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CXCR4s in Teleosts: Two Paralogous Chemokine Receptors and Their Roles in Hematopoietic Stem/Progenitor Cell Homeostasis

Xin-Jiang Lu, Kai Zhu, Hong-Xia Shen, Li Nie and Jiong Chen
J Immunol January 20, 2020, ji1901100; DOI: https://doi.org/10.4049/jimmunol.1901100
Xin-Jiang Lu
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China; Laboratory of Biochemistry and Molecular Biology, School of Marine Sciences, Ningbo University, Ningbo 315211, People's Republic of China; and Key Laboratory of Applied Marine Biotechnology of Ministry of Education, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China
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Kai Zhu
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China; Laboratory of Biochemistry and Molecular Biology, School of Marine Sciences, Ningbo University, Ningbo 315211, People's Republic of China; and Key Laboratory of Applied Marine Biotechnology of Ministry of Education, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China
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Hong-Xia Shen
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China; Laboratory of Biochemistry and Molecular Biology, School of Marine Sciences, Ningbo University, Ningbo 315211, People's Republic of China; and Key Laboratory of Applied Marine Biotechnology of Ministry of Education, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China
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Li Nie
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China; Laboratory of Biochemistry and Molecular Biology, School of Marine Sciences, Ningbo University, Ningbo 315211, People's Republic of China; and Key Laboratory of Applied Marine Biotechnology of Ministry of Education, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China
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Jiong Chen
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China; Laboratory of Biochemistry and Molecular Biology, School of Marine Sciences, Ningbo University, Ningbo 315211, People's Republic of China; and Key Laboratory of Applied Marine Biotechnology of Ministry of Education, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China
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Key Points

  • CXCR4a and CXCR4b prefer to bind LPS and SDF-1 in teleosts, respectively.

  • CXCR4b inhibits HSPC proliferation in ayu by regulating ROS levels.

  • CXCR4a+ HSPCs are prone to differentiate into myeloid cells in ayu.

Abstract

Hematopoietic stem/progenitor cells (HSPCs) generate the entire repertoire of immune cells in vertebrates and play a crucial role during infection. Although two copies of CXC motif chemokine receptor 4 (CXCR4) genes are generally identified in teleosts, the function of teleost CXCR4 genes in HSPCs is less known. In this study, we identified two CXCR4 genes from a teleost, ayu (Plecoglossus altivelis), named PaCXCR4a and PaCXCR4b. PaCXCR4b was constitutively expressed in ayu HSPCs, whereas PaCXCR4a was induced by LPS treatment. The stromal-derived factor-1–binding activity of CXCR4b was significantly higher than that of CXCR4a, whereas the LPS-binding activity of CXCR4a was significantly higher than that of CXCR4b in the teleosts ayu, large yellow croaker (Larimichthys crocea), and tiger puffer (Takifugu rubripes). CXCR4a+ HSPCs were mobilized into blood by LPS, whereas CXCR4b+ HSPCs were mobilized by leukocyte cell–derived chemotaxin-2. PaSDF-1 and PaCXCR4b, but not PaCXCR4a, inhibited HSPC proliferation by regulating reactive oxygen species levels. Compared with PaCXCR4b+ HSPCs, PaCXCR4a+ HSPCs preferentially differentiated into myeloid cells in ayu by maintaining high stem cell leukemia expression. These data suggest that the two copies of CXCR4s achieve a division of labor in the regulation of teleost HSPC homeostasis, supporting the concept that subfunctionalization after gene duplication in teleosts may stabilize the immune system.

Footnotes

  • This work was supported by the Program for the Natural Science Foundation of China (31972821; 31772876; 41776151), the Zhejiang Provincial Natural Science Foundation of China (LR18C040001; LZ18C190001), the Scientific Innovation Team Project of Ningbo (2015C110018) and the K.C. Wong Magna Fund in Ningbo University.

  • The sequences presented in this article have been submitted to GenBank (https://www.ncbi.nlm.nih.gov/genbank/) under accession numbers MN148390, MN148391, MN148393, MN158722, MN158723, MN158724, MN156535, and MN156536, MN628572, MN628573.

  • The online version of this article contains supplemental material.

  • Received September 10, 2019.
  • Accepted December 11, 2019.
  • Copyright © 2020 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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CXCR4s in Teleosts: Two Paralogous Chemokine Receptors and Their Roles in Hematopoietic Stem/Progenitor Cell Homeostasis
Xin-Jiang Lu, Kai Zhu, Hong-Xia Shen, Li Nie, Jiong Chen
The Journal of Immunology January 20, 2020, ji1901100; DOI: 10.4049/jimmunol.1901100

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CXCR4s in Teleosts: Two Paralogous Chemokine Receptors and Their Roles in Hematopoietic Stem/Progenitor Cell Homeostasis
Xin-Jiang Lu, Kai Zhu, Hong-Xia Shen, Li Nie, Jiong Chen
The Journal of Immunology January 20, 2020, ji1901100; DOI: 10.4049/jimmunol.1901100
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Print ISSN 0022-1767        Online ISSN 1550-6606