Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesions
Necrotizing soft tissue infections (NSTI) progress to severe necrosis and result in fatal sepsis within a short time. Vibrio vulnificus is a causative agent and can spread from the initial infection site through soft tissue finally to the systemic circulation of the host. The motility and chemotaxis...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2020-12-01
|
| Series: | Virulence |
| Subjects: | |
| Online Access: | http://dx.doi.org/10.1080/21505594.2020.1782707 |
| _version_ | 1818966693083348992 |
|---|---|
| author | Kohei Yamazaki Takashige Kashimoto Takehiro Kado Yukihiro Akeda Kazuki Yoshioka Toshio Kodama Mai Yamamoto Masashi Okamura Tsutomu Kakuda Shunji Ueno |
| author_facet | Kohei Yamazaki Takashige Kashimoto Takehiro Kado Yukihiro Akeda Kazuki Yoshioka Toshio Kodama Mai Yamamoto Masashi Okamura Tsutomu Kakuda Shunji Ueno |
| author_sort | Kohei Yamazaki |
| collection | DOAJ |
| description | Necrotizing soft tissue infections (NSTI) progress to severe necrosis and result in fatal sepsis within a short time. Vibrio vulnificus is a causative agent and can spread from the initial infection site through soft tissue finally to the systemic circulation of the host. The motility and chemotaxis of this bacterium are essential for proliferation and lethality in a murine model of the infection, but their role in pathogenicity has not been characterized. In this study, we revealed the roles of motility and chemotaxis during the process of V. vulnificus infection. We compared a nonmotile mutant and two nonchemotactic mutants with their parent strain (WT) with regard to bacterial spread using an in vivo imaging system (IVIS) and invasion by detection of bacteria from the muscle and spleen of a murine infection model. WT rapidly spread throughout the infected thigh and invaded deep muscle causing severe tissue damage. The detection rate in the systemic circulation and the lethality were high. On the other hand, the nonmotile mutant stayed at the inoculation site, and the nonchemotactic mutants spread only slowly through the soft tissue of the infected thigh. Detection in the systemic circulation, the degree of tissue damage, and the lethality of nonchemotactic mutants were significantly reduced in mice compared with WT. This study demonstrated that chemotaxis is essential for invasion from the infection site to the deep and distant tissues and the main pathogenic factor for the rapid progression leading to sepsis in V. vulnificus NSTI. |
| first_indexed | 2024-12-20T13:36:57Z |
| format | Article |
| id | doaj.art-c9bbd95c7c684f50907d2ffa4618575f |
| institution | Directory Open Access Journal |
| issn | 2150-5594 2150-5608 |
| language | English |
| last_indexed | 2024-12-20T13:36:57Z |
| publishDate | 2020-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Virulence |
| spelling | doaj.art-c9bbd95c7c684f50907d2ffa4618575f2022-12-21T19:38:55ZengTaylor & Francis GroupVirulence2150-55942150-56082020-12-0111183984710.1080/21505594.2020.17827071782707Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesionsKohei Yamazaki0Takashige Kashimoto1Takehiro Kado2Yukihiro Akeda3Kazuki Yoshioka4Toshio Kodama5Mai Yamamoto6Masashi Okamura7Tsutomu Kakuda8Shunji Ueno9Kitasato UniversityKitasato UniversityKitasato UniversityOsaka University HospitalKitasato UniversityInternational Research Center for Infectious Diseases, Research Institute for Microbial DiseasesOkayama Prefectural UniversityKitasato UniversityKitasato UniversityKitasato UniversityNecrotizing soft tissue infections (NSTI) progress to severe necrosis and result in fatal sepsis within a short time. Vibrio vulnificus is a causative agent and can spread from the initial infection site through soft tissue finally to the systemic circulation of the host. The motility and chemotaxis of this bacterium are essential for proliferation and lethality in a murine model of the infection, but their role in pathogenicity has not been characterized. In this study, we revealed the roles of motility and chemotaxis during the process of V. vulnificus infection. We compared a nonmotile mutant and two nonchemotactic mutants with their parent strain (WT) with regard to bacterial spread using an in vivo imaging system (IVIS) and invasion by detection of bacteria from the muscle and spleen of a murine infection model. WT rapidly spread throughout the infected thigh and invaded deep muscle causing severe tissue damage. The detection rate in the systemic circulation and the lethality were high. On the other hand, the nonmotile mutant stayed at the inoculation site, and the nonchemotactic mutants spread only slowly through the soft tissue of the infected thigh. Detection in the systemic circulation, the degree of tissue damage, and the lethality of nonchemotactic mutants were significantly reduced in mice compared with WT. This study demonstrated that chemotaxis is essential for invasion from the infection site to the deep and distant tissues and the main pathogenic factor for the rapid progression leading to sepsis in V. vulnificus NSTI.http://dx.doi.org/10.1080/21505594.2020.1782707vibrio vulnificusnecrotizing soft tissue infectionpathogenic factorchemotaxismouse modelin vivo imaging |
| spellingShingle | Kohei Yamazaki Takashige Kashimoto Takehiro Kado Yukihiro Akeda Kazuki Yoshioka Toshio Kodama Mai Yamamoto Masashi Okamura Tsutomu Kakuda Shunji Ueno Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesions Virulence vibrio vulnificus necrotizing soft tissue infection pathogenic factor chemotaxis mouse model in vivo imaging |
| title | Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesions |
| title_full | Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesions |
| title_fullStr | Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesions |
| title_full_unstemmed | Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesions |
| title_short | Chemotactic invasion in deep soft tissue by Vibrio vulnificus is essential for the progression of necrotic lesions |
| title_sort | chemotactic invasion in deep soft tissue by vibrio vulnificus is essential for the progression of necrotic lesions |
| topic | vibrio vulnificus necrotizing soft tissue infection pathogenic factor chemotaxis mouse model in vivo imaging |
| url | http://dx.doi.org/10.1080/21505594.2020.1782707 |
| work_keys_str_mv | AT koheiyamazaki chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT takashigekashimoto chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT takehirokado chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT yukihiroakeda chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT kazukiyoshioka chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT toshiokodama chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT maiyamamoto chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT masashiokamura chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT tsutomukakuda chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions AT shunjiueno chemotacticinvasionindeepsofttissuebyvibriovulnificusisessentialfortheprogressionofnecroticlesions |