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. 1994 Mar 29;91(7):2752–2756. doi: 10.1073/pnas.91.7.2752

Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyl-terminal tails.

I F Charo 1, S J Myers 1, A Herman 1, C Franci 1, A J Connolly 1, S R Coughlin 1
PMCID: PMC43448  PMID: 8146186

Abstract

Monocyte chemoattractant protein 1 (MCP-1) is a member of the chemokine family of cytokines that mediate leukocyte chemotaxis. The potent and specific activation of monocytes by MCP-1 may mediate the monocytic infiltration of tissues in atherosclerosis and other inflammatory diseases. We have isolated cDNAs that encode two MCP-1-specific receptors with alternatively spliced carboxyl tails. Expression of the receptors in Xenopus oocytes conferred robust mobilization of intracellular calcium in response to nanomolar concentrations of MCP-1 but not to related chemokines. The MCP-1 receptors are most closely related to the receptor for the chemokines macrophage inflammatory protein 1 alpha and RANTES (regulated on activation, normal T expressed and secreted). The identification of the MCP-1 receptor and cloning of two distinct isoforms provide powerful tools for understanding the specificity and signaling mechanisms of this important chemokine.

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Selected References

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  1. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  2. Cushing S. D., Berliner J. A., Valente A. J., Territo M. C., Navab M., Parhami F., Gerrity R., Schwartz C. J., Fogelman A. M. Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc Natl Acad Sci U S A. 1990 Jul;87(13):5134–5138. doi: 10.1073/pnas.87.13.5134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dohlman H. G., Thorner J., Caron M. G., Lefkowitz R. J. Model systems for the study of seven-transmembrane-segment receptors. Annu Rev Biochem. 1991;60:653–688. doi: 10.1146/annurev.bi.60.070191.003253. [DOI] [PubMed] [Google Scholar]
  4. Franke R. R., König B., Sakmar T. P., Khorana H. G., Hofmann K. P. Rhodopsin mutants that bind but fail to activate transducin. Science. 1990 Oct 5;250(4977):123–125. doi: 10.1126/science.2218504. [DOI] [PubMed] [Google Scholar]
  5. Furutani Y., Nomura H., Notake M., Oyamada Y., Fukui T., Yamada M., Larsen C. G., Oppenheim J. J., Matsushima K. Cloning and sequencing of the cDNA for human monocyte chemotactic and activating factor (MCAF). Biochem Biophys Res Commun. 1989 Feb 28;159(1):249–255. doi: 10.1016/0006-291x(89)92430-3. [DOI] [PubMed] [Google Scholar]
  6. Gao J. L., Kuhns D. B., Tiffany H. L., McDermott D., Li X., Francke U., Murphy P. M. Structure and functional expression of the human macrophage inflammatory protein 1 alpha/RANTES receptor. J Exp Med. 1993 May 1;177(5):1421–1427. doi: 10.1084/jem.177.5.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gayle R. B., 3rd, Sleath P. R., Srinivason S., Birks C. W., Weerawarna K. S., Cerretti D. P., Kozlosky C. J., Nelson N., Vanden Bos T., Beckmann M. P. Importance of the amino terminus of the interleukin-8 receptor in ligand interactions. J Biol Chem. 1993 Apr 5;268(10):7283–7289. [PubMed] [Google Scholar]
  8. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  9. Holmes W. E., Lee J., Kuang W. J., Rice G. C., Wood W. I. Structure and functional expression of a human interleukin-8 receptor. Science. 1991 Sep 13;253(5025):1278–1280. doi: 10.1126/science.1840701. [DOI] [PubMed] [Google Scholar]
  10. Jones M. L., Mulligan M. S., Flory C. M., Ward P. A., Warren J. S. Potential role of monocyte chemoattractant protein 1/JE in monocyte/macrophage-dependent IgA immune complex alveolitis in the rat. J Immunol. 1992 Sep 15;149(6):2147–2154. [PubMed] [Google Scholar]
  11. Koch A. E., Kunkel S. L., Harlow L. A., Johnson B., Evanoff H. L., Haines G. K., Burdick M. D., Pope R. M., Strieter R. M. Enhanced production of monocyte chemoattractant protein-1 in rheumatoid arthritis. J Clin Invest. 1992 Sep;90(3):772–779. doi: 10.1172/JCI115950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kozak M. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 1987 Oct 26;15(20):8125–8148. doi: 10.1093/nar/15.20.8125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lee J., Horuk R., Rice G. C., Bennett G. L., Camerato T., Wood W. I. Characterization of two high affinity human interleukin-8 receptors. J Biol Chem. 1992 Aug 15;267(23):16283–16287. [PubMed] [Google Scholar]
  14. Moser B., Schumacher C., von Tscharner V., Clark-Lewis I., Baggiolini M. Neutrophil-activating peptide 2 and gro/melanoma growth-stimulatory activity interact with neutrophil-activating peptide 1/interleukin 8 receptors on human neutrophils. J Biol Chem. 1991 Jun 5;266(16):10666–10671. [PubMed] [Google Scholar]
  15. Murphy P. M., Tiffany H. L. Cloning of complementary DNA encoding a functional human interleukin-8 receptor. Science. 1991 Sep 13;253(5025):1280–1283. doi: 10.1126/science.1891716. [DOI] [PubMed] [Google Scholar]
  16. Namba T., Sugimoto Y., Negishi M., Irie A., Ushikubi F., Kakizuka A., Ito S., Ichikawa A., Narumiya S. Alternative splicing of C-terminal tail of prostaglandin E receptor subtype EP3 determines G-protein specificity. Nature. 1993 Sep 9;365(6442):166–170. doi: 10.1038/365166a0. [DOI] [PubMed] [Google Scholar]
  17. Nelken N. A., Coughlin S. R., Gordon D., Wilcox J. N. Monocyte chemoattractant protein-1 in human atheromatous plaques. J Clin Invest. 1991 Oct;88(4):1121–1127. doi: 10.1172/JCI115411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Neote K., DiGregorio D., Mak J. Y., Horuk R., Schall T. J. Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell. 1993 Feb 12;72(3):415–425. doi: 10.1016/0092-8674(93)90118-a. [DOI] [PubMed] [Google Scholar]
  19. Oppenheim J. J., Zachariae C. O., Mukaida N., Matsushima K. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu Rev Immunol. 1991;9:617–648. doi: 10.1146/annurev.iy.09.040191.003153. [DOI] [PubMed] [Google Scholar]
  20. Rollins B. J., Morrison E. D., Stiles C. D. Cloning and expression of JE, a gene inducible by platelet-derived growth factor and whose product has cytokine-like properties. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3738–3742. doi: 10.1073/pnas.85.11.3738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rollins B. J., Sunday M. E. Suppression of tumor formation in vivo by expression of the JE gene in malignant cells. Mol Cell Biol. 1991 Jun;11(6):3125–3131. doi: 10.1128/mcb.11.6.3125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rollins B. J., Yoshimura T., Leonard E. J., Pober J. S. Cytokine-activated human endothelial cells synthesize and secrete a monocyte chemoattractant, MCP-1/JE. Am J Pathol. 1990 Jun;136(6):1229–1233. [PMC free article] [PubMed] [Google Scholar]
  23. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993 Apr 29;362(6423):801–809. doi: 10.1038/362801a0. [DOI] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Van Riper G., Siciliano S., Fischer P. A., Meurer R., Springer M. S., Rosen H. Characterization and species distribution of high affinity GTP-coupled receptors for human rantes and monocyte chemoattractant protein 1. J Exp Med. 1993 Mar 1;177(3):851–856. doi: 10.1084/jem.177.3.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Vu T. K., Hung D. T., Wheaton V. I., Coughlin S. R. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell. 1991 Mar 22;64(6):1057–1068. doi: 10.1016/0092-8674(91)90261-v. [DOI] [PubMed] [Google Scholar]
  27. Wadsworth H. L., Chazenbalk G. D., Nagayama Y., Russo D., Rapoport B. An insertion in the human thyrotropin receptor critical for high affinity hormone binding. Science. 1990 Sep 21;249(4975):1423–1425. doi: 10.1126/science.2169649. [DOI] [PubMed] [Google Scholar]
  28. Walter S., Bottazzi B., Govoni D., Colotta F., Mantovani A. Macrophage infiltration and growth of sarcoma clones expressing different amounts of monocyte chemotactic protein/JE. Int J Cancer. 1991 Sep 30;49(3):431–435. doi: 10.1002/ijc.2910490321. [DOI] [PubMed] [Google Scholar]
  29. Wang J. M., McVicar D. W., Oppenheim J. J., Kelvin D. J. Identification of RANTES receptors on human monocytic cells: competition for binding and desensitization by homologous chemotactic cytokines. J Exp Med. 1993 Mar 1;177(3):699–705. doi: 10.1084/jem.177.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wang J. M., Sica A., Peri G., Walter S., Padura I. M., Libby P., Ceska M., Lindley I., Colotta F., Mantovani A. Expression of monocyte chemotactic protein and interleukin-8 by cytokine-activated human vascular smooth muscle cells. Arterioscler Thromb. 1991 Sep-Oct;11(5):1166–1174. doi: 10.1161/01.atv.11.5.1166. [DOI] [PubMed] [Google Scholar]
  31. Weber C., Aepfelbacher M., Haag H., Ziegler-Heitbrock H. W., Weber P. C. Tumor necrosis factor induces enhanced responses to platelet-activating factor and differentiation in human monocytic Mono Mac 6 cells. Eur J Immunol. 1993 Apr;23(4):852–859. doi: 10.1002/eji.1830230413. [DOI] [PubMed] [Google Scholar]
  32. Wolpe S. D., Cerami A. Macrophage inflammatory proteins 1 and 2: members of a novel superfamily of cytokines. FASEB J. 1989 Dec;3(14):2565–2573. doi: 10.1096/fasebj.3.14.2687068. [DOI] [PubMed] [Google Scholar]
  33. Ylä-Herttuala S., Lipton B. A., Rosenfeld M. E., Särkioja T., Yoshimura T., Leonard E. J., Witztum J. L., Steinberg D. Expression of monocyte chemoattractant protein 1 in macrophage-rich areas of human and rabbit atherosclerotic lesions. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5252–5256. doi: 10.1073/pnas.88.12.5252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yoshimura T., Leonard E. J. Identification of high affinity receptors for human monocyte chemoattractant protein-1 on human monocytes. J Immunol. 1990 Jul 1;145(1):292–297. [PubMed] [Google Scholar]
  35. Yoshimura T., Robinson E. A., Tanaka S., Appella E., Kuratsu J., Leonard E. J. Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med. 1989 Apr 1;169(4):1449–1459. doi: 10.1084/jem.169.4.1449. [DOI] [PMC free article] [PubMed] [Google Scholar]

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