Pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system

Abstract Trigeminal (TG), dorsal root (DRG), and nodose/jugular (NG/JG) ganglia each possess specialized and distinct functions. We used RNA sequencing of two-cycle sorted Pirt-positive neurons to identify genes exclusively expressing in L3–L5 DRG, T10-L1 DRG, NG/JG, and TG mouse ganglion neurons. T...

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Autores principales: Anahit H. Hovhannisyan, Hyeonwi Son, Jennifer Mecklenburg, Priscilla Ann Barba-Escobedo, Meilinn Tram, Ruben Gomez, John Shannonhouse, Yi Zou, Korri Weldon, Shivani Ruparel, Zhao Lai, Alexei V. Tumanov, Yu Shin Kim, Armen N. Akopian
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:0068e9c9db544ba09762a26e0082f9492021-12-02T17:41:18ZPituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system10.1038/s41598-021-97084-y2045-2322https://doaj.org/article/0068e9c9db544ba09762a26e0082f9492021-09-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-97084-yhttps://doaj.org/toc/2045-2322Abstract Trigeminal (TG), dorsal root (DRG), and nodose/jugular (NG/JG) ganglia each possess specialized and distinct functions. We used RNA sequencing of two-cycle sorted Pirt-positive neurons to identify genes exclusively expressing in L3–L5 DRG, T10-L1 DRG, NG/JG, and TG mouse ganglion neurons. Transcription factor Phox2b and Efcab6 are specifically expressed in NG/JG while Hoxa7 is exclusively present in both T10-L1 and L3–L5 DRG neurons. Cyp2f2, Krt18, and Ptgds, along with pituitary hormone prolactin (Prl), growth hormone (Gh), and proopiomelanocortin (Pomc) encoding genes are almost exclusively in TG neurons. Immunohistochemistry confirmed selective expression of these hormones in TG neurons and dural nerves; and showed GH expression in subsets of TRPV1+ and CGRP+ TG neurons. We next examined GH roles in hypersensitivity in the spinal versus trigeminal systems. Exogenous GH produced mechanical hypersensitivity when injected intrathecally, but not intraplantarly. GH-induced thermal hypersensitivity was not detected in the spinal system. GH dose-dependently generated orofacial and headache-like periorbital mechanical hypersensitivity after administration into masseter muscle and dura, respectively. Periorbital mechanical hypersensitivity was reversed by a GH receptor antagonist, pegvisomant. Overall, pituitary hormone genes are selective for TG versus other ganglia somatotypes; and GH has distinctive functional significance in the trigeminal versus spinal systems.Anahit H. HovhannisyanHyeonwi SonJennifer MecklenburgPriscilla Ann Barba-EscobedoMeilinn TramRuben GomezJohn ShannonhouseYi ZouKorri WeldonShivani RuparelZhao LaiAlexei V. TumanovYu Shin KimArmen N. AkopianNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-18 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Anahit H. Hovhannisyan
Hyeonwi Son
Jennifer Mecklenburg
Priscilla Ann Barba-Escobedo
Meilinn Tram
Ruben Gomez
John Shannonhouse
Yi Zou
Korri Weldon
Shivani Ruparel
Zhao Lai
Alexei V. Tumanov
Yu Shin Kim
Armen N. Akopian
Pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system
description Abstract Trigeminal (TG), dorsal root (DRG), and nodose/jugular (NG/JG) ganglia each possess specialized and distinct functions. We used RNA sequencing of two-cycle sorted Pirt-positive neurons to identify genes exclusively expressing in L3–L5 DRG, T10-L1 DRG, NG/JG, and TG mouse ganglion neurons. Transcription factor Phox2b and Efcab6 are specifically expressed in NG/JG while Hoxa7 is exclusively present in both T10-L1 and L3–L5 DRG neurons. Cyp2f2, Krt18, and Ptgds, along with pituitary hormone prolactin (Prl), growth hormone (Gh), and proopiomelanocortin (Pomc) encoding genes are almost exclusively in TG neurons. Immunohistochemistry confirmed selective expression of these hormones in TG neurons and dural nerves; and showed GH expression in subsets of TRPV1+ and CGRP+ TG neurons. We next examined GH roles in hypersensitivity in the spinal versus trigeminal systems. Exogenous GH produced mechanical hypersensitivity when injected intrathecally, but not intraplantarly. GH-induced thermal hypersensitivity was not detected in the spinal system. GH dose-dependently generated orofacial and headache-like periorbital mechanical hypersensitivity after administration into masseter muscle and dura, respectively. Periorbital mechanical hypersensitivity was reversed by a GH receptor antagonist, pegvisomant. Overall, pituitary hormone genes are selective for TG versus other ganglia somatotypes; and GH has distinctive functional significance in the trigeminal versus spinal systems.
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author Anahit H. Hovhannisyan
Hyeonwi Son
Jennifer Mecklenburg
Priscilla Ann Barba-Escobedo
Meilinn Tram
Ruben Gomez
John Shannonhouse
Yi Zou
Korri Weldon
Shivani Ruparel
Zhao Lai
Alexei V. Tumanov
Yu Shin Kim
Armen N. Akopian
author_facet Anahit H. Hovhannisyan
Hyeonwi Son
Jennifer Mecklenburg
Priscilla Ann Barba-Escobedo
Meilinn Tram
Ruben Gomez
John Shannonhouse
Yi Zou
Korri Weldon
Shivani Ruparel
Zhao Lai
Alexei V. Tumanov
Yu Shin Kim
Armen N. Akopian
author_sort Anahit H. Hovhannisyan
title Pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system
title_short Pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system
title_full Pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system
title_fullStr Pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system
title_full_unstemmed Pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system
title_sort pituitary hormones are specifically expressed in trigeminal sensory neurons and contribute to pain responses in the trigeminal system
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/0068e9c9db544ba09762a26e0082f949
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