Proteomics of Tribolium castaneum seminal fluid proteins: Identification of an angiotensin-converting enzyme as a key player in regulation of reproduction

Journal of Proteomics

Volumn 78, Issue , 2013, Pages 83-93

  Xu, Jingjing ^a   Baulding, James ^a   Palli, Subba Reddy ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Angiotensin converting enzyme; Male reproduction; Red flour beetle; Seminal fluid proteins; Tribolium castaneum

Indexed keywords

APROTININ; CYSTEINE RICH PROTEIN 61; DIPEPTIDYL CARBOXYPEPTIDASE; HEAT SHOCK COGNATE PROTEIN 70; ODORANT BINDING PROTEIN; PROTEIN DERIVATIVE; RNA; SEMINAL PLASMA PROTEIN; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; WD 40 PROTEIN;

ACCESSORY SEX GLAND; ARTICLE; CONTROLLED STUDY; EGG PRODUCTION; FEMALE; GENE EXPRESSION; GENETIC CODE; MALE; MATING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REPRODUCTION; RNA INTERFERENCE; SEMINAL PLASMA; SEMINAL VESICLE; TRIBOLIUM CASTANEUM;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; INSECT PROTEINS; MALE; PEPTIDYL-DIPEPTIDASE A; REPRODUCTION; SEMEN; SEMINAL PLASMA PROTEINS; TRIBOLIUM;

TRIBOLIUM CASTANEUM;

EID: 84871778239     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.11.011     Document Type: Article

References (43)

1. Mann T., Lutwak-Mann C. Passage of chemicals into human and animal semen: mechanisms and significance. Crit Rev Toxicol 1982, 11:1-14.
2. Koene J.M., Sloot W., Montagne-Wajer K., Cummins S.F., Degnan B.M., Smith J.S., et al. Male accessory gland protein reduces egg laying in a simultaneous hermaphrodite. PLoS One 2010, 5:e10117.
3. Lung O., Wolfner M.F. Identification and characterization of the major Drosophila melanogaster mating plug protein. Insect Biochem Mol Biol 2001, 31:543-551.
4. Avila F.W., Wolfner M.F. Acp36DE is required for uterine conformational changes in mated Drosophila females. Proc Natl Acad Sci U S A 2009, 106:15796-15800.
5. Ravi Ram K., Wolfner M.F. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol 2007, 47:427-445.
6. Wigby S., Chapman T. Sex peptide causes mating costs in female Drosophila melanogaster. Curr Biol 2005, 15:316-321.
7. McGraw L.A., Clark A.G., Wolfner M.F. Post-mating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 2008, 179:1395-1408.
8. Findlay G.D., MacCoss M.J., Swanson W.J. Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome Res 2009, 19:886-896.
9. Mueller J.L., Ravi Ram K., McGraw L.A., Bloch Qazi M.C., Siggia E.D., Clark A.G., et al. Cross-species comparison of Drosophila male accessory gland protein genes. Genetics 2005, 171:131-143.
10. Findlay G.D., Yi X., Maccoss M.J., Swanson W.J. Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol 2008, 6:e178.
11. Wigby S., Sirot L.K., Linklater J.R., Buehner N., Calboli F.C., Bretman A., et al. Seminal fluid protein allocation and male reproductive success. Curr Biol 2009, 19:751-757.
12. Parthasarathy R., Tan A., Sun Z., Chen Z., Rankin M., Palli S.R. Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mech Dev 2009, 126:563-579.
13. Avila F.W., Sirot L.K., LaFlamme B.A., Rubinstein C.D., Wolfner M.F. Insect seminal fluid proteins: identification and function. Annu Rev Entomol 2011, 56:21-40.
14. Swanson W.J., Clark A.G., Waldrip-Dail H.M., Wolfner M.F., Aquadro C.F. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci U S A 2001, 98:7375-7379.
15. Dottorini T., Nicolaides L., Ranson H., Rogers D.W., Crisanti A., Catteruccia F. A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior. Proc Natl Acad Sci U S A 2007, 104:16215-16220.
16. Sirot L.K., Poulson R.L., McKenna M.C., Girnary H., Wolfner M.F., Harrington L.C. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol 2008, 38:176-189.
17. Coleman S., Drahn B., Petersen G., Stolorov J., Kraus K. A Drosophila male accessory gland protein that is a member of the serpin superfamily of proteinase inhibitors is transferred to females during mating. Insect Biochem Mol Biol 1995, 25:203-207.
18. Irving J.A., Pike R.N., Lesk A.M., Whisstock J.C. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res 2000, 10:1845-1864.
19. Irving J.A., Steenbakkers P.J., Lesk A.M., den Camp HJ Op, Pike R.N., Whisstock J.C. Serpins in prokaryotes. Mol Biol Evol 2002, 19:1881-1890.
20. Silverman G.A., Bird P.I., Carrell R.W., Church F.C., Coughlin P.B., Gettins P.G., et al. The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J Biol Chem 2001, 276:33293-33296.
21. Mueller J.L., Ripoll D.R., Aquadro C.F., Wolfner M.F. Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid. Proc Natl Acad Sci U S A 2004, 101:13542-13547.
22. Hagaman J.R., Moyer J.S., Bachman E.S., Sibony M., Magyar P.L., Welch J.E., et al. Angiotensin-converting enzyme and male fertility. Proc Natl Acad Sci U S A 1998, 95:2552-2557.
23. Rylett C.M., Walker M.J., Howell G.J., Shirras A.D., Isaac R.E. Male accessory glands of Drosophila melanogaster make a secreted angiotensin I-converting enzyme (ANCE), suggesting a role for the peptide-processing enzyme in seminal fluid. J Exp Biol 2007, 210:3601-3606.
24. Fuches S., Frenzel K., Hubert C., Lyng R., Muller L., Michaud A., et al. Male fertility is dependent on dipeptidase activity of testis ACE. Nal. Med. 2005, 11:1140-1142.
25. Tian L., Ji B.Z., Liu S.W., Jin F., Gao J., Li S. Juvenile hormone III produced in male accessory glands of the longhorned beetle, Apriona germari, is transferred to female ovaries during copulation. Arch Insect Biochem Physiol 2010, 75:57-67.
26. Wilson T.G., DeMoor S., Lei J. Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the Methoprene-tolerant(27) mutant phenotype. Insect Biochem Mol Biol 2003, 33:1167-1175.
27. Borges J.C., Ramos C.H. Protein folding assisted by chaperones. Protein Pept Lett 2005, 12:257-261.
28. Walker M.J., Rylett C.M., Keen J.N., Audsley N., Sajid M., Shirras A.D., et al. Proteomic identification of Drosophila melanogaster male accessory gland proteins, including a pro-cathepsin and a soluble gamma-glutamyl transpeptidase. Proteome Sci 2006, 4:9.
29. Xu P., Atkinson R., Jones D.N., Smith D.P. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 2005, 45:193-200.
30. Ha T.S., Smith D.P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 2006, 26:8727-8733.
31. Matsuo T., Sugaya S., Yasukawa J., Aigaki T., Fuyama Y. Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 2007, 5:e118.
32. Fujii S., Amrein H. Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. EMBO J 2002, 21:5353-5363.
33. Ayroles J.F., Carbone M.A., Stone E.A., Jordan K.W., Lyman R.F., Magwire M.M., et al. Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 2009, 41:299-307.
34. Arya G.H., Weber A.L., Wang P., Magwire M.M., Negron Y.L., Mackay T.F., et al. Natural variation, functional pleiotropy and transcriptional contexts of odorant binding protein genes in Drosophila melanogaster. Genetics 2010, 186:1475-1485.
35. Wang Y.L., Kuo J.H., Lee S.C., Liu J.S., Hsieh Y.C., Shih Y.T., et al. Cobra CRISP functions as an inflammatory modulator via a novel Zn2+- and heparan sulfate-dependent transcriptional regulation of endothelial cell adhesion molecules. J Biol Chem 2010, 285:37872-37883.
36. Koppers A.J., Reddy T., O'Bryan M.K. The role of cysteine-rich secretory proteins in male fertility. Asian J Androl 2011, 13:111-117.
37. Jalkanen J., Huhtaniemi I., Poutanen M. Mouse cysteine-rich secretory protein 4 (CRISP4): a member of the Crisp family exclusively expressed in the epididymis in an androgen-dependent manner. Biol Reprod 2005, 72:1268-1274.
38. Foster J.A., Gerton G.L. Autoantigen 1 of the guinea pig sperm acrosome is the homologue of mouse Tpx-1 and human TPX1 and is a member of the cysteine-rich secretory protein (CRISP) family. Molec Reprod Dev 1996, 44:221-229.
39. Schambony A., Gentzel M., Wolfes H., Raida M., Neumann U., Topfer-Petersen E. Equine CRISP-3: primary structure and expression in the male genital tract. Biochim Biophys Acta 1998, 1387:206-216.
40. Baer B., Heazlewood J.L., Taylor N.L., Eubel H., Millar A.H. The seminal fluid proteome of the honeybee Apis mellifera. Proteomics 2009, 9:2085-2097.
41. Ignotz G.G., Cho M.Y., Suarez S.S. Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir. Biol Reprod 2007, 77:906-913.
42. Wagstaff B.J., Begun D.J. Molecular population genetics of accessory gland protein genes and testis-expressed genes in Drosophila mojavensis and D. arizonae. Genetics 2005, 171:1083-1101.
43. South A., Sirot L.K., Lewis S.M. Identification of predicted seminal fluid proteins in Tribolium castaneum. Insect Mol Biol 2011, 20:447-456.