg KB. Quantitative changes in total RNA, total poly(A), and ribosomes in early mouse embryos. Dev Biol 1982; 89:362-378.
37. Boutinaud M, Jammes H. Growth hormone increases Stat5 and Stat1 expression in lactating goat mammary gland: a specific effect compared to milking frequency. Domest Anim Endocrinol 2004; 27:363-378.
38. Pantaleon M, Whiteside EJ, Harvey MB, Barnard RT, Waters MJ, Kaye PL. Functional growth hormone (GH) receptors and GH are expressed by preimplantation mouse embryos: A role for GH in earlygenesis? Proc Natl Acad Sci U S A 1997; 94:5125-5130.
39. Crispi S, Sanzari E, Monfregola J, De Felice N, Fimiani G, Ambrosio R, D'Urso M, Ursini MV. Characterization of the human STAT5A and STAT5B promoters: evidence of a positive and negative mechanism of transcriptional regulation. FEBS Lett 2004; 562:27-34.
40. Copeland NG, Gilbert DJ, Schindler C, Zhong Z, Wen Z, Darnell JE Jr, Mui AL, Miyajima A, Quelle FW, Ihle JN, Jenkins NA. Distribution of the mammalian Stat gene family in mouse chromosomes. Genomics 1995; 29:225-228.
41. Bounial C, Nguyen E, Debey P. Endogenous transcription occurs at the 1-cell stage in the mouse embryos. Exp Cell Res 1995; 218:57-62.
42. Aoki F, Worrad DM, Schultz RM. Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol 1997; 181:296-307.
43. Meydan N, Grunberger T, Dadi H, Shahar M, Arpaia E, Lapidot Z, Leeder JS, Freedman M, Cohen A, Gazit A, Levitzki A, Roifman CM. Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 1996; 379:645-648.
44. Blake RA, Broome MA, Liu X, Wu J, Gishizky M, Sun L, Courtneidge SA. SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol Cell Biol 2000; 20:9018-9027.
45. Talmor-Cohen A, Tomashov-Matar R, Tsai WB, Kinsey WH, Shalgi R. Fyn kinase-tubulin interaction during meiosis of rat eggs. Reproduction 2004; 128:387-393.
46. Nakasato M, Nagata M, Aoki F. Expression of cytokine receptors in preimplantation mouse embryos. J Mamm Ova Res 2004; 21:128-133.
47. Leong PL, Xi S, Drenning SD, Dyer KF, Wentzel AL, Lemer EC, Smithgall TE, Grandis JR. Differential function of STAT5 isoforms in head and neck cancer growth control. Oncogene 2002; 21:2846-2853.
48. Storz P, Doppler H, Pfizenmaier K, Muller G. Insulin selectively activates STAT5b, but not STAT5a, via a JAK2-independent signalling pathway in Kym-1 rhabdomyosarcoma cells. FEBS Lett 1999; 464:159-163.
49. Rosen RL, Winestock KD, Chen G, Liu X, Hennighausen L, Finbloom DS. Granulocyte-macrophage colony-stimulating factor preferentially activates the 94-kD STAT5A and an 80-kD STAT5A isoform in human peripheral blood monocytes. Blood 1996; 88:1206-1214.
50. Morita H, Tahara T, Matsumoto A, Kato T, Miyazaki H, Ohashi H. Functional analysis of the cytoplasmic domain of the human Mpl receptor for tyrosine-phosphorylation of the signaling molecules, proliferation and differentiation. FEBS Lett 1996; 395:228-234.
51. Friedrich K, Kammer W, Erhardt I, Brandlein S, Sebald W, Moriggl R. Activation of STAT5 by IL-4 relies on Janus kinase function but not on receptor tyrosine phosphorylation, and can contribute to both cell proliferation and gene regulation. Int Immunol 1999; 11:1283-1294.
52. Demoulin JB, Uyttenhove C, Lejeune D, Mui A, Groner B, Renauld JC. STAT5 activation is required for interleukin-9-dependent growth and transformation of lymphoid cells. Cancer Res 2000; 60:3971-3977.
53. Grimley PM, Dong F, Rui H. Stat5a and Stat5b: fraternal twins of signal transduction and transcriptional activation. Cytokine Growth Factor Rev 1999; 10:131-157.
54. Bachvarova R, Moy K. Autoradiographic studies on the distribution of labeled maternal RNA in early mouse embryos. J Exp Zool 1985; 233:397-403.
55. Bolton VN, Oades PJ, Johnson MH. The relationship between cleavage, DNA replication, and gene expression in the mouse 2-cell embryo. J Embryol Exp Morphol 1984; 79:139-163.
56. Schultz RM, Davis W Jr, Stein P, Svoboda P. Reprogramming of gene expression during preimplantation development. J Exp Zool 1999; 285:276-282.
57. Ito M, Nakasato M, Suzuki T, Sakai S, Nagata M, Aoki F. Localization of Janus kinase 2 to the nuclei of mature oocytes and early cleavage stage mouse embryos. Biol Reprod 2004; 71:89-96.
58. Sato K, Nagao T, Iwasaki T, Nishihira Y, Fukami Y. Src-dependent phosphorylation of the EGF receptor Tyr-845 mediates Stat-p21waf1 pathway in A431 cells. Genes Cells 2003; 8:995-1003.
59. Moon SK, Jung SY, Kim CH. Transcription factor Sp1 mediates p38MAPK-dependent activation of the p21WAF1 gene promoter in vascular smooth muscle cells by pyrrolidine dithiocarbamate. Biochem Biophys Res Commun 2004; 316:605-611.