» Articles » PMID: 38497789

Single-cell RNA Sequencing Unveils the Hidden Powers of Zebrafish Kidney for Generating Both Hematopoiesis and Adaptive Antiviral Immunity

Overview
Journal Elife
Specialty Biology
Date 2024 Mar 18
PMID 38497789
Authors
Affiliations
Soon will be listed here.
Abstract

The vertebrate kidneys play two evolutionary conserved roles in waste excretion and osmoregulation. Besides, the kidney of fish is considered as a functional ortholog of mammalian bone marrow that serves as a hematopoietic hub for generating blood cell lineages and immunological responses. However, knowledge about the properties of kidney hematopoietic cells, and the functionality of the kidney in fish immune systems remains to be elucidated. To this end, our present study generated a comprehensive atlas with 59 hematopoietic stem/progenitor cell (HSPC) and immune-cells types from zebrafish kidneys via single-cell transcriptome profiling analysis. These populations included almost all known cells associated with innate and adaptive immunity, and displayed differential responses to viral infection, indicating their diverse functional roles in antiviral immunity. Remarkably, HSPCs were found to have extensive reactivities to viral infection, and the trained immunity can be effectively induced in certain HSPCs. In addition, the antigen-stimulated adaptive immunity can be fully generated in the kidney, suggesting the kidney acts as a secondary lymphoid organ. These results indicated that the fish kidney is a dual-functional entity with functionalities of both primary and secondary lymphoid organs. Our findings illustrated the unique features of fish immune systems, and highlighted the multifaced biology of kidneys in ancient vertebrates.

Citing Articles

Rapid Natural Killer Cell Gene Responses, Generated by TLR Ligand-Induced Trained Immunity, Provide Protection to Bacterial Infection in Mutant Zebrafish ().

Muire P, Hanson L, Petrie-Hanson L Int J Mol Sci. 2025; 26(3).

PMID: 39940731 PMC: 11818001. DOI: 10.3390/ijms26030962.


Small Fish, Big Answers: Zebrafish and the Molecular Drivers of Metastasis.

Martinez-Lopez M, Lopez-Gil J Int J Mol Sci. 2025; 26(3).

PMID: 39940643 PMC: 11817282. DOI: 10.3390/ijms26030871.


Cross-species single-cell RNA-seq analysis reveals disparate and conserved cardiac and extracardiac inflammatory responses upon heart injury.

Cortada E, Yao J, Xia Y, Dundar F, Zumbo P, Yang B Commun Biol. 2024; 7(1):1611.

PMID: 39627536 PMC: 11615278. DOI: 10.1038/s42003-024-07315-x.


Catching the Big Fish in Big Data: A Meta-Analysis of Zebrafish Kidney scRNA-Seq Datasets Highlights Conserved Molecular Profiles of Macrophages and Neutrophils in Vertebrates.

Bobrovskikh A, Zubairova U, Naumenko L, Doroshkov A Biology (Basel). 2024; 13(10).

PMID: 39452082 PMC: 11505477. DOI: 10.3390/biology13100773.


Single-cell RNA sequencing unveils the hidden powers of zebrafish kidney for generating both hematopoiesis and adaptive antiviral immunity.

Hu C, Zhang N, Hong Y, Tie R, Fan D, Lin A Elife. 2024; 13.

PMID: 38497789 PMC: 10948150. DOI: 10.7554/eLife.92424.

References
1.
Barreto V, Pan-Hammarstrom Q, Zhao Y, Hammarstrom L, Misulovin Z, Nussenzweig M . AID from bony fish catalyzes class switch recombination. J Exp Med. 2005; 202(6):733-8. PMC: 2212934. DOI: 10.1084/jem.20051378. View

2.
Cooper M, Alder M . The evolution of adaptive immune systems. Cell. 2006; 124(4):815-22. DOI: 10.1016/j.cell.2006.02.001. View

3.
Perng Y, Lenschow D . ISG15 in antiviral immunity and beyond. Nat Rev Microbiol. 2018; 16(7):423-439. PMC: 7097117. DOI: 10.1038/s41579-018-0020-5. View

4.
Ribeil J, Zermati Y, Vandekerckhove J, Cathelin S, Kersual J, Dussiot M . Hsp70 regulates erythropoiesis by preventing caspase-3-mediated cleavage of GATA-1. Nature. 2006; 445(7123):102-5. DOI: 10.1038/nature05378. View

5.
Philipson B, OConnor R, May M, June C, Albelda S, Milone M . 4-1BB costimulation promotes CAR T cell survival through noncanonical NF-κB signaling. Sci Signal. 2020; 13(625). PMC: 7883633. DOI: 10.1126/scisignal.aay8248. View