Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotes
The cytokine interleukin 1 (IL-1) is an evolutionary innovation of vertebrates. Fish and amphibian have one IL1 gene, while mammals have two copies of IL1, IL1A and IL1B, with distinct expression patterns and differences in their proteolytic activation. Our current understanding of the evolutionary...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
The Royal Society
2022-08-01
|
| Series: | Open Biology |
| Subjects: | |
| Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsob.220049 |
| _version_ | 1797840278775660544 |
|---|---|
| author | Eva Hasel de Carvalho Eva Bartok Helen Stölting Baubak Bajoghli Maria Leptin |
| author_facet | Eva Hasel de Carvalho Eva Bartok Helen Stölting Baubak Bajoghli Maria Leptin |
| author_sort | Eva Hasel de Carvalho |
| collection | DOAJ |
| description | The cytokine interleukin 1 (IL-1) is an evolutionary innovation of vertebrates. Fish and amphibian have one IL1 gene, while mammals have two copies of IL1, IL1A and IL1B, with distinct expression patterns and differences in their proteolytic activation. Our current understanding of the evolutionary history of IL-1 is mainly based on phylogenetic analysis, but this approach provides no information on potentially different functions of IL-1 homologues, and it remains unclear which biological activities identified for IL-1α and IL-1β in mammals are present in lower vertebrates. Here, we use in vitro and in vivo experimental models to examine the expression patterns and cleavage of IL-1 proteins from various species. We found that IL-1 in the teleost medaka shares the transcriptional patterns of mammalian IL-1α, and its processing also resembles that of mammalian IL-1α, which is sensitive to cysteine protease inhibitors specific for the calpain and cathepsin families. By contrast, IL-1 proteins in reptiles also include biological properties of IL-1β. Therefore, we propose that the duplication of the ancestral IL1 gene led to the segregation of expression patterns and protein processing that characterizes the two extant forms of IL-1 in mammals. |
| first_indexed | 2024-04-09T16:12:22Z |
| format | Article |
| id | doaj.art-7266a6c4cd554be4b35062fcf59132a3 |
| institution | Directory Open Access Journal |
| issn | 2046-2441 |
| language | English |
| last_indexed | 2024-04-09T16:12:22Z |
| publishDate | 2022-08-01 |
| publisher | The Royal Society |
| record_format | Article |
| series | Open Biology |
| spelling | doaj.art-7266a6c4cd554be4b35062fcf59132a32023-04-24T09:16:43ZengThe Royal SocietyOpen Biology2046-24412022-08-0112810.1098/rsob.220049Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotesEva Hasel de Carvalho0Eva Bartok1Helen Stölting2Baubak Bajoghli3Maria Leptin4European Molecular Biology Laboratory (EMBL), Directors' Research, Meyerhofstrasse 1, 69117 Heidelberg, GermanyInstitute of Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, Venusberg Campus 1, 53127 Bonn, GermanyNational Heart and Lung Institute, Faculty of Medicine, Imperial College London, London, UKEuropean Molecular Biology Laboratory (EMBL), Directors' Research, Meyerhofstrasse 1, 69117 Heidelberg, GermanyEuropean Molecular Biology Laboratory (EMBL), Directors' Research, Meyerhofstrasse 1, 69117 Heidelberg, GermanyThe cytokine interleukin 1 (IL-1) is an evolutionary innovation of vertebrates. Fish and amphibian have one IL1 gene, while mammals have two copies of IL1, IL1A and IL1B, with distinct expression patterns and differences in their proteolytic activation. Our current understanding of the evolutionary history of IL-1 is mainly based on phylogenetic analysis, but this approach provides no information on potentially different functions of IL-1 homologues, and it remains unclear which biological activities identified for IL-1α and IL-1β in mammals are present in lower vertebrates. Here, we use in vitro and in vivo experimental models to examine the expression patterns and cleavage of IL-1 proteins from various species. We found that IL-1 in the teleost medaka shares the transcriptional patterns of mammalian IL-1α, and its processing also resembles that of mammalian IL-1α, which is sensitive to cysteine protease inhibitors specific for the calpain and cathepsin families. By contrast, IL-1 proteins in reptiles also include biological properties of IL-1β. Therefore, we propose that the duplication of the ancestral IL1 gene led to the segregation of expression patterns and protein processing that characterizes the two extant forms of IL-1 in mammals.https://royalsocietypublishing.org/doi/10.1098/rsob.220049evolutioncytokinemedakainnate immune system |
| spellingShingle | Eva Hasel de Carvalho Eva Bartok Helen Stölting Baubak Bajoghli Maria Leptin Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotes Open Biology evolution cytokine medaka innate immune system |
| title | Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotes |
| title_full | Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotes |
| title_fullStr | Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotes |
| title_full_unstemmed | Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotes |
| title_short | Revisiting the origin of interleukin 1 in anamniotes and sub-functionalization of interleukin 1 in amniotes |
| title_sort | revisiting the origin of interleukin 1 in anamniotes and sub functionalization of interleukin 1 in amniotes |
| topic | evolution cytokine medaka innate immune system |
| url | https://royalsocietypublishing.org/doi/10.1098/rsob.220049 |
| work_keys_str_mv | AT evahaseldecarvalho revisitingtheoriginofinterleukin1inanamniotesandsubfunctionalizationofinterleukin1inamniotes AT evabartok revisitingtheoriginofinterleukin1inanamniotesandsubfunctionalizationofinterleukin1inamniotes AT helenstolting revisitingtheoriginofinterleukin1inanamniotesandsubfunctionalizationofinterleukin1inamniotes AT baubakbajoghli revisitingtheoriginofinterleukin1inanamniotesandsubfunctionalizationofinterleukin1inamniotes AT marialeptin revisitingtheoriginofinterleukin1inanamniotesandsubfunctionalizationofinterleukin1inamniotes |