Substance P aggravates ligature-induced periodontitis in mice
Periodontitis is one of the most common oral diseases in humans, affecting over 40% of adult Americans. Pain-sensing nerves, or nociceptors, sense local environmental changes and often contain neuropeptides. Recent studies have suggested that nociceptors magnify host response and regulate bone loss...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-04-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1099017/full |
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| author | Yasir Dilshad Siddiqui Yasir Dilshad Siddiqui Xuguang Nie Sheng Wang Yasaman Abbasi Lauren Park Xiaoxuan Fan Vivek Thumbigere-Math Man-Kyo Chung |
| author_facet | Yasir Dilshad Siddiqui Yasir Dilshad Siddiqui Xuguang Nie Sheng Wang Yasaman Abbasi Lauren Park Xiaoxuan Fan Vivek Thumbigere-Math Man-Kyo Chung |
| author_sort | Yasir Dilshad Siddiqui |
| collection | DOAJ |
| description | Periodontitis is one of the most common oral diseases in humans, affecting over 40% of adult Americans. Pain-sensing nerves, or nociceptors, sense local environmental changes and often contain neuropeptides. Recent studies have suggested that nociceptors magnify host response and regulate bone loss in the periodontium. A subset of nociceptors projected to periodontium contains neuropeptides, such as calcitonin gene-related peptide (CGRP) or substance P (SP). However, the specific roles of neuropeptides from nociceptive neural terminals in periodontitis remain to be determined. In this study, we investigated the roles of neuropeptides on host responses and bone loss in ligature-induced periodontitis. Deletion of tachykinin precursor 1 (Tac1), a gene that encodes SP, or treatment of gingiva with SP antagonist significantly reduced bone loss in ligature-induced periodontitis, whereas deletion of calcitonin related polypeptide alpha (Calca), a gene that encodes CGRP, showed a marginal role on bone loss. Ligature-induced recruitment of leukocytes, including neutrophils, and increase in cytokines leading to bone loss in periodontium was significantly less in Tac1 knockout mice. Furthermore, intra-gingival injection of SP, but not neurokinin A, induced a vigorous inflammatory response and osteoclast activation in alveolar bone and facilitated bone loss in ligature-induced periodontitis. Altogether, our data suggest that SP plays significant roles in regulating host responses and bone resorption in ligature-induced periodontitis. |
| first_indexed | 2024-04-09T18:09:10Z |
| format | Article |
| id | doaj.art-9388d39561084a27a0d657ad3692daaf |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-09T18:09:10Z |
| publishDate | 2023-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-9388d39561084a27a0d657ad3692daaf2023-04-14T04:44:25ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-04-011410.3389/fimmu.2023.10990171099017Substance P aggravates ligature-induced periodontitis in miceYasir Dilshad Siddiqui0Yasir Dilshad Siddiqui1Xuguang Nie2Sheng Wang3Yasaman Abbasi4Lauren Park5Xiaoxuan Fan6Vivek Thumbigere-Math7Man-Kyo Chung8Program in Neuroscience, Center to Advance Chronic Pain Research, Department of Neural and Pain Sciences, School of Dentistry, University of Maryland, Baltimore, MD, United StatesDepartment of Preventive Dentistry, College of Dentistry, Jouf University, Sakaka, Saudi ArabiaProgram in Neuroscience, Center to Advance Chronic Pain Research, Department of Neural and Pain Sciences, School of Dentistry, University of Maryland, Baltimore, MD, United StatesProgram in Neuroscience, Center to Advance Chronic Pain Research, Department of Neural and Pain Sciences, School of Dentistry, University of Maryland, Baltimore, MD, United StatesProgram in Neuroscience, Center to Advance Chronic Pain Research, Department of Neural and Pain Sciences, School of Dentistry, University of Maryland, Baltimore, MD, United StatesProgram in Neuroscience, Center to Advance Chronic Pain Research, Department of Neural and Pain Sciences, School of Dentistry, University of Maryland, Baltimore, MD, United StatesDepartment of Microbiology and Immunology, Flow Cytometry Shared Service, University of Maryland School of Medicine, Baltimore, MD, United StatesDepartment of Advanced Oral Sciences and Therapeutics, University of Maryland School of Dentistry, Baltimore, MD, United StatesProgram in Neuroscience, Center to Advance Chronic Pain Research, Department of Neural and Pain Sciences, School of Dentistry, University of Maryland, Baltimore, MD, United StatesPeriodontitis is one of the most common oral diseases in humans, affecting over 40% of adult Americans. Pain-sensing nerves, or nociceptors, sense local environmental changes and often contain neuropeptides. Recent studies have suggested that nociceptors magnify host response and regulate bone loss in the periodontium. A subset of nociceptors projected to periodontium contains neuropeptides, such as calcitonin gene-related peptide (CGRP) or substance P (SP). However, the specific roles of neuropeptides from nociceptive neural terminals in periodontitis remain to be determined. In this study, we investigated the roles of neuropeptides on host responses and bone loss in ligature-induced periodontitis. Deletion of tachykinin precursor 1 (Tac1), a gene that encodes SP, or treatment of gingiva with SP antagonist significantly reduced bone loss in ligature-induced periodontitis, whereas deletion of calcitonin related polypeptide alpha (Calca), a gene that encodes CGRP, showed a marginal role on bone loss. Ligature-induced recruitment of leukocytes, including neutrophils, and increase in cytokines leading to bone loss in periodontium was significantly less in Tac1 knockout mice. Furthermore, intra-gingival injection of SP, but not neurokinin A, induced a vigorous inflammatory response and osteoclast activation in alveolar bone and facilitated bone loss in ligature-induced periodontitis. Altogether, our data suggest that SP plays significant roles in regulating host responses and bone resorption in ligature-induced periodontitis.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1099017/fullTac1substance Pperiodontitismouse modelosteoclastscytokines |
| spellingShingle | Yasir Dilshad Siddiqui Yasir Dilshad Siddiqui Xuguang Nie Sheng Wang Yasaman Abbasi Lauren Park Xiaoxuan Fan Vivek Thumbigere-Math Man-Kyo Chung Substance P aggravates ligature-induced periodontitis in mice Frontiers in Immunology Tac1 substance P periodontitis mouse model osteoclasts cytokines |
| title | Substance P aggravates ligature-induced periodontitis in mice |
| title_full | Substance P aggravates ligature-induced periodontitis in mice |
| title_fullStr | Substance P aggravates ligature-induced periodontitis in mice |
| title_full_unstemmed | Substance P aggravates ligature-induced periodontitis in mice |
| title_short | Substance P aggravates ligature-induced periodontitis in mice |
| title_sort | substance p aggravates ligature induced periodontitis in mice |
| topic | Tac1 substance P periodontitis mouse model osteoclasts cytokines |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1099017/full |
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