The gap junctional protein INX-14 functions in oocyte precursors to promote C. elegans sperm guidance

Developmental Biology

Volumn 359, Issue 1, 2011, Pages 47-58

  Edmonds, Johnathan W ^a   McKinney, Shauna L ^b   Prasain, Jeevan K ^c   Miller, Michael A ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

C. elegans; Chemotaxis; Fertilization; FOXO; Gap junction; Innexin; Oocyte; Pannexin; Prostaglandin; Sperm

Indexed keywords

GAP JUNCTION PROTEIN; PROSTAGLANDIN; PROTEIN INX 14; PROTEIN INX 8; PROTEIN INX 9; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENTAL GENE; ELECTRON MICROSCOPY; GENE CONTROL; GENE LOSS; GENETIC ANALYSIS; GERM CELL; HERMAPHRODITIC SPECIES; IMMUNOCYTOCHEMISTRY; INX 14 GENE; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPERMATOCYTE; SPERMATOZOON MIGRATION; SPERMATOZOON MOTILITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

CAENORHABDITIS ELEGANS; INVERTEBRATA;

EID: 80053604526     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.08.014     Document Type: Article

References (63)

1. Ackert C.L., Gittens J.E., O'Brien M.J., Eppig J.J., Kidder G.M. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev. Biol. 2001, 233:258-270.
2. Aitken R.J., Kelly R.W. Analysis of the direct effects of prostaglandins on human sperm function. J. Reprod. Fertil. 1985, 73:139-146.
3. Altun Z.F., Chen B., Wang Z.W., Hall D.H. High resolution map of Caenorhabditis elegans gap junction proteins. Dev. Dyn. 2009, 238:1936-1950.
4. Anderson E., Albertini D.F. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J. Cell Biol. 1976, 71:680-686.
5. Baranova A., Ivanov D., Petrash N., Pestova A., Skoblov M., Kelmanson I., Shagin D., Nazarenko S., Geraymovych E., Litvin O., Tiunova A., Born T.L., Usman N., Staroverov D., Lukyanov S., Panchin Y. The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 2004, 83:706-716.
6. Bevans C.G., Kordel M., Rhee S.K., Harris A.L. Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J. Biol. Chem. 1998, 273:2808-2816.
7. Bottino D., Mogilner A., Roberts T., Stewart M., Oster G. How nematode sperm crawl. J. Cell Sci. 2002, 115:367-384.
8. Dbouk H.A., Mroue R.M., El-Sabban M.E., Talhouk R.S. Connexins: a myriad of functions extending beyond assembly of gap junction channels. Cell Commun. Signal 2009, 7:4.
9. Dekel N. Cellular, biochemical and molecular mechanisms regulating oocyte maturation. Mol. Cell. Endocrinol. 2005, 234:19-25.
10. Edmonds J.W., Prasain J.K., Dorand D., Yang Y., Hoang H.D., Vibbert J., Kubagawa H.M., Miller M.A. Insulin/FOXO signaling regulates ovarian prostaglandins critical for reproduction. Dev. Cell 2010, 19:858-871.
11. Eisenbach M., Giojalas L.C. Sperm guidance in mammals - an unpaved road to the egg. Nat. Rev. Mol. Cell Biol. 2006, 7:276-285.
12. Gershon E., Plaks V., Dekel N. Gap junctions in the ovary: expression, localization and function. Mol. Cell. Endocrinol. 2008, 282:18-25.
13. Gilula N.B., Epstein M.L., Beers W.H. Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J. Cell Biol. 1978, 78:58-75.
14. Gittens J.E., Kidder G.M. Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries. J. Cell Sci. 2005, 118:5071-5078.
15. Golovko M.Y., Murphy E.J. An improved LC-MS/MS procedure for brain prostanoid analysis using brain fixation with head-focused microwave irradiation and liquid-liquid extraction. J. Lipid Res. 2008, 49:893-902.
16. Goodenough D.A. Bulk isolation of mouse hepatocyte gap junctions. Characterization of the principal protein, connexin. J. Cell Biol. 1974, 61:557-563.
17. Gottlieb C., Svanborg K., Eneroth P., Bygdeman M. Effect of prostaglandins on human sperm function in vitro and seminal adenosine triphosphate content. Fertil. Steril. 1988, 49:322-327.
18. Govindan J.A., Cheng H., Harris J.E., Greenstein D. Galphao/i and Galphas signaling function in parallel with the MSP/Eph receptor to control meiotic diapause in C. elegans. Curr. Biol. 2006, 16:1257-1268.
19. Govindan J.A., Nadarajan S., Kim S., Starich T.A., Greenstein D. Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans. Development 2009, 136:2211-2221.
20. Grant B., Hirsh D. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 1999, 10:4311-4326.
21. Guidobaldi H.A., Teves M.E., Unates D.R., Anastasia A., Giojalas L.C. Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PLoS One 2008, 3:e3040.
22. Hall D.H., Winfrey V.P., Blaeuer G., Hoffman L.H., Furuta T., Rose K.L., Hobert O., Greenstein D. Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev. Biol. 1999, 212:101-123.
23. Han S.M., Cottee P.A., Miller M.A. Sperm and oocyte communication mechanisms controlling C. elegans fertility. Dev. Dyn. 2010, 239:1265-1281.
24. Harris A.L. Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys. 2001, 34:325-472.
25. Henderson S.T., Bonafe M., Johnson T.E. daf-16 protects the nematode Caenorhabditis elegans during food deprivation. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61:444-460.
26. Juneja S.C., Barr K.J., Enders G.C., Kidder G.M. Defects in the germ line and gonads of mice lacking connexin43. Biol. Reprod. 1999, 60:1263-1270.
27. Kamath R.S., Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003, 30:313-321.
28. Kanai N., Lu R., Satriano J.A., Bao Y., Wolkoff A.W., Schuster V.L. Identification and characterization of a prostaglandin transporter. Science 1995, 268:866-869.
29. Kelly W.G., Schaner C.E., Dernburg A.F., Lee M.H., Kim S.K., Villeneuve A.M., Reinke V. X-chromosome silencing in the germline of C. elegans. Development 2002, 129:479-492.
30. Kidder G.M., Mhawi A.A. Gap junctions and ovarian folliculogenesis. Reproduction 2002, 123:613-620.
31. Kubagawa H.M., Watts J.L., Corrigan C., Edmonds J.W., Sztul E., Browse J., Miller M.A. Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nat. Cell Biol. 2006, 8:1143-1148.
32. L'Hernault S.W. The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol. Cell. Endocrinol. 2009, 306:59-65.
33. Lim H., Paria B.C., Das S.K., Dinchuk J.E., Langenbach R., Trzaskos J.M., Dey S.K. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 1997, 91:197-208.
34. Lishko P.V., Botchkina I.L., Kirichok Y. Progesterone activates the principal Ca2+ channel of human sperm. Nature 2011, 471:387-391.
35. Miller M.A., Nguyen V.Q., Lee M.H., Kosinski M., Schedl T., Caprioli R.M., Greenstein D. A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 2001, 291:2144-2147.
36. Miyata S., Begun J., Troemel E.R., Ausubel F.M. DAF-16-dependent suppression of immunity during reproduction in Caenorhabditis elegans. Genetics 2008, 178:903-918.
37. Mroue R.M., El-Sabban M.E., Talhouk R.S. Connexins and the gap in context. Integr. Biol. (Camb) 2011, 3:255-266.
38. Murdoch W.J., Hansen T.R., McPherson L.A. A review-role of eicosanoids in vertebrate ovulation. Prostaglandins 1993, 46:85-115.
39. Murphy R.C., Barkley R.M., Zemski Berry K., Hankin J., Harrison K., Johnson C., Krank J., McAnoy A., Uhlson C., Zarini S. Electrospray ionization and tandem mass spectrometry of eicosanoids. Anal. Biochem. 2005, 346:1-42.
40. Nicholson B.J. Gap junctions - from cell to molecule. J. Cell Sci. 2003, 116:4479-4481.
41. Niessen H., Harz H., Bedner P., Kramer K., Willecke K. Selective permeability of different connexin channels to the second messenger inositol 1,4,5-trisphosphate. J. Cell Sci. 2000, 113(Pt 8):1365-1372.
42. Oh S.W., Mukhopadhyay A., Dixit B.L., Raha T., Green M.R., Tissenbaum H.A. Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat. Genet. 2006, 38:251-257.
43. Panchin Y.V. Evolution of gap junction proteins-the pannexin alternative. J. Exp. Biol. 2005, 208:1415-1419.
44. Phelan P., Starich T.A. Innexins get into the gap. Bioessays 2001, 23:388-396.
45. Phelan P., Bacon J.P., Davies J.A., Stebbings L.A., Todman M.G., Avery L., Baines R.A., Barnes T.M., Ford C., Hekimi S., Lee R., Shaw J.E., Starich T.A., Curtin K.D., Sun Y.A., Wyman R.J. Innexins: a family of invertebrate gap-junction proteins. Trends Genet. 1998, 14:348-349.
46. Reaume A.G., de Sousa P.A., Kulkarni S., Langille B.L., Zhu D., Davies T.C., Juneja S.C., Kidder G.M., Rossant J. Cardiac malformation in neonatal mice lacking connexin43. Science 1995, 267:1831-1834.
47. Reid G., Wielinga P., Zelcer N., van der Heijden I., Kuil A., de Haas M., Wijnholds J., Borst P. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9244-9249.
48. Rose K.L., Winfrey V.P., Hoffman L.H., Hall D.H., Furuta T., Greenstein D. The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 1997, 192:59-77.
49. Schedl T., Kimble J. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 1988, 119:43-61.
50. 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, 128:1287-1298.
51. Schuster V.L. Prostaglandin transport. Prostaglandins Other Lipid Mediat. 2002, 68-69:633-647.
52. Seydoux G., Dunn M.A. Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development 1997, 124:2191-2201.
53. Sijen T., Fleenor J., Simmer F., Thijssen K.L., Parrish S., Timmons L., Plasterk R.H., Fire A. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 2001, 107:465-476.
54. Simon A.M., Goodenough D.A., Li E., Paul D.L. Female infertility in mice lacking connexin 37. Nature 1997, 385:525-529.
55. Starich T., Sheehan M., Jadrich J., Shaw J. Innexins in C. elegans. Cell Commun. Adhes. 2001, 8:311-314.
56. Strunker T., Goodwin N., Brenker C., Kashikar N.D., Weyand I., Seifert R., Kaupp U.B. The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 2011, 471:382-386.
57. Tamba S., Yodoi R., Segi-Nishida E., Ichikawa A., Narumiya S., Sugimoto Y. Timely interaction between prostaglandin and chemokine signaling is a prerequisite for successful fertilization. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14539-14544.
58. Teves M.E., Barbano F., Guidobaldi H.A., Sanchez R., Miska W., Giojalas L.C. Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil. Steril. 2006, 86:745-749.
59. Timmons L., Fire A. Specific interference by ingested dsRNA. Nature 1998, 395:854.
60. Unger V.M., Kumar N.M., Gilula N.B., Yeager M. Three-dimensional structure of a recombinant gap junction membrane channel. Science 1999, 283:1176-1180.
61. Watts J.L., Browse J. Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5854-5859.
62. Whitten S.J., Miller M.A. The role of gap junctions in Caenorhabditis elegans oocyte maturation and fertilization. Dev. Biol. 2007, 301:432-446.
63. Yamamoto I., Kosinski M.E., Greenstein D. Start me up: cell signaling and the journey from oocyte to embryo in C. elegans. Dev. Dyn. 2005, 235:571-585.