Mmp-induced fat body cell dissociation promotes pupal development and moderately averts pupal diapause by activating lipid metabolism

Abstract

In Lepidoptera and Diptera, the fat body dissociates into single cells in nondiapause pupae, but it does not dissociate in diapause pupae until diapause termination. Using the cotton bollworm, Helicoverpa armigera , as a model of pupal diapause insects, we illustrated the catalytic mechanism and physiological importance of fat body cell dissociation in regulating pupal development and diapause. In nondiapause pupae, cathepsin L (CatL) activates matrix metalloproteinases (Mmps) that degrade extracellular matrix proteins and cause fat body cell dissociation. Mmp-induced fat body cell dissociation activates lipid metabolism through transcriptional regulation, and the resulting energetic supplies increase brain metabolic activity (i.e., mitochondria respiration and insulin signaling) and thus promote pupal development. In diapause pupae, low activities of CatL and Mmps prevent fat body cell dissociation and lipid metabolism from occurring, maintaining pupal diapause. Importantly, as demonstrated by chemical inhibitor treatments and CRISPR-mediated gene knockouts, Mmp inhibition delayed pupal development and moderately increased the incidence of pupal diapause, while Mmp stimulation promoted pupal development and moderately averted pupal diapause. This study advances our recent understanding of fat body biology and insect diapause regulation.

Physiological and transcriptional changes associated with obligate aestivation in the cabbage stem flea beetle (Psylliodes chrysocephala)

“…This process could potentially trigger fat body cell dissociation and activate lipid metabolism during aestivation. This cathepsin L-like proteinase function was observed, for example, in the pupae of the non-diapausing moth Helicoverpa armigera (Jia and Li, 2023). Post-aestivating adults, especially females, may heavily rely on these lipid reserves for oviposition and migration behavior (Sinclair, 2015;Sinclair and Marshall, 2018;Wolda and Denlinger, 1984).…”

Histone acetylation is associated with pupal diapause in cotton bollworm, Helicoverpa armigera

“…Furthermore, we validated the expression of 14 differentially expressed genes that exhibit potential association with diapause, including energy metabolism-related genes: ATP-binding cassette subfamily C member 4 (ABCC4), Tafazzin, facilitated trehalose transporter Tret1-2, facilitated trehalose transporter Tret1 [27][28][29] ; resistance-related genes: cytochrome P450 6B7 (CYP6B7), cytochrome P450 6B2 (CYP6B2), cytochrome b5 (cyt-b5) 30 ; immune response-related genes: Scolexin B and Lebocin 4 and some reported genes may be involved in diapause: Cathepsin L, Zonadhesin, juvenile hormone esterase (JHE), eukaryotic translation initiation factor 4E1 (eIF4E1), and Transcription factor JunD. [31][32][33][34][35] TSA treatment elevated most of these genes, confirming the transcriptome analysis (Fig. 7(e)).…”

Matrix metalloproteinase 2 contributes to adult eclosion and immune response in the small hive beetle, Aethina tumida

“…, 2014; Jia et al. , 2018; Jia & Li, 2023). However, 5 MMP genes have been identified in Periplaneta americana , and 9 were identified in Aedes aegypti (Kantor et al.…”