Tumor suppressor Lzap regulates cell cycle progression, doming, and zebrafish epiboly

Developmental Dynamics

Volumn 240, Issue 6, 2011, Pages 1613-1625

  Liu, Dan ^a   Wang, Wen Der ^b,d   Melville, David B ^b   Cha, Yong I ^b,c   Yin, Zhirong ^b   Issaeva, Natalia ^b   Knapik, Ela W ^b   Yarbrough, Wendell G ^a,b,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d NATIONAL CHIAYI UNIVERSITY   (Taiwan)

Author keywords

Cell cycle; Epiboly; Lzap; Tumor suppressor; Zebrafish

Indexed keywords

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLASTOMERE; BRAIN; CARCINOGENESIS; CELL ADHESION; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIVISION; CELL MIGRATION; CONTROLLED STUDY; DIGESTIVE SYSTEM; EMBRYO; EMBRYO CELL; EPIBOLY; EPITHELIUM CELL; GASTRULATION; GENE ACTIVITY; GENE FUNCTION; LZAP GENE; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARYNX; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL CYCLE; CELL MOVEMENT; EMBRYO, NONMAMMALIAN; GENES, TUMOR SUPPRESSOR; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; NERVE TISSUE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 79955741986     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22644     Document Type: Article

References (55)

1. Abrams EW, Mullins MC. 2009. Early zebrafish development: it's in the maternal genes. Curr Opin Genet Dev 19: 396-403.
2. Amon A. 1999. The spindle checkpoint. Curr Opin Genet Dev 9: 69-75.
3. An H, Lu X, Liu D, Yarbrough WG. 2011. LZAP inhibits p38 MAPK (p38) phosphorylation and activity by facilitating p38 association with the wild-type p53 induced phosphatase 1 (WIP1). PLoS ONE 6: e16427.
4. Arendt D, Nubler-Jung K. 1999. Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk-rich amniote eggs. Mech Dev 81: 3-22.
5. Barrallo-Gimeno A, Holzschuh J, Driever W, Knapik EW. 2004. Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 131: 1463-1477.
6. Bruce AE, Howley C, Dixon Fox M, Ho RK. 2005. T-box gene eomesodermin and the homeobox-containing Mix/Bix gene mtx2 regulate epiboly movements in the zebrafish. Dev Dyn 233: 105-114.
7. Cao Y, Zhao J, Sun Z, Zhao Z, Postlethwait J, Meng A. 2004. fgf17b, a novel member of Fgf family, helps patterning zebrafish embryos. Dev Biol 271: 130-143.
8. Cha YI, Kim SH, Sepich D, Buchanan FG, Solnica-Krezel L, DuBois RN. 2006. Cyclooxygenase-1-derived PGE2 promotes cell motility via the G-protein-coupled EP4 receptor during vertebrate gastrulation. Genes Dev 20: 77-86.
9. Cheng JC, Miller AL, Webb SE. 2004. Organization and function of microfilaments during late epiboly in zebrafish embryos. Dev Dyn 231: 313-323.
10. Ching YP, Qi Z, Wang JH. 2000. Cloning of three novel neuronal Cdk5 activator binding proteins. Gene 242: 285-294.
11. Dosch R, Wagner DS, Mintzer KA, Runke G, Wiemelt AP, Mullins MC. 2004. Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. Dev Cell 6: 771-780.
12. Duffy KT, McAleer MF, Davidson WR, Kari L, Kari C, Liu CG, Farber SA, Cheng KC, Mest JR, Wickstrom E, Dicker AP, Rodeck U. 2005. Coordinate control of cell cycle regulatory genes in zebrafish development tested by cyclin D1 knockdown with morpholino phosphorodiamidates and hydroxyprolyl-phosphono peptide nucleic acids. Nucleic Acids Res 33: 4914-4921.
13. Granero-Molto F, Sarmah S, O'Rear L, Spagnoli A, Abrahamson D, Saus J, Hudson BG, Knapik EW. 2008. Goodpasture antigen-binding protein and its spliced variant, ceramide transfer protein, have different functions in the modulation of apoptosis during zebrafish development. J Biol Chem 283: 20495-20504.
14. Holloway BA, Gomez de la Torre Canny S, Ye Y, Slusarski DC, Freisinger CM, Dosch R, Chou MM, Wagner DS, Mullins MC. 2009. A novel role for MAPKAPK2 in morphogenesis during zebrafish development. PLoS Genet 5: e1000413.
15. Horowitz MA, Schaffer DB, Diamond GR, Katowitz JA, Quinn GE. 1983. Management of traumatic hyphema. JAMA 250: 3046-3047.
16. Ikegami R, Hunter P, Yager TD. 1999. Developmental activation of the capability to undergo checkpoint-induced apoptosis in the early zebrafish embryo. Dev Biol 209: 409-433.
17. Jeong K, Jeong JY, Lee HO, Choi E, Lee H. 2010. Inhibition of Plk1 induces mitotic infidelity and embryonic growth defects in developing zebrafish embryos. Dev Biol 345: 34-48.
18. Jiang H, Luo S, Li H. 2005. Cdk5 activator-binding protein C53 regulates apoptosis induced by genotoxic stress via modulating the G2/M DNA damage checkpoint. J Biol Chem 280: 20651-20659.
19. Jiang H, Wu J, He C, Yang W, Li H. 2009. Tumor suppressor protein C53 antagonizes checkpoint kinases to promote cyclin-dependent kinase 1 activation. Cell Res 19: 458-468.
20. Joly JS, Joly C, Schulte-Merker S, Boulekbache H, Condamine H. 1993. The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos. Development 119: 1261-1275.
21. Kane DA, Kimmel CB. 1993. The zebrafish midblastula transition. Development 119: 447-456.
22. Kane DA, Hammerschmidt M, Mullins MC, Maischein HM, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Haffter P, Heisenberg CP, Jiang YJ, Kelsh RN, Odenthal J, Warga RM, Nusslein-Volhard C. 1996. The zebrafish epiboly mutants. Development 123: 47-55.
23. Kane DA, McFarland KN, Warga RM. 2005. Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development 132: 1105-1116.
24. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
25. Kishimoto Y, Koshida S, Furutani-Seiki M, Kondoh H. 2004. Zebrafish maternal-effect mutations causing cytokinesis defect without affecting mitosis or equatorial vasa deposition. Mech Dev 121: 79-89.
26. Lachnit M, Kur E, Driever W. 2008. Alterations of the cytoskeleton in all three embryonic lineages contribute to the epiboly defect of Pou5f1/Oct4 deficient MZspg zebrafish embryos. Dev Biol 315: 1-17.
27. Lin F, Chen S, Sepich DS, Panizzi JR, Clendenon SG, Marrs JA, Hamm HE, Solnica-Krezel L. 2009. Galpha12/13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton. J Cell Biol 184: 909-921.
28. Ma C, Fan L, Ganassin R, Bols N, Collodi P. 2001. Production of zebrafish germ-line chimeras from embryo cell cultures. Proc Natl Acad Sci U S A 98: 2461-2466.
29. Martinez-Barbera JP, Toresson H, Da Rocha S, Krauss S. 1997. Cloning and expression of three members of the zebrafish Bmp family: Bmp2a, Bmp2b and Bmp4. Gene 198: 53-59.
30. McFarland KN, Warga RM, Kane DA. 2005. Genetic locus half baked is necessary for morphogenesis of the ectoderm. Dev Dyn 233: 390-406.
31. Montero JA, Kilian B, Chan J, Bayliss PE, Heisenberg CP. 2003. Phosphoinositide 3-kinase is required for process outgrowth and cell polarization of gastrulating mesendodermal cells. Curr Biol 13: 1279-1289.
32. Montero-Balaguer M, Lang MR, Sachdev SW, Knappmeyer C, Stewart RA, De La Guardia A, Hatzopoulos AK, Knapik EW. 2006. The mother superior mutation ablates foxd3 activity in neural crest progenitor cells and depletes neural crest derivatives in zebrafish. Dev Dyn 235: 3199-3212.
33. Musacchio A, Hardwick KG. 2002. The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731-741.
34. Negron JF, Lockshin RA. 2004. Activation of apoptosis and caspase-3 in zebrafish early gastrulae. Dev Dyn 231: 161-170.
35. Pfaff KL, Straub CT, Chiang K, Bear DM, Zhou Y, Zon LI. 2007. The zebra fish cassiopeia mutant reveals that SIL is required for mitotic spindle organization. Mol Cell Biol 27: 5887-5897.
36. Ramel MC, Buckles GR, Baker KD, Lekven AC. 2005. WNT8 and BMP2B co-regulate non-axial mesoderm patterning during zebrafish gastrulation. Dev Biol 287: 237-248.
37. Reim G, Brand M. 2006. Maternal control of vertebrate dorsoventral axis formation and epiboly by the POU domain protein Spg/Pou2/Oct4. Development 133: 2757-2770.
38. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA, Ekker SC. 2007. p53 activation by knockdown technologies. PLoS Genet 3: e78.
39. Schulte-Merker S, van Eeden FJ, Halpern ME, Kimmel CB, Nusslein-Volhard C. 1994. no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120: 1009-1015.
40. Shimizu T, Yabe T, Muraoka O, Yonemura S, Aramaki S, Hatta K, Bae YK, Nojima H, Hibi M. 2005. E-cadherin is required for gastrulation cell movements in zebrafish. Mech Dev 122: 747-763.
41. Sibon OC, Stevenson VA, Theurkauf WE. 1997. DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388: 93-97.
42. Sibon OC, Laurencon A, Hawley R, Theurkauf WE. 1999. The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr Biol 9: 302-312.
43. Sidi S, Goutel C, Peyrieras N, Rosa FM. 2003. Maternal induction of ventral fate by zebrafish radar. Proc Natl Acad Sci U S A 100: 3315-3320.
44. Solnica-Krezel L. 2005. Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol 15: R213-R228.
45. Solnica-Krezel L. 2006. Gastrulation in zebrafish -- all just about adhesion? Curr Opin Genet Dev 16: 433-441.
46. Tang R, Dodd A, Lai D, McNabb WC, Love DR. 2007. Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin (Shanghai) 39: 384-390.
47. Wagner DS, Dosch R, Mintzer KA, Wiemelt AP, Mullins MC. 2004. Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev Cell 6: 781-790.
48. Wang J, He X, Luo Y, Yarbrough WG. 2006. A novel ARF-binding protein (LZAP) alters ARF regulation of HDM2. Biochem J 393: 489-501.
49. Wang J, An H, Mayo MW, Baldwin AS, Yarbrough WG. 2007. LZAP, a putative tumor suppressor, selectively inhibits NF-kappaB. Cancer Cell 12: 239-251.
50. Wilkins SJ, Yoong S, Verkade H, Mizoguchi T, Plowman SJ, Hancock JF, Kikuchi Y, Heath JK, Perkins AC. 2008. Mtx2 directs zebrafish morphogenetic movements during epiboly by regulating microfilament formation. Dev Biol 314: 12-22.
51. Wilm TP, Solnica-Krezel L. 2005. Essential roles of a zebrafish prdm1/blimp1 homolog in embryo patterning and organogenesis. Development 132: 393-404.
52. Yamashita M. 2003. Apoptosis in zebrafish development. Comp Biochem Physiol B Biochem Mol Biol 136: 731-742.
53. Yarbrough WG, Bessho M, Zanation A, Bisi JE, Xiong Y. 2002. Human tumor suppressor ARF impedes S-phase progression independent of p53. Cancer Res 62: 1171-1177.
54. Yin Z, Jones GN, Towns WH Jr, Zhang X, Abel ED, Binkley PF, Jarjoura D, Kirschner LS. 2008. Heart-specific ablation of Prkar1a causes failure of heart development and myxomagenesis. Circulation 117: 1414-1422.
55. Zamir E, Kam Z, Yarden A. 1997. Transcription-dependent induction of G1 phase during the zebra fish midblastula transition. Mol Cell Biol 17: 529-536.