Protein phosphorylation changes reveal new candidates in the regulation of egg activation and early embryogenesis in D. melanogaster

Developmental Biology

Volumn 370, Issue 1, 2012, Pages 125-134

  Krauchunas, Amber R ^a   Horner, Vanessa L ^a,b   Wolfner, Mariana F ^a  

^a Department of Obstetrics Gynecology   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Egg activation; Phosphorylation; Proteomics

Indexed keywords

MESSENGER RNA; PHOSPHOPEPTIDE;

ARTICLE; CALCIUM BINDING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FEMALE; GENE; GENE FUNCTION; GENE SILENCING; GENETIC ASSOCIATION; INSECT GENETICS; MALE; MEIOSIS; MITOSIS; MRITYU GENE; NONHUMAN; OOCYTE ACTIVATION; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEOMICS; REGULATORY MECHANISM; RNA DEGRADATION; RNA INTERFERENCE;

DROSOPHILA MELANOGASTER;

EID: 84865647770     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.07.024     Document Type: Article

References (71)

1. Ahn N.G., Resing K.A. Toward the phosphoproteome. Nat. Biotechnol. 2001, 19:317-318.
2. Allis C.D., Waring G.L., Mahowald A.P. Mass isolation of pole cells from Drosophila melanogaster. Dev. Biol. 1977, 56:372-381.
3. Alves V.S., Motta F.L., Roffe M., Delamano A., Pesquero J.B., Castilho B.A. GCN2 activation and eIF2alpha phosphorylation in the maturation of mouse oocytes. Biochem. Biophys. Res. Commun. 2009, 378:41-44.
4. Backs J., Stein P., Backs T., Duncan F.E., Grueter C.E., McAnally J., Qi X., Schultz R.M., Olson E.N. The gamma isoform of CaM kinase II controls mouse egg activation by regulating cell cycle resumption. Proc. Nat. Acad. Sci. U. S. A. 2010, 107:81-86.
5. Barisic M., Sohm B., Mikolcevic P., Wandke C., Rauch V., Ringer T., Hess M., Bonn G., Geley S. Spindly/CCDC99 is required for efficient chromosome congression and mitotic checkpoint regulation. Mol. Biol. Cell. 2010, 21:1968-1981.
6. Boswell R.E., Mahowald A.P. tudor, A gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 1985, 43:97-104.
7. Carbon S., Ireland A., Mungall C.J., Shu S., Marshall B., Lewis S. AmiGO: online access to ontology and annotation data. Bioinformatics 2009, 25:288-289.
8. Cargnello M., Roux P.P. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 2011, 75:50-83.
9. Chan Y.W., Fava L.L., Uldschmid A., Schmitz M.H., Gerlich D.W., Nigg E.A., Santamaria A. Mitotic control of kinetochore-associated dynein and spindle orientation by human Spindly. J. Cell Biol. 2009, 185:859-874.
10. Chang H.Y., Minahan K., Merriman J.A., Jones K.T. Calmodulin-dependent protein kinase gamma 3 (CamKIIgamma3) mediates the cell cycle resumption of metaphase II eggs in mouse. Development 2009, 136:4077-4081.
11. Chik J.K., Schriemer D.C., Childs S.J., McGhee J.D. Proteome of the Caenorhabditis elegans oocyte. J. Proteome Res. 2011.
12. Chintapalli V.R., Wang J., Dow J.A. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 2007, 39:715-720.
13. Dix C.I., Raff J.W. Drosophila Spd-2 recruits PCM to the sperm centriole, but is dispensable for centriole duplication. Curr. Biol. 2007, 17:1759-1764.
14. Doane W.W. Completion of meiosis in uninseminated eggs of Drosophila melanogaster. Science 1960, 132:677-678.
15. 2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev. Biol. 2008, 315:257-279.
16. Eisen A., Kiehart D.P., Wieland S.J., Reynolds G.T. Temporal sequence and spatial distribution of early events of fertilization in single sea urchin eggs. J. Cell Biol. 1984, 99:1647-1654.
17. Fan H.Y., Sun Q.Y. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 2004, 70:535-547.
18. Giet R., McLean D., Descamps S., Lee M.J., Raff J.W., Prigent C., Glover D.M. Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules. J. Cell Biol. 2002, 156:437-451.
19. Gilkey J.C., Jaffe L.F., Ridgway E.B., Reynolds G.T. A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J. Cell Biol. 1978, 76:448-466.
20. Griffis E.R., Stuurman N., Vale R.D. Spindly, a novel protein essential for silencing the spindle assembly checkpoint, recruits dynein to the kinetochore. J. Cell Biol. 2007, 177:1005-1015.
21. Hansen D.V., Tung J.J., Jackson P.K. CaMKII and polo-like kinase 1 sequentially phosphorylate the cytostatic factor Emi2/XErp1 to trigger its destruction and meiotic exit. Proc. Nat. Acad. Sci. U. S. A. 2006, 103:608-613.
22. Heifetz Y., Yu J., Wolfner M.F. Ovulation triggers activation of Drosophila oocytes. Dev. Biol. 2001, 234:416-424.
23. Horner V.L., Czank A., Jang J.K., Singh N., Williams B.C., Puro J., Kubli E., Hanes S.D., McKim K.S., Wolfner M.F., Goldberg M.L. The Drosophila calcipressin sarah is required for several aspects of egg activation. Curr. Biol. 2006, 16:1441-1446.
24. Horner V.L., Wolfner M.F. Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev. Dyn. 2008, 237:527-544.
25. Horner V.L., Wolfner M.F. Mechanical stimulation by osmotic and hydrostatic pressure activates Drosophila oocytes in vitro in a calcium-dependent manner. Dev. Biol. 2008, 316:100-109.
26. Karr T.L. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech. Dev. 1991, 34:101-111.
27. Karr T.L., Alberts B.M. Organization of the cytoskeleton in early Drosophila embryos. J. Cell Biol. 1986, 102:1494-1509.
28. Kim A.M., Vogt S., O'Halloran T.V., Woodruff T.K. Zinc availability regulates exit from meiosis in maturing mammalian oocytes. Nat. Chem. Biol. 2010, 6:674-681.
29. Kinoshita E., Kinoshita-Kikuta E., Koike T. Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat. Protoc. 2009, 4:1513-1521.
30. Kinoshita E., Kinoshita-Kikuta E., Takiyama K., Koike T. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 2006, 5:749-757.
31. Lee L.A., Van Hoewyk D., Orr-Weaver T.L. The Drosophila cell cycle kinase PAN GU forms an active complex with PLUTONIUM and GNU to regulate embryonic divisions. Genes Dev. 2003, 17:2979-2991.
32. Lin H.F., Wolfner M.F. The Drosophila maternal-effect gene fs(1)Ya encodes a cell cycle-dependent nuclear envelope component required for embryonic mitosis. Cell 1991, 64:49-62.
33. Liu J., Maller J.L. Calcium elevation at fertilization coordinates phosphorylation of XErp1/Emi2 by Plx1 and CaMK II to release metaphase arrest by cytostatic factor. Curr. Biol. 2005, 15:1458-1468.
34. Markoulaki S., Matson S., Ducibella T. Fertilization stimulates long-lasting oscillations of CaMKII activity in mouse eggs. Dev. Biol. 2004, 272:15-25.
35. McKnight S.L., Miller O.L. Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell 1976, 8:305-319.
36. Mische S., He Y., Ma L., Li M., Serr M., Hays T.S. Dynein light intermediate chain: an essential subunit that contributes to spindle checkpoint inactivation. Mol. Biol. Cell 2008, 19:4918-4929.
37. Mochida S., Hunt T. Calcineurin is required to release Xenopus egg extracts from meiotic M phase. Nature 2007, 449:336-340.
38. Monsma S.A., Wolfner M.F. Structure and expression of a Drosophila male accessory gland gene whose product resembles a peptide pheromone precursor. Genes Dev. 1988, 2:1063-1073.
39. Newby L.M., Jackson F.R. Regulation of a specific circadian clock output pathway by lark, a putative RNA-binding protein with repressor activity. J. Neurobiol. 1996, 31:117-128.
40. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 1982, 30:675-686.
41. Ni J.Q., Zhou R., Czech B., Liu L.P., Holderbaum L., Yang-Zhou D., Shim H.S., Tao R., Handler D., Karpowicz P., Binari R., Booker M., Brennecke J., Perkins L.A., Hannon G.J., Perrimon N. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat. Methods 2011, 8:405-407.
42. Nie M., Xie Y., Loo J.A., Courey A.J. Genetic and proteomic evidence for roles of Drosophila SUMO in cell cycle control, Ras signaling, and early pattern formation. PLoS One 2009, 4:e5905.
43. Nishiyama T., Yoshizaki N., Kishimoto T., Ohsumi K. Transient activation of calcineurin is essential to initiate embryonic development in Xenopus laevis. Nature 2007, 449:341-345.
44. Ostlund G., Schmitt T., Forslund K., Kostler T., Messina D.N., Roopra S., Frings O., Sonnhammer E.L. InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucl. Acids Res. 2010, 38:D196-D203.
45. Page A.W., Orr-Weaver T.L. Activation of the meiotic divisions in Drosophila oocytes. Dev. Biol. 1997, 183:195-207.
46. Pennetta G., Hiesinger P.R., Fabian-Fine R., Meinertzhagen I.A., Bellen H.J. Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron 2002, 35:291-306.
47. Poon I.K., Jans D.A. Regulation of nuclear transport: central role in development and transformation?. Traffic 2005, 6:173-186.
48. Rauh N.R., Schmidt A., Bormann J., Nigg E.A., Mayer T.U. Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation. Nature 2005, 437:1048-1052.
49. Renault A.D., Zhang X.H., Alphey L.S., Frenz L.M., Glover D.M., Saunders R.D., Axton J.M. Giant nuclei is essential in the cell cycle transition from meiosis to mitosis. Development 2003, 130:2997-3005.
50. Roux M., Townley I., Raisch M., Reade A., Bradham C., Humphreys G., Gunaratne H., Killian C., Moy G., Su Y. A functional genomic and proteomic perspective of sea urchin calcium signaling and egg activation. Dev. Biol. 2006, 300:416-433.
51. Roux M.M., Radeke M.J., Goel M., Mushegian A., Foltz K.R. 2DE identification of proteins exhibiting turnover and phosphorylation dynamics during sea urchin egg activation. Dev. Biol. 2008, 313:630-647.
52. Sackton K.L., Buehner N.A., Wolfner M.F. Modulation of MAPK activities during egg activation in Drosophila. Fly (Austin) 2007, 1:222-227.
53. Sackton K.L., Lopez J.M., Berman C.L., Wolfner M.F. YA is needed for proper nuclear organization to transition between meiosis and mitosis in Drosophila. BMC Dev. Biol. 2009, 9:43.
54. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
55. Singson A., Hang J.S., Parry J.M. Genes required for the common miracle of fertilization in Caenorhabditis elegans. Int. J. Dev. Biol. 2008, 52:647-656.
56. 2+ release. Development 2010, 137:2659-2669.
57. Swann K., Yu Y. The dynamics of calcium oscillations that activate mammalian eggs. Int. J. Dev. Biol. 2008, 52:585-594.
58. Tadros W., Goldman A.L., Babak T., Menzies F., Vardy L., Orr-Weaver T., Hughes T.R., Westwood J.T., Smibert C.A., Lipshitz H.D. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev. Cell 2007, 12:143-155.
59. Takeo S., Hawley R.S., Aigaki T. Calcineurin and its regulation by Sra/RCAN is required for completion of meiosis in Drosophila. Dev. Biol. 2010, 344:957-967.
60. Takeo S., Tsuda M., Akahori S., Matsuo T., Aigaki T. The calcineurin regulator sra plays an essential role in female meiosis in Drosophila. Curr. Biol. 2006, 16:1435-1440.
61. Tatone C., Iorio R., Francione A., Gioia L., Colonna R. Biochemical and biological effects of KN-93, an inhibitor of calmodulin-dependent protein kinase II, on the initial events of mouse egg activation induced by ethanol. J. Reprod. Fertil. 1999, 115:151-157.
62. UniprotConsortium Ongoing and future developments at the Universal Protein Resource. Nucl. Acids Res. 2011, 39:D214-9.
63. Villaescusa J.C., Allard P., Carminati E., Kontogiannea M., Talarico D., Blasi F., Farookhi R., Verrotti A.C. Clast4, the murine homologue of human eIF4E-Transporter, is highly expressed in developing oocytes and post-translationally modified at meiotic maturation. Gene 2006, 367:101-109.
64. Went D.F., Krause G. Egg activation in Pimpla turionellae (Hym.). Naturwissenschaften 1974, 61:407-408.
65. Wu W.W., Wang G., Baek S.J., Shen R.F. Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J. Proteome Res. 2006, 5:651-658.
66. Yang Y., Thannhauser T.W., Li L., Zhang S. Development of an integrated approach for evaluation of 2-D gel image analysis: impact of multiple proteins in single spots on comparative proteomics in conventional 2-D gel/MALDI workflow. Electrophoresis 2007, 28:2080-2094.
67. Yu J., Garfinkel A.B., Wolfner M.F. Interaction of the essential Drosophila nuclear protein YA with P0/AP3 in the cytoplasm and in vitro: implications for developmental regulation of YA's subcellular location. Dev. Biol. 2002, 244:429-441.
68. Yu J., Liu J., Song K., Turner S.G., Wolfner M.F. Nuclear entry of the Drosophila melanogaster nuclear lamina protein YA correlates with developmentally regulated changes in its phosphorylation state. Dev. Biol. 1999, 210:124-134.
69. Zalokar M. Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev. Biol. 1976, 49:425-437.
70. Zhai B., Villen J., Beausoleil S.A., Mintseris J., Gygi S.P. Phosphoproteome analysis of Drosophila melanogaster embryos. J. Proteome Res. 2008, 7:1675-1682.
71. Zhang Q.H., Wei L., Tong J.S., Qi S.T., Li S., Ou X.H., Ouyang Y.C., Hou Y., An L.G., Schatten H., Sun Q.Y. Localization and function of mSpindly during mouse oocyte meiotic maturation. Cell Cycle 2010, 9.