C. elegans Dicer interacts with the P-granule component GLH-1 and both regulate germline RNPs

Developmental Biology

Volumn 350, Issue 2, 2011, Pages 370-381

  Beshore, Erica L ^a   McEwen, Tamara J ^a   Jud, Molly C ^b,c   Marshall, Jordan K ^a,d   Schisa, Jennifer A ^b   Bennett, Karen L ^a  

^a University of Missouri   (United States)

^b CENTRAL MICHIGAN UNIVERSITY   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d HOWARD UNIVERSITY   (United States)

Author keywords

Jun N terminal kinase (JNK); KGB 1; MiRNA pathway; Oocyte RNP granules; Processing bodies

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; DICER; INITIATION FACTOR; MICRORNA; PROTEIN GLH 1; PROTEIN KGB 1; RIBONUCLEOPROTEIN; RNA HELICASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL NUCLEUS; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME REGULATION; GENE CONTROL; GENE DELETION; GENE LOCATION; GERM CELL; NONHUMAN; NUCLEAR PORE; OOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

EID: 79151482190     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.12.005     Document Type: Article

References (72)

1. Adler J., Parmryd I. Quantifying co-localization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytom. A 2010, 77A:733-742.
2. Amiri A., Keiper B.D., Kawasaki I., et al. An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans. Development 2001, 128:3899-3912.
3. Anderson P., Kedersha N. RNA granules. J. Cell Biol.: Mini-Review 2006, 172(6):803-808.
4. Balagopal V., Parker R. Polysomes. P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol. 2009, 21(3):403-408.
5. Barbee S.A., Lubin A.L., Evans T.C. A novel function for the Sm proteins in germ granule localization during C. elegans embryogenesis. Curr. Biol. 2002, 12:1502-1506.
6. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
7. Claycomb J.M., Batista P.J., Pang K.M., et al. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 2009, 139(1):123-134.
8. Colaiácovo M.P., Stanfield G.M., Reddy K.C., et al. A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 2002, 162(1):113-128.
9. Davis L.I., Blobel G. Identification and characterization of a nuclear pore complex protein. Cell 1986, 45(5):699-709.
10. Ding L., Spencer A., Morita K., et al. The developmental timing regulator AIN-1 interacts with miRISCs and may target the Argonaute protein ALG-1 to cytoplasmic P bodies in C. elegans. Mol. Cell 2005, 19:437-447.
11. Draper B.W., Mello C.C., Bowerman B., et al. MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 1996, 87(2):205-216.
12. Duchaine T.F., Wohlschlegel J.A., Kennedy, et al. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 2006, 124:343-354.
13. Eddy E.M. Germ plasm and differentiation of the germ cell line. Int. Rev. Cytol. 1975, 43:229-280.
14. Emmerth S., Schober H., Gaidatzis D., et al. Nuclear retention of fission yeast Dicer is a prerequisite for RNAi-mediated heterochromatin assembly. Dev. Cell 2010, 18:102-113.
15. Etemad-Moghadam B., Guo S., Kemphues K.J. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 1995, 83(5):743-752.
16. Findley S.D., Tamanaha M., Clegg N.J., et al. Maelstrom, a Drosophila spindle-class gene, encodes a protein that co-localizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 2003, 130(5):859-871.
17. Gruidl M.E., Smith P.A., Kuznicki K.A., et al. Multiple potential germline helicases are components of the germline-specific P granules of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 1996, 93:13837-13842.
18. Guedes S., Priess J.R. The C. elegans MEX-1 protein is present in germline blastomeres and is a P granule component. Development 1997, 124(3):731-739.
19. Guo S., Kemphues K.J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 1995, 81(4):611-620.
20. Hay B., Jan L.Y., Jan Y.N. A protein component of Drosophila polar granules is encoded by Vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 1988, 55(4):577-578.
21. Jacobs D., Glossip D., Xing H., et al. Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev. 1999, 13:163-175.
22. Jakymiw A., Lian S., Eystathioy T., et al. Disruption of GW bodies impairs mammalian RNA interference. Nat. Cell Biol. 2005, 7(12):1267-1273.
23. Jin Z., Xie T. Dcr-1 maintains Drosophila ovarian stem cells. Curr. Biol. 2007, 17:539-544.
24. Jones A.R., Francis R., Schedl T. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 1996, 180:165-183.
25. Jud M., Razelun J., Bickel J., et al. Conservation of large foci formation in arrested oocytes of Caenorhabditis nematodes. Dev. Genes Evol. 2007, 217(3):221-226.
26. Jud M.C., Czerwinski M.J., Wood M.P., et al. Large P body-like RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway. Dev. Biol. 2008, 318:38-51.
27. Kamath R.S., Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003, 30(4):313-321.
28. Kawasaki I., Shim Y.H., Kirchner J., et al. PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 1998, 94:635-645.
29. Kawasaki I., Amiri A., Fan Y., et al. The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics 2004, 167(2):645-661.
30. Kedersha N.L., Gupta M., Li W., et al. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2alpha to the assembly of mammalian stress granules. J. Cell Biol. 1999, 147:1431-1442.
31. Knight S.W., Bass B.L. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science 2001, 293(5538):2269-2271.
32. Kotaja N., Bhattacharyya S.N., Jaskiewicz L., et al. The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and mircroRNA pathway components. Proc. Natl Acad. Sci. USA 2006, 103:2647-2652.
33. Kuznicki K.A., Smith P.A., Leung-Chiu W.M., et al. Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P-granule components are critical for fertility in C. elegans. Development 2000, 13:2907-2916.
34. Lasko P.F., Ashburner M. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 1988, 335(6191):611-617.
35. Liu J., Rivas F.V., Wohlsclegel J., et al. A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 2005, 7(12):1261-1266.
36. Liu J., Valencia-Sanchez M.A., Hannon G., et al. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 2005, 7(7):719-723.
37. Liu N., Han H., Lasko P. Vasa promotes Drosophila germline stem cell differentiation by activating Mei-P26 translation by directly interacting with a (U)-rich motif in its 3′ UTR. Genes Dev. 2009, 23(23):2742-2752.
38. Megosh H.B., Cox D.N., Campbell C., et al. The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr. Biol. 2006, 16:1884-1894.
39. Mello C.C., Schubert C., Draper B., et al. The PIE-1 protein and germline specification in C. elegans embryos. Nature 1996, 382(6593):710-712.
40. Minasaki R., Puoti A., Streit A. The DEAD-box protein MEL-46 is required in the germ line of the nematode Caenorhabditis elegans. BMC Dev. Biol. 2009, 9(35):1-14.
41. Murchison E.P., Stein P., Xuan Z., et al. Critical roles for Dicer in the female germline. Genes Dev. 2007, 21:682-683.
42. Nagamori I., Sassone-Corsi P. The chromatoid body of male germ cells. Cell Cycle 2008, 7(22):3503-3508.
43. Nakagawa A., Shi Y., Kage-Nakadai E., Mitani S., et al. Caspase-dependent conversion of Dicer ribonuclease into a death-promoting deoxyribonuclease. Science 2010, 328:327-334.
44. Navarro R.E., Shim E.Y., Kohara Y., et al. cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans. Development 2001, 128:3221-3232.
45. Noble S.L., Allen B.L., Goh L.K., et al. Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development. J. Cell Biol. 2008, 182(3):559-572.
46. Orlicky S., Tang X., Willems A., et al. Structural basis for phosphodependent substrate selection and orientation by the SCF Cdc4 ubiquitin ligase. Cell 2003, 112:243-256.
47. Orsborn A.M., Li W., McEwen T.J., et al. GLH-1, the C. elegans P-granule protein, is controlled by the JNK KGB-1 and by the COP9 subunit CSN-5. Development 2007, 18:3383-3392.
48. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29(9):2002-2007.
49. Roussell D.L., Bennett K.L. GLH-1: a germline putative RNA helicase from Caenorhabditis has four zinc fingers. Proc. Natl Acad. Sci. USA 1993, 90:9300-9304.
50. Schedl T., Kimble J. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 1988, 119(1):43-61.
51. Schisa J.A., Pitt J.N., Priess J.R. Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 2001, 128(8):1287-1298.
52. Sen G.L., Blau H.M. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 2005, 7(6):633-636.
53. Sharrocks A.D., Yang S.H., Galanis A. Docking domains and substrate specificity determination for MAP kinases. Trends Biochem. Sci. 2000, 25:448-453.
54. Sheth U., Pitt J., Dennis, et al. Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells. Development 2010, 137(8):1305-1314.
55. Shimada M., Yokosawa H., Kawahara H. OMA-1 is a P granules-associated protein that is required for germline specification in Caenorhabditis elegans embryos. Genes Cells 2006, 11(4):383-396.
56. Smith P.A., Leung-Chiu W.M., Montgomery R., et al. The GLH proteins, Caenorhabditis elegans P-granule components, associate with CSN-5 and KGB-1, proteins necessary for fertility, and with ZYX-1 a predicted cytoskeletal protein. Dev. Biol. 2002, 251:333-347.
57. Spike C., Meyer N., Racen E., et al. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 2008, 178(4):1973-1987.
58. Strome S., Lehmann R. Germ versus soma decisions: lessons from flies and worms. Science 2007, 316(5823):392-393.
59. Strome S., Wood W.B. Immunofluorescence visualization of germline-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 1982, 79:1558-1562.
60. Strome S., Wood W.B. Generation of asymmetry and segregation of germline granules in early C. elegans embryos. Cell 1983, 35:15-25.
61. Styhler S., Nakamura A., Swan A., et al. Vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 1998, 125(9):1569-1578.
62. Subramaniam K., Seydoux G. nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 1999, 126(21):4861-4871.
63. Tabara H., Hill R.J., Mello C.C., et al. pos-1 encodes a cytoplasmic zinc-finger protein essential for germline specification in C. elegans. Development 1999, 126(1):1-11.
64. Tomancak P., Guichet A., Zavorszky P., et al. Oocyte polarity depends on regulation of gurken by Vasa. Development 1998, 125(9):1723-1732.
65. Tourrière H., Chebli K., Zekri L., et al. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 2003, 160:823-831.
66. Updike D.L., Strome S. A genomewide RNAi screen for genes that affect the stability, distribution and function of P granules in Caenorhabditis elegans. Genetics 2009, 183:1397-1419.
67. Villanueva A., Lozano J., Morales A., et al. jkk-1 and mek-1 regulate body movement coordination and response to heavy metals through jnk-1 in Caenorhabditis elegans. EMBO J. 2001, 20(18):5114-5128.
68. Voronina E., Seydoux G. The nucleoporin Nup98 is required for the integrity and function of germline P granules in C. elegans. Development 2010, 137(9):1441-1450.
69. Welker N.C., Habig J.W., Bass B.L. Genes mis-regulated in C. elegans deficient in Dicer, RDE-4, or RDE-1 are enriched for innate immunity genes. RNA 2007, 13(7):1090-1102.
70. Wickens M., Goldstrohm A. A place to die, a place to sleep. Science 2003, 300:753-755.
71. Wolke U., Jezuit E.A., Priess J.R. Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 2007, 134(12):2227-2236.
72. Ye X., Nalepa G., Welcker M., et al. Recognition of phosphodegron motifs in human cyclin E by the SCF Fbw7 ubiquitin ligase. J. Biol. Chem. 2004, 279:50110-50119.