Extensive expansion and diversification of the chemokine gene family in zebrafish: Identification of a novel chemokine subfamily CX

Hisayuki Nomiyama, Kunio Hieshima, Naoki Osada, Yoko Kato-Unoki, Kaori Otsuka-Ono, Sumio Takegawa, Toshiaki Izawa, Akio Yoshizawa, Yutaka Kikuchi, Sumio Tanase, Retsu Miura, Jun Kusuda, Miki Nakao, Osamu Yoshie

Research output: Contribution to journalArticle

116 Citations (Scopus)

Abstract

Background: The chemokine family plays important roles in cell migration and activation. In humans, at least 44 members are known. Based on the arrangement of the four conserved cysteine residues, chemokines are now classified into four subfamilies, CXC, CC, XC and CX3C. Given that zebrafish is an important experimental model and teleost fishes constitute an evolutionarily diverse group that forms half the vertebrate species, it would be useful to compare the zebrafish chemokine system with those of mammals. Prior to this study, however, only incomplete lists of the zebrafish chemokine genes were reported. Results: We systematically searched chemokine genes in the zebrafish genome and EST databases, and identified more than 100 chemokine genes. These genes were CXC, CC and XC subfamily members, while no CX3C gene was identified. We also searched chemokine genes in pufferfish fugu and Tetraodon, and found only 18 chemokine genes in each species. The majority of the identified chemokine genes are unique to zebrafish or teleost fishes. However, several groups of chemokines are moderately similar to human chemokines, and some chemokines are orthologous to human homeostatic chemokines CXCL12 and CXCL14. Zebrafish also possesses a novel species-specific subfamily consisting of five members, which we term the CX subfamily. The CX chemokines lack one of the two N-terminus conserved cysteine residues but retain the third and the fourth ones. (Note that the XC subfamily only retains the second and fourth of the signature cysteines residues.) Phylogenetic analysis and genome organization of the chemokine genes showed that successive tandem duplication events generated the CX genes from the CC subfamily. Recombinant CXL-chr24a, one of the CX subfamily members on chromosome 24, showed marked chemotactic activity for carp leukocytes. The mRNA was expressed mainly during a certain period of the embryogenesis, suggesting its role in the zebrafish development. Conclusion: The phylogenic and genomic organization analyses suggest that a substantial number of chemokine genes in zebrafish were generated by zebrafish-specific tandem duplication events. During such duplications, a novel chemokine subfamily termed CX was generated in zebrafish. Only two human chemokines CXCL12 and CXCL14 have the orthologous chemokines in zebrafish. The diversification observed in the numbers and sequences of chemokines in the fish may reflect the adaptation of the individual species to their respective biological environment.

Original languageEnglish
Article number222
JournalBMC Genomics
Volume9
DOIs
Publication statusPublished - May 15 2008

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Zebrafish
Chemokines
Genes
Cysteine
Chemokine CXCL12
Fishes
Takifugu
Tetraodontiformes
Genome
Carps
Expressed Sequence Tags

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Genetics

Cite this

Nomiyama, H., Hieshima, K., Osada, N., Kato-Unoki, Y., Otsuka-Ono, K., Takegawa, S., ... Yoshie, O. (2008). Extensive expansion and diversification of the chemokine gene family in zebrafish: Identification of a novel chemokine subfamily CX. BMC Genomics, 9, [222]. https://doi.org/10.1186/1471-2164-9-222

Extensive expansion and diversification of the chemokine gene family in zebrafish : Identification of a novel chemokine subfamily CX. / Nomiyama, Hisayuki; Hieshima, Kunio; Osada, Naoki; Kato-Unoki, Yoko; Otsuka-Ono, Kaori; Takegawa, Sumio; Izawa, Toshiaki; Yoshizawa, Akio; Kikuchi, Yutaka; Tanase, Sumio; Miura, Retsu; Kusuda, Jun; Nakao, Miki; Yoshie, Osamu.

In: BMC Genomics, Vol. 9, 222, 15.05.2008.

Research output: Contribution to journalArticle

Nomiyama, H, Hieshima, K, Osada, N, Kato-Unoki, Y, Otsuka-Ono, K, Takegawa, S, Izawa, T, Yoshizawa, A, Kikuchi, Y, Tanase, S, Miura, R, Kusuda, J, Nakao, M & Yoshie, O 2008, 'Extensive expansion and diversification of the chemokine gene family in zebrafish: Identification of a novel chemokine subfamily CX', BMC Genomics, vol. 9, 222. https://doi.org/10.1186/1471-2164-9-222
Nomiyama, Hisayuki ; Hieshima, Kunio ; Osada, Naoki ; Kato-Unoki, Yoko ; Otsuka-Ono, Kaori ; Takegawa, Sumio ; Izawa, Toshiaki ; Yoshizawa, Akio ; Kikuchi, Yutaka ; Tanase, Sumio ; Miura, Retsu ; Kusuda, Jun ; Nakao, Miki ; Yoshie, Osamu. / Extensive expansion and diversification of the chemokine gene family in zebrafish : Identification of a novel chemokine subfamily CX. In: BMC Genomics. 2008 ; Vol. 9.
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abstract = "Background: The chemokine family plays important roles in cell migration and activation. In humans, at least 44 members are known. Based on the arrangement of the four conserved cysteine residues, chemokines are now classified into four subfamilies, CXC, CC, XC and CX3C. Given that zebrafish is an important experimental model and teleost fishes constitute an evolutionarily diverse group that forms half the vertebrate species, it would be useful to compare the zebrafish chemokine system with those of mammals. Prior to this study, however, only incomplete lists of the zebrafish chemokine genes were reported. Results: We systematically searched chemokine genes in the zebrafish genome and EST databases, and identified more than 100 chemokine genes. These genes were CXC, CC and XC subfamily members, while no CX3C gene was identified. We also searched chemokine genes in pufferfish fugu and Tetraodon, and found only 18 chemokine genes in each species. The majority of the identified chemokine genes are unique to zebrafish or teleost fishes. However, several groups of chemokines are moderately similar to human chemokines, and some chemokines are orthologous to human homeostatic chemokines CXCL12 and CXCL14. Zebrafish also possesses a novel species-specific subfamily consisting of five members, which we term the CX subfamily. The CX chemokines lack one of the two N-terminus conserved cysteine residues but retain the third and the fourth ones. (Note that the XC subfamily only retains the second and fourth of the signature cysteines residues.) Phylogenetic analysis and genome organization of the chemokine genes showed that successive tandem duplication events generated the CX genes from the CC subfamily. Recombinant CXL-chr24a, one of the CX subfamily members on chromosome 24, showed marked chemotactic activity for carp leukocytes. The mRNA was expressed mainly during a certain period of the embryogenesis, suggesting its role in the zebrafish development. Conclusion: The phylogenic and genomic organization analyses suggest that a substantial number of chemokine genes in zebrafish were generated by zebrafish-specific tandem duplication events. During such duplications, a novel chemokine subfamily termed CX was generated in zebrafish. Only two human chemokines CXCL12 and CXCL14 have the orthologous chemokines in zebrafish. The diversification observed in the numbers and sequences of chemokines in the fish may reflect the adaptation of the individual species to their respective biological environment.",
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T2 - Identification of a novel chemokine subfamily CX

AU - Nomiyama, Hisayuki

AU - Hieshima, Kunio

AU - Osada, Naoki

AU - Kato-Unoki, Yoko

AU - Otsuka-Ono, Kaori

AU - Takegawa, Sumio

AU - Izawa, Toshiaki

AU - Yoshizawa, Akio

AU - Kikuchi, Yutaka

AU - Tanase, Sumio

AU - Miura, Retsu

AU - Kusuda, Jun

AU - Nakao, Miki

AU - Yoshie, Osamu

PY - 2008/5/15

Y1 - 2008/5/15

N2 - Background: The chemokine family plays important roles in cell migration and activation. In humans, at least 44 members are known. Based on the arrangement of the four conserved cysteine residues, chemokines are now classified into four subfamilies, CXC, CC, XC and CX3C. Given that zebrafish is an important experimental model and teleost fishes constitute an evolutionarily diverse group that forms half the vertebrate species, it would be useful to compare the zebrafish chemokine system with those of mammals. Prior to this study, however, only incomplete lists of the zebrafish chemokine genes were reported. Results: We systematically searched chemokine genes in the zebrafish genome and EST databases, and identified more than 100 chemokine genes. These genes were CXC, CC and XC subfamily members, while no CX3C gene was identified. We also searched chemokine genes in pufferfish fugu and Tetraodon, and found only 18 chemokine genes in each species. The majority of the identified chemokine genes are unique to zebrafish or teleost fishes. However, several groups of chemokines are moderately similar to human chemokines, and some chemokines are orthologous to human homeostatic chemokines CXCL12 and CXCL14. Zebrafish also possesses a novel species-specific subfamily consisting of five members, which we term the CX subfamily. The CX chemokines lack one of the two N-terminus conserved cysteine residues but retain the third and the fourth ones. (Note that the XC subfamily only retains the second and fourth of the signature cysteines residues.) Phylogenetic analysis and genome organization of the chemokine genes showed that successive tandem duplication events generated the CX genes from the CC subfamily. Recombinant CXL-chr24a, one of the CX subfamily members on chromosome 24, showed marked chemotactic activity for carp leukocytes. The mRNA was expressed mainly during a certain period of the embryogenesis, suggesting its role in the zebrafish development. Conclusion: The phylogenic and genomic organization analyses suggest that a substantial number of chemokine genes in zebrafish were generated by zebrafish-specific tandem duplication events. During such duplications, a novel chemokine subfamily termed CX was generated in zebrafish. Only two human chemokines CXCL12 and CXCL14 have the orthologous chemokines in zebrafish. The diversification observed in the numbers and sequences of chemokines in the fish may reflect the adaptation of the individual species to their respective biological environment.

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