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. 1992 Dec 1;176(6):1773–1778. doi: 10.1084/jem.176.6.1773

Immunoglobulin E plus antigen challenge induces a novel intercrine/chemokine in mouse mast cells

PMCID: PMC2119461  PMID: 1281219

Abstract

In an attempt to characterize genes participating in the allergic late phase reaction, we have isolated a novel intercrine/chemokine (called MARC) from a cDNA library of the stimulated mouse mast cell line, CPII. As measured by Northern blotting, it is strongly upregulated at the mRNA level after the physiological challenge of the cells with immunoglobulin (Ig)E plus antigen. Unstimulated cells completely lack significant, stable expression, as do a number of other, different cell lines (uninduced and induced) and mouse tissues. In contrast to the Northern blot analysis, a polymerase chain reaction (PCR) analysis, performed on CPII cells and on Percoll gradient purified mouse peritoneal mast cells, revealed a basal level of transcription in the uninduced stage. After 2 h of IgE plus antigen challenge, a quantitative reverse transcriptase-PCR, using a spiked in MIMIC, showed a level of transcripts more than 100-fold higher in the CPII cells and 5-20-fold higher in purified mouse peritoneal cavity mast cells. This rapid induction after the Fc epsilon RI challenge, the identification of the gene as a member of the chemokine family, and its upregulated expression in peritoneal mast cells, all suggest an involvement in certain acute and chronic pathological mast cell-driven diseases.

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Selected References

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  1. Beaumont C., Dugast I., Renaudie F., Souroujon M., Grandchamp B. Transcriptional regulation of ferritin H and L subunits in adult erythroid and liver cells from the mouse. Unambiguous identification of mouse ferritin subunits and in vitro formation of the ferritin shells. J Biol Chem. 1989 May 5;264(13):7498–7504. [PubMed] [Google Scholar]
  2. Burd P. R., Freeman G. J., Wilson S. D., Berman M., DeKruyff R., Billings P. R., Dorf M. E. Cloning and characterization of a novel T cell activation gene. J Immunol. 1987 Nov 1;139(9):3126–3131. [PubMed] [Google Scholar]
  3. Burd P. R., Rogers H. W., Gordon J. R., Martin C. A., Jayaraman S., Wilson S. D., Dvorak A. M., Galli S. J., Dorf M. E. Interleukin 3-dependent and -independent mast cells stimulated with IgE and antigen express multiple cytokines. J Exp Med. 1989 Jul 1;170(1):245–257. doi: 10.1084/jem.170.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Butcher E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 1991 Dec 20;67(6):1033–1036. doi: 10.1016/0092-8674(91)90279-8. [DOI] [PubMed] [Google Scholar]
  5. Caput D., Beutler B., Hartog K., Thayer R., Brown-Shimer S., Cerami A. Identification of a common nucleotide sequence in the 3'-untranslated region of mRNA molecules specifying inflammatory mediators. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1670–1674. doi: 10.1073/pnas.83.6.1670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chang H. C., Hsu F., Freeman G. J., Griffin J. D., Reinherz E. L. Cloning and expression of a gamma-interferon-inducible gene in monocytes: a new member of a cytokine gene family. Int Immunol. 1989;1(4):388–397. doi: 10.1093/intimm/1.4.388. [DOI] [PubMed] [Google Scholar]
  7. Davatelis G., Tekamp-Olson P., Wolpe S. D., Hermsen K., Luedke C., Gallegos C., Coit D., Merryweather J., Cerami A. Cloning and characterization of a cDNA for murine macrophage inflammatory protein (MIP), a novel monokine with inflammatory and chemokinetic properties. J Exp Med. 1988 Jun 1;167(6):1939–1944. doi: 10.1084/jem.167.6.1939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fujimiya H., Nakashima S., Miyata H., Nozawa Y. Effect of a novel antiallergic drug, pemirolast, on activation of rat peritoneal mast cells: inhibition of exocytotic response and membrane phospholipid turnover. Int Arch Allergy Appl Immunol. 1991;96(1):62–67. doi: 10.1159/000235536. [DOI] [PubMed] [Google Scholar]
  9. Gaugitsch H. W., Hofer E., Huber N. E., Schnabl E., Baumruker T. A new superfamily of lymphoid and melanoma cell proteins with extensive homology to Schistosoma mansoni antigen Sm23. Eur J Immunol. 1991 Feb;21(2):377–383. doi: 10.1002/eji.1830210219. [DOI] [PubMed] [Google Scholar]
  10. Gaugitsch H. W., Prieschl E. E., Kalthoff F., Huber N. E., Baumruker T. A novel transiently expressed, integral membrane protein linked to cell activation. Molecular cloning via the rapid degradation signal AUUUA. J Biol Chem. 1992 Jun 5;267(16):11267–11273. [PubMed] [Google Scholar]
  11. Hodgson C. P., Fisk R. Z., Arora P., Chotani M. Nucleotide sequence of mouse virus-like (VL30) retrotransposon BVL-1. Nucleic Acids Res. 1990 Feb 11;18(3):673–673. doi: 10.1093/nar/18.3.673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Irving S. G., Zipfel P. F., Balke J., McBride O. W., Morton C. C., Burd P. R., Siebenlist U., Kelly K. Two inflammatory mediator cytokine genes are closely linked and variably amplified on chromosome 17q. Nucleic Acids Res. 1990 Jun 11;18(11):3261–3270. doi: 10.1093/nar/18.11.3261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Koerner T. J., Hamilton T. A., Introna M., Tannenbaum C. S., Bast R. C., Jr, Adams D. O. The early competence genes JE and KC are differentially regulated in murine peritoneal macrophages in response to lipopolysaccharide. Biochem Biophys Res Commun. 1987 Dec 31;149(3):969–974. doi: 10.1016/0006-291x(87)90503-1. [DOI] [PubMed] [Google Scholar]
  14. Levitt N., Briggs D., Gil A., Proudfoot N. J. Definition of an efficient synthetic poly(A) site. Genes Dev. 1989 Jul;3(7):1019–1025. doi: 10.1101/gad.3.7.1019. [DOI] [PubMed] [Google Scholar]
  15. Miller M. D., Hata S., De Waal Malefyt R., Krangel M. S. A novel polypeptide secreted by activated human T lymphocytes. J Immunol. 1989 Nov 1;143(9):2907–2916. [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Rollins B. J., Stier P., Ernst T., Wong G. G. The human homolog of the JE gene encodes a monocyte secretory protein. Mol Cell Biol. 1989 Nov;9(11):4687–4695. doi: 10.1128/mcb.9.11.4687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schall T. J., Bacon K., Toy K. J., Goeddel D. V. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature. 1990 Oct 18;347(6294):669–671. doi: 10.1038/347669a0. [DOI] [PubMed] [Google Scholar]
  20. Schall T. J. Biology of the RANTES/SIS cytokine family. Cytokine. 1991 May;3(3):165–183. doi: 10.1016/1043-4666(91)90013-4. [DOI] [PubMed] [Google Scholar]
  21. Schall T. J., Jongstra J., Dyer B. J., Jorgensen J., Clayberger C., Davis M. M., Krensky A. M. A human T cell-specific molecule is a member of a new gene family. J Immunol. 1988 Aug 1;141(3):1018–1025. [PubMed] [Google Scholar]
  22. Schall T. J., Simpson N. J., Mak J. Y. Molecular cloning and expression of the murine RANTES cytokine: structural and functional conservation between mouse and man. Eur J Immunol. 1992 Jun;22(6):1477–1481. doi: 10.1002/eji.1830220621. [DOI] [PubMed] [Google Scholar]
  23. Seder R. A., Plaut M., Barbieri S., Urban J., Jr, Finkelman F. D., Paul W. E. Purified Fc epsilon R+ bone marrow and splenic non-B, non-T cells are highly enriched in the capacity to produce IL-4 in response to immobilized IgE, IgG2a, or ionomycin. J Immunol. 1991 Aug 1;147(3):903–909. [PubMed] [Google Scholar]
  24. Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986 Aug 29;46(5):659–667. doi: 10.1016/0092-8674(86)90341-7. [DOI] [PubMed] [Google Scholar]
  25. Sherry B., Tekamp-Olson P., Gallegos C., Bauer D., Davatelis G., Wolpe S. D., Masiarz F., Coit D., Cerami A. Resolution of the two components of macrophage inflammatory protein 1, and cloning and characterization of one of those components, macrophage inflammatory protein 1 beta. J Exp Med. 1988 Dec 1;168(6):2251–2259. doi: 10.1084/jem.168.6.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Stoeckle M. Y., Barker K. A. Two burgeoning families of platelet factor 4-related proteins: mediators of the inflammatory response. New Biol. 1990 Apr;2(4):313–323. [PubMed] [Google Scholar]
  27. Van Damme J., Proost P., Lenaerts J. P., Opdenakker G. Structural and functional identification of two human, tumor-derived monocyte chemotactic proteins (MCP-2 and MCP-3) belonging to the chemokine family. J Exp Med. 1992 Jul 1;176(1):59–65. doi: 10.1084/jem.176.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wodnar-Filipowicz A., Moroni C. Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions. Proc Natl Acad Sci U S A. 1990 Jan;87(2):777–781. doi: 10.1073/pnas.87.2.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Yoshimura T., Yuhki N., Moore S. K., Appella E., Lerman M. I., Leonard E. J. Human monocyte chemoattractant protein-1 (MCP-1). Full-length cDNA cloning, expression in mitogen-stimulated blood mononuclear leukocytes, and sequence similarity to mouse competence gene JE. FEBS Lett. 1989 Feb 27;244(2):487–493. doi: 10.1016/0014-5793(89)80590-3. [DOI] [PubMed] [Google Scholar]
  31. Zipfel P. F., Balke J., Irving S. G., Kelly K., Siebenlist U. Mitogenic activation of human T cells induces two closely related genes which share structural similarities with a new family of secreted factors. J Immunol. 1989 Mar 1;142(5):1582–1590. [PubMed] [Google Scholar]
  32. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

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