Genetics, Vol. 160, 211-224, January 2002, Copyright © 2002

The Drosophila melanogaster Seminal Fluid Protein Acp62F Is a Protease Inhibitor That Is Toxic Upon Ectopic Expression

Oliver Lunga, Uyen Trama, Casey M. Finnertya, Marcie A. Eipper-Mainsa, John M. Kalba, and Mariana F. Wolfnera
a Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853

Corresponding author: Mariana F. Wolfner, 423 Biotechnology Bldg., Cornell University, Ithaca, NY 14853., mfw5{at}cornell.edu (E-mail)

Communicating editor: C.-I WU

Drosophila melanogaster seminal fluid proteins stimulate sperm storage and egg laying in the mated female but also cause a reduction in her life span. We report here that of eight Drosophila seminal fluid proteins (Acps) and one non-Acp tested, only Acp62F is toxic when ectopically expressed. Toxicity to preadult male or female Drosophila occurs upon one exposure, whereas multiple exposures are needed for toxicity to adult female flies. Of the Acp62F received by females during mating, ~10% enters the circulatory system while ~90% remains in the reproductive tract. We show that in the reproductive tract, Acp62F localizes to the lumen of the uterus and the female's sperm storage organs. Analysis of Acp62F's sequence, and biochemical assays, reveals that it encodes a trypsin inhibitor with sequence and structural similarities to extracellular serine protease inhibitors from the nematode Ascaris. In light of previous results demonstrating entry of Acp62F into the mated female's hemolymph, we propose that Acp62F is a candidate for a molecule to contribute to the Acp-dependent decrease in female life span. We propose that Acp62F's protease inhibitor activity exerts positive protective functions in the mated female's reproductive tract but that entry of a small amount of this protein into the female's hemolymph could contribute to the cost of mating.





This article has been cited by other articles:


Home page
J HeredHome page
M. F. Wolfner
Battle and Ballet: Molecular Interactions between the Sexes in Drosophila
J. Hered., July 1, 2009; 100(4): 399 - 410.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. Wong, S. N. Albright, J. D. Giebel, K. R. Ram, S. Ji, A. C. Fiumera, and M. F. Wolfner
A Role for Acp29AB, a Predicted Seminal Fluid Lectin, in Female Sperm Storage in Drosophila melanogaster
Genetics, October 1, 2008; 180(2): 921 - 931.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
F. C. Almeida and R. DeSalle
Evidence of Adaptive Evolution of Accessory Gland Proteins in Closely Related Species of the Drosophila repleta Group
Mol. Biol. Evol., September 1, 2008; 25(9): 2043 - 2053.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. A. McGraw, A. G. Clark, and M. F. Wolfner
Post-mating Gene Expression Profiles of Female Drosophila melanogaster in Response to Time and to Four Male Accessory Gland Proteins
Genetics, July 1, 2008; 179(3): 1395 - 1408.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. L. Mueller, J. R. Linklater, K. Ravi Ram, T. Chapman, and M. F. Wolfner
Targeted Gene Deletion and Phenotypic Analysis of the Drosophila melanogaster Seminal Fluid Protease Inhibitor Acp62F
Genetics, March 1, 2008; 178(3): 1605 - 1614.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. Wong, M. C. Turchin, M. F. Wolfner, and C. F. Aquadro
Evidence for Positive Selection on Drosophila melanogaster Seminal Fluid Protease Homologs
Mol. Biol. Evol., March 1, 2008; 25(3): 497 - 506.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
A. K. Allen and A. C. Spradling
The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function
Development, January 15, 2008; 135(2): 311 - 321.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
S. A. Ramm, P. L. Oliver, C. P. Ponting, P. Stockley, and R. D. Emes
Sexual Selection and the Adaptive Evolution of Mammalian Ejaculate Proteins
Mol. Biol. Evol., January 1, 2008; 25(1): 207 - 219.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
T. Dottorini, L. Nicolaides, H. Ranson, D. W. Rogers, A. Crisanti, and F. Catteruccia
A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior
PNAS, October 9, 2007; 104(41): 16215 - 16220.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
B. J. Wagstaff and D. J. Begun
Adaptive Evolution of Recently Duplicated Accessory Gland Protein Genes in Desert Drosophila
Genetics, October 1, 2007; 177(2): 1023 - 1030.
[Abstract] [Full Text] [PDF]


Home page
Integr. Comp. Biol.Home page
K. Ravi Ram and M. F. Wolfner
Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction
Integr. Comp. Biol., September 1, 2007; 47(3): 427 - 445.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
M. K. N. Lawniczak and D. J. Begun
Molecular population genetics of female-expressed mating-induced serine proteases in Drosophila melanogaster
Mol. Biol. Evol., September 1, 2007; 24(9): 1944 - 1951.
[Abstract] [Full Text] [PDF]


Home page
Proc R Soc BHome page
K. M Fedorka, J. E Linder, W. Winterhalter, and D. Promislow
Post-mating disparity between potential and realized immune response in Drosophila melanogaster
Proc R Soc B, May 7, 2007; 274(1614): 1211 - 1217.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. L. Mueller, J. L. Page, and M. F. Wolfner
An Ectopic Expression Screen Reveals the Protective and Toxic Effects of Drosophila Seminal Fluid Proteins
Genetics, February 1, 2007; 175(2): 777 - 783.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
K. Ravi Ram, L. K. Sirot, and M. F. Wolfner
Predicted seminal astacin-like protease is required for processing of reproductive proteins in Drosophila melanogaster
PNAS, December 5, 2006; 103(49): 18674 - 18679.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
T. M. Panhuis and W. J. Swanson
Molecular Evolution and Population Genetic Analysis of Candidate Female Reproductive Genes in Drosophila
Genetics, August 1, 2006; 173(4): 2039 - 2047.
[Abstract] [Full Text] [PDF]


Home page
Phil Trans R Soc BHome page
T. M Panhuis, N. L Clark, and W. J Swanson
Rapid evolution of reproductive proteins in abalone and Drosophila
Phil Trans R Soc B, February 28, 2006; 361(1466): 261 - 268.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
L. Ford, D. B. Guiliano, Y. Oksov, A. K. Debnath, J. Liu, S. A. Williams, M. L. Blaxter, and S. Lustigman
Characterization of a Novel Filarial Serine Protease Inhibitor, Ov-SPI-1, from Onchocerca volvulus, with Potential Multifunctional Roles during Development of the Parasite
J. Biol. Chem., December 9, 2005; 280(49): 40845 - 40856.
[Abstract] [Full Text] [PDF]


Home page
Proc R Soc BHome page
A. A Maklakov, N. Kremer, and G. Arnqvist
Adaptive male effects on female ageing in seed beetles
Proc R Soc B, December 7, 2005; 272(1580): 2485 - 2489.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. L. Mueller, K. R. Ram, L. A. McGraw, M. C. Bloch Qazi, E. D. Siggia, A. G. Clark, C. F. Aquadro, and M. F. Wolfner
Cross-Species Comparison of Drosophila Male Accessory Gland Protein Genes
Genetics, September 1, 2005; 171(1): 131 - 143.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
S. Jagadeeshan and R. S. Singh
Rapidly Evolving Genes of Drosophila: Differing Levels of Selective Pressure in Testis, Ovary, and Head Tissues Between Sibling Species
Mol. Biol. Evol., September 1, 2005; 22(9): 1793 - 1801.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
B. J. Wagstaff and D. J. Begun
Comparative Genomics of Accessory Gland Protein Genes in Drosophila melanogaster and D. pseudoobscura
Mol. Biol. Evol., April 1, 2005; 22(4): 818 - 832.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
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
PNAS, January 18, 2005; 102(3): 743 - 748.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. C. Fiumera, B. L. Dumont, and A. G. Clark
Sperm Competitive Ability in Drosophila melanogaster Associated With Variation in Male Reproductive Proteins
Genetics, January 1, 2005; 169(1): 243 - 257.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
W. J. Swanson, A. Wong, M. F. Wolfner, and C. F. Aquadro
Evolutionary Expressed Sequence Tag Analysis of Drosophila Female Reproductive Tracts Identifies Genes Subjected to Positive Selection
Genetics, November 1, 2004; 168(3): 1457 - 1465.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
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
PNAS, September 14, 2004; 101(37): 13542 - 13547.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
M. N. Arbeitman, A. A. Fleming, M. L. Siegal, B. H. Null, and B. S. Baker
A genomic analysis of Drosophila somatic sexual differentiation and its regulation
Development, May 1, 2004; 131(9): 2007 - 2021.
[Abstract] [Full Text] [PDF]


Home page
Behav EcolHome page
E. H. Morrow, G. Arnqvist, and S. Pitnick
Adaptation versus pleiotropy: why do males harm their mates?
Behav. Ecol., November 1, 2003; 14(6): 802 - 806.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
W. J. Swanson
Sex peptide and the sperm effect in Drosophila melanogaster
PNAS, August 19, 2003; 100(17): 9643 - 9644.
[Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
T. Chapman, J. Bangham, G. Vinti, B. Seifried, O. Lung, M. F. Wolfner, H. K. Smith, and L. Partridge
From the Cover: The sex peptide of Drosophila melanogaster: Female post-mating responses analyzed by using RNA interference
PNAS, August 19, 2003; 100(17): 9923 - 9928.
[Abstract] [Full Text] [PDF]