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

Abstract

SUMMARY Angiotensin I-converting enzyme (ACE) expressed on the surface of endothelial cells is responsible for the last step in the synthesis of circulating angiotensin II and the inactivation of bradykinin. Mammalian ACE is also expressed in the prostate with other components of the renin–angiotensin system, and in developing spermatids, where the peptidase activity is known to be critical for normal sperm function. The importance of an ACE gene to male fertility has also been demonstrated in Drosophila melanogaster, where Ance is expressed in spermatids, and hypomorphic alleles of Ance cause a defect in spermiogenesis. Here we show that ANCE, which shares many enzymatic properties with mammalian ACE, is also a product of the male accessory gland of D. melanogaster. It is expressed in the secondary cells and is associated with the electron dense granule within the large vesicles of these cells. ACE proteolytic activity is lost from the accessory glands during mating,consistent with transfer to the mated female in the seminal fluid. The accessory gland ACE-like activity might have an evolutionarily conserved function processing biologically active peptides with a role in male fertility.

Bone morphogenetic protein- and mating-dependent secretory cell growth and migration in the Drosophila accessory gland

“…Our data highlight some surprising parallels between the accessory gland and the prostate, in addition to those previously reported (2). Like the prostate, the structure of the accessory gland epithelium changes significantly with age.…”

“…In the fruit fly, Drosophila melanogaster, the paired accessory glands promote normal sperm storage and utilization, and influence female postmating behaviors, increasing egg production and reducing subsequent receptivity to males (1). The glands secrete proteases, antiproteases, other glycoproteins, and cellular material into seminal fluid via mechanisms that have not been fully characterized (2)(3)(4).…”

“…Although most of the epithelium consists of so-called main cells, which secrete key accessory gland proteins like sex peptide (6), it also includes about 40 distally located, distinctively rounded secondary cells that contain large secretory vacuoles (2,11).…”

Multinucleated smooth muscles and mononucleated as well as multinucleated striated muscles develop during establishment of the male reproductive organs of Drosophila melanogaster

“…The paragonia are essential for the reproduction of D. melanogaster (Rylett et al, 2007), and their structure and function have been well investigated also in other insect species (Freitas et al, 2007;Radhakrishnan et al, 2009). The epithelium of the paragonia secretes a variety of peptides and protein hormones into the seminal fluid.…”

Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: Potential tools for control of female feeding and reproduction

“…ACEs are found in the testes and male reproductive glands (as well as other tissues) of insects and mammals (Isaac et al, 1999;Leung and Sernia, 2003;Rylett et al, 2007) and have dramatic effects on the reproductive biology of both groups of organisms (Hagaman et al, 1998;Isaac et al, 1999;Ekbote et al, 2003;Kondoh et al, 2005). Of particular interest, the effect of male-derived ACEs on female fecundity has been investigated in the mosquito, Anopheles stephensi.…”