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. 1988 Jun;8(6):2402–2410. doi: 10.1128/mcb.8.6.2402

Cloning and expression of two human genes encoding calcium-binding proteins that are regulated during myeloid differentiation.

E Lagasse 1, R G Clerc 1
PMCID: PMC363438  PMID: 3405210

Abstract

The cellular mechanisms involved in chronic inflammatory processes are poorly understood. This is especially true for the role of macrophages, which figure prominently in the inflammatory response. Two proteins, MRP8 and MRP14, which are expressed in infiltrate macrophages during inflammatory reactions but not in normal tissue macrophages, have been characterized. Here we report that MRP8 and MRP14 mRNAs are specifically expressed in human cells of myeloid origin and that their expression is regulated during monocyte-macrophage and granulocyte differentiation. To initiate the analysis of cis-acting elements governing the tissue-specific expression of the MRP genes, we cloned the human genes encoding MRP8 and MRP14. Both genes contain three exons, are single copy, and have a strikingly similar organization. They belong to a novel subfamily of highly homologous calcium-binding proteins which includes S100 alpha, S100 beta, intestinal calcium-binding protein, P11, and calcyclin (2A9). A transient expression assay was devised to investigate the tissue-specific regulatory elements responsible for MRP gene expression after differentiation in leukemia HL60 cells. The results of this investigation demonstrated that the cis-acting elements responsible for MRP expression are present on the cloned DNA fragment containing the MRP gene loci.

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Selected References

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  1. Baba M. L., Goodman M., Berger-Cohn J., Demaille J. G., Matsuda G. The early adaptive evolution of calmodulin. Mol Biol Evol. 1984 Nov;1(6):442–455. doi: 10.1093/oxfordjournals.molbev.a040330. [DOI] [PubMed] [Google Scholar]
  2. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  3. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  4. Brüggen J., Tarcsay L., Cerletti N., Odink K., Rutishauser M., Holländer G., Sorg C. The molecular nature of the cystic fibrosis antigen. Nature. 1988 Feb 18;331(6157):570–570. doi: 10.1038/331570a0. [DOI] [PubMed] [Google Scholar]
  5. Burmeister G., Tarcsay L., Sorg C. Generation and characterization of a monoclonal antibody (1C5) to human migration inhibitory factor (MIF). Immunobiology. 1986 Jul;171(4-5):461–474. doi: 10.1016/S0171-2985(86)80077-8. [DOI] [PubMed] [Google Scholar]
  6. Calabretta B., Battini R., Kaczmarek L., de Riel J. K., Baserga R. Molecular cloning of the cDNA for a growth factor-inducible gene with strong homology to S-100, a calcium-binding protein. J Biol Chem. 1986 Sep 25;261(27):12628–12632. [PubMed] [Google Scholar]
  7. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  8. Collins S. J., Gallo R. C., Gallagher R. E. Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature. 1977 Nov 24;270(5635):347–349. doi: 10.1038/270347a0. [DOI] [PubMed] [Google Scholar]
  9. Collins S. J., Ruscetti F. W., Gallagher R. E., Gallo R. C. Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc Natl Acad Sci U S A. 1978 May;75(5):2458–2462. doi: 10.1073/pnas.75.5.2458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Desplan C., Heidmann O., Lillie J. W., Auffray C., Thomasset M. Sequence of rat intestinal vitamin D-dependent calcium-binding protein derived from a cDNA clone. Evolutionary implications. J Biol Chem. 1983 Nov 25;258(22):13502–13505. [PubMed] [Google Scholar]
  11. Dorin J. R., Novak M., Hill R. E., Brock D. J., Secher D. S., van Heyningen V. A clue to the basic defect in cystic fibrosis from cloning the CF antigen gene. Nature. 1987 Apr 9;326(6113):614–617. doi: 10.1038/326614a0. [DOI] [PubMed] [Google Scholar]
  12. Ferrari S., Calabretta B., deRiel J. K., Battini R., Ghezzo F., Lauret E., Griffin C., Emanuel B. S., Gurrieri F., Baserga R. Structural and functional analysis of a growth-regulated gene, the human calcyclin. J Biol Chem. 1987 Jun 15;262(17):8325–8332. [PubMed] [Google Scholar]
  13. Foecking M. K., Hofstetter H. Powerful and versatile enhancer-promoter unit for mammalian expression vectors. Gene. 1986;45(1):101–105. doi: 10.1016/0378-1119(86)90137-x. [DOI] [PubMed] [Google Scholar]
  14. Fujisawa J., Seiki M., Kiyokawa T., Yoshida M. Functional activation of the long terminal repeat of human T-cell leukemia virus type I by a trans-acting factor. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2277–2281. doi: 10.1073/pnas.82.8.2277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Furutani Y., Notake M., Fukui T., Ohue M., Nomura H., Yamada M., Nakamura S. Complete nucleotide sequence of the gene for human interleukin 1 alpha. Nucleic Acids Res. 1986 Apr 25;14(8):3167–3179. doi: 10.1093/nar/14.8.3167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gerke V., Weber K. The regulatory chain in the p36-kd substrate complex of viral tyrosine-specific protein kinases is related in sequence to the S-100 protein of glial cells. EMBO J. 1985 Nov;4(11):2917–2920. doi: 10.1002/j.1460-2075.1985.tb04023.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gil A., Proudfoot N. J. Position-dependent sequence elements downstream of AAUAAA are required for efficient rabbit beta-globin mRNA 3' end formation. Cell. 1987 May 8;49(3):399–406. doi: 10.1016/0092-8674(87)90292-3. [DOI] [PubMed] [Google Scholar]
  18. Glenney J. R., Jr, Tack B. F. Amino-terminal sequence of p36 and associated p10: identification of the site of tyrosine phosphorylation and homology with S-100. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7884–7888. doi: 10.1073/pnas.82.23.7884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Glisin V., Crkvenjakov R., Byus C. Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry. 1974 Jun 4;13(12):2633–2637. doi: 10.1021/bi00709a025. [DOI] [PubMed] [Google Scholar]
  20. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Harris P., Ralph P. Human leukemic models of myelomonocytic development: a review of the HL-60 and U937 cell lines. J Leukoc Biol. 1985 Apr;37(4):407–422. doi: 10.1002/jlb.37.4.407. [DOI] [PubMed] [Google Scholar]
  22. Hofmann T., Kawakami M., Hitchman A. J., Harrison J. E., Dorrington K. J. The amino acid sequence of porcine intestinal calcium-binding protein. Can J Biochem. 1979 Jun;57(6):737–748. doi: 10.1139/o79-092. [DOI] [PubMed] [Google Scholar]
  23. Isobe T., Ishioka N., Masuda T., Takahashi Y., Ganno S., Okuyama T. A rapid separation of S100 subunits by high performance liquid chromatography: the subunit compositions of S100 proteins. Biochem Int. 1983 Mar;6(3):419–426. [PubMed] [Google Scholar]
  24. Isobe T., Okuyama T. The amino-acid sequence of S-100 protein (PAP I-b protein) and its relation to the calcium-binding proteins. Eur J Biochem. 1978 Sep 1;89(2):379–388. doi: 10.1111/j.1432-1033.1978.tb12539.x. [DOI] [PubMed] [Google Scholar]
  25. Isobe T., Okuyama T. The amino-acid sequence of the alpha subunit in bovine brain S-100a protein. Eur J Biochem. 1981 May;116(1):79–86. doi: 10.1111/j.1432-1033.1981.tb05303.x. [DOI] [PubMed] [Google Scholar]
  26. Jelinek W. R., Schmid C. W. Repetitive sequences in eukaryotic DNA and their expression. Annu Rev Biochem. 1982;51:813–844. doi: 10.1146/annurev.bi.51.070182.004121. [DOI] [PubMed] [Google Scholar]
  27. Jensen R., Marshak D. R., Anderson C., Lukas T. J., Watterson D. M. Characterization of human brain S100 protein fraction: amino acid sequence of S100 beta. J Neurochem. 1985 Sep;45(3):700–705. doi: 10.1111/j.1471-4159.1985.tb04048.x. [DOI] [PubMed] [Google Scholar]
  28. Kretsinger R. H. Structure and evolution of calcium-modulated proteins. CRC Crit Rev Biochem. 1980;8(2):119–174. doi: 10.3109/10409238009105467. [DOI] [PubMed] [Google Scholar]
  29. Krol A., Lund E., Dahlberg J. E. The two embryonic U1 RNA genes of Xenopus laevis have both common and gene-specific transcription signals. EMBO J. 1985 Jun;4(6):1529–1535. doi: 10.1002/j.1460-2075.1985.tb03813.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kuwano R., Usui H., Maeda T., Fukui T., Yamanari N., Ohtsuka E., Ikehara M., Takahashi Y. Molecular cloning and the complete nucleotide sequence of cDNA to mRNA for S-100 protein of rat brain. Nucleic Acids Res. 1984 Oct 11;12(19):7455–7465. doi: 10.1093/nar/12.19.7455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lawn R. M., Fritsch E. F., Parker R. C., Blake G., Maniatis T. The isolation and characterization of linked delta- and beta-globin genes from a cloned library of human DNA. Cell. 1978 Dec;15(4):1157–1174. doi: 10.1016/0092-8674(78)90043-0. [DOI] [PubMed] [Google Scholar]
  32. MacManus J. P., Watson D. C., Yaguchi M. The purification and complete amino acid sequence of the 9000-Mr Ca2+-binding protein from rat placenta. Identity with the vitamin D-dependent intestinal Ca2+-binding protein. Biochem J. 1986 Apr 15;235(2):585–595. doi: 10.1042/bj2350585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. McPherson M. A., Dormer R. L., Bradbury N. A., Dodge J. A., Goodchild M. C. Defective beta-adrenergic secretory responses in submandibular acinar cells from cystic fibrosis patients. Lancet. 1986 Nov 1;2(8514):1007–1008. doi: 10.1016/s0140-6736(86)92616-4. [DOI] [PubMed] [Google Scholar]
  34. Michels E., Stenzinger W., Sorg C. Functional characteristics of murine macrophages responding to migration inhibitory factors. Eur J Immunol. 1984 Oct;14(10):902–905. doi: 10.1002/eji.1830141008. [DOI] [PubMed] [Google Scholar]
  35. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Murao S., Gemmell M. A., Callaham M. F., Anderson N. L., Huberman E. Control of macrophage cell differentiation in human promyelocytic HL-60 leukemia cells by 1,25-dihydroxyvitamin D3 and phorbol-12-myristate-13-acetate. Cancer Res. 1983 Oct;43(10):4989–4996. [PubMed] [Google Scholar]
  37. Nathans J., Hogness D. S. Isolation and nucleotide sequence of the gene encoding human rhodopsin. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4851–4855. doi: 10.1073/pnas.81.15.4851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Naylor L. H., Lilley D. M., van de Sande J. H. Stress-induced cruciform formation in a cloned d(CATG)10 sequence. EMBO J. 1986 Sep;5(9):2407–2413. doi: 10.1002/j.1460-2075.1986.tb04511.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nielsen P. J., McMaster G. K., Trachsel H. Cloning of eukaryotic protein synthesis initiation factor genes: isolation and characterization of cDNA clones encoding factor eIF-4A. Nucleic Acids Res. 1985 Oct 11;13(19):6867–6880. doi: 10.1093/nar/13.19.6867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nordheim A., Rich A. Negatively supercoiled simian virus 40 DNA contains Z-DNA segments within transcriptional enhancer sequences. Nature. 1983 Jun 23;303(5919):674–679. doi: 10.1038/303674a0. [DOI] [PubMed] [Google Scholar]
  41. Odink K., Cerletti N., Brüggen J., Clerc R. G., Tarcsay L., Zwadlo G., Gerhards G., Schlegel R., Sorg C. Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature. 1987 Nov 5;330(6143):80–82. doi: 10.1038/330080a0. [DOI] [PubMed] [Google Scholar]
  42. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  43. Ruskin B., Krainer A. R., Maniatis T., Green M. R. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell. 1984 Aug;38(1):317–331. doi: 10.1016/0092-8674(84)90553-1. [DOI] [PubMed] [Google Scholar]
  44. Sharp P. A. Speculations on RNA splicing. Cell. 1981 Mar;23(3):643–646. doi: 10.1016/0092-8674(81)90425-6. [DOI] [PubMed] [Google Scholar]
  45. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  46. Sundström C., Nilsson K. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int J Cancer. 1976 May 15;17(5):565–577. doi: 10.1002/ijc.2910170504. [DOI] [PubMed] [Google Scholar]
  47. Sussman D. J., Milman G. Short-term, high-efficiency expression of transfected DNA. Mol Cell Biol. 1984 Aug;4(8):1641–1643. doi: 10.1128/mcb.4.8.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Szebenyi D. M., Obendorf S. K., Moffat K. Structure of vitamin D-dependent calcium-binding protein from bovine intestine. Nature. 1981 Nov 26;294(5839):327–332. doi: 10.1038/294327a0. [DOI] [PubMed] [Google Scholar]

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