The germinal center kinase GCK-1 is a negative regulator of MAP kinase activation and apoptosis in the C. elegans germline

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Schouest, Katherine R ^a,b   Kurasawa, Yasuhiro ^a   Furuta, Tokiko ^a   Hisamoto, Naoki ^c,d   Matsumoto, Kunihiro ^c,d   Schumacher, Jill M ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c NAGOYA UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; GERMINAL CENTER KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; GCK 1 PROTEIN, C ELEGANS; GCK-1 PROTEIN, C ELEGANS; GERMINAL CENTER KINASES; MITOGEN ACTIVATED PROTEIN KINASE 1; MPK 1 PROTEIN, C ELEGANS; MPK-1 PROTEIN, C ELEGANS; PROTEIN SERINE THREONINE KINASE;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; ENZYME ACTIVATION; ENZYME INHIBITION; GERM LINE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PROTEIN DEFICIENCY; PROTEIN FUNCTION; PROTEIN INTERACTION; ANIMAL; BIOLOGICAL MODEL; CELL PROLIFERATION; CYTOPLASM; FEMALE; GENE EXPRESSION REGULATION; MALE; METABOLISM; OOCYTE; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE;

ANIMALIA; CAENORHABDITIS ELEGANS;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL PROLIFERATION; CYTOPLASM; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; OOCYTES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE;

EID: 70449435874     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007450     Document Type: Article

References (70)

1. Dan I, Ong SE, Watanabe NM, Blagoev B, Nielsen MM, et al. (2002) Cloning of MASK, a novel member of the mammalian germinal center kinase III subfamily, with apoptosis-inducing properties. J Biol Chem 277: 5929-5939.
2. Pombo CM, Force T, Kyriakis J, Nogueira E, Fidalgo M, et al. (2007) The GCK II and III subfamilies of the STE20 group kinases. Front Biosci 12: 850-859.
3. Ling P, Lu TJ, Yuan CJ, Lai MD (2008) Biosignaling of mammalian Ste20-related kinases. Cell Signal 20: 1237-1247.
4. Radu M, Chernoff J (2009) The DeMSTification of mammalian Ste20 kinases. Curr Biol 19: R421-425.
5. Wu C, Whiteway M, Thomas DY, Leberer E (1995) Molecular characterization of Ste20p, a potential mitogen-activated protein or extracellular signal-regulated kinase kinase (MEK) kinase kinase from Saccharomyces cerevisiae. J Biol Chem 270: 15984-15992.
6. Drogen F, O'Rourke SM, Stucke VM, Jaquenoud M, Neiman AM, et al. (2000) Phosphorylation of the MEKK Ste11p by the PAK-like kinase Ste20p is required for MAP kinase signaling in vivo. Curr Biol 10: 630-639.
7. Dan I, Watanabe NM, Kusumi A (2001) The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11: 220-230.
8. Pombo CM, Kehrl JH, Sanchez I, Katz P, Avruch J, et al. (1995) Activation of the SAPK pathway by the human STE20 homologue germinal centre kinase. Nature 377: 750-754.
9. Graves JD, Gotoh Y, Draves KE, Ambrose D, Han DK, et al. (1998) Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1. EMBO J 17: 2224-2234.
10. Hirai S, Katoh M, Terada M, Kyriakis JM, Zon LI, et al. (1997) MST/MLK2, a member of the mixed lineage kinase family, directly phosphorylates and activates SEK1, an activator of c-Jun N-terminal kinase/stress-activated protein kinase. J Biol Chem 272: 15167-15173.
11. Lin JL, Chen HC, Fang HI, Robinson D, Kung HJ, et al. (2001) MST4, a new Ste20-related kinase that mediates cell growth and transformation via modulating ERK pathway. Oncogene 20: 6559-6569.
12. Nicke B, Bastien J, Khanna SJ, Warne PH, Cowling V, et al. (2005) Involvement of MINK, a Ste20 family kinase, in Ras oncogene-induced growth arrest in human ovarian surface epithelial cells. Mol Cell 20: 673-685.
13. Hao W, Takano T, Guillemette J, Papillon J, Ren G, et al. (2006) Induction of apoptosis by the Ste20-like kinase SLK, a germinal center kinase that activates apoptosis signal-regulating kinase and p38. J Biol Chem 281: 3075-3084.
14. Chen Z, Cobb MH (2001) Regulation of stress-responsive MAP kinase pathways by TAO2. J Biol Chem 276: 16070-16075.
15. Hutchison M, Berman KS, Cobb MH (1998) Isolation of TAO1, a Protein Kinase That Activates MEKs in Stress-activated Protein Kinase Cascades. J Biol Chem 273: 28625-28632.
16. O'Neill E, Kolch W (2005) Taming the Hippo: Raf-1 controls apoptosis by suppressing MST2/Hippo. Cell Cycle 4: 365-367.
17. Sabourin LA, Rudnicki MA (1999) Induction of apoptosis by SLK, a Ste20-related kinase. Oncogene 18: 7566-7575.
18. Tassi E, Biesova Z, Di Fiore PP, Gutkind JS, Wong WT (1999) Human JIK, a novel member of the STE20 kinase family that inhibits JNK and is negatively regulated by epidermal growth factor. J Biol Chem 274: 33287-33295.
19. Hipfner DR, Cohen SM (2003) The Drosophila sterile-20 kinase slik controls cell proliferation and apoptosis during imaginal disc development. PLoS Biol 1: E35.
20. Krens SF, Spaink HP, Snaar J (2006) Functions of the MAPK family in vertebrate-development. FEBS Letters 580: 4984-4990.
21. Bradham C, McClay DR (2006) p38 MAPK in development and cancer. Cell Cycle 5: 824-828.
22. Fan HY, Sun QY (2004) Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 70: 535-547.
23. Maller JL, Schwab MS, Roberts BT, Gross SD, Taieb FE, et al. (2001) The pathway of MAP kinase mediation of CSF arrest in Xenopus oocytes. Biol Cell 93: 27-33.
24. Lee MH, Ohmachi M, Arur S, Nayak S, Francis R, et al. (2007) Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 177: 2039-2062.
25. Miller MA, Nguyen VQ, Lee MH, Kosinski M, Schedl T, et al. (2001) A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291: 2144-2147.
26. Church DL, Guan KL, Lambie EJ (1995) Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121: 2525-2535.
27. Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011-1022.
28. McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205: 111-128.
29. Kosinski M, McDonald K, Schwartz J, Yamamoto I, Greenstein D (2005) C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes. Development 132: 3357-3369.
30. Miller MA, Ruest PJ, Kosinski M, Hanks SK, Greenstein D (2003) An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev 17: 187-200.
31. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, et al. (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987-1001.
32. Schedl T, Kimble J (1988) fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119: 43-61.
33. MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674-1687.
34. Hirsh D, Oppenheim D, Klass M (1976) Development of the reproductive system of Caenorhabditis elegans. Dev Biol 49: 200-219.
35. McCarter J, Bartlett B, Dang T, Schedl T (1997) Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev Biol 181: 121-143.
36. Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, et al. (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107: 465-476.
37. Kelly WG, Schaner CE, Dernburg AF, Lee MH, Kim SK, et al. (2002) X-chromosome silencing in the germline of C. elegans. Development 129: 479-492.
38. Lieb JD, Albrecht MR, Chuang PT, Meyer BJ (1998) MIX-1: an essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation. Cell 92: 265-277.
39. Burrows AE, Sceurman BK, Kosinski ME, Richie CT, Sadler PL, et al. (2006) The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133: 697-709.
40. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, et al. (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/ PP1 phosphatase in budding yeast and nematodes. Cell 102: 279-291.
41. Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157: 219-229.
42. Lackner MR, Kim SK (1998) Genetic analysis of the Caenorhabditis elegans MAP kinase gene mpk-1. Genetics 150: 103-117.
43. Lee MH, Hook B, Lamont LB, Wickens M, Kimble J (2006) LIP-1 phosphatase controls the extent of germline proliferation in Caenorhabditis elegans. EMBO J 25: 88-96.
44. Ohmachi M, Rocheleau CE, Church D, Lambie E, Schedl T, et al. (2002) C. elegans ksr-1 and ksr-2 Have Both Unique and Redundant Functions and Are Required for MPK-1 ERK Phosphorylation. Curr Biol 12: 427-433.
45. Clifford R, Lee MH, Nayak S, Ohmachi M, Giorgini F, et al. (2000) FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 127: 5265-5276.
46. Fantz DA, Jacobs D, Glossip D, Kornfeld K (2001) Docking sites on substrate proteins direct extracellular signal-regulated kinase to phosphorylate specific residues. J Biol Chem 276: 27256-27265.
47. Gartner A, Milstein S, Ahmed S, Hodgkin J, Hengartner MO (2000) A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 5: 435-443.
48. Corl AB, Berger KH, Ophir-Shohat G, Gesch J, Simms JA, et al. (2009) Happyhour, a Ste20 family kinase, implicates EGFR signaling in ethanol-induced behaviors. Cell 137: 949-960.
49. Haccard O, Lewellyn A, Hartley RS, Erikson E, Maller JL (1995) Induction of Xenopus oocyte meiotic maturation by MAP kinase. Dev Biol 168: 677-682.
50. Minshull J, Sun H, Tonks NK, Murray AW (1994) A MAP kinase-dependent spindle assembly checkpoint in Xenopus egg extracts. Cell 79: 475-486.
51. Ferrell JE, Jr. (1999) Xenopus oocyte maturation: new lessons from a good egg. Bioessays 21: 833-842.
52. Meinecke B, Krischek C (2003) MAPK/ERK kinase (MEK) signalling is required for resumption of meiosis in cultured cumulus-enclosed pig oocytes. Zygote 11: 7-16.
53. Verlhac MH, Kubiak JZ, Clarke HJ, Maro B (1994) Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120: 1017-1025.
54. Eisenmann DM, Kim SK (1997) Mechanism of activation of the Caenorhabditis elegans ras homologue let-60 by a novel, temperature-sensitive, gain-of-function mutation. Genetics 146: 553-565.
55. Hughes SC, Fehon RG (2006) Phosphorylation and activity of the tumor suppressor Merlin and the ERM protein Moesin are coordinately regulated by the Slik kinase. J Cell Biol 175: 305-313.
56. Hay BA, Guo M (2003) Coupling cell growth, proliferation, and death. Hippo weighs in. Dev Cell 5: 361-363.
57. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
58. de Bono M, Tobin DM, Davis MW, Avery L, Bargmann CI (2002) Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419: 899-903.
59. Siegfried KR, Kidd AR, 3rd, Chesney MA, Kimble J (2004) The sys-1 and sys-3 genes cooperate with Wnt signaling to establish the proximal-distal axis of the Caenorhabditis elegans gonad. Genetics 166: 171-186.
60. Ceol CJ, Stegmeier F, Harrison MM, Horvitz HR (2006) Identification and classification of genes that act antagonistically to let-60 Ras signaling in Caenorhabditis elegans vulval development. Genetics 173: 709-726.
61. Gengyo-Ando K, Mitani S (2000) Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem Biophys Res Commun 269: 64-69.
62. Wallenfang MR, Seydoux G (2000) Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 408: 89-92.
63. Timmons L, Fire A (1998) Specific interference by ingested dsRNA. Nature 395: 854.
64. Corrigan C, Subramanian R, Miller MA (2005) Eph and NMDA receptors control Ca2+/calmodulin-dependent protein kinase II activation during C. elegans oocyte meiotic maturation. Development 132: 5225-5237.
65. Hsu JC (1996) Multiple comparison: theory and methods. New York: Chapman and Hall.
66. Crittenden SL, Troemel ER, Evans TC, Kimble J (1994) GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120: 2901-2911.
67. Hansen D, Hubbard EJ, Schedl T (2004) Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev Biol 268: 342-357.
68. Goldstein P (1986) Nuclear aberrations and loss of synaptonemal complexes in response to diethylstilbestrol (DES) in Caenorhabditis elegans hermaphrodites. Mutat Res 174: 99-107.
69. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
70. Bishop JD, Han Z, Schumacher JM (2005) The Caenorhabditis elegans Aurora B kinase AIR-2 phosphorylates and is required for the localization of a BimC kinesin to meiotic and mitotic spindles. Mol Biol Cell 16: 742-756.