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

Yingyi Huang, Xiang Liu, Shuo Li, Chen Li, Hong-Yan Wang, Qun Liu, Jian-Yang Chen, Yingying Zhang, Yanan Li, Xianghui Zhang, Qian Wang, Kaiqiang Liu, Yu-Yan Liu, Yue Pang, Shanshan Liu, Guangyi Fan and Changwei Shao ()
Additional contact information
Yingyi Huang: Chinese Academy of Fishery Sciences
Xiang Liu: Chinese Academy of Fishery Sciences
Shuo Li: Chinese Academy of Fishery Sciences
Chen Li: Chinese Academy of Fishery Sciences
Hong-Yan Wang: Chinese Academy of Fishery Sciences
Qun Liu: BGI Research
Jian-Yang Chen: BGI Research
Yingying Zhang: BGI Research
Yanan Li: Chinese Academy of Fishery Sciences
Xianghui Zhang: Chinese Academy of Fishery Sciences
Qian Wang: Chinese Academy of Fishery Sciences
Kaiqiang Liu: Chinese Academy of Fishery Sciences
Yu-Yan Liu: Chinese Academy of Fishery Sciences
Yue Pang: Liaoning Normal University
Shanshan Liu: BGI Research
Guangyi Fan: BGI Research
Changwei Shao: Chinese Academy of Fishery Sciences

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: 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+ VLRA+ 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.

Date: 2024
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DOI: 10.1038/s41467-024-51763-2

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