Identification and characterization of three CXC chemokines in Asian swamp eel (Monopterus albus) uncover a third CXCL11_like group in fish

Hanwen Yuan, Youshen Li, Panpan Han, Guangming Tian, Wenbing Zhang, Huizhi Guo, Qiaoqing Xu (Corresponding Author), Tiehui Wang (Corresponding Author)

Research output: Contribution to journalArticle

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Abstract

Chemokines direct cell migration in development and immune defense, and bridge between innate and adaptive immune responses. The chemokine gene family has been rapidly evolving and has undergone species/lineage-specific expansion. Mammals possess inflammatory CXC chemokines CXCL1-8/15 and CXCL9-11 sub-groups, and homeostatic CXCL12-14, 16–17. Orthologues of mammalian CXCL12-14, three chemokines related to CXCL1-8/15 (CXCL8_L1-3), two chemokines related to CXC9-11 (CXCL11_L1-2), and five fish-specific chemokines (CXCL_F1-5) have been described in teleosts. In this study, we reported three novel CXC chemokines in Asian swamp eel Monopterus albus, a commercially important freshwater fish species in China. Two of them belong to the fish-specific CXCL_F2 group, named CXCL_F2a/b, that share 89.5% amino acid identity. The other (CXCL11_L3) belongs to a third CXCL11_L related to the mammalian CXCL9-11 subfamily found only in percomorph fish species, and is the only CXCL9-11 related molecules in this lineage. Mammalian CXCL9-11 attract Th1 cells, and block the migration of Th2 cells in an immune response. This study suggests that all major lineages of teleosts have a CXCL9-11 related chemokine that will aid future functional investigation of CXCL11_L in fish. Cxcl_f2a is highly expressed constitutively in the skin of swamp eels that may attract immune cells to protect the skin in the absence of scales. Cxcl11_l3 and cxcl_f2b are highly expressed in immune tissues/organs and are up-regulated by the viral mimic poly I:C, but not bacterial infection in vivo, suggesting their role in anti-viral defense. The two cxcl_f2 paralogues are differentially expressed and modulated, indicating sub- and/or neo-functionalization.
Original languageEnglish
Article number103454
Number of pages9
JournalDevelopmental and Comparative Immunology
Volume101
Early online date19 Jul 2019
DOIs
Publication statusE-pub ahead of print - 19 Jul 2019

Fingerprint

Smegmamorpha
CXC Chemokines
Chemokines
Fishes
Cell Movement
Chemokine CXCL1
Poly I-C
Th2 Cells
Skin
Th1 Cells
Adaptive Immunity
Fresh Water
Bacterial Infections
Innate Immunity
Mammals
China
Amino Acids
Genes

Keywords

  • Asian swamp eel (Monopterus albus)
  • CXCL11_L3
  • CXCL_F2
  • Evolution
  • Modulation
  • MOLECULAR CHARACTERIZATION
  • EXPRESSION ANALYSIS
  • CATFISH
  • GRASS CARP
  • CROAKER LARIMICHTHYS-CROCEA
  • INTERFERON REGULATORY FACTOR
  • GENE
  • SEQUENCE
  • SUPERFAMILY
  • RECEPTORS

ASJC Scopus subject areas

  • Immunology
  • Developmental Biology

Cite this

Identification and characterization of three CXC chemokines in Asian swamp eel (Monopterus albus) uncover a third CXCL11_like group in fish. / Yuan, Hanwen; Li, Youshen; Han, Panpan; Tian, Guangming; Zhang, Wenbing; Guo, Huizhi; Xu, Qiaoqing (Corresponding Author); Wang, Tiehui (Corresponding Author).

In: Developmental and Comparative Immunology, Vol. 101, 103454, 12.2019.

Research output: Contribution to journalArticle

Yuan, Hanwen ; Li, Youshen ; Han, Panpan ; Tian, Guangming ; Zhang, Wenbing ; Guo, Huizhi ; Xu, Qiaoqing ; Wang, Tiehui. / Identification and characterization of three CXC chemokines in Asian swamp eel (Monopterus albus) uncover a third CXCL11_like group in fish. In: Developmental and Comparative Immunology. 2019 ; Vol. 101.
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abstract = "Chemokines direct cell migration in development and immune defense, and bridge between innate and adaptive immune responses. The chemokine gene family has been rapidly evolving and has undergone species/lineage-specific expansion. Mammals possess inflammatory CXC chemokines CXCL1-8/15 and CXCL9-11 sub-groups, and homeostatic CXCL12-14, 16–17. Orthologues of mammalian CXCL12-14, three chemokines related to CXCL1-8/15 (CXCL8_L1-3), two chemokines related to CXC9-11 (CXCL11_L1-2), and five fish-specific chemokines (CXCL_F1-5) have been described in teleosts. In this study, we reported three novel CXC chemokines in Asian swamp eel Monopterus albus, a commercially important freshwater fish species in China. Two of them belong to the fish-specific CXCL_F2 group, named CXCL_F2a/b, that share 89.5{\%} amino acid identity. The other (CXCL11_L3) belongs to a third CXCL11_L related to the mammalian CXCL9-11 subfamily found only in percomorph fish species, and is the only CXCL9-11 related molecules in this lineage. Mammalian CXCL9-11 attract Th1 cells, and block the migration of Th2 cells in an immune response. This study suggests that all major lineages of teleosts have a CXCL9-11 related chemokine that will aid future functional investigation of CXCL11_L in fish. Cxcl_f2a is highly expressed constitutively in the skin of swamp eels that may attract immune cells to protect the skin in the absence of scales. Cxcl11_l3 and cxcl_f2b are highly expressed in immune tissues/organs and are up-regulated by the viral mimic poly I:C, but not bacterial infection in vivo, suggesting their role in anti-viral defense. The two cxcl_f2 paralogues are differentially expressed and modulated, indicating sub- and/or neo-functionalization.",
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T1 - Identification and characterization of three CXC chemokines in Asian swamp eel (Monopterus albus) uncover a third CXCL11_like group in fish

AU - Yuan, Hanwen

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AU - Han, Panpan

AU - Tian, Guangming

AU - Zhang, Wenbing

AU - Guo, Huizhi

AU - Xu, Qiaoqing

AU - Wang, Tiehui

N1 - Acknowledgment This study was supported by the Foundation of Guangdong Provincial Key Laboratory of Marine Biotechnology (No. GPKLMB201801), the Fund of Key Laboratory of Aquaculture Disease Control, and the Ministry of Agriculture and National Natural Science Foundation of China (31460689).

PY - 2019/7/19

Y1 - 2019/7/19

N2 - Chemokines direct cell migration in development and immune defense, and bridge between innate and adaptive immune responses. The chemokine gene family has been rapidly evolving and has undergone species/lineage-specific expansion. Mammals possess inflammatory CXC chemokines CXCL1-8/15 and CXCL9-11 sub-groups, and homeostatic CXCL12-14, 16–17. Orthologues of mammalian CXCL12-14, three chemokines related to CXCL1-8/15 (CXCL8_L1-3), two chemokines related to CXC9-11 (CXCL11_L1-2), and five fish-specific chemokines (CXCL_F1-5) have been described in teleosts. In this study, we reported three novel CXC chemokines in Asian swamp eel Monopterus albus, a commercially important freshwater fish species in China. Two of them belong to the fish-specific CXCL_F2 group, named CXCL_F2a/b, that share 89.5% amino acid identity. The other (CXCL11_L3) belongs to a third CXCL11_L related to the mammalian CXCL9-11 subfamily found only in percomorph fish species, and is the only CXCL9-11 related molecules in this lineage. Mammalian CXCL9-11 attract Th1 cells, and block the migration of Th2 cells in an immune response. This study suggests that all major lineages of teleosts have a CXCL9-11 related chemokine that will aid future functional investigation of CXCL11_L in fish. Cxcl_f2a is highly expressed constitutively in the skin of swamp eels that may attract immune cells to protect the skin in the absence of scales. Cxcl11_l3 and cxcl_f2b are highly expressed in immune tissues/organs and are up-regulated by the viral mimic poly I:C, but not bacterial infection in vivo, suggesting their role in anti-viral defense. The two cxcl_f2 paralogues are differentially expressed and modulated, indicating sub- and/or neo-functionalization.

AB - Chemokines direct cell migration in development and immune defense, and bridge between innate and adaptive immune responses. The chemokine gene family has been rapidly evolving and has undergone species/lineage-specific expansion. Mammals possess inflammatory CXC chemokines CXCL1-8/15 and CXCL9-11 sub-groups, and homeostatic CXCL12-14, 16–17. Orthologues of mammalian CXCL12-14, three chemokines related to CXCL1-8/15 (CXCL8_L1-3), two chemokines related to CXC9-11 (CXCL11_L1-2), and five fish-specific chemokines (CXCL_F1-5) have been described in teleosts. In this study, we reported three novel CXC chemokines in Asian swamp eel Monopterus albus, a commercially important freshwater fish species in China. Two of them belong to the fish-specific CXCL_F2 group, named CXCL_F2a/b, that share 89.5% amino acid identity. The other (CXCL11_L3) belongs to a third CXCL11_L related to the mammalian CXCL9-11 subfamily found only in percomorph fish species, and is the only CXCL9-11 related molecules in this lineage. Mammalian CXCL9-11 attract Th1 cells, and block the migration of Th2 cells in an immune response. This study suggests that all major lineages of teleosts have a CXCL9-11 related chemokine that will aid future functional investigation of CXCL11_L in fish. Cxcl_f2a is highly expressed constitutively in the skin of swamp eels that may attract immune cells to protect the skin in the absence of scales. Cxcl11_l3 and cxcl_f2b are highly expressed in immune tissues/organs and are up-regulated by the viral mimic poly I:C, but not bacterial infection in vivo, suggesting their role in anti-viral defense. The two cxcl_f2 paralogues are differentially expressed and modulated, indicating sub- and/or neo-functionalization.

KW - Asian swamp eel (Monopterus albus)

KW - CXCL11_L3

KW - CXCL_F2

KW - Evolution

KW - Modulation

KW - MOLECULAR CHARACTERIZATION

KW - EXPRESSION ANALYSIS

KW - CATFISH

KW - GRASS CARP

KW - CROAKER LARIMICHTHYS-CROCEA

KW - INTERFERON REGULATORY FACTOR

KW - GENE

KW - SEQUENCE

KW - SUPERFAMILY

KW - RECEPTORS

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DO - 10.1016/j.dci.2019.103454

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JO - Developmental and Comparative Immunology

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SN - 0145-305X

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