Developmental and sex-specific differences in expression of neuropeptides derived from allatotropin gene in the silkmoth Bombyx mori

Abstract

Allatotropin (AT) and related neuropeptides are widespread bioactive molecules that regulate development, food intake and muscle contractions in insects and other invertebrates. In moths, alternative splicing of the at gene generates three mRNA precursors encoding AT with different combinations of three structurally similar AT-like peptides (ATLI-III). We used in situ hybridization and immunohistochemistry to map the differential expression of these transcripts during the postembryonic development of Bombyx mori. Transcript encoding AT alone was expressed in numerous neurons of the central nervous system and frontal ganglion, whereas transcripts encoding AT with ATLs were produced by smaller specific subgroups of neurons in larval stages. Metamorphosis was associated with considerable developmental changes and sex-specific differences in the expression of all transcripts. The most notable was the appearance of AT/ATL transcripts (1) in the brain lateral neurosecretory cells producing prothoracicotropic hormone; (2) in the male-specific cluster of about 20 neurons in the posterior region of the terminal abdominal ganglion; (3) in the female-specific medial neurons in the abdominal ganglia AG2-7. Immunohistochemical staining showed that these neurons produced a mixture of various neuropeptides and innervated diverse peripheral organs. Our data suggest that AT/ATL neuropeptides are involved in multiple stage- and sex-specific functions during the development of B. mori.

Multiple neuropeptides produced by sex-specific neurons control activity of the male accessory glands and gonoducts in the silkworm Bombyx mori

“…Detailed analysis of neuropeptide expression revealed male-specific cluster of peptidergic neurons that differentiate during metamorphosis in the TAG. Using a combination of ISH and immunohistochemistry 7,14,15 , we detected expression of four different groups of neuropeptides (CT-DH, AT, ATLI-III, AST-C, and MIPs) in these neurons. This cluster contains ~20 posterio-medial neurons (~25 μm in diameter) in the male abdominal neuromere 9 (AN9) and we named them the M ale A dult N eurons of AN 9 (MAN9) (Figs 1–4).…”

“…The allatotropin gene is transcribed in three variants of alternatively spliced mRNA precursors. All three precursors encode allatotropin (AT) and various combinations of allatotropin-like peptides (ATLI-III) 7,16 . Expression of all three transcripts has recently been described in the entire CNS during development of B. mori 7 , so in this paper we will focus on the TAG.…”

“…All three precursors encode allatotropin (AT) and various combinations of allatotropin-like peptides (ATLI-III) 7,16 . Expression of all three transcripts has recently been described in the entire CNS during development of B. mori 7 , so in this paper we will focus on the TAG. Larvae showed AT expression in two dorso-medial PM7 neurons and M 5 neurosecretory cells in the AN7 and several small neurons in the AN9 (Fig.…”

“…IMNs differentiate through early pupal stages and their number is multiplied during metamorphosis in the anterior clusters in females and in the posterior cluster in males. In males a posterior cluster of IMN exit via terminal nerves to innervate the sperm duct and accessory glands 6,7 .…”

“…Approximately 40 neuropeptide families have been identified in B. mori 8–13 . Using in situ hybridization (ISH) and immunohistochemistry we identified sex-specific differences in expression of several neuropeptide genes in the TAG during comprehensive mapping of neuropeptide localization in the central nervous system (CNS) of B. mori 7,8 . Here, we describe developmental changes in expression of calcitonin-like diuretic hormone (CT-DH), allatotropin (AT), allatostatin C (AST-C) and myoinhibitory peptide (MIP) in the TAG.…”