Fates and targets of male accessory gland proteins in mated female Drosophila melanogaster

Insect Biochemistry and Molecular Biology

Volumn 35, Issue 9, 2005, Pages 1059-1071

  Ravi Ram, K ^a   Ji, S ^a   Wolfner, M F ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Acp; Mating plug; Ovary; Reproduction; Seminal receptacle; Sperm storage; Spermathecae

Indexed keywords

DROSOPHILA PROTEIN;

ANIMAL; ARTICLE; COPULATION; DROSOPHILA MELANOGASTER; FEMALE; MALE; METABOLISM; PHYSIOLOGY; REPRODUCTION;

ANIMALS; COPULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; REPRODUCTION;

DROSOPHILA MELANOGASTER;

EID: 20544443241     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2005.05.001     Document Type: Article

References (68)

1. T. Aigaki, I. Fleischmann, P.S. Chen, and E. Kubli Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster Neuron 7 1991 1 20
2. M.J. Bertram, D.M. Neubaum, and M.F. Wolfner Localization of the Drosophila male accessory gland protein Acp36DE in the mated female suggests a role in sperm storage Insect Biochem. Mol. Biol. 26 1996 971 980
3. M.C. Bloch Qazi, and M.F. Wolfner An early role for the Drosophila melanogaster male seminal fluid protein Acp36DE in female sperm storage J. Exp. Biol. 206 2003 3521 3528
4. M.C. Bloch Qazi, Y. Heifetz, and M.F. Wolfner The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster Dev. Biol. 256 2003 195 211
5. R.E. Boswell, and A.P. Mahowald Tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster Cell 43 1985 97 104
6. T. Chapman, and S.J. Davies Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies Peptides 25 2004 1477 1490
7. T. Chapman, L.F. Liddle, J.M. Kalb, M.F. Wolfner, and L. Partridge Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products Nature 373 1995 241 244
8. T. Chapman, D.M. Neubaum, M.F. Wolfner, and L. Patridge The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster Proc. R. Soc. London B 267 2000 1097 1105
9. T. Chapman, J. Bangham, G. Vinti, B. Seifried, O. Lung, M.F. Wolfner, H. Smith, and L. Patridge The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference Proc. Natl. Acad. Sci. USA 100 2003 9923 9928
10. P.S. Chen The functional morphology and biochemistry of insect male accessory glands and their secretions Ann. Rev. Entomol. 29 1984 233 255
11. P.S. Chen, E. Stumm-Zollinger, T. Aigaki, J. Balmer, M. Bienz, and P. Bohlen A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster Cell 54 1988 291 298
12. A.G. Clark, M. Aguade, T. Prout, L.G. Harshman, and C.H. Langley Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster Genetics 139 1995 189 201
13. D.J. Cohen, D.A. Ellerman, D. Busso, M.M. Morgenfeld, A.D. Piazza, M. Hayashi, E.T. Young, M. Kasahara, and P.S. Cuasnicu Evidence that human epididymal protein ARP plays a role in gamete fusion through complementary sites on the surface of the human egg Biol. Reprod. 65 2001 1000 1005
14. S. Coleman, B. Drahn, G. Petersen, J. Stolorov, and K. Kraus A Drosophila male accessory gland that is a member of the serpin super family of proteinase-inhibitors is transferred to females during mating Insect Biochem. Mol. Biol. 25 1995 203 207
15. A.J. DiBenedetto, D.M. Lakich, W.D. Kruger, J.M. Belote, B.S. Baker, and M.F. Wolfner Sequences expressed sex-specifically in Drosophila melanogaster adults Dev. Biol. 119 1987 242 251
16. M.A. Elaroussi, and H.F. DeLuca A new member to the astacin family of metalloendopeptidases: a novel 1,25-dihydroxyvitamin D-3-stimulated mRNA from chorioallantoic membrane of quail Biochem. Biophys. Acta 1217 1994 1 8
17. A.C. Fiumera, B.L. Dumont, and A.G. Clark Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins Genetics 169 2005 243 257
18. T. Friedel, and C. Gillott Contribution of male-produced proteins to vitellogenesis in Melanoplus sanguinipes J. Insect Physiol. 23 1977 145 151
19. G. Geier, and R. Zwilling Cloning and characterization of a cDNA coding for Astacus embryonic astacin, a member of the astacin family of metalloproteases from the crayfish Astacus astacus Eur. J. Biochem. 253 1998 796 803
20. D.G. Gilbert Ejaculate esterase 6 and initial sperm use by female Drosophila melanogaster J. Insect Physiol. 27 1981 641 650
21. C. Gillott Male accessory gland secretions: modulators of female reproductive physiology and behavior Ann. Rev. Entomol. 48 2003 163 184
22. K. Guan, and J.E. Dixon Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione-s-transferase Anal. Biochem. 192 1991 262 267
23. L. Harshman, and T. Prout Sperm displacement without sperm transfer Evolution 48 1994 758 766
24. Y. Heifetz, O. Lung, E.A. Frongillo Jr., and M.F. Wolfner The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary Curr. Biol. 10 2000 99 102
25. Y. Heifetz, L.N. Vandenberg, H.I. Cohn, and M.F. Wolfner Two cleavage products of the Drosophila accessory gland protein ovulin can independently induce ovulation Proc. Natl. Acad. Sci. USA 102 2005 743 748
26. L.A. Herndon, and M.F. Wolfner A Drosophila seminal fluid protein, Acp26Aa, stimulates egg-laying in females for 1 day after mating Proc. Natl. Acad. Sci. USA 92 1995 10114 10118
27. A.K. Holloway, and D.J. Begun Molecular evolution and population genetics of duplicated accessory gland protein genes in Drosophila Mol. Biol. Evol. 21 2004 1625 1628
28. J. Huignard Transfer and fate of male secretions deposited in the spermatophore of females of Acanthoscelides obtectus say (Coleoptera: Bruchidae) J. Insect Physiol. 29 1983 55 63
29. K. Inohaya, S. Yasumasu, K. Araki, K. Naruse, K. Yamazaki, I. Yasumasu, I. Iuchi, and K. Yamagami Species-dependent migration of fish hatching gland cells that express astacin-like proteases in common Dev. Growth Differ. 39 1997 191 197
30. J.M. Kalb, A.J. DiBenedetto, and M.F. Wolfner Probing the function of Drosophila melanogaster accessory glands by directed cell ablation Proc. Natl. Acad. Sci. USA 90 1993 8093 8097
31. C. Katagiri, R. Maeda, C. Yamashika, K. Mita, T.D. Sargent, and S. Yasumasu Molecular cloning of Xenopus hatching enzyme and its specific expression in hatching gland cells Int. J. Dev. Biol. 41 1997 19 25
32. B.P. Kaufman, and M. Demerec Utilization of sperm by the female Drosophila melanogaster Am. Nat. 76 1942 445 469
33. S. Kumar, K. Tamura, I.B. Jakobsen, and M. Nei MEGA2: molecular evolutionary genetics analysis software Bioinformatics 17 2001 1244 1245
34. M. Lay, W. Loher, and R. Hartmann Pathways and destinations of some male gland secretions in female Locusta migrtoria migratorioides (R&F) after insemination Arch. Insect Biochem. Physiol. 55 2004 1 25
35. G.J. Lefevre, and U.B. Jonsson Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster Genetics 47 1962 1719 1736
36. R.A. Leopold, A.C. Terranova, B.J. Thorson, and M.E. Degrugillier The biosynthesis of the male house-fly accessory secretion and its fate in the mated female J. Insect Physiol. 17 1971 987 1003
37. H. Liu, and E. Kubli Sex peptide is the molecular basis of the sperm effect in Drosophila melanogaster Proc. Natl. Acad. Sci. USA 100 2003 9929 9933
38. O. Lung, and M.F. Wolfner Drosophila seminal fluid proteins enter the circulatory system of the mated female fly by crossing the posterior vaginal wall Insect Biochem. Mol. Biol. 29 1999 1043 1052
39. O. Lung, and M.F. Wolfner Identification and characterization of the major Drosophila melanogaster mating plug protein Insect Biochem. Mol. Biol. 31 2001 543 551
40. O. Lung, U. Tram, C.M. Finnerty, M. Eipper-Mains, J.M. Kalb, and M.F. Wolfner The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression Genetics 160 2002 211 224
41. A.P. Mahowald, T.J. Goralski, and J.H. Caulton In vitro activation of Drosophila eggs Dev. Biol. 98 1983 437 445
42. A. Manning The control of sexual receptivity in female Drosophila Anim. Behav. 15 1967 239 250
43. S.A. Monsma, and M.F. Wolfner Structure and expression of a Drosophila male accessory gland whose product resembles a peptide pheromone precursor Genes Dev. 2 1988 1063 1073
44. S.A. Monsma, H.A. Harada, and M.F. Wolfner Synthesis of two male accessory gland proteins and their fate after transfer to the female during mating Dev. Biol. 142 1990 465 475
45. J.L. Mueller, D.R. Ripoll, C.F. Aquadro, and M.F. Wolfner Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid Proc. Natl. Acad. Sci. USA 101 2004 13542 13547
46. Mueller, J.L., Ravi Ram, K., McGraw, L.A., Bloch Qazi, M.C., Siggia, E.D., Clark, A.G., Aquadro, C.F., Wolfner, M.F., 2005. Cross-species comparison of Drosophila male accessory gland protein genes, in press.
47. V. Murer, J.F. Spetz, U. Hengst, L.M. Altrogge, A. de Agostini, and D. Monard Male fertility defects in mice lacking the serine protease inhibitor protease nexin-1 Proc. Natl. Acad. Sci. USA 98 2001 3029 3033
48. D.M. Neubaum, and M.F. Wolfner Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently Genetics 153 1999 845 857
49. J.H. Olson, X. Xiang, T. Ziegert, A. Kittelson, A. Rawls, A.L. Bieber, and D.E. Chandler Allurin; A 21-kDa sperm chemoattractant from Xenopus egg jelly, is related to mammalian sperm-binding proteins Proc. Natl. Acad. Sci. USA 98 2001 11205 11210
50. M. Ottiger, M. Soller, R.F. Stocker, and E. Kubli Binding sites of Drosophila melanogaster sex peptide pheromones J. Neurobiol. 44 2000 57 71
51. J.T. Patterson Studies in the genetics of Drosophila. III. The Drosophilidae of the southwest Univ. Texas Publs. 4313 1943 7 216
52. J. Peng, S. Chen, S. Büsser, H. Liu, T. Honegger, and E. Kubli Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila Curr. Biol. 15 2005 207 213
53. T. Prout, and A.G. Clark Seminal fluid causes temporarily reduced egg hatch in previously mated females Proc. R. Soc. London B 267 2000 201 203
54. K. Ravi Ram, and S.R. Ramesh Male accessory gland proteins in Drosophila: a multifaceted field Indian J. Exp. Biol. 41 2003 1372 1383
55. A. Romero, M.J. Romao, P.F. Varela, I. Kolln, J.M. Dias, A.L. Carvalho, L. Sanz, E. Topfer-Petersen, and J.J. Calvete The crystal structures of two spermadhesins reveal the CUB domain fold Nat. Struct. Biol. 4 1997 783 788
56. M. Rosetto, A.G. Manetti, P.C. Giordano, L. Marri, R. Amons, C.T. Baldari, D. Marchini, and R. Dallai Molecular characterization of ceratotoxin C, a novel antibacterial female-specific peptide of the ceratotoxin family from the medfly Ceratitis capitata Eur. J. Biochem. 241 1996 330 337
57. P. Saudan, K. Hauck, M. Soller, Y. Choffat, M. Ottiger, and M. Sporri Ductus ejaculatorius peptide 99B (DUP99B), a novel Drosophila melanogaster sex-peptide pheromone Eur. J. Biochem. 269 2002 989 997
58. U. Schäfer Genes for male specific transcripts in Drosophila melanogaster Mol. Gen. Genet. 202 1986 219 225
59. E. Simmerl, M. Schäfer, and U. Schäfer Structure and regulation of a gene cluster for male accessory gland transcripts in Drosophila melanogaster Insect Biochem. Mol. Biol. 25 1995 127 137
60. M. Soller, M. Bownes, and E. Kubli Control of oocyte maturation in sexually mature Drosophila females Dev. Biol. 208 1999 337 351
61. W.J. Swanson, A.G. Clark, H.M. Waldrip-Dail, M.F. Wolfner, and C.F. Aquadro Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila Proc. Natl. Acad. Sci. USA 98 2001 2509 2514
62. U. Tram, and M.F. Wolfner Male seminal fluid proteins are essential for sperm storage in Drosohila melanogaster Genetics 153 1999 837 844
63. S. Wigby, and T. Chapman Sex peptide causes mating costs in female Drosophila melanogaster Curr. Biol. 15 2005 316 321
64. M.F. Wolfner The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila Heredity 88 2002 85 93
65. M.F. Wolfner, H.A. Harada, M.J. Bertram, T.J. Stelick, K.W. Kraus, and J.M. Kalb New genes for male accessory gland proteins in Drosophila melanogaster Insect Biochem. Mol. Biol. 27 1997 825 834
66. M.F. Wolfner, S. Applebaum, and Y. Heifetz Insect gonadal glands and their gene products L. Gilbert K. Iatrou S. Gill Comprehensive Insect Physiology, Biochemistry, Pharmacology and Molecular Biology 2004 Elsevier Amsterdam 179 212
67. L. Xue, and M. Noll Drosophila female sexual behavior induced by sterile males showing copulation complementation Proc. Natl. Acad. Sci. USA 97 2000 3272 3275
68. L. Xue, X. Li, and M. Noll Multiple protein functions of paired in Drosophila development and their conservation in the Gooseberry and Pax3 homologs Development 128 2001 395 405