Cloning, Expression, Cellular Distribution, and Role in Chemotaxis of a C5a Receptor in Rainbow Trout: The First Identification of a C5a Receptor in a Nonmammalian Species

Journal of Immunology

Volumn 172, Issue 7, 2004, Pages 4381-4390

  Boshra, Hani ^a   Li, Jun ^a   Peters, Rodney ^a   Hansen, John ^b   Matlapudi, Anjan ^a   Sunyer, J Oriol ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^c UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHYLATOXIN; ANTIBODY; CHEMOATTRACTANT; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C4A; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENTARY DNA;

AMINO TERMINAL SEQUENCE; ARTICLE; B LYMPHOCYTE; CELLULAR DISTRIBUTION; COMPLEMENT ACTIVATION; DNA ISOLATION; DNA SEQUENCE; EXON; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC CONSERVATION; GENOME; GRANULOCYTE; INFLAMMATION; MOLECULAR CLONING; MOLECULAR EVOLUTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DOMAIN; RAINBOW TROUT; RECEPTOR BINDING; SEQUENCE HOMOLOGY; TELEOST;

EID: 1642364114     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.7.4381     Document Type: Article

References (71)

1. Hugli, T. E. 1984. Structure and function of the anaphylatoxins. Springer Semin. Immunopathol. 7:193.
2. Ember, J. A., and T. E. Hugli. 1997. Complement factors and their receptors. Immunopharmacology 38:3.
3. Kohl, J. 2001. Anaphylatoxins and infectious and non-infectious inflammatory diseases. Mol. Immunol. 38:175.
4. Daffem, P. J., P. H. Pfeifer, J. A. Ember, and T. E. Hugli. 1995. C3a is a chemotaxin for human eosinophils but not for neutrophils. I. C3a stimulation of neutrophils is secondary to eosinophil activation. J. Exp. Med. 181:2119.
5. Giembycz, M. A., M. A. Lindsay, P. G. Hellewell, and K. Hartmann. 1997. C3a and C5a stimulate chemotaxis of human mast cells. Blood 89:4566.
6. Ehrengruber, M. U., T. Geiser, and D. A. Deranleau. 1994. Activation of human neutrophils by C3a and C5A: comparison of the effects on shape changes, chemotaxis, secretion, and respiratory burst. FEBS Lett. 346:181.
7. Kacani, L., Z. Banki, J. Zwirner, H. Schennach, Z. Bajtay, A. Erdei, H. Stoiber, and M. P. Dierich. 2001. C5a and C5a(desArg) enhance the susceptibility of monocyte-derived macrophages to HIV infection. J. Immunol. 166:3410.
8. Monsinjon, T., P. Gasque, P. Chan, A. Ischenko, J. J. Brady, and M. C. Fontaine. 2003. Regulation by complement C3a and C5a anaphylatoxins of cytokine production in human umbilical vein endothelial cells. FASEB J. 17:1003.
9. Taylor, J. S., M. J. Thomas, and G. L. Stahl. 1998. Eicosanoid production from porcine neutrophils and platelets: differential production with various agonists. J. Biol. Chem. 273:32535.
10. Johnson, A. R., T. E. Hugli, and H. J. Muller-Eberhard. 1975. Release of histamine from rat mast cells by the complement peptides C3a and C5a. Immunology 28:1067.
11. Schulman, E. S., T. J. Post, P. M. Henson, and P. C. Giclas. 1988. Differential effects of the complement peptides, C5a and C5a des Arg on human basophil and lung mast cell histamine release. J. Clin. Invest. 81:918.
12. Scieszka, J. F., L. L. Maggiora, S. D. Wright, and M. J. Cho. 1991. Role of complements C3 and C5 in the phagocytosis of liposomes by human neutrophils. Pharm. Res. 8:65.
13. Mollnes, T. E., O. L. Brekke, M. Fung, H. Fure, D. Christiansen, G. Bergseth, V. Videm, K. T. Lappegard, J. Kohl, and J. D. Lambris. 2002. Essential role of the C5a receptor in E. coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. [Published erratum appears in 2002 Blood 100:2691]. Blood 100:1869.
14. Mollnes, T. E., O. L. Brekke, M. Fung, H. Fure, D. Christiansen, G. Bergseth, V. Videm, K. T. Lappegard, J. Kohl, and J. D. Lambris. 2002. Essential role of the C5a receptor in E. coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. [Published erratum appears in 2002 Blood 100:2691]. Blood 100:1869.
15. Mulligan, M. S., E. Schmid, G. O. Till, T. E. Hugli, H. P. Friedl, R. A. Roth, and P. A. Ward. 1997. C5a-dependent up-regulation in vivo of lung vascular P-selectin. J. Immunol. 158:1857.
16. Tempero, R. M., M. A. Hollingsworth, M. D. Burdick, A. M. Finch, S. M. Taylor, S. M. Vogen, E. L. Morgan, and S. D. Sanderson. 1997. Molecular adjuvant effects of a conformationally biased agonist of human C5a anaphylatoxin. J. Immunol. 158:1377.
17. Ulrich, J. T., W. Cieplak, N. J. Paczkowski, S. M. Taylor, and S. D. Sanderson. 2000. Induction of an antigen-specific CTL response by a conformationally biased agonist of human C5a anaphylatoxin as a molecular adjuvant. J. Immunol. 164:5492.
18. 2-terminal domain. J. Immunol. 151:3785.
19. Nataf, S., N. Davoust, R. S. Ames, and S. R. Barnum. 1999. Human T cells express the C5a receptor and are chemoattracted to C5a. J. Immunol. 162:4018.
20. Wetsel, R. A. 1995. Expression of the complement C5a anaphylatoxin receptor (C5aR) on non-myeloid cells. Immunol. Lett. 44:183.
21. Jones, J., S. R. Whittemore, D. L. Haviland, R. A. Wetsel, and S. R. Barnum. 1995. Expression of the complement C5a anaphylatoxin receptor (C5aR) on nonmyeloid cells. J. Neuroimmunol. 61:71.
22. Haviland, D. L., R. L. McCoy, W. T. Whitehead, H. Akama, E. P. Molmenti, A. Brown, J. C. Haviland, W. C. Parks, D. H. Perlmutter, and R. A. Wetsel. 1995. Cellular expression of the C5a anaphylatoxin receptor (C5aR): demonstration of C5aR on nonmyeloid cells of the liver and lung. J. Immunol. 154:1861.
23. Gerard, N. P., and C. Gerard. 1991. The chemotactic receptor for human C5a anaphylatoxin. Nature 349:614.
24. Gerard, C., L. Bao, O. Orozco, M. Pearson, D. Kunz, and N. P. Gerard. 1992. Structural diversity in the extracellular faces of peptidergic G-protein-coupled receptors: molecular cloning of the mouse C5a anaphylatoxin receptor. J. Immunol. 149:2600.
25. Akatsu, H., T. Miwa, C. Sakurada, Y. Fukuoka, J. A. Ember, T. Yamamoto, T. E. Hugli, and H. Okada. 1997. CDNA cloning and characterization of rat C5a anaphylatoxin receptor. Microbiol. Immunol. 41:575.
26. Fukuoka, Y., J. A. Ember, A. Yasui, and T. E. Hugli. 1998. Cloning and characterization of the guinea pig C5a anaphylatoxin receptor: interspecies diversity among the C5a receptors. Int. Immunol. 10:275.
27. Youker, K. A., L. H. Michael, A. G. Kumar, C. M. Ballantyne, C. W. Smith, M. L. Entman, and J. J. Perret. 1995. Cloning and functional expression of the canine anaphylatoxin C5a receptor: evidence for high interspecies variability. Mol. Cell. Biochem. 147:5.
28. Bachvarov, D. R., S. Houle, M. Bachvarova, J. Bouthillier, S. A. St. Pierre, Y. Fukuoka, J. A. Ember, and F. Marceau. 1999. Cloning and preliminary pharmacological characterization of the anaphylatoxin C5a receptor in the rabbit. Br. J. Pharmacol. 128:321.
29. Ohno, M., T. Hirata, M. Enomoto, T. Araki, H. Ishimaru, and T. A. Takahashi. 2000. A putative chemoattractant receptor, C5L2, is expressed in granulocyte and immature dendritic cells, but not in mature dendritic cells. Mol. Immunol. 37:407.
30. Okinaga, S., D. Slattery, A. Humbles, Z. Zsengeller, O. Morteau, M. B. Kinrade, T. M. Brodbeck, J. E. Krause, H. R. Choe, N. P. Gerard, et al. 2003. C5L2, a nonsignaling C5A binding protein. Biochemistry 42:9406.
31. 74. J. Biol. Chem. 277:7165.
32. 77/acylation-stimulating protein. J. Biol. Chem. 278:11123.
33. Al-Sharif, W. Z., J. O. Sunyer, J. D. Lambris, and L. C. Smith. 1998. Sea urchin coelomocytes specifically express a homologue of the complement component C3. J. Immunol. 160:2983.
34. Smith, L. C., L. A. Clow, and D. P. Terwilliger. 2001. The ancestral complement system in sea urchins. Immunol. Rev. 180:16.
35. Smith, L. C., K. Azumi, and M. Nonaka. 1999. Complement systems in invertebrates: the ancient alternative and lectin pathways. Immunopharmacology 42:107.
36. Nonaka, M. 2001. Evolution of the complement system. Curr. Opin. Immunol. 13:69.
37. Sunyer, J. O., and J. D. Lambris. 1998. Evolution and diversity of the complement system of poikilothermic vertebrates. Immunol. Rev. 166:39.
38. Nonaka, M., and S. L. Smith. 2000. Complement system of bony and cartilaginous fish. Fish Shellfish Immunol. 10:215.
39. Sunyer, J. O., I. K. Zarkadis, A. Sahu, and J. D. Lambris. 1996. Multiple forms of complement C3 in trout that differ in binding to complement activators. Proc. Natl. Acad. Sci. USA 93:8546.
40. Sunyer, J. O., L. Tort, and J. D. Lambris. 1997. Diversity of the third form of complement, C3, in fish: functional characterization of five forms of C3 in the diploid fish Sparus aurora. Biochem J. 326:877.
41. Sunyer, J. O., L. Tort, and J. D. Lambris. 1997. Structural C3 diversity in fish: characterization of five forms of C3 in the diploid fish Sparus aurata. J. Immunol. 158:2813.
42. Sunyer, J. O., I. K. Zarkadis, and J. D. Lambris. 1998. Complement diversity: a mechanism for generating immune diversity? Immunol. Today 19:519.
43. Kuroda, N., K. Naruse, A. Shima, M. Nonaka, and M. Sasaki. 2000. Molecular cloning and linkage analysis of complement C3 and C4 genes of the Japanese medaka fish. Immunogenetics 51:117.
44. Nakao, M., J. Mutsuro, R. Obo, K. Fujiki, M. Nonaka, and T. Yano. 2000. Molecular cloning and protein analysis of divergent forms of the complement component C3 from a bony fish, the common carp (Cyprinus carpio): presence of variants lacking the catalytic histidine. Eur. J. Immunol. 30:858.
45. Zarkadis, I. K., M. R. Sarrias, G. Sfyroera, J. O. Sunyer, and J. D. Lambris. 2001. Cloning and structure of three rainbow trout C3 molecules: a plausible explanation for their functional diversity. Dev. Comp. Immunol. 25:11.
46. Nonaka, M., M. Irie, K. Tanabe, T. Kaidoh, S. Natsuume-Sakai, and M. Takahashi. 1985. Identification and characterization of a variant of the third component of complement (C3) in rainbow trout (Salmo gairdneri) serum. J. Biol. Chem. 260:809.
47. Sunyer, J. O., H. Boshra, G. Lorenzo, D. Parra, B. Freedman, and N. Bosch. 2003. Evolution of complement as an effector system in innate and adaptive immunity. Immunol. Res. 27:549.
48. Nonaka, M., S. Natsuume-Sakai, and M. Takahashi. 1981. The complement system in rainbow trout (Salmo gairdneri). II. Purification and characterization of the fifth component (C5). J. Immunol. 126:1495.
49. Franchini, S., I. K. Zarkadis, G. Sfyroera, A. Sahu, W. T. Moore, D. Mastellos, S. E. LaPatra, and J. D. Lambris. 2001. Cloning and purification of the rainbow trout fifth component of complement (C5). Dev. Comp. Immunol. 25:419.
50. Hamdani, S. H., D. N. McMillan, E. F. Pettersen, H. Wergeland, C. Endresen, A. E. Ellis, and C. J. Secombes. 1998. Isolation of rainbow trout neutrophils with an anti-granulocyte monoclonal antibody. Vet. Immunol. Immunopathol. 63:369.
51. Smith, S. L. 1998. Shark complement: an assessment. Immunol. Rev. 166:67.
52. Kato, Y., M. Nakao, J. Mutsuro, I. K. Zarkadis, and T. Yano. 2003. The complement component C5 of the common carp (Cyprinus carpio): cDNA cloning of two distinct isotypes that differ in a functional site. Immunogenetics 54:807.
53. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876.
54. K, H., and W. Stoffel. 1993. TMbase: a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 374:166.
55. Hansen, J. D., P. Strassburger, and L. Du Pasquier. 1997. Conservation of a master hematopoietic switch gene during vertebrate evolution: isolation and characterization of Ikaros from teleost and amphibian species. Eur. J. Immunol. 27:3049.
56. Antrum, R. M., and J. S. Solomkin. 1985. Regulation of monocyte function by complement activation products. J. Surg. Res. 38:468.
57. Fletcher, M. P., G. L. Stahl, and J. C. Longhurst. 1990. In vivo and in vitro assessment of porcine neutrophil activation responses to chemoattractants: flow cytometric evidence for the selective absence of formyl peptide receptors. J. Leukocyte Biol. 47:355.
58. Gerard, C., and N. P. Gerard. 1994. C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu. Rev. Immunol. 12:775.
59. Cain, S. A., T. Coughlan, and P. N. Monk. 2001. Mapping the ligand-binding site on the C5a receptor: arginine 74 of C5a contacts aspartate 282 of the C5a receptor. Biochemistry 40:14047.
60. Chen, Z., X. Zhang, N. C. Gonnella, T. C. Pellas, W. C. Boyar, and F. Ni. 1998. Residues 21-30 within the extracellular N-terminal region of the C5a receptor represent a binding domain for the C5a anaphylatoxin. J. Biol. Chem. 273:10411.
61. Huber-Lang, M. S., J. V. Sarma, S. R. McGuire, K. T. Lu, V. A. Padgaonkar, E. M. Younkin, R. F. Guo, C. H. Weber, E. R. Zuiderweg, F. S. Zetoune, et al. 2003. Structure-function relationships of human C5a and C5aR. J. Immunol. 170:6115.
62. Laudes, I. J., J. C. Chu, M. Huber-Lang, R. F. Guo, N. C. Riedemann, J. V. Sarma, F. Mahdi, H. S. Murphy, C. Speyer, K. T. Lu, et al. 2002. Expression and function of C5a receptor in mouse microvascular endothelial cells. J. Immunol. 169:5962.
63. Morgan, E. L., J. A. Ember, S. D. Sanderson, W. Scholz, R. Buchner, R. D. Ye, and T. E. Hugli. 1993. Anti-C5a receptor antibodies: characterization of neutralizing antibodies specific for a peptide, C5aR-(9-29), derived from the predicted amino-terminal sequence of the human C5a receptor. J. Immunol. 151:377.
64. Werfel, T., M. Oppermann, J. H. Butterfield, G. Begemann, J. Elsner, O. Gotze, and J. Zwirner. 1996. The human mast cell line HMC-1 expresses C5a receptors and responds to C5a but not to C5a(desArg). Scand. J. Immunol. 44:30.
65. DeLuca, D., M. Wilson, and G. W. Warr. 1983. Lymphocyte heterogeneity in the trout, Salmo gairdneri, defined with monoclonal antibodies to IgM. Eur. J. Immunol. 13:546.
66. Jansson, E., K. O. Gronvik, A. Johannisson, K. Naslund, E. Westergren, and L. Pilstrom. 2003. Monoclonal antibodies to lymphocytes of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 14:239.
67. Kfoury, J. R., A. Kuroda, C. Nakayasu, H. Fukuda, and N. Okamoto. 1999. Analysis of rainbow trout peripheral blood leucocytes separated by flow cytometry cell sorting. Fish Pathol. 34:1.
68. Watanabe, H., M. Kuraya, R. Kasukawa, H. Yanagisawa, M. Yanagisawa, and T. Fujita. 1995. Analysis of C5a receptor by monoclonal antibody. J. Immunol. Methods 185:19.
69. Ottonello, L., A. Corcione, G. Tortolina, I. Airoldi, E. Albesiano, A. Favre, R. D'Agostino, F. Malavasi, V. Pistoia, and F. Dallegri. 1999. rC5a directs the in vitro migration of human memory and naive tonsillar B lymphocytes: implications for B cell trafficking in secondary lymphoid tissues. J. Immunol. 162:6510.
70. Soruri, A., S. Kim, Z. Kiafard, and J. Zwirner. 2003. Characterization of C5aR expression on murine myeloid and lymphoid cells by the use of a novel monoclonal antibody. Immunol. Lett. 88:47.
71. Rottllant, J., D. Parra, R. Peters, H. Boshra, and J. O. Sunyer. Generation, purification and functional characterization of three C3a anaphylatoxins in rainbow trout: role in leukocyte chemotaxis and respiratory burst. Dev. Comp. Immunol. In press.