Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model.
Severe intraoral pain induces difficulty in eating and speaking, leading to a decline in the quality of life. However, the molecular mechanisms underlying intraoral pain remain unclear. Here, we investigated gene modulation in the trigeminal ganglion and intraoral pain-related behavior in a rat mode...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0284617 |
| _version_ | 1797829919790596096 |
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| author | Suzuro Hitomi Tomotaka Nodai Shoichiro Kokabu Takemi Shikayama Misa Sago-Ito Chihiro Nakatomi Kiyoshi Terawaki Yuji Omiya Masamichi Shinoda Kentaro Ono |
| author_facet | Suzuro Hitomi Tomotaka Nodai Shoichiro Kokabu Takemi Shikayama Misa Sago-Ito Chihiro Nakatomi Kiyoshi Terawaki Yuji Omiya Masamichi Shinoda Kentaro Ono |
| author_sort | Suzuro Hitomi |
| collection | DOAJ |
| description | Severe intraoral pain induces difficulty in eating and speaking, leading to a decline in the quality of life. However, the molecular mechanisms underlying intraoral pain remain unclear. Here, we investigated gene modulation in the trigeminal ganglion and intraoral pain-related behavior in a rat model of acetic acid-induced oral ulcerative mucositis. Oral ulceration was observed on day 2 after acetic acid treatment to the oral mucosa of male Wistar rats, causing spontaneous pain and mechanical allodynia. Deoxyribonucleic acid microarray analysis of trigeminal ganglion tissue indicated that Hamp (a hepcidin gene that regulates cellular iron transport) was the most upregulated gene. In the oral ulcerative mucositis model, the upregulation of Hamp was also induced in the ulcer region but not in the liver, with no increase in hepcidin levels in the plasma and saliva, indicating that hepcidin was produced locally in the ulcer region in the model. Systemic antibiotic pretreatment did not increase the mRNA levels of Hamp in the trigeminal ganglion and ulcer regions. Hepcidin injection into the oral mucosa enhanced neuronal excitability in response to noxious mechanical stimulation of the oral mucosa in trigeminal spinal subnucleus interpolaris/caudalis neurons. These results imply that oral ulcerative mucositis induces oral mucosal pain because of infectious inflammation of the ulcerative area and potentiates Hamp, which represents anti-bacterial and anti-peptidase gene expression in the ulcer region and trigeminal ganglion. The regulation of cellular iron transport by hepcidin is likely involved in oral ulcerative mucositis-induced pain. |
| first_indexed | 2024-04-09T13:27:51Z |
| format | Article |
| id | doaj.art-c5b38d86523848e28058a019a27e70a8 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-04-09T13:27:51Z |
| publishDate | 2023-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-c5b38d86523848e28058a019a27e70a82023-05-10T05:31:54ZengPublic Library of Science (PLoS)PLoS ONE1932-62032023-01-01184e028461710.1371/journal.pone.0284617Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model.Suzuro HitomiTomotaka NodaiShoichiro KokabuTakemi ShikayamaMisa Sago-ItoChihiro NakatomiKiyoshi TerawakiYuji OmiyaMasamichi ShinodaKentaro OnoSevere intraoral pain induces difficulty in eating and speaking, leading to a decline in the quality of life. However, the molecular mechanisms underlying intraoral pain remain unclear. Here, we investigated gene modulation in the trigeminal ganglion and intraoral pain-related behavior in a rat model of acetic acid-induced oral ulcerative mucositis. Oral ulceration was observed on day 2 after acetic acid treatment to the oral mucosa of male Wistar rats, causing spontaneous pain and mechanical allodynia. Deoxyribonucleic acid microarray analysis of trigeminal ganglion tissue indicated that Hamp (a hepcidin gene that regulates cellular iron transport) was the most upregulated gene. In the oral ulcerative mucositis model, the upregulation of Hamp was also induced in the ulcer region but not in the liver, with no increase in hepcidin levels in the plasma and saliva, indicating that hepcidin was produced locally in the ulcer region in the model. Systemic antibiotic pretreatment did not increase the mRNA levels of Hamp in the trigeminal ganglion and ulcer regions. Hepcidin injection into the oral mucosa enhanced neuronal excitability in response to noxious mechanical stimulation of the oral mucosa in trigeminal spinal subnucleus interpolaris/caudalis neurons. These results imply that oral ulcerative mucositis induces oral mucosal pain because of infectious inflammation of the ulcerative area and potentiates Hamp, which represents anti-bacterial and anti-peptidase gene expression in the ulcer region and trigeminal ganglion. The regulation of cellular iron transport by hepcidin is likely involved in oral ulcerative mucositis-induced pain.https://doi.org/10.1371/journal.pone.0284617 |
| spellingShingle | Suzuro Hitomi Tomotaka Nodai Shoichiro Kokabu Takemi Shikayama Misa Sago-Ito Chihiro Nakatomi Kiyoshi Terawaki Yuji Omiya Masamichi Shinoda Kentaro Ono Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model. PLoS ONE |
| title | Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model. |
| title_full | Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model. |
| title_fullStr | Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model. |
| title_full_unstemmed | Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model. |
| title_short | Hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model. |
| title_sort | hepcidin expression in the trigeminal ganglion and the oral mucosa in an oral ulcerative mucositis rat model |
| url | https://doi.org/10.1371/journal.pone.0284617 |
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