Abstract
Glycoprotein hormone receptors mediate a diverse range of physiological functions in vertebrate and invertebrate organisms. The heterodimeric glycoprotein hormone GPA2/GPB5 and its receptor LGR1, constitute a recently discovered invertebrate neuroendocrine signaling system that remains to be functionally characterized. We previously reported that LGR1 is expressed in the testes of adult Aedes aegypti mosquitoes, where its immunoreactivity is particularly regionalized. Here, we show that LGR1 immunoreactivity is associated with the centriole adjunct of spermatids and is observed transiently during spermatogenesis in mosquitoes, where it may act to mediate the regulation of flagellar development. RNA interference to downregulate LGR1 expression was accomplished by feeding mosquito larvae with bacteria that produced LGR1-specific dsRNA, which led to defects in spermatozoa, characterized with shortened flagella. LGR1 knockdown mosquitoes also retained ∼60% less spermatozoa in reproductive organs and demonstrated reduced fertility compared to controls. To date, the endocrine regulation of spermatogenesis in mosquitoes remains an understudied research area. The distribution of LGR1 and detrimental effects of its knockdown on spermatogenesis in A. aegypti indicates that this heterodimeric glycoprotein hormone signaling system contributes significantly to the regulation of male reproductive biology in this important disease-vector.
Highlights
The mosquito Aedes aegypti serves as a vector for a variety of pathogens causing diseases including Zika, yellow fever, chikungunya and dengue virus, the latter of which is the most widespread arbovirus disease in humans infecting nearly 400 million people annually (Bhatt et al, 2013)
In early spermatids, which are characterized with condensed, round-shaped nuclei, leucine-rich repeat-containing G protein-coupled receptor 1 (LGR1) immunoreactivity concentrates to single spots that are polarized to either end of the nuclei and, as nuclear elongation proceeds in late spermatids, receptor immunoreactivity is prominently detected as an elongated structure distinct from but remaining closely associated to the nuclei (Figures 1B,C)
Our data indicates that LGR1 functions to regulate flagellar development during spermatogenesis since LGR1 immunoreactivity was regionalized to the centriole adjunct of spermatids, a region that houses proteins important for producing the axoneme
Summary
The mosquito Aedes aegypti serves as a vector for a variety of pathogens causing diseases including Zika, yellow fever, chikungunya and dengue virus, the latter of which is the most widespread arbovirus disease in humans infecting nearly 400 million people annually (Bhatt et al, 2013). Promising control strategies that aim to curb viral transmission by mosquitoes target their reproductive physiology. A second promising control strategy to reduce disease transmission by mosquitoes involves introducing the bacterium Wolbachia to mosquito populations, which renders the sperm of infected males incapable of fertilization (LePage and Bordenstein, 2013). From the apex to the base of the testis, cysts progressively increase in size and maturity so that smaller compartments with undifferentiated spermatogonia are found on distal ends, whereas larger cysts containing mature spermatozoa are located at the base (Wandall, 1986; Clements, 2000). Upon copulation with a female, the seminal vesicle is emptied, and a new wave of spermatogenesis occurs to ensure that a continuous supply of sperm is made available for a subsequent mating (Clements, 2000). While much is known regarding the regulation and control of reproductive processes in female insects including oogenesis, research dedicated to understanding the regulation and control of spermatogenesis by factors including neuropeptides and/or neurohormones remains largely unexplored (Raikhel et al, 2005)
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