Protein kinase VRK-1 regulates cell invasion and EGL-17/FGF signaling in Caenorhabditis elegans

Developmental Biology

Volumn 335, Issue 1, 2009, Pages 12-21

  Klerkx, Elke P F ^a   Alarcón, Pilar ^a   Waters, Katherine ^b   Reinke, Valerie ^b   Sternberg, Paul W ^c   Askjaer, Peter ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Anchor cell; Caenorhabditis elegans; Cell invasion; Cell polarity; Cell signaling; FGF; Uterus; Vaccinia related kinase; vrk 1; Vulva

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; HYBRID PROTEIN; MUTANT PROTEIN; PROTEIN KINASE; UNCLASSIFIED DRUG; VACCINIA RELATED KINASE 1;

ALLELE; ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CELL INVASION; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; GERM LINE; GONAD DEVELOPMENT; HERMAPHRODITISM; LARVAL STAGE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; UTERUS; VENTRAL ROOT; VULVA;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 70349783801     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.08.007     Document Type: Article

References (65)

1. Aihara H., Nakagawa T., Yasui K., Ohta T., Hirose S., Dhomae N., Takio K., Kaneko M., Takeshima Y., Muramatsu M., and Ito T. Nucleosomal histone kinase-1 phosphorylates H2A Thr 119 during mitosis in the early Drosophila embryo. Genes Dev. 18 (2004) 877-888
2. Berset T., Hoier E.F., Battu G., Canevascini S., and Hajnal A. Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 291 (2001) 1055-1058
3. Blumenthal, T., 2005. Trans-splicing and operons. WormBook. 1-9, WormBook, ed. doi/10.1895/wormbook.1.5.1, http://www.wormbook.org.
4. Bossis G., Malnou C.E., Farras R., Andermarcher E., Hipskind R., Rodriguez M., Schmidt D., Muller S., Jariel-Encontre I., and Piechaczyk M. Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Mol. Cell Biol. 25 (2005) 6964-6979
5. Broday L., Kolotuev I., Didier C., Bhoumik A., Gupta B.P., Sternberg P.W., Podbilewicz B., and Ronai Z. The small ubiquitin-like modifier (SUMO) is required for gonadal and uterine-vulval morphogenesis in Caenorhabditis elegans. Genes Dev. 18 (2004) 2380-2391
6. Burdine R.D., Branda C.S., and Stern M.J. EGL-17(FGF) expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. elegans. Development 125 (1998) 1083-1093
7. Chen N., and Greenwald I. The lateral signal for LIN-12/Notch in C. elegans vulval development comprises redundant secreted and transmembrane DSL proteins. Dev. Cell 6 (2004) 183-192
8. Cui M., and Han M. Cis regulatory requirements for vulval cell-specific expression of the Caenorhabditis elegans fibroblast growth factor gene egl-17. Dev. Biol. 257 (2003) 104-116
9. Cullen C.F., Brittle A.L., Ito T., and Ohkura H. The conserved kinase NHK-1 is essential for mitotic progression and unifying acentrosomal meiotic spindles in Drosophila melanogaster. J. Cell Biol. 171 (2005) 593-602
10. DeVore D.L., Horvitz H.R., and Stern M.J. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. Cell 83 (1995) 611-620
11. Ferguson E.L., and Horvitz H.R. Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 110 (1985) 17-72
12. Fitzgerald M.C., and Schwarzbauer J.E. Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr. Biol. 8 (1998) 1285-1288
13. Geiss-Friedlander R., and Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8 (2007) 947-956
14. Gorjanacz M., Klerkx E.P., Galy V., Santarella R., Lopez-Iglesias C., Askjaer P., and Mattaj I.W. Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. EMBO J. 26 (2007) 132-143
15. Gupta B.P., and Sternberg P.W. Tissue-specific regulation of the LIM homeobox gene lin-11 during development of the Caenorhabditis elegans egg-laying system. Dev. Biol. 247 (2002) 102-115
16. Hanna-Rose W., and Han M. COG-2, a sox domain protein necessary for establishing a functional vulval-uterine connection in Caenorhabditis elegans. Development 126 (1999) 169-179
17. Harfe B.D., Branda C.S., Krause M., Stern M.J., and Fire A. MyoD and the specification of muscle and non-muscle fates during postembryonic development of the C. elegans mesoderm. Development 125 (1998) 2479-2488
18. Hill R.J., and Sternberg P.W. The gene lin-3 encodes an inductive signal for vulval development in C. elegans. Nature 358 (1992) 470-476
19. Huang P., Pleasance E.D., Maydan J.S., Hunt-Newbury R., O'Neil N.J., Mah A., Baillie D.L., Marra M.A., Moerman D.G., and Jones S.J. Identification and analysis of internal promoters in Caenorhabditis elegans operons. Genome Res. 17 (2007) 1478-1485
20. Hwang B.J., and Sternberg P.W. A cell-specific enhancer that specifies lin-3 expression in the C. elegans anchor cell for vulval development. Development 131 (2004) 143-151
21. Hwang B.J., Meruelo A.D., and Sternberg P.W. C. elegans EVI1 proto-oncogene, EGL-43, is necessary for Notch-mediated cell fate specification and regulates cell invasion. Development 134 (2007) 669-679
22. Inoue T., Sherwood D.R., Aspock G., Butler J.A., Gupta B.P., Kirouac M., Wang M., Lee P.Y., Kramer J.M., Hope I., Burglin T.R., and Sternberg P.W. Gene expression markers for Caenorhabditis elegans vulval cells. Mech. Dev. 119 Suppl. 1 (2002) S203-S209
23. Ivanovska I., Khandan T., Ito T., and Orr-Weaver T.L. A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev. 19 (2005) 2571-2582
24. Kamath R.S., and Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30 (2003) 313-321
25. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., and Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
26. Kang T.H., and Kim K.T. Negative regulation of ERK activity by VRK3-mediated activation of VHR phosphatase. Nat. Cell Biol. 8 (2006) 863-869
27. Kelly W.G., Xu S., Montgomery M.K., and Fire A. Distinct requirements for somatic and germline expression of a generally expressed Caenorhabditis elegans gene. Genetics 146 (1997) 227-238
28. Kimble J. Alterations in cell lineage following laser ablation of cells in the somatic gonad of Caenorhabditis elegans. Dev. Biol. 87 (1981) 286-300
29. Kimble J., and Hirsh D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev. Biol. 70 (1979) 396-417
30. Klerkx E.P., Lazo P.A., and Askjaer P. Emerging biological functions of the vaccinia-related kinase (VRK) family. Histol. Histopathol 24 (2009) 749-759
31. Leight E.R., Glossip D., and Kornfeld K. Sumoylation of LIN-1 promotes transcriptional repression and inhibition of vulval cell fates. Development 132 (2005) 1047-1056
32. Liu J., Rolef Ben-Shahar T., Riemer D., Treinin M., Spann P., Weber K., Fire A., and Gruenbaum Y. Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell 11 (2000) 3937-3947
33. Lopez-Borges S., and Lazo P.A. The human vaccinia-related kinase 1 (VRK1) phosphorylates threonine-18 within the mdm-2 binding site of the p53 tumour suppressor protein. Oncogene 19 (2000) 3656-3664
34. McKay S.J., Johnsen R., Khattra J., Asano J., Baillie D.L., Chan S., Dube N., Fang L., Goszczynski B., Ha E., Halfnight E., Hollebakken R., Huang P., Hung K., Jensen V., Jones S.J., Kai H., Li D., Mah A., Marra M., McGhee J., Newbury R., Pouzyrev A., Riddle D.L., Sonnhammer E., Tian H., Tu D., Tyson J.R., Vatcher G., Warner A., Wong K., Zhao Z., and Moerman D.G. Gene expression profiling of cells, tissues, and developmental stages of the nematode C. elegans. Cold Spring Harb. Symp. Quant. Biol. 68 (2003) 159-169
35. Newman A.P., White J.G., and Sternberg P.W. Morphogenesis of the C. elegans hermaphrodite uterus. Development 122 (1996) 3617-3626
36. Newman A.P., Acton G.Z., Hartwieg E., Horvitz H.R., and Sternberg P.W. The lin-11 LIM domain transcription factor is necessary for morphogenesis of C. elegans uterine cells. Development 126 (1999) 5319-5326
37. Newman A.P., Inoue T., Wang M., and Sternberg P.W. The Caenorhabditis elegans heterochronic gene lin-29 coordinates the vulval-uterine-epidermal connections. Curr. Biol. 10 (2000) 1479-1488
38. Nichols R.J., and Traktman P. Characterization of three paralogous members of the mammalian vaccinia related kinase family. J. Biol. Chem 279 (2004) 7934-7946
39. Nichols R.J., Wiebe M.S., and Traktman P. The vaccinia-related kinases phosphorylate the N′ terminus of BAF, regulating its interaction with DNA and its retention in the nucleus. Mol. Biol. Cell. 17 (2006) 2451-2464
40. Piano F., Schetter A.J., Morton D.G., Gunsalus K.C., Reinke V., Kim S.K., and Kemphues K.J. Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans. Curr. Biol. 12 (2002) 1959-1964
41. Poulin G., Dong Y., Fraser A.G., Hopper N.A., and Ahringer J. Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans. EMBO J. 24 (2005) 2613-2623
42. Rimann I., and Hajnal A. Regulation of anchor cell invasion and uterine cell fates by the egl-43 Evi-1 proto-oncogene in Caenorhabditis elegans. Dev. Biol. 308 (2007) 187-195
43. Santos C.R., Rodriguez-Pinilla M., Vega F.M., Rodriguez-Peralto J.L., Blanco S., Sevilla A., Valbuena A., Hernandez T., van Wijnen A.J., Li F., de Alava E., Sanchez-Cespedes M., and Lazo P.A. VRK1 signaling pathway in the context of the proliferation phenotype in head and neck squamous cell carcinoma. Mol. Cancer Res 4 (2006) 177-185
44. Sasson I.E., and Stern M.J. FGF and PI3 kinase signaling pathways antagonistically modulate sex muscle differentiation in C. elegans. Development 131 (2004) 5381-5392
45. Sevilla A., Santos C.R., Barcia R., Vega F.M., and Lazo P.A. c-Jun phosphorylation by the human vaccinia-related kinase 1 (VRK1) and its cooperation with the N-terminal kinase of c-Jun (JNK). Oncogene 23 (2004) 8950-8958
46. Sevilla A., Santos C.R., Vega F.M., and Lazo P.A. Human vaccinia-related kinase 1 (VRK1) activates the ATF2 transcriptional activity by novel phosphorylation on Thr-73 and Ser-62 and cooperates with JNK. J. Biol. Chem. 279 (2004) 27458-27465
47. Seydoux G., Savage C., and Greenwald I. Isolation and characterization of mutations causing abnormal eversion of the vulva in Caenorhabditis elegans. Dev. Biol. 157 (1993) 423-436
48. Sharma-Kishore R., White J.G., Southgate E., and Podbilewicz B. Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis. Development 126 (1999) 691-699
49. Shaye D.D., and Greenwald I. Endocytosis-mediated downregulation of LIN-12/Notch upon Ras activation in Caenorhabditis elegans. Nature 420 (2002) 686-690
50. Sherwood D.R. Cell invasion through basement membranes: an anchor of understanding. Trends Cell Biol. 16 (2006) 250-256
51. Sherwood D.R., and Sternberg P.W. Anchor cell invasion into the vulval epithelium in C. elegans. Dev. Cell 5 (2003) 21-31
52. Sherwood D.R., Butler J.A., Kramer J.M., and Sternberg P.W. FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans. Cell 121 (2005) 951-962
53. Sternberg P.W. Lateral inhibition during vulval induction in Caenorhabditis elegans. Nature 335 (1988) 551-554
54. Sternberg, P. W., 2005. Vulval development. WormBook. 1-28, WormBook, ed. doi/10.1895/wormbook.1.6.1, http://www.wormbook.org.
55. Sternberg P.W., and Horvitz H.R. Pattern formation during vulval development in C. elegans. Cell 44 (1986) 761-772
56. Stiernagle, T., 2006. Maintenance of C. elegans. WormBook. 1-11, WormBook, ed. doi/10.1895/wormbook.1.101.1, http://www.wormbook.org.
57. Sulston J.E., and Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56 (1977) 110-156
58. Sundaram, M. V., 2006. RTK/Ras/MAPK signaling. WormBook. 1-19, WormBook, ed. doi/10.1895/wormbook.1.80.1, http://www.wormbook.org.
59. Tan P.B., Lackner M.R., and Kim S.K. MAP kinase signaling specificity mediated by the LIN-1 Ets/LIN-31 WH transcription factor complex during C. elegans vulval induction. Cell 93 (1998) 569-580
60. Thomas J.H., Stern M.J., and Horvitz H.R. Cell interactions coordinate the development of the C. elegans egg-laying system. Cell 62 (1990) 1041-1052
61. Tiensuu T., Larsen M.K., Vernersson E., and Tuck S. lin-1 has both positive and negative functions in specifying multiple cell fates induced by Ras/MAP kinase signaling in C. elegans. Dev. Biol. 286 (2005) 338-351
62. Valbuena A., Lopez-Sanchez I., and Lazo P.A. Human VRK1 is an early response gene and its loss causes a block in cell cycle progression. PLoS ONE 3 (2008) e1642
63. Vazquez-Manrique R.P., Gonzalez-Cabo P., Ortiz-Martin I., Ros S., Baylis H.A., and Palau F. The frataxin-encoding operon of Caenorhabditis elegans shows complex structure and regulation. Genomics 89 (2007) 392-401
64. Yoo A.S., Bais C., and Greenwald I. Crosstalk between the EGFR and LIN-12/Notch pathways in C. elegans vulval development. Science 303 (2004) 663-666
65. Ziel J.W., Hagedorn E.J., Audhya A., and Sherwood D.R. UNC-6 (netrin) orients the invasive membrane of the anchor cell in C. elegans. Nat. Cell Biol. 11 (2009) 183-189