Acquisition of essential somatic cell cycle regulatory protein expression and implied activity occurs at the second to third cell division in mouse preimplantation embryos

FEBS Letters

Volumn 579, Issue 2, 2005, Pages 398-408

  Xie, Yufen ^a   Sun, Tong ^a   Wang, Q Tian ^b   Wang, Yingchun ^a   Wang, Fangfei ^a   Puscheck, Elizabeth ^a   Rappolee, Daniel A ^a  

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

^b STANFORD UNIVERSITY   (United States)

Author keywords

DP 1; Implantation; Lethal gene; Max; Mouse embryo; Myc proto oncogene; Placenta; Proliferation; Retinoblastoma; Trophoblast; Trophoblast stem cell

Indexed keywords

CELL CYCLE PROTEIN; MAX PROTEIN; MYC PROTEIN; PHOSPHOPROTEIN; PROTEIN DP1; REGULATOR PROTEIN; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIVISION; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; EMBRYO; GENE EXPRESSION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SOMATIC CELL;

NASA DISCIPLINE DEVELOPMENTAL BIOLOGY; NON-NASA CENTER;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL CYCLE PROTEINS; CELL DIVISION; CELL NUCLEUS; CELLS, CULTURED; DNA-BINDING PROTEINS; EMBRYO; EMBRYO IMPLANTATION; FEMALE; G1 PHASE; GENE EXPRESSION; GENES, LETHAL; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PREGNANCY; PROTO-ONCOGENE PROTEINS C-MYC; RETINOBLASTOMA PROTEIN; RNA, MESSENGER; TRANSCRIPTION FACTOR DP1; TRANSCRIPTION FACTORS;

EID: 11844301607     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2004.10.109     Document Type: Article

References (65)

1. K. Ahmad, and R.K. Naz Antibodies to sperm surface antigens and the c-myc proto-oncogene product inhibit early embryonic development in mice Biol. Reprod. 45 1991 841 850
2. C.E. Asker, K.P. Magnusson, S.P. Piccoli, K. Andersson, G. Klein, M.D. Cole, and K.G. Wiman Mouse and rat B-myc share amino acid sequence homology with the c-myc transcriptional activator domain and contain a B-myc specific carboxy terminal region Oncogene 11 1995 1963 1969
3. P. Bhatnagar, V.E. Papaioannou, and J.D. Biggers CSF-1 and mouse preimplantation development in vitro Development 121 1995 1333 1339
4. A.N. Billin, A.L. Eilers, K.L. Coulter, J.S. Logan, and D.E. Ayer MondoA, a novel basic helix-loop-helix-leucine zipper transcriptional activator that constitutes a positive branch of a max-like network Mol. Cell Biol. 20 2000 8845 8854
5. A.N. Billin, A.L. Eilers, C. Queva, and D.E. Ayer Mlx, a novel Max-like BHLHZip protein that interacts with the Max network of transcription factors J. Biol. Chem. 274 1999 36344 36350
6. T. Boulikas Phosphorylation of transcription factors and control of the cell cycle Crit. Rev. Eukaryot. Gene Expr. 5 1995 1 77
7. C.A. Brenner, R.R. Adler, D.A. Rappolee, R.A. Pedersen, and Z. Werb Genes for extracellular-matrix-degrading metalloproteinases and their inhibitor, TIMP, are expressed during early mammalian development Genes Dev. 3 1989 848 859
8. A.J. Canhoto, A. Chestukhin, L. Litovchick, and J.A. DeCaprio Phosphorylation of the retinoblastoma-related protein p130 in growth-arrested cells Oncogene 19 2000 5116 5122
9. N. Chai, Y. Patel, K. Jacobson, J. McMahon, A. McMahon, and D.A. Rappolee FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos Dev. Biol. 198 1998 105 115
10. Y.F. Chen, H.H. Chiu, C.H. Wu, J.Y. Wang, F.M. Chen, W.H. Tzou, S.J. Shin, and S.R. Lin Retinoblastoma protein (pRB) was significantly phosphorylated through a Ras-to-MAPK pathway in mutant K-ras stably transfected human adrenocortical cells DNA Cell Biol. 22 2003 657 664
11. C.F. Chuang, and S.Y. Ng Functional divergence of the MAP kinase pathway. ERK1 and ERK2 activate specific transcription factors FEBS Lett. 346 1994 229 234
12. L.B. Corson, Y. Yamanaka, K.M. Lai, and J. Rossant Spatial and temporal patterns of ERK signaling during mouse embryogenesis Development 130 2003 4527 4537
13. C.V. Dang, and W.M. Lee Identification of the human c-myc protein nuclear translocation signal Mol. Cell Biol. 8 1988 4048 4054
14. J. De Greve, J. Battey, J. Fedorko, M. Birrer, G. Evan, F. Kaye, E. Sausville, and J. Minna The human L-myc gene encodes multiple nuclear phosphoproteins from alternatively processed mRNAs Mol. Cell Biol. 8 1988 4381 4388
15. A.D. Domashenko, K.E. Latham, and K.S. Hatton Expression of myc-family, myc-interacting, and myc-target genes during preimplantation mouse development Mol. Reprod. Dev. 47 1997 57 65
16. M. Doree, and S. Galas The cyclin-dependent protein kinases and the control of cell division FASEB J. 8 1994 1114 1121
17. Y. Durocher, A. Chapdelaine, and S. Chevalier Tyrosine protein kinase activity of human hyperplastic prostate and carcinoma cell lines PC3 and DU145 Cancer Res. 49 1989 4818 4823
18. D.W. Goodrich, N.P. Wang, Y.W. Qian, E.Y. Lee, and W.H. Lee The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle Cell 67 1991 293 302
19. R.H. Grafstrom, W. Pan, and R.H. Hoess Defining the substrate specificity of cdk4 kinase-cyclin D1 complex Carcinogenesis 20 1999 193 198
20. C.H. Graham, T.S. Hawley, R.G. Hawley, J.R. MacDougall, R.S. Kerbel, N. Khoo, and P.K. Lala Establishment and characterization of first trimester human trophoblast cells with extended lifespan Exp. Cell Res. 206 1993 204 211
21. M.A. Gregory, Y. Qi, and S.R. Hann Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization J. Biol. Chem. 278 2003 51606 51612
22. A.V. Grinberg, C.D. Hu, and T.K. Kerppola Visualization of Myc/Max/Mad family dimers and the competition for dimerization in living cells Mol. Cell Biol. 24 2004 4294 4308
23. S. Gupta, and R.J. Davis MAP kinase binds to the NH2-terminal activation domain of c-Myc FEBS Lett. 353 1994 281 285
24. S. Gupta, A. Seth, and R.J. Davis Transactivation of gene expression by Myc is inhibited by mutation at the phosphorylation sites Thr-58 and Ser-62 Proc. Natl. Acad. Sci. USA 90 1993 3216 3220
25. M. Gusse, J. Ghysdael, G. Evan, T. Soussi, and M. Mechali Translocation of a store of maternal cytoplasmic c-myc protein into nuclei during early development Mol. Cell Biol. 9 1989 5395 5403
26. C. Hasel, B. Rau, S. Perner, J. Strater, and P. Moller Differential and mutually exclusive expression of CD95 and CD95 ligand in epithelia of normal pancreas and chronic pancreatitis Lab Invest. 81 2001 317 326
27. B. Hogan, R. Beddington, F. Constantini, and B. Lacy Manipulating the mouse embryo, A laboratory manual 2002 Cold Spring Harbor Laboratory Cold Spring Harbor
28. P.J. Hurlin, C. Queva, P.J. Koskinen, E. Steingrimsson, D.E. Ayer, N.G. Copeland, N.A. Jenkins, and R.N. Eisenman Mad3 and Mad4: novel Max-interacting transcriptional repressors that suppress c-myc dependent transformation and are expressed during neural and epidermal differentiation EMBO J. 14 1995 5646 5659
29. N. Iwamori, K. Naito, K. Sugiura, H. Kagii, M. Yamashita, S. Ohashi, S. Goto, K. Yamanouch, and H. Tojo Phosphorylation of mitogen-activated protein kinase cascade during early embryo development in the mouse Reprod. Fertil. Dev. 12 2000 209 214
30. N. Iwamori, K. Naito, K. Sugiura, and H. Tojo Preimplantation-embryo- specific cell cycle regulation is attributed to the low expression level of retinoblastoma protein FEBS Lett. 526 2002 119 123
31. K. Kamemura, B.K. Hayes, F.I. Comer, and G.W. Hart Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: alternative glycosylation/phosphorylation of THR-58, a known mutational hot spot of c-Myc in lymphomas, is regulated by mitogens J. Biol. Chem. 277 2002 19229 19235
32. E.S. Knudsen, and J.Y. Wang Dual mechanisms for the inhibition of E2F binding to RB by cyclin-dependent kinase-mediated RB phosphorylation Mol. Cell Biol. 17 1997 5771 5783
33. M.J. Kohn, R.T. Bronson, E. Harlow, N.J. Dyson, and L. Yamasaki Dp1 is required for extra-embryonic development Development 130 2003 1295 1305
34. E.W. Lam, and N.B. La Thangue DP and E2F proteins: coordinating transcription with cell cycle progression Curr. Opin. Cell Biol. 6 1994 859 866
35. R.E. Leach, U.K. Rout, J.F. Schultz, D.E. Saunders, and D.R. Armant Ethanol elevates c-Myc levels in cultured mouse preimplantation embryos Alcohol Clin. Exp. Res. 23 1999 778 784
36. E. Lees, B. Faha, V. Dulic, S.I. Reed, and E. Harlow Cyclin E/cdk2 and cyclin A/cdk2 kinases associate with p107 and E2F in a temporally distinct manner Genes Dev. 6 1992 1874 1885
37. J. Liu, E.E. Puscheck, F. Wang, A. Trostinskaia, D. Barisic, G. Maniere, D. Wygle, W. Zhong, E.H.H.M. Rings, and D.A. Rappolee Serine-threonine kinases and transcription factors active in signal transduction are detected at high levels of phosphorylation during mitosis in preimplantation embryos and trophoblast stem cells Reproduction 128 2004 643 654
38. B. Lutterbach, and S.R. Hann Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis Mol. Cell Biol. 14 1994 5510 5522
39. X. Mayol, X. Grana, A. Baldi, N. Sang, Q. Hu, and A. Giordano Cloning of a new member of the retinoblastoma gene family (pRb2) which binds to the E1A transforming domain Oncogene 8 1993 2561 2566
40. D.O. Morgan Principles of CDK regulation Nature 374 1995 131 134
41. K. Noguchi, C. Kitanaka, H. Yamana, A. Kokubu, T. Mochizuki, and Y. Kuchino Regulation of c-Myc through phosphorylation at Ser-62 and Ser-71 by c-Jun N-terminal kinase J. Biol. Chem. 274 1999 32580 32587
42. S.K. Pal, R. Crowell, A.A. Kiessling, and G.M. Cooper Expression of proto-oncogenes in mouse eggs and preimplantation embryos Mol. Reprod. Dev. 35 1993 8 15
43. A. Palena, R. Mangiacasale, A.R. Magnano, L. Barberi, R. Giordano, C. Spadafora, and P. Lavia E2F transcription factors are differentially expressed in murine gametes and early embryos Mech. Dev. 97 2000 211 215
44. W. Pan, T. Sun, R. Hoess, and R. Grafstrom Defining the minimal portion of the retinoblastoma protein that serves as an efficient substrate for cdk4 kinase/cyclin D1 complex Carcinogenesis 19 1998 765 769
45. B.C. Paria, S.K. Dey, and G.K. Andrews Antisense c-myc effects on preimplantation mouse embryo development Proc. Natl. Acad. Sci. USA 89 1992 10051 10055
46. M.D. Planas-Silva, and R.A. Weinberg The restriction point and control of cell proliferation Curr. Opin. Cell Biol. 9 1997 768 772
47. B.J. Pulverer, C. Fisher, K. Vousden, T. Littlewood, G. Evan, and J.R. Woodgett Site-specific modulation of myc cotransformation by residues phosphorylated in vivo Oncogene 9 1994 59 70
48. D.A. Rappolee, C. Basilico, Y. Patel, and Z. Werb Expression and function of FGF-4 in peri-implantation development in mouse embryos Development 120 1994 2259 2269
49. D.A. Rappolee, C.A. Brenner, R. Schultz, D. Mark, and Z. Werb Developmental expression of PDGF, TGF-alpha, and TGF-beta genes in preimplantation mouse embryos Science 241 1988 1823 1825
50. D.A. Rappolee, Y. Patel, and K. Jacobson Expression of fibroblast growth factor receptors in peri-implantation mouse embryos Mol. Reprod. Dev. 51 1998 254 264
51. D.A. Rappolee, A. Wang, D. Mark, and Z. Werb Novel method for studying mRNA phenotypes in single or small numbers of cells J. Cell. Biochem. 39 1989 1 11
52. R. Sears, F. Nuckolls, E. Haura, Y. Taya, K. Tamai, and J.R. Nevins Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability Genes Dev. 14 2000 2501 2514
53. R. Sears, K. Ohtani, and J.R. Nevins Identification of positively and negatively acting elements regulating expression of the E2F2 gene in response to cell growth signals Mol. Cell Biol. 17 1997 5227 5235
54. A. Seth, F.A. Gonzalez, S. Gupta, D.L. Raden, and R.J. Davis Signal transduction within the nucleus by mitogen-activated protein kinase J. Biol. Chem. 267 1992 24796 24804
55. A. Seth, S. Gupta, and R.J. Davis Cell cycle regulation of the c-Myc transcriptional activation domain Mol. Cell Biol. 13 1993 4125 4136
56. H. Shen-Li, R.C. O'Hagan, H. Hou Jr., J.W. Horner 2nd, H.W. Lee, and R.A. DePinho Essential role for Max in early embryonic growth and development Genes Dev. 14 2000 17 22
57. E. Smith, G.A. Coetzee, and B. Frenkel Glucocorticoids inhibit cell cycle progression in differentiating osteoblasts via glycogen synthase kinase-3beta J. Biol. Chem. 277 2002 18191 18197
58. S. Tanaka, T. Kunath, A.K. Hadjantonakis, A. Nagy, and J. Rossant Promotion of trophoblast stem cell proliferation by FGF4 Science 282 1998 2072 2075
59. Q.T. Wang, K. Piotrowska, M.A. Ciemerych, L. Milenkovic, M.P. Scott, R.W. Davis, and M. Zernicka-Goetz A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo Dev. Cell 6 2004 133 144
60. Q.T. Wang, W. Xiao, M. Mindrinos, and R.W. Davis Yeast tRNA as carrier in the isolation of microscale RNA for global amplification and expression profiling Biotechniques 33 2002 788 pp. 790, 792 passim
61. Wang Y., Puscheck, E.E., Xie, Y., Wygle, D., Trostinskaia, A.B., Wang, F., Barisic, D., Maniere, G. and Rappolee D.A. (2004) MAPK pathway is downstream of embryonic and maternal signaling and is important in mediating mitogenic and morphogenetic signals in preimplantation mouse embryos. Dev. Biol. (submittd)
62. Y. Wang, F. Wang, T. Sun, A. Trostinskaia, D. Wygle, E. Puscheck, and D.A. Rappolee Entire mitogen activated protein kinase (MAPK) pathway is present in preimplantation mouse embryos Dev. Dyn. 231 2004 72 87
63. M. Watanabe, N. Masuyama, M. Fukuda, and E. Nishida Regulation of intracellular dynamics of Smad4 by its leucine-rich nuclear export signal EMBO Rep. 1 2000 176 182
64. L. Wu, A. de Bruin, H.I. Saavedra, M. Starovic, A. Trimboli, Y. Yang, J. Opavska, P. Wilson, J.C. Thompson, M.C. Ostrowski, T.J. Rosol, L.A. Woollett, M. Weinstein, J.C. Cross, M.L. Robinson, and G. Leone Extra-embryonic function of Rb is essential for embryonic development and viability Nature 421 2003 942 947
65. Zhong, W., Wang, Y., Lewis, J.J., Xie, Y. and Rappolee, D.A. (2004) SAPK/JNK1, 2 mediates rapid stress-induced, dose-dependent apoptotic and mitogenic suppression and slower apoptotic and cell cycle arrest in placental cells and embryos. Dev. Biol. (submitted)