Discovery of an unconventional lamprey lymphocyte lineage highlights divergent features in vertebrate adaptive immune system evolution

Lymphocyte receptors independently evolved in both jawed and jawless vertebrates with similar adaptive immune responses. However, the diversity of functional subtypes and molecular architecture in jawless vertebrate lymphocytes, comparable to jawed species, is not well defined. Here, we profile the gills, intestines, and blood of the lamprey, Lampetra morii, with single-cell RNA sequencing, using a full-length transcriptome as a reference. Our findings reveal higher tissue-specific heterogeneity among T-like cells in contrast to B-like cells. Notably, we identify a unique T-like cell subtype expressing a homolog of the nonlymphoid hematopoietic growth factor receptor, MPL-like (MPL-L). These MPL-L+ T-like cells exhibit features distinct from T cells of jawed vertebrates, particularly in their elevated expression of hematopoietic genes. We further discovered that MPL-L<sup>+</sup> VLRA<sup>+</sup> T-like cells are widely present in the typhlosole, gill, liver, kidney, and skin of lamprey and they proliferate in response to both a T cell mitogen and recombinant human thrombopoietin. These findings provide new insights into the adaptive immune response in jawless vertebrates, shedding new light on the evolution of adaptive immunity.

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Publication Details

Journal
Nature Communications
Published
2024-09-03
DOI
https://doi.org/10.1038/s41467-024-51763-2
Citations
11
Primary Topic
Immune Cell Function and Interaction
Type
article
Field-Weighted Citation Impact
2.65

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article

Discovery of an unconventional lamprey lymphocyte lineage highlights divergent features in vertebrate adaptive immune system evolution

Yingyi Huang, Jian-Yang Chen, Hongyan Wang, Changwei Shao et al.
11 citations
Nature Communications
Immune Cell Function and Interaction
2.65
article

Discovery of an unconventional lamprey lymphocyte lineage highlights divergent features in vertebrate adaptive immune system evolution

Yingyi Huang, Jian-Yang Chen, Hongyan Wang, Changwei Shao, Guangyi Fan, Yue Pang, Kaiqiang Liu, Chen Li, Yanan Li, Shuo Li, Xiang Liu, Shanshan Liu, Qian Wang, Qun Liu, Yuyan Liu, Yingying Zhang, Xianghui Zhang
article en
11 citations

Abstract

Lymphocyte receptors independently evolved in both jawed and jawless vertebrates with similar adaptive immune responses. However, the diversity of functional subtypes and molecular architecture in jawless vertebrate lymphocytes, comparable to jawed species, is not well defined. Here, we profile the gills, intestines, and blood of the lamprey, Lampetra morii, with single-cell RNA sequencing, using a full-length transcriptome as a reference. Our findings reveal higher tissue-specific heterogeneity among T-like cells in contrast to B-like cells. Notably, we identify a unique T-like cell subtype expressing a homolog of the nonlymphoid hematopoietic growth factor receptor, MPL-like (MPL-L). These MPL-L+ T-like cells exhibit features distinct from T cells of jawed vertebrates, particularly in their elevated expression of hematopoietic genes. We further discovered that MPL-L<sup>+</sup> VLRA<sup>+</sup> T-like cells are widely present in the typhlosole, gill, liver, kidney, and skin of lamprey and they proliferate in response to both a T cell mitogen and recombinant human thrombopoietin. These findings provide new insights into the adaptive immune response in jawless vertebrates, shedding new light on the evolution of adaptive immunity.

Nature CommunicationsVol. 15(1)
BGI Group (China) (CN), University of Copenhagen (DK), Liaoning Normal University (CN), Qingdao National Laboratory for Marine Science and Technology (CN), BGI Research (CN), Chinese Academy of Fishery Sciences (CN)
Taishan Scholar Foundation of Shandong Province, National Key Research and Development Program of China, Central Public-interest Scientific Institution Basal Research Fund, Chinese Academy of Fishery Sciences
Zero hunger
Openalex Percentile: Top 10%
Immune Cell Function and Interaction
2.65
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