Defining the Origins and Evolution of the Chemokine/Chemokine Receptor System

Journal of Immunology - Tập 176 Số 1 - Trang 401-415 - 2006
Mark E. DeVries1, Alyson A. Kelvin1, Luoling Xu1, Longsi Ran1, John F. Robinson2, David J. Kelvin1
1*Division of Experimental Therapeutics and Department of Immunology, University of Toronto, Toronto General Research Institute, Toronto General Hospital, University Health Network, Toronto, Ontario, Canada; and
2Robarts Research Institute, London, Ontario, Canada

Tóm tắt

Abstract The chemokine system has a critical role in mammalian immunity, but the evolutionary history of chemokines and chemokine receptors are ill-defined. We used comparative whole genome analysis of fruit fly, sea urchin, sea squirt, pufferfish, zebrafish, frog, and chicken to identify chemokines and chemokine receptors in each species. We report 127 chemokine and 70 chemokine receptor genes in the 7 species, with zebrafish having the most chemokines, 63, and chemokine receptors, 24. Fruit fly, sea urchin, and sea squirt have no identifiable chemokines or chemokine receptors. This study represents the most comprehensive analysis of the chemokine system to date and the only complete characterization of chemokine systems outside of mouse and human. We establish a clear evolutionary model of the chemokine system and trace the origin of the chemokine system to ∼650 million years ago, identifying critical steps in their evolution and demonstrating a more extensive chemokine system in fish than previously thought.

Từ khóa


Tài liệu tham khảo

Schluter, S. F., J. J. Marchalonis. 2003. Cloning of shark RAG2 and characterization of the RAG1/RAG2 gene locus. FASEB J. 17: 470-472.

Flajnik, M. F., M. Kasahara. 2001. Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15: 351-362.

Imler, J. L., L. Zheng. 2004. Biology of Toll receptors: lessons from insects and mammals. J. LeukocyteBiol. 75: 18-26.

Nonaka, M., F. Yoshizaki. 2004. Primitive complement system of invertebrates. Immunol. Rev. 198: 203-215.

Kumar, S., S. B. Hedges. 1998. A molecular timescale for vertebrate evolution. Nature 392: 917-920.

Nikoh, N., N. Iwabe, K. Kuma, M. Ohno, T. Sugiyama, Y. Watanabe, K. Yasui, Z. Shi-cui, K. Hori, Y. Shimura, T. Miyata. 1997. An estimate of divergence time of Parazoa and Eumetazoa and that of Cephalochordata and Vertebrata by aldolase and triose phosphate isomerase clocks. J. Mol. Evol. 45: 97-106.

Cho, C., R. J. Miller. 2002. Chemokine receptors and neural function. J. Neurovirol. 8: 573-584.

Lu, M., E. A. Grove, R. J. Miller. 2002. Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc. Natl. Acad. Sci. USA 99: 7090-7095.

Zou, Y. R., A. H. Kottmann, M. Kuroda, I. Taniuchi, D. R. Littman. 1998. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393: 595-599.

DeVries, M. E., L. Ran, D. J. Kelvin. 1999. On the edge: the physiological and pathophysiological role of chemokines during inflammatory and immunological responses. Semin. Immunol. 11: 95-104.

Belperio, J. A., M. P. Keane, D. A. Arenberg, C. L. Addison, J. E. Ehlert, M. D. Burdick, R. M. Strieter. 2000. CXC chemokines in angiogenesis. J. LeukocyteBiol. 68: 1-8.

Laing, K. J., C. J. Secombes. 2004. Chemokines Dev. Comp. Immunol. 28: 443-444.

Borish, L. C., J. W. Steinke. 2003. Cytokines and chemokines. J. Allergy Clin. Immunol. 111: S460-S475.

Rossi, D., A. Zlotnik. 2000. The biology of chemokines and their receptors. Annu. Rev. Immunol. 18: 217-242.

Fredriksson, R., M. C. Lagerstrom, L. G. Lundin, H. B. Schioth. 2003. The G-protein-coupled receptors in the human genome form five main families: phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63: 1256-1272.

Ma, Q., D. Jones, P. R. Borghesani, R. A. Segal, T. Nagasawa, T. Kishimoto, R. T. Bronson, T. A. Springer. 1998. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 95: 9448-9453.

Du, P. L.. 2004. Innate immunity in early chordates and the appearance of adaptive immunity. C. R. Biol. 327: 591-601.

Rice, P., I. Longden, A. Bleasby. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16: 276-277.

Thompson, J. D., D. G. Higgins, T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.

Strieter, R. M., P. J. Polverini, S. L. Kunkel, D. A. Arenberg, M. D. Burdick, J. Kasper, J. Dzuiba, J. Van Damme, A. Walz, D. Marriott, et al 1995. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J. Biol. Chem. 270: 27348-27357.

Harrison, J. K., Y. Jiang, S. Chen, Y. Xia, D. Maciejewski, R. K. McNamara, W. J. Streit, M. N. Salafranca, S. Adhikari, D. A. Thompson, P. Botti, K. B. Bacon, L. Feng. 1998. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. USA 95: 10896-10901.

Fraticelli, P., M. Sironi, G. Bianchi, D. D’Ambrosio, C. Albanesi, A. Stoppacciaro, M. Chieppa, P. Allavena, L. Ruco, G. Girolomoni, et al 2001. Fractalkine (CX3CL1) as an amplification circuit of polarized Th1 responses. J. Clin. Invest. 107: 1173-1181.

Lucas, A. D., C. Bursill, T. J. Guzik, J. Sadowski, K. M. Channon, D. R. Greaves. 2003. Smooth muscle cells in human atherosclerotic plaques express the fractalkine receptor CX3CR1 and undergo chemotaxis to the CX3C chemokine fractalkine (CX3CL1). Circulation 108: 2498-2504.

Suzuki, G., H. Sawa, Y. Kobayashi, Y. Nakata, K. Nakagawa, A. Uzawa, H. Sakiyama, S. Kakinuma, K. Iwabuchi, K. Nagashima. 1999. Pertussis toxin-sensitive signal controls the trafficking of thymocytes across the corticomedullary junction in the thymus. J. Immunol. 162: 5981-5985.

Doitsidou, M., M. Reichman-Fried, J. Stebler, M. Koprunner, J. Dorries, D. Meyer, C. V. Esguerra, T. Leung, E. Raz. 2002. Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111: 647-659.

Shellenberger, T. D., M. Wang, M. Gujrati, A. Jayakumar, R. M. Strieter, M. D. Burdick, C. G. Ioannides, C. L. Efferson, A. K. El Naggar, D. Roberts, et al 2004. BRAK/CXCL14 is a potent inhibitor of angiogenesis and a chemotactic factor for immature dendritic cells. Cancer Res. 64: 8262-8270.

Kurth, I., K. Willimann, P. Schaerli, T. Hunziker, I. Clark-Lewis, B. Moser. 2001. Monocyte selectivity and tissue localization suggests a role for breast and kidney-expressed chemokine (BRAK) in macrophage development. J. Exp. Med. 194: 855-861.

Shields, D. C.. 2003. Molecular evolution of CXC chemokines and receptors. Trends Immunol. 24: 355

Cui, X., L. F. Lee, W. M. Reed, H. J. Kung, S. M. Reddy. 2004. Marek’s disease virus-encoded vIL-8 gene is involved in early cytolytic infection but dispensable for establishment of latency. J. Virol. 78: 4753-4760.

Parcells, M. S., S. F. Lin, R. L. Dienglewicz, V. Majerciak, D. R. Robinson, H. C. Chen, Z. Wu, G. R. Dubyak, P. Brunovskis, H. D. Hunt, et al 2001. Marek’s disease virus (MDV) encodes an interleukin-8 homolog (vIL-8): characterization of the vIL-8 protein and a vIL-8 deletion mutant MDV. J. Virol. 75: 5159-5173.

Trede, N. S., D. M. Langenau, D. Traver, A. T. Look, L. I. Zon. 2004. The use of zebrafish to understand immunity. Immunity 20: 367-379.

He, C., E. Peatman, P. Baoprasertkul, H. Kucuktas, Z. Liu. 2004. Multiple CC chemokines in channel catfish and blue catfish as revealed by analysis of expressed sequence tags. Immunogenetics 56: 379-387.

Laing, K. J., C. J. Secombes. 2004. Chemokines. Dev. Comp. Immunol. 28: 443-444.

Huising, M. O., R. J. Stet, C. P. Kruiswijk, H. F. Savelkoul, B. M. Lidy Verburg-van Kemenade. 2003. Molecular evolution of CXC chemokines: extant CXC chemokines originate from the CNS. Trends Immunol. 24: 307-313.

Aparicio, S., J. Chapman, E. Stupka, N. Putnam, J. M. Chia, P. Dehal, A. Christoffels, S. Rash, S. Hoon, A. Smit, et al 2002. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297: 1301-1310.

Dehal, P., Y. Satou, R. K. Campbell, J. Chapman, B. Degnan, A. De Tomaso, B. Davidson, A. Di Gregorio, M. Gelpke, D. M. Goodstein, et al 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298: 2157-2167.

Kunwar, P. S., R. Lehmann. 2003. Developmental biology: germ-cell attraction. Nature 421: 226-227.

Angerer, L. M., R. C. Angerer. 2003. Patterning the sea urchin embryo: gene regulatory networks, signaling pathways, and cellular interactions. Curr. Top. Dev. Biol. 53: 159-198.

McLysaght, A., K. Hokamp, K. H. Wolfe. 2002. Extensive genomic duplication during early chordate evolution. Nat. Genet. 31: 200-204.

Schughart, K., C. Kappen, F. H. Ruddle. 1989. Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc. Natl. Acad. Sci. USA 86: 7067-7071.

Kappen, C., F. H. Ruddle. 1993. Evolution of a regulatory gene family: HOM/HOX genes. Curr. Opin. Genet. Dev. 3: 931-938.

Bailey, W. J., J. Kim, G. P. Wagner, F. H. Ruddle. 1997. Phylogenetic reconstruction of vertebrate Hox cluster duplications. Mol. Biol. Evol. 14: 843-853.

Ferrier, D. E., C. Minguillon, P. W. Holland, J. Garcia-Fernandez. 2000. The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14. Evol. Dev. 2: 284-293.

Hughes, A. L., J. da Silva, R. Friedman. 2001. Ancient genome duplications did not structure the human Hox-bearing chromosomes. Genome Res. 11: 771-780.

Force, A., A. Amores, J. H. Postlethwait. 2002. Hox cluster organization in the jawless vertebrate Petromyzon marinus. J. Exp. Zool. 294: 30-46.

Irvine, S. Q., J. L. Carr, W. J. Bailey, K. Kawasaki, N. Shimizu, C. T. Amemiya, F. H. Ruddle. 2002. Genomic analysis of Hox clusters in the sea lamprey Petromyzon marinus. J. Exp. Zool. 294: 47-62.

Hay, D. L., D. M. Smith. 2001. Knockouts and transgenics confirm the importance of adrenomedullin in the vasculature. Trends Pharmacol. Sci. 22: 57-59.

Amores, A., A. Force, Y. L. Yan, L. Joly, C. Amemiya, A. Fritz, R. K. Ho, J. Langeland, V. Prince, Y. L. Wang, et al 1998. Zebrafish hox clusters and vertebrate genome evolution. Science 282: 1711-1714.

Shuai, K., B. Liu. 2003. Regulation of JAK-STAT signalling in the immune system. Nat. Rev. Immunol. 3: 900-911.

Campbell, D. J., G. F. Debes, B. Johnston, E. Wilson, E. C. Butcher. 2003. Targeting T cell responses by selective chemokine receptor expression. Semin. Immunol. 15: 277-286.

Du Pasquier, L.. 2004. Speculations on the origin of the vertebrate immune system. Immunol. Lett. 92: 3-9.

Kuroda, N., T. S. Uinuk-Ool, A. Sato, I. E. Samonte, F. Figueroa, W. E. Mayer, J. Klein. 2003. Identification of chemokines and a chemokine receptor in cichlid fish, shark, and lamprey. Immunogenetics 54: 884-895.

Knaut, H., C. Werz, R. Geisler, C. Nusslein-Volhard. 2003. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421: 279-282.

Hughes, M. K., A. L. Hughes. 1993. Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. Mol. Biol. Evol. 10: 1360-1369.