CK11, a teleost chemokine with a potent antimicrobial activity

Estefanía Muñoz-Atienza; Carolina Aquilino; Khairul Syahputra; Azmi Al-Jubury; Carlos Araújo; Jakob Skov; Per W. Kania; Pablo E. Hernández; Kurt Buchmann; Luis M. Cintas; Carolina Tafalla

doi:10.4049/jimmunol.1800568

CK11, a teleost chemokine with a potent antimicrobial activity

Estefanía Muñoz-Atienza, Carolina Aquilino, Khairul Syahputra, Azmi Al-Jubury, Carlos Araújo, Jakob Skov, Per W. Kania, Pablo E. Hernández, Kurt Buchmann, Luis M. Cintas, Carolina Tafalla^*

^*Corresponding author for this work

16 Citations (Scopus)

Abstract

CK11 is a rainbow trout (Oncorhynchus mykiss) CC chemokine phylogenetically related to both mammalian CCL27 and CCL28 chemokines, strongly transcribed in skin and gills in homeostasis, for which an immune role had not been reported to date. In the current study, we have demonstrated that CK11 is not chemotactic for unstimulated leukocyte populations from central immune organs or mucosal tissues but instead exerts a potent antimicrobial activity against a wide range of rainbow trout pathogens. Our results show that CK11 strongly inhibits the growth of different rainbow trout Gram-positive and Gram-negative bacteria, namely Lactococcus garvieae, Aeromonas salmonicida subsp. salmonicida, and Yersinia ruckeri and a parasitic ciliate Ichthyophthirius multifiliis. Similarly to mammalian chemokines and antimicrobial peptides, CK11 exerted its antimicrobial activity, rapidly inducing membrane permeability in the target pathogens. Further transcriptional studies confirmed the regulation of CK11 transcription in response to exposure to some of these pathogens in specific conditions. Altogether, our studies related to phylogenetic relations, tissue distribution, and biological activity point to CK11 as a potential common ancestor of mammalian CCL27 and CCL28. To our knowledge, this study constitutes the first report of a fish chemokine with antimicrobial activity, thus establishing a novel role for teleost chemokines in antimicrobial immunity that supports an evolutionary relationship between chemokines and antimicrobial peptides.

Original language	English
Journal	Journal of Immunology
Volume	202
Issue number	3
Pages (from-to)	857-870
Number of pages	14
ISSN	0022-1767
DOIs	https://doi.org/10.4049/jimmunol.1800568
Publication status	Published - 2019

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title = "CK11, a teleost chemokine with a potent antimicrobial activity",

abstract = "CK11 is a rainbow trout (Oncorhynchus mykiss) CC chemokine phylogenetically related to both mammalian CCL27 and CCL28 chemokines, strongly transcribed in skin and gills in homeostasis, for which an immune role had not been reported to date. In the current study, we have demonstrated that CK11 is not chemotactic for unstimulated leukocyte populations from central immune organs or mucosal tissues but instead exerts a potent antimicrobial activity against a wide range of rainbow trout pathogens. Our results show that CK11 strongly inhibits the growth of different rainbow trout Gram-positive and Gram-negative bacteria, namely Lactococcus garvieae, Aeromonas salmonicida subsp. salmonicida, and Yersinia ruckeri and a parasitic ciliate Ichthyophthirius multifiliis. Similarly to mammalian chemokines and antimicrobial peptides, CK11 exerted its antimicrobial activity, rapidly inducing membrane permeability in the target pathogens. Further transcriptional studies confirmed the regulation of CK11 transcription in response to exposure to some of these pathogens in specific conditions. Altogether, our studies related to phylogenetic relations, tissue distribution, and biological activity point to CK11 as a potential common ancestor of mammalian CCL27 and CCL28. To our knowledge, this study constitutes the first report of a fish chemokine with antimicrobial activity, thus establishing a novel role for teleost chemokines in antimicrobial immunity that supports an evolutionary relationship between chemokines and antimicrobial peptides.",

author = "Estefan{\'i}a Mu{\~n}oz-Atienza and Carolina Aquilino and Khairul Syahputra and Azmi Al-Jubury and Carlos Ara{\'u}jo and Jakob Skov and Kania, {Per W.} and Hern{\'a}ndez, {Pablo E.} and Kurt Buchmann and Cintas, {Luis M.} and Carolina Tafalla",

year = "2019",

doi = "10.4049/jimmunol.1800568",

language = "English",

volume = "202",

pages = "857--870",

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TY - JOUR

T1 - CK11, a teleost chemokine with a potent antimicrobial activity

AU - Muñoz-Atienza, Estefanía

AU - Aquilino, Carolina

AU - Syahputra, Khairul

AU - Al-Jubury, Azmi

AU - Araújo, Carlos

AU - Skov, Jakob

AU - Kania, Per W.

AU - Hernández, Pablo E.

AU - Buchmann, Kurt

AU - Cintas, Luis M.

AU - Tafalla, Carolina

PY - 2019

Y1 - 2019

N2 - CK11 is a rainbow trout (Oncorhynchus mykiss) CC chemokine phylogenetically related to both mammalian CCL27 and CCL28 chemokines, strongly transcribed in skin and gills in homeostasis, for which an immune role had not been reported to date. In the current study, we have demonstrated that CK11 is not chemotactic for unstimulated leukocyte populations from central immune organs or mucosal tissues but instead exerts a potent antimicrobial activity against a wide range of rainbow trout pathogens. Our results show that CK11 strongly inhibits the growth of different rainbow trout Gram-positive and Gram-negative bacteria, namely Lactococcus garvieae, Aeromonas salmonicida subsp. salmonicida, and Yersinia ruckeri and a parasitic ciliate Ichthyophthirius multifiliis. Similarly to mammalian chemokines and antimicrobial peptides, CK11 exerted its antimicrobial activity, rapidly inducing membrane permeability in the target pathogens. Further transcriptional studies confirmed the regulation of CK11 transcription in response to exposure to some of these pathogens in specific conditions. Altogether, our studies related to phylogenetic relations, tissue distribution, and biological activity point to CK11 as a potential common ancestor of mammalian CCL27 and CCL28. To our knowledge, this study constitutes the first report of a fish chemokine with antimicrobial activity, thus establishing a novel role for teleost chemokines in antimicrobial immunity that supports an evolutionary relationship between chemokines and antimicrobial peptides.

AB - CK11 is a rainbow trout (Oncorhynchus mykiss) CC chemokine phylogenetically related to both mammalian CCL27 and CCL28 chemokines, strongly transcribed in skin and gills in homeostasis, for which an immune role had not been reported to date. In the current study, we have demonstrated that CK11 is not chemotactic for unstimulated leukocyte populations from central immune organs or mucosal tissues but instead exerts a potent antimicrobial activity against a wide range of rainbow trout pathogens. Our results show that CK11 strongly inhibits the growth of different rainbow trout Gram-positive and Gram-negative bacteria, namely Lactococcus garvieae, Aeromonas salmonicida subsp. salmonicida, and Yersinia ruckeri and a parasitic ciliate Ichthyophthirius multifiliis. Similarly to mammalian chemokines and antimicrobial peptides, CK11 exerted its antimicrobial activity, rapidly inducing membrane permeability in the target pathogens. Further transcriptional studies confirmed the regulation of CK11 transcription in response to exposure to some of these pathogens in specific conditions. Altogether, our studies related to phylogenetic relations, tissue distribution, and biological activity point to CK11 as a potential common ancestor of mammalian CCL27 and CCL28. To our knowledge, this study constitutes the first report of a fish chemokine with antimicrobial activity, thus establishing a novel role for teleost chemokines in antimicrobial immunity that supports an evolutionary relationship between chemokines and antimicrobial peptides.

U2 - 10.4049/jimmunol.1800568

DO - 10.4049/jimmunol.1800568

M3 - Journal article

C2 - 30610164

AN - SCOPUS:85060285095

SN - 0022-1767

VL - 202

SP - 857

EP - 870

JO - Journal of Immunology

JF - Journal of Immunology

IS - 3

ER -

CK11, a teleost chemokine with a potent antimicrobial activity

Abstract

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