The role of protein phosphatase 4 in regulating microtubule severing in the Caenorhabditis elegans embryo

Genetics

Volumn 181, Issue 3, 2009, Pages 933-943

  Han, Xue ^a,b,e   Gomes, José Eduardo ^c   Birmingham, Cheryl L ^a,b,f   Pintard, Lionel ^c   Sugimoto, Asako ^d   Mains, Paul E ^a,b,g  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c INSTITUT JACQUES MONOD   (France)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

^e UNIVERSITY OF ALBERTA   (Canada)

^f Integran Technologies Inc   (Canada)

^g NONE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; MBK 2 PROTEIN; MEI 1 PROTEIN; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 4; PHOSPHOTRANSFERASE; REGULATOR PROTEIN; RNA; UBIQUITIN; UNCLASSIFIED DRUG;

CAENORHABDITIS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVE SITE; GENE; GENE INTERACTION; GENOTYPE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MEIOSIS; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHATASE FOUR REGULATORY SUBUNIT 1 GENE; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA INTERFERENCE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENE KNOCKDOWN TECHNIQUES; MEIOSIS; MICROTUBULES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN SUBUNITS;

CAENORHABDITIS ELEGANS;

EID: 62549096891     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.096016     Document Type: Review

References (70)

1. ALBERTSON, D. G., 1984 Formation of ihc lirsi cleavage spindle in nematode embryos. Dev. Biol. 101: 61-72.
2. ALBERTSON, D. G., and J. N. THOMSON, 1993 Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1: 15-26.
3. BRENNER, S., 1974 The genetics of Caemorhabditis elegans. Genetics 77: 71-94.
4. BREWIS, N. D., A. J. STREET, A. R. PRESCOTT and P. T. COHEN, 1993 PPX, a novel protein serine/threonine phosphatase localized to centrosomes. EMBO J. 12: 987-996.
5. BURK, D. H., R. ZHONG and Z. H. YE, 2007 The katanin microtubule severing protein in plants. J. Integr. Plant Biol. 49: 1174-1182.
6. CHEN, J., R. T. PETERSON and S. L. SCHREIRER, 1998 Alpha 4 associates with protein phosphatases 2A, 4, and 6, Biochem. Biophys, Res. Commun. 247: 827-832.
7. CANDININ, T. R., and P. E. MAINS, 1993 Genetic studies of met-1 gene activity during the transition from meiosis to mitosis in Caenorhabditis elegans. Genetics 134: 199-210.
8. CLARK-MAGUIRE, S., and P. E. MAINS, 1994a Localization of the mei-1 gene product of Caenorhabditis elegans, a meiotic-specific spindle component. J. Cell Biol. 126: 199-209.
9. CLARK-MAGUIRE, S., and P. E. MAINS, 1994b mei-1, a gene required for meiotic spindle formation in Caenorhabditis elegans, is a member of a family of ATPases. Genetics 136: 533-346.
10. COHEN, P. T., A. PHILP and C. VAZQUEZ- MARTIN, 2005 Protein phosphatase 4: from obscurity to vital functions. FEES Lett. 579: 3278-3286.
11. DOBSOX, C. M., T. WAI, D. LECLERC, H. KADIR, M. XARANG, et al., 2002 Identification of the gene responsible for the cblB complementation group or vitamin B12-dependent methylmalonic aciduria, Hum. Mol. Genet. 11: 3361-3369.
12. DOW, M. R., and P. E. MAINS, 1998 Genetic and molecular characterization of the Caenorhabditis elegans gene, mel-26, a postmeiotic negative regulator of mei-1, a meiotic-specific spindle component, Genetics 150: 119-128.
13. DYMEK, E. E., P. A. LEFEBVRE and E. E Smith, 2004 PF15p is the Chlamydomonas homologue of the Katanin p80 subunit and is required for assembly of flagellar central microtubules. Eukaryot. Cell 3: 870-879.
14. EDGLEY, M. L., D. L., BAILLIE, D. L. RIDDLE and A. M. Rose. 2006 Genetic balancers in WormBook, edited by THE C. ELEGANS RESEARCH COMMENITY. WormBook, hup://www.wormbook.org.
15. FIRE, A., S. XU, M. K. MONTGOMERY, S. A. KOSTAS, S, E. DRIVER et al., 1998 Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
16. FRASER, A. G., R. S. KAMATH, P. ZIPPERLEN, M. MARTINEZ-CAMPOS, M. SOHRMANN et al., 2000 Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325-330.
17. FURUKAWA, M., Y. J. HE, C. BORCHERS and Y. Xiong. 2003 Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat. Cell Biol. 5: 1001-1007.
18. GENGYO-ANDO, K., and S. MITANI, 2000 Charactetizatiou of mutations induced by ethyl methauesulfouate, UV, and trimethylpsoralen in the nemalode Canarhabditis eleans. Biochem, Biophys. Res. Commun. 269: 64-69.
19. GINGRAS, A. C., M. CABALLERO, M. ZARSKE, A. SANCHEZ, T. R. HAZBUN et al., 2005 A nuvel. evolutionarily conserved protein phosphatase complex involved in cisplalin scusitivity Mol. Cell. Proteomics 4: 1725-1740.
20. GLICKMAN, M. H., and A. CIECHNOVER, 2002 The ubiquitin-pruteasome proteolvtic pathway: destruction for the sake of construction. Physiol. Rev. 82: 373-428.
21. GOMES, J. E., S. E. ENCALADA, K. A. SWAN, C. A. SHELTON, J. C. CARTER et al., 2001 The maternal gene spn-4 encoded a predicted RRM protein required for mitotic spiutdle orientation and cell fate patterning in early C. elegans emhryos. Development 128: 4301-1314.
22. HARTMAN, P. S., and R. K. HERMAN, 1982 Radiation-sensitive mutants of Caenorhabditis elegans. Genetics 102: 159-178.
23. HASTIE, C. J., G. K. CARNEGIE, N. MORRICE and P. T. COHEN, 2000 A novel 50 kDa protein forms complexes with protein phosphatase 4 and is located al centrosomal microtubule organizing centres. Biochem. J. 347(Pt. 3): 845-855.
24. HELPS, X. R., N. D. BREWIS, R. LINERUTH, T. DAVIS, K. KAISER et al., 1998 Protein phosphatase 4 is an essential enzyme required for orgauisatiou of microtubules at centrosomes in Diosophila embryos. J. Cell Sci. 111(Pt. 10): 1331-1310.
25. HODGKIN, J., H. R. HORVITZ and S. BRENNER, 1979 Nondisjunction mutants of the nematode Caeenohabditis elegans. Genetics 91: 67-94.
26. HUNTER, T., 2007 The age of crosstalk: phosphorylation, ubiquitinalion, and beyond. Mol. Cell 28: 730-738.
27. KAMATH, R. S., and J. AHRINGER, 2003 Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
28. KAMATH, R. S., A. G. ERASER, Y. DONG, G. POULIN, R. DURBIN et al., 2003 Systematic functional analysis of the Caenorhabditis elegans genome using RNAi, Nature 421: 231-237.
29. KARABAY, A., W. YU, J. M. SOLOWSKA, D. H. BAIRD and P. W. BAAS, 2004 Axonal growth is sensitive to the levels of katanin, a protein that severs microtubules. J. Neurosci. 24: 5778-5788.
30. KEMPHUES, K. J., N. WOLF, W. B. WOOD and D. HIRSH, 1986 Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans. Dev. Biol. 113: 449-460.
31. KIM, S. H., A. H. HOLWAY, S. WOLFF, A. DILLIN and W. M. MICHAEL, 2007 SMK-1/PPH-4.1-mediated silencing of the CHK-1 response to DNA damage in early C. elegans embryos. J. Cell Biol. 179: 41-52.
32. KLOEKER, S., and B. E. WADZINSKI, 1999 Purification and identification of a novel subunit or protein serine/threonine phosphatase 4. J. Biol. Chem. 274: 5339-5347.
33. LEE, M. H., and T. SCHEDL, 2001 Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev. 15: 2408-2420.
34. LEWIS, J. A., and J. T. FLEMING, 1995 Basic culture methods. Methods Cell Biol. 48: 3-29.
35. LI, S., C. M. ARMSTRONG, N. BERTIN, H. GE, S. MILSTEIN et al., 2004 A map of the interactome network of the metazoan C. elegans. Science 303: 540-543.
36. LOHRET, T. A., F. J. MCNALLY and F. M. QUARMBY, 1998 A role for katanin-mediated axonemal severing during Chlamydomonas deflageilation. Mol. Biol. Cell 9: 1195-1207.
37. LU, C., and P. E. MAINS, 2005 Mutations of a redundant α-tubulin gene affect Caenorhabditis elegans early embryonic cleavage via MEI-1 /katanin-dependent and -independent pathways. Genetics 170: 115-126.
38. LU, C., and P. E. MAINS, 2007 The C. elegans anaphase promoting complex and MBK-2/DYRK kinase act redundantly with CUF-3/ MEL-26 ubiquitin ligase to degrade MEI-1 microtubule-severing activity after meiosis. Dev. Biol. 302: 438-447.
39. LU, C., M. SRAYKO and P. E. MAINS, 2004 The Caenorhabditis elegans microtubulc-severing complex MEI-1/MEI-2 katanin interacts differently with two superficially redundant beta-tubulin isotvpes. Mol. Biol. Cell 15: 142-150.
40. MAINS, P. E., K. J. KEMPHUES, S. A. SPRUNGER, I. A. SULSTON and W. B. WOOD, 1990a Mutations affecting the meiolic and mitotic divisions of the early Caenorhabditis elegans embryo. Genetics 126: 593-605.
41. MAINS, P. E., I. A. SULSTON and W. B. WOOD, 1990b Dominant maternal-effect mutations causing embryonic lethality in Caenorhabditis elegans. Genetics 125: 351-369.
42. MATTHEWS, L. R., P. CARTER, D. THIERRY- MIEG and K. KEMPHUES, 1998 ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles. J. Cell Biol. 141: 1159-1168.
43. MCCARTER, J., B. BARTLETT, T. DANG and T. SCHEDL, 1999 On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205: 111-128.
44. MCNALLY, K., A. AUDHYA, K. OEGEMA and F. J. MCNALLY, 2006 Katanin controls mitotic and meiotic spindle length. J. Cell Biol. 175: 881-891.
45. MCNALLY, K. P., D. BUSTER and F. J. MCNALLY, 2002 Katanin-mediated microtubule severing can be regulated by multiple mechanisms. Cell Motil Cytoskeleton 53: 337-349.
46. MING PANG, K., T. ISHIDATE, K. NAKAMURA, M. SHIRAYAMA, C. TRZEPACZ et al., 2004 The minibrain kinase homolog, mbk-2, is required for spindle positioning and asymmetric cell division in early C. elegans embryos. Dev. Biol. 265: 127-139.
47. NANAHOSHI, M., Y. TSUJISHITA, C. TOKUNAGA, S. INUI, N. SAKAGUCHI et al., 1999 Alpha4 protein as a common regulator of type 2A-related serine/threonine protein phosphatases. FEBS Lett. 446: 108-112.
48. PANOWSKI, S. H., S. WOLFF, H. AGUILANIU, J. DURIEUX and A. DILLIN, 2007 PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans. Nature 447: 550-555.
49. PELLETTIERI, J., V. REINKE, S. K. KIM and G. SEYDOUX, 2003 Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev. Cell 5: 451-462.
50. PETROSKI, M. D., and R. J. DESHAIES, 2005 Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6: 9-20.
51. PHILLIPS, J. B., R. FYGZAK, G. C. ELLIS and B. BOWERMAN, 2004 Roles for two partially redundant alpha-tubulins during mitosis in early Caenorhabditis elegans embryos. Cell Motil. Cytoskeleton 58: 112-126.
52. PINTARD, L., J. H. WILLIS, A. WILLEMS, J. L. JOHNSON, M, SRAYKO et al., 2003 The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425: 311-316.
53. QUINTIN, S., P. E. MAINS, A. ZINKE and A. A. HYMAN, 2003 The mbk-2 kinase is required for inactivation of MEI-1/katanin in the one-cell Caenorhabditis elegans embryo. EMBO Rep. 4: 1175-1181.
54. SCHATTEN, G., 1994 The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev. Biol. 165: 299-335.
55. SHARMA, N., J. BRYANT, D. WLOGA, R. DONALDSON, R. C. DAVIS et al., 2007 Katanin regulates dynamics of microtubules and biogenesis of motile cilia. J. Cell Biol. 178: 1065-1079.
56. SONNICHSEN, B., L. B. KOSKI, A. WALSH, P. MARSCHALL, B. NEUMANN et al., 2005 Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462-469.
57. SRAYKO, M., D. W. BUSTER, O. A. BAZIRGAN, F. J. MCNALLY and P. E. MAINS, 2000 MEI-1/MFI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev. 14: 1072-1084.
58. SRAYKO, M., F. T. O'TOOLE, A. A. HYMAN and T. MÜLLER-REICHERT, 2006 Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr. Biol. 16: 1944-1949.
59. STITZEL, M. L., J. PELLETTIERI and G. SEYDOUX, 2006 The C. elegans DYRK kinase MBK-2 marks oocyte proteins for degradation in response to meiotic maturation. Curr. Biol. 16: 56-62.
60. STITZEL, M. L., K. C. CHENG and G. SEYDOUX, 2007 Regulation of MBK-2/Dyrk kinase by dynamic cortical anchoring during the oocyte-to-zygote transition. Curr. Biol. 17: 1545-1554.
61. SULSTON, J. E., E. SCHIERENBERG, J. G. WHITE and J. N. THOMSON, 1983 The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100: 64-119.
62. SLMIYOSHI, E., A. SUGIMOTO and M. YAMAMOTO, 2002 Protein phosphatase 4 is required for centrosome maturation in mitosis and sperm meiosis in C. elegans. J. Ceil Sci. 115: 1403-1410.
63. TIMMONS, L., D. L. COURT and A. FIRE, 2001 Ingestion orbacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112.
64. TOYO-OKA, K., D. MORI, Y. YANO, M. SHIOTA, 14. IWAO et al., 2008 Protein phosphatase 4 catalytic subunit regulates Cdk1 activity and microtubule organization via NDEL1 dephosphorylation. J. Cell Biol. 180: 1133-1147.
65. VAN DER WIJK, T., C. BIANCHETOT and J. DEN HERTOG, 2005 Regulation of receptor protein-tyrosine phosphatase dimerization. Methods 35: 73-79.
66. WADA, T., T. MIYATA, R. INAGI, M. NANGAKU, M. WAGATSUMA et al., 2001 Cloning and characterization of a novel subunit of protein serine/threonine phosphatase 4 from mesangial cells. J. Am. Soc. Nephrol. 12: 2601-2608.
67. XU, L., Y. WEI, J. REBOUL, P. VAGLIO, X. H. SHIN et al., 2003 BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425: 316-321.
68. YANG, H., K. MCNALLY and F. J. MCNALLY, 2003 MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans. Dev. Biol. 260: 245-259.
69. YANG, H. Y., P. E. MAINS and F. J. MCNALLY, 2005 Kinesin-1 mediates translocation of the meiotic spindle to the oocyte cortex through KCA-1, a novel cargo adapter. J. Cell Biol. 169: 447-457.
70. ZHANG, D., G. G. ROGERS, D. W. BUSTER and D. J. SHARP, 2007 Three microtubule severing enzymes contribute to the "Pacman-flux" machinery that moves chromosomes. J. Cell Biol. 177: 231-242.