Skip to main content
NCBI home page
Cell Regulation logoLink to Cell Regulation
. 1991 May;2(5):403–412. doi: 10.1091/mbc.2.5.403

Novel expression pattern of a new member of the MIP-1 family of cytokine-like genes.

A Orlofsky 1, M S Berger 1, M B Prystowsky 1
PMCID: PMC361810  PMID: 1832565

Abstract

Granulocyte/macrophage colony-stimulating factor (GM-CSF) specifically induces the growth of myeloid progenitors and their maturation into neutrophils and macrophages. We have identified a series of previously uncharacterized hematopoietic-specific mRNAs that are expressed in myelopoietic mouse bone marrow cultures stimulated by GM-CSF. One of these messages, C10, encodes a new member of the family of cytokine-like genes related to macrophage inflammatory protein-1 (MIP-1). Members of this family are all induced by one or more stimuli related to inflammation, wound repair, or immune response. In contrast, C10 mRNA showed little or no accumulation in response to such activating agents and was greatly reduced on activation of a T-cell line. On the other hand, C10 mRNA, unlike MIP-1, was acutely stimulated during the first day of bone marrow culture in GM-CSF, and it was also strongly elevated during the induction of neutrophilic differentiation of 32D cl3 cells by granulocyte colony-stimulating factor. The implications of this unusual expression pattern are discussed.

Full text

PDF
403

Images in this article

404Image
on p.404
408Image
on p.408
408Image
on p.408

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arai K. I., Lee F., Miyajima A., Miyatake S., Arai N., Yokota T. Cytokines: coordinators of immune and inflammatory responses. Annu Rev Biochem. 1990;59:783–836. doi: 10.1146/annurev.bi.59.070190.004031. [DOI] [PubMed] [Google Scholar]
  2. Brown K. D., Zurawski S. M., Mosmann T. R., Zurawski G. A family of small inducible proteins secreted by leukocytes are members of a new superfamily that includes leukocyte and fibroblast-derived inflammatory agents, growth factors, and indicators of various activation processes. J Immunol. 1989 Jan 15;142(2):679–687. [PubMed] [Google Scholar]
  3. Broxmeyer H. E., Sherry B., Lu L., Cooper S., Carow C., Wolpe S. D., Cerami A. Myelopoietic enhancing effects of murine macrophage inflammatory proteins 1 and 2 on colony formation in vitro by murine and human bone marrow granulocyte/macrophage progenitor cells. J Exp Med. 1989 Nov 1;170(5):1583–1594. doi: 10.1084/jem.170.5.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Cannistra S. A., Rambaldi A., Spriggs D. R., Herrmann F., Kufe D., Griffin J. D. Human granulocyte-macrophage colony-stimulating factor induces expression of the tumor necrosis factor gene by the U937 cell line and by normal human monocytes. J Clin Invest. 1987 Jun;79(6):1720–1728. doi: 10.1172/JCI113012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cicco N. A., Lindemann A., Content J., Vandenbussche P., Lübbert M., Gauss J., Mertelsmann R., Herrmann F. Inducible production of interleukin-6 by human polymorphonuclear neutrophils: role of granulocyte-macrophage colony-stimulating factor and tumor necrosis factor-alpha. Blood. 1990 May 15;75(10):2049–2052. [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. Davatelis G., Wolpe S. D., Sherry B., Dayer J. M., Chicheportiche R., Cerami A. Macrophage inflammatory protein-1: a prostaglandin-independent endogenous pyrogen. Science. 1989 Feb 24;243(4894 Pt 1):1066–1068. doi: 10.1126/science.2646711. [DOI] [PubMed] [Google Scholar]
  9. Farber J. M. A macrophage mRNA selectively induced by gamma-interferon encodes a member of the platelet factor 4 family of cytokines. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5238–5242. doi: 10.1073/pnas.87.14.5238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  11. Graham G. J., Wright E. G., Hewick R., Wolpe S. D., Wilkie N. M., Donaldson D., Lorimore S., Pragnell I. B. Identification and characterization of an inhibitor of haemopoietic stem cell proliferation. Nature. 1990 Mar 29;344(6265):442–444. doi: 10.1038/344442a0. [DOI] [PubMed] [Google Scholar]
  12. Ihle J. N., Keller J. Interleukin 3 regulation of hematopoietic stem cell differentiation. Prog Clin Biol Res. 1985;184:85–94. [PubMed] [Google Scholar]
  13. Introna M., Bast R. C., Jr, Tannenbaum C. S., Hamilton T. A., Adams D. O. The effect of LPS on expression of the early "competence" genes JE and KC in murine peritoneal macrophages. J Immunol. 1987 Jun 1;138(11):3891–3896. [PubMed] [Google Scholar]
  14. Jaffe B. D., Sabath D. E., Johnson G. D., Moscinski L. C., Johnson K. R., Rovera G., Nauseef W. M., Prystowsky M. B. Myeloperoxidase and oncogene expression in GM-CSF induced bone marrow differentiation. Oncogene. 1988 Feb;2(2):167–174. [PubMed] [Google Scholar]
  15. Kaczmarek L., Calabretta B., Baserga R. Expression of cell-cycle-dependent genes in phytohemagglutinin-stimulated human lymphocytes. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5375–5379. doi: 10.1073/pnas.82.16.5375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kawahara R. S., Deuel T. F. Platelet-derived growth factor-inducible gene JE is a member of a family of small inducible genes related to platelet factor 4. J Biol Chem. 1989 Jan 15;264(2):679–682. [PubMed] [Google Scholar]
  17. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  18. Leonard E. J., Yoshimura T. Human monocyte chemoattractant protein-1 (MCP-1). Immunol Today. 1990 Mar;11(3):97–101. doi: 10.1016/0167-5699(90)90035-8. [DOI] [PubMed] [Google Scholar]
  19. Lindemann A., Riedel D., Oster W., Meuer S. C., Blohm D., Mertelsmann R. H., Herrmann F. Granulocyte/macrophage colony-stimulating factor induces interleukin 1 production by human polymorphonuclear neutrophils. J Immunol. 1988 Feb 1;140(3):837–839. [PubMed] [Google Scholar]
  20. Lipes M. A., Napolitano M., Jeang K. T., Chang N. T., Leonard W. J. Identification, cloning, and characterization of an immune activation gene. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9704–9708. doi: 10.1073/pnas.85.24.9704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Morgan C., Pollard J. W., Stanley E. R. Isolation and characterization of a cloned growth factor dependent macrophage cell line, BAC1.2F5. J Cell Physiol. 1987 Mar;130(3):420–427. doi: 10.1002/jcp.1041300316. [DOI] [PubMed] [Google Scholar]
  23. Moscinski L. C., Prystowsky M. B. Identification of a series of differentiation-associated gene sequences from GM-CSF stimulated bone marrow. Oncogene. 1990 Jan;5(1):31–37. [PubMed] [Google Scholar]
  24. Obaru K., Fukuda M., Maeda S., Shimada K. A cDNA clone used to study mRNA inducible in human tonsillar lymphocytes by a tumor promoter. J Biochem. 1986 Mar;99(3):885–894. doi: 10.1093/oxfordjournals.jbchem.a135549. [DOI] [PubMed] [Google Scholar]
  25. Ohmori Y., Hamilton T. A. A macrophage LPS-inducible early gene encodes the murine homologue of IP-10. Biochem Biophys Res Commun. 1990 May 16;168(3):1261–1267. doi: 10.1016/0006-291x(90)91164-n. [DOI] [PubMed] [Google Scholar]
  26. Orlofsky A., Stanley E. R. CSF-1-induced gene expression in macrophages: dissociation from the mitogenic response. EMBO J. 1987 Oct;6(10):2947–2952. doi: 10.1002/j.1460-2075.1987.tb02599.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reed J. C., Sabath D. E., Hoover R. G., Prystowsky M. B. Recombinant interleukin 2 regulates levels of c-myc mRNA in a cloned murine T lymphocyte. Mol Cell Biol. 1985 Dec;5(12):3361–3368. doi: 10.1128/mcb.5.12.3361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Sabath D. E., Podolin P. L., Comber P. G., Prystowsky M. B. cDNA cloning and characterization of interleukin 2-induced genes in a cloned T helper lymphocyte. J Biol Chem. 1990 Jul 25;265(21):12671–12678. [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. 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]
  34. Shirafuji N., Matsuda S., Ogura H., Tani K., Kodo H., Ozawa K., Nagata S., Asano S., Takaku F. Granulocyte colony-stimulating factor stimulates human mature neutrophilic granulocytes to produce interferon-alpha. Blood. 1990 Jan 1;75(1):17–19. [PubMed] [Google Scholar]
  35. Sporn S. A., Eierman D. F., Johnson C. E., Morris J., Martin G., Ladner M., Haskill S. Monocyte adherence results in selective induction of novel genes sharing homology with mediators of inflammation and tissue repair. J Immunol. 1990 Jun 1;144(11):4434–4441. [PubMed] [Google Scholar]
  36. Tekamp-Olson P., Gallegos C., Bauer D., McClain J., Sherry B., Fabre M., van Deventer S., Cerami A. Cloning and characterization of cDNAs for murine macrophage inflammatory protein 2 and its human homologues. J Exp Med. 1990 Sep 1;172(3):911–919. doi: 10.1084/jem.172.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Valtieri M., Tweardy D. J., Caracciolo D., Johnson K., Mavilio F., Altmann S., Santoli D., Rovera G. Cytokine-dependent granulocytic differentiation. Regulation of proliferative and differentiative responses in a murine progenitor cell line. J Immunol. 1987 Jun 1;138(11):3829–3835. [PubMed] [Google Scholar]
  39. Vanguri P., Farber J. M. Identification of CRG-2. An interferon-inducible mRNA predicted to encode a murine monokine. J Biol Chem. 1990 Sep 5;265(25):15049–15057. [PubMed] [Google Scholar]
  40. Willman C. L., Stewart C. C., Miller V., Yi T. L., Tomasi T. B. Regulation of MHC class II gene expression in macrophages by hematopoietic colony-stimulating factors (CSF). Induction by granulocyte/macrophage CSF and inhibition by CSF-1. J Exp Med. 1989 Nov 1;170(5):1559–1567. doi: 10.1084/jem.170.5.1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wilson S. D., Burd P. R., Billings P. R., Martin C. A., Dorf M. E. The expression and regulation of a potential lymphokine gene (TCA3) in CD4 and CD8 T cell clones. J Immunol. 1988 Sep 1;141(5):1563–1570. [PubMed] [Google Scholar]
  42. 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]
  43. Wolpe S. D., Davatelis G., Sherry B., Beutler B., Hesse D. G., Nguyen H. T., Moldawer L. L., Nathan C. F., Lowry S. F., Cerami A. Macrophages secrete a novel heparin-binding protein with inflammatory and neutrophil chemokinetic properties. J Exp Med. 1988 Feb 1;167(2):570–581. doi: 10.1084/jem.167.2.570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yuo A., Kitagawa S., Ohsaka A., Ohta M., Miyazono K., Okabe T., Urabe A., Saito M., Takaku F. Recombinant human granulocyte colony-stimulating factor as an activator of human granulocytes: potentiation of responses triggered by receptor-mediated agonists and stimulation of C3bi receptor expression and adherence. Blood. 1989 Nov 1;74(6):2144–2149. [PubMed] [Google Scholar]
  45. 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]
  46. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]

Articles from Cell Regulation are provided here courtesy of American Society for Cell Biology

RESOURCES