Structural and functional analysis of the newt lymphatic system
Abstract Regeneration competent vertebrates such as newts and salamanders possess a weakened adaptive immune system characterized by multiple connections between the lymphatic system and the blood vascular system called lymphatic hearts. The role of lymphatic vasculature and these lymphaticovenous c...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-04-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-34169-w |
| _version_ | 1827956817712381952 |
|---|---|
| author | Chihena H. Banda Makoto Shiraishi Kohei Mitsui Yoshimoto Okada Kanako Danno Ryohei Ishiura Kaho Maemura Chikafumi Chiba Akira Mizoguchi Kyoko Imanaka-Yoshida Kazuaki Maruyama Mitsunaga Narushima |
| author_facet | Chihena H. Banda Makoto Shiraishi Kohei Mitsui Yoshimoto Okada Kanako Danno Ryohei Ishiura Kaho Maemura Chikafumi Chiba Akira Mizoguchi Kyoko Imanaka-Yoshida Kazuaki Maruyama Mitsunaga Narushima |
| author_sort | Chihena H. Banda |
| collection | DOAJ |
| description | Abstract Regeneration competent vertebrates such as newts and salamanders possess a weakened adaptive immune system characterized by multiple connections between the lymphatic system and the blood vascular system called lymphatic hearts. The role of lymphatic vasculature and these lymphaticovenous connections in regeneration is unknown. We used in-vivo near-infrared lymphangiography, ultra-high frequency ultrasonography, micro-CT lymphangiography, and histological serial section 3-dimentional computer reconstruction to evaluate the lymphatic territories of Cynops pyrrhogaster. We used our model and supermicrosurgery to show that lymphatic hearts are not essential for lymphatic circulation and limb regeneration. Instead, newts possess a novel intraosseous network of lymphatics inside the bone expressing VEGFR-3, LYVE-1 and CD-31. However, we were unable to show Prox-1 expression by these vessels. We demonstrate that adult newt bone marrow functions as both a lymphatic drainage organ and fat reservoir. This study reveals the fundamental anatomical differences between the immune system of urodeles and mammals and provides a model for investigating lymphatics and regeneration. |
| first_indexed | 2024-04-09T15:10:34Z |
| format | Article |
| id | doaj.art-48338754934c42c68e2407ece054e298 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-09T15:10:34Z |
| publishDate | 2023-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-48338754934c42c68e2407ece054e2982023-04-30T11:14:34ZengNature PortfolioScientific Reports2045-23222023-04-0113111810.1038/s41598-023-34169-wStructural and functional analysis of the newt lymphatic systemChihena H. Banda0Makoto Shiraishi1Kohei Mitsui2Yoshimoto Okada3Kanako Danno4Ryohei Ishiura5Kaho Maemura6Chikafumi Chiba7Akira Mizoguchi8Kyoko Imanaka-Yoshida9Kazuaki Maruyama10Mitsunaga Narushima11Department of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityDepartment of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityDepartment of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityDepartment of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityDepartment of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityDepartment of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityDepartment of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityFaculty of Life and Environmental Sciences, University of TsukubaDepartment of Personalized Cancer Immunotherapy, Graduate School of Medicine, Mie UniversityDepartment of Pathology and Matrix Biology, Graduate School of Medicine, Mie UniversityDepartment of Pathology and Matrix Biology, Graduate School of Medicine, Mie UniversityDepartment of Plastic and Reconstructive Surgery, Graduate School of Medicine, Mie UniversityAbstract Regeneration competent vertebrates such as newts and salamanders possess a weakened adaptive immune system characterized by multiple connections between the lymphatic system and the blood vascular system called lymphatic hearts. The role of lymphatic vasculature and these lymphaticovenous connections in regeneration is unknown. We used in-vivo near-infrared lymphangiography, ultra-high frequency ultrasonography, micro-CT lymphangiography, and histological serial section 3-dimentional computer reconstruction to evaluate the lymphatic territories of Cynops pyrrhogaster. We used our model and supermicrosurgery to show that lymphatic hearts are not essential for lymphatic circulation and limb regeneration. Instead, newts possess a novel intraosseous network of lymphatics inside the bone expressing VEGFR-3, LYVE-1 and CD-31. However, we were unable to show Prox-1 expression by these vessels. We demonstrate that adult newt bone marrow functions as both a lymphatic drainage organ and fat reservoir. This study reveals the fundamental anatomical differences between the immune system of urodeles and mammals and provides a model for investigating lymphatics and regeneration.https://doi.org/10.1038/s41598-023-34169-w |
| spellingShingle | Chihena H. Banda Makoto Shiraishi Kohei Mitsui Yoshimoto Okada Kanako Danno Ryohei Ishiura Kaho Maemura Chikafumi Chiba Akira Mizoguchi Kyoko Imanaka-Yoshida Kazuaki Maruyama Mitsunaga Narushima Structural and functional analysis of the newt lymphatic system Scientific Reports |
| title | Structural and functional analysis of the newt lymphatic system |
| title_full | Structural and functional analysis of the newt lymphatic system |
| title_fullStr | Structural and functional analysis of the newt lymphatic system |
| title_full_unstemmed | Structural and functional analysis of the newt lymphatic system |
| title_short | Structural and functional analysis of the newt lymphatic system |
| title_sort | structural and functional analysis of the newt lymphatic system |
| url | https://doi.org/10.1038/s41598-023-34169-w |
| work_keys_str_mv | AT chihenahbanda structuralandfunctionalanalysisofthenewtlymphaticsystem AT makotoshiraishi structuralandfunctionalanalysisofthenewtlymphaticsystem AT koheimitsui structuralandfunctionalanalysisofthenewtlymphaticsystem AT yoshimotookada structuralandfunctionalanalysisofthenewtlymphaticsystem AT kanakodanno structuralandfunctionalanalysisofthenewtlymphaticsystem AT ryoheiishiura structuralandfunctionalanalysisofthenewtlymphaticsystem AT kahomaemura structuralandfunctionalanalysisofthenewtlymphaticsystem AT chikafumichiba structuralandfunctionalanalysisofthenewtlymphaticsystem AT akiramizoguchi structuralandfunctionalanalysisofthenewtlymphaticsystem AT kyokoimanakayoshida structuralandfunctionalanalysisofthenewtlymphaticsystem AT kazuakimaruyama structuralandfunctionalanalysisofthenewtlymphaticsystem AT mitsunaganarushima structuralandfunctionalanalysisofthenewtlymphaticsystem |