Transcriptome and secretome profiling of sensory neurons reveals sex differences in pathways relevant to insulin sensing and insulin secretion

Moon, Sohyun; Alsarkhi, Lamyaa; Lin, Tai‐Tu; Inoue, Ryota; Tahiri, Azeddine; Colson, Cecilia; Cai, Weikang; Shirakawa, Jun; Qian, Wei‐Jun; Zhao, Jerry Yingtao; Ouaamari, Abdelfattah El

doi:10.1096/fj.202300941r

Title: Transcriptome and secretome profiling of sensory neurons reveals sex differences in pathways relevant to insulin sensing and insulin secretion

Journal Article · Mon Sep 11 00:00:00 EDT 2023 · FASEB Journal

DOI:https://doi.org/10.1096/fj.202300941r· OSTI ID:2229625

Moon, Sohyun ^[1]; Alsarkhi, Lamyaa ^[2]; Lin, Tai‐Tu ^[3]; Inoue, Ryota ^[4]; Tahiri, Azeddine ^[2]; Colson, Cecilia ^[5];

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^[4];

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New York Institute of Technology College of Osteopathic Medicine, Old Westbury, NY (United States)
New York Medical College, Valhalla, NY (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Gunma University, Maebashi (Japan)
Rutgers The State University of New Jersey, New Brunswick, NJ (United States)

Sensory neurons in the dorsal root ganglia (DRG) convey somatosensory and metabolic cues to the central nervous system and release substances from stimulated terminal endings in peripheral organs. Sex-biased variations driven by the sex chromosome complement (XX and XY) have been implicated in the sensory–islet crosstalk. However, the molecular underpinnings of these male–female differences are not known. Here, we aim to characterize the molecular repertoire and the secretome profile of the lower thoracic spinal sensory neurons and to identify molecules with sex-biased insulin sensing- and/or insulin secretion-modulating activity that are encoded independently of circulating gonadal sex hormones. We used transcriptomics and proteomics to uncover differentially expressed genes and secreted molecules in lower thoracic T5-12 DRG sensory neurons derived from sexually immature 3-week-old male and female C57BL/6J mice. Comparative transcriptome and proteome analyses revealed differential gene expression and protein secretion in DRG neurons in males and females. Furthermore, the transcriptome analysis identified, among others, higher insulin signaling/sensing capabilities in female DRG neurons; secretome screening uncovered several sex-specific candidate molecules with potential regulatory functions in pancreatic β cells. Together, these data suggest a putative role of sensory interoception of insulin in the DRG–islet crosstalk with implications in sensory feedback loops in the regulation of β-cell activity in a sex-biased manner. Finally, we provide a valuable resource of molecular and secretory targets that can be leveraged for understanding insulin interoception and insulin secretion and inform the development of novel studies/approaches to fathom the role of the sensory–islet axis in the regulation of energy balance in males and females.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE; Human Islet Research Network (HIRN); National Institutes of Health (NIH); Robert Wood Johnson Foundation (RWJF)

Grant/Contract Number:: AC05-76RL01830; UC4 DK104162; R01 DK122167; U01 DK124020; NINDS R15 NS130456; 74260

OSTI ID:: 2229625

Report Number(s):: PNNL-SA-189945

Journal Information:: FASEB Journal, Vol. 37, Issue 10; ISSN 0892-6638

Publisher:: Federation of American Societies for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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