Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing mice
Abstract Mechanisms of sex-dependent orofacial pain are widely understudied. A significant gap in knowledge exists about comprehensive regulation of tissue-specific trigeminal sensory neurons in diseased state of both sexes. Using RNA sequencing of FACS sorted retro-labeled sensory neurons innervati...
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Nature Portfolio
2023-08-01
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Online Access: | https://doi.org/10.1038/s41598-023-40380-6 |
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author | Tarek Ibrahim Ping Wu Li-Ju Wang Chang Fang-Mei Josue Murillo Jaclyn Merlo Sergey S. Shein Alexei V. Tumanov Zhao Lai Korri Weldon Yidong Chen Shivani Ruparel |
author_facet | Tarek Ibrahim Ping Wu Li-Ju Wang Chang Fang-Mei Josue Murillo Jaclyn Merlo Sergey S. Shein Alexei V. Tumanov Zhao Lai Korri Weldon Yidong Chen Shivani Ruparel |
author_sort | Tarek Ibrahim |
collection | DOAJ |
description | Abstract Mechanisms of sex-dependent orofacial pain are widely understudied. A significant gap in knowledge exists about comprehensive regulation of tissue-specific trigeminal sensory neurons in diseased state of both sexes. Using RNA sequencing of FACS sorted retro-labeled sensory neurons innervating tongue tissue, we determined changes in transcriptomic profiles in males and female mice under naïve as well as tongue-tumor bearing conditions Our data revealed the following interesting findings: (1) FACS sorting obtained higher number of neurons from female trigeminal ganglia (TG) compared to males; (2) Naïve female neurons innervating the tongue expressed immune cell markers such as Csf1R, C1qa and others, that weren’t expressed in males. This was validated by Immunohistochemistry. (3) Accordingly, immune cell markers such as Csf1 exclusively sensitized TRPV1 responses in female TG neurons. (4) Male neurons were more tightly regulated than female neurons upon tumor growth and very few differentially expressed genes (DEGs) overlapped between the sexes, (5) Male DEGs contained higher number of transcription factors whereas female DEGs contained higher number of enzymes, cytokines and chemokines. Collectively, this is the first study to characterize the effect of sex as well as of tongue-tumor on global gene expression, pathways and molecular function of tongue-innervating sensory neurons. |
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language | English |
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spelling | doaj.art-79d7679fdfd14c77bc043fef711445ae2023-11-20T09:20:23ZengNature PortfolioScientific Reports2045-23222023-08-0113111510.1038/s41598-023-40380-6Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing miceTarek Ibrahim0Ping Wu1Li-Ju Wang2Chang Fang-Mei3Josue Murillo4Jaclyn Merlo5Sergey S. Shein6Alexei V. Tumanov7Zhao Lai8Korri Weldon9Yidong Chen10Shivani Ruparel11Department of Endodontics, School of Dentistry, University of Texas Health Science Center at San AntonioDepartment of Endodontics, School of Dentistry, University of Texas Health Science Center at San AntonioGreehey Children’s Cancer Institute, University of Texas Health San AntonioDepartment of Endodontics, School of Dentistry, University of Texas Health Science Center at San AntonioDepartment of Endodontics, School of Dentistry, University of Texas Health Science Center at San AntonioDepartment of Endodontics, School of Dentistry, University of Texas Health Science Center at San AntonioDepartment of Microbiology, Immunology and Molecular Genetics, University of Texas Health San AntonioDepartment of Microbiology, Immunology and Molecular Genetics, University of Texas Health San AntonioGreehey Children’s Cancer Institute, University of Texas Health San AntonioGreehey Children’s Cancer Institute, University of Texas Health San AntonioGreehey Children’s Cancer Institute, University of Texas Health San AntonioDepartment of Endodontics, School of Dentistry, University of Texas Health Science Center at San AntonioAbstract Mechanisms of sex-dependent orofacial pain are widely understudied. A significant gap in knowledge exists about comprehensive regulation of tissue-specific trigeminal sensory neurons in diseased state of both sexes. Using RNA sequencing of FACS sorted retro-labeled sensory neurons innervating tongue tissue, we determined changes in transcriptomic profiles in males and female mice under naïve as well as tongue-tumor bearing conditions Our data revealed the following interesting findings: (1) FACS sorting obtained higher number of neurons from female trigeminal ganglia (TG) compared to males; (2) Naïve female neurons innervating the tongue expressed immune cell markers such as Csf1R, C1qa and others, that weren’t expressed in males. This was validated by Immunohistochemistry. (3) Accordingly, immune cell markers such as Csf1 exclusively sensitized TRPV1 responses in female TG neurons. (4) Male neurons were more tightly regulated than female neurons upon tumor growth and very few differentially expressed genes (DEGs) overlapped between the sexes, (5) Male DEGs contained higher number of transcription factors whereas female DEGs contained higher number of enzymes, cytokines and chemokines. Collectively, this is the first study to characterize the effect of sex as well as of tongue-tumor on global gene expression, pathways and molecular function of tongue-innervating sensory neurons.https://doi.org/10.1038/s41598-023-40380-6 |
spellingShingle | Tarek Ibrahim Ping Wu Li-Ju Wang Chang Fang-Mei Josue Murillo Jaclyn Merlo Sergey S. Shein Alexei V. Tumanov Zhao Lai Korri Weldon Yidong Chen Shivani Ruparel Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing mice Scientific Reports |
title | Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing mice |
title_full | Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing mice |
title_fullStr | Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing mice |
title_full_unstemmed | Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing mice |
title_short | Sex-dependent differences in the genomic profile of lingual sensory neurons in naïve and tongue-tumor bearing mice |
title_sort | sex dependent differences in the genomic profile of lingual sensory neurons in naive and tongue tumor bearing mice |
url | https://doi.org/10.1038/s41598-023-40380-6 |
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