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. 1989 Mar;9(3):1336–1341. doi: 10.1128/mcb.9.3.1336

Differential transcription of exon 1 of the human c-fms gene in placental trophoblasts and monocytes.

J Visvader 1, I M Verma 1
PMCID: PMC362728  PMID: 2524648

Abstract

Structural analysis of the 5' end of the human c-fms gene revealed that a large intron of about 25 kilobases separates an upstream noncoding exon (exon 1) from the signal peptide-containing exon (exon 2). Northern (RNA) blot analysis, S1 nuclease mapping, and primer extensions showed that exon 1 is transcribed in placenta but not in cells of the monocytic lineage. This is due to the differential usage of promoters, separated by approximately 25 kilobases, in a cell-specific manner. One major c-fms transcript was observed in U-937 cells, whereas multiple initiation sites for transcription appeared to be utilized in placental cells. Nucleotide sequence comparisons showed that the 3' end of the human platelet-derived growth factor receptor gene lies approximately 350 base pairs upstream of the major initiation sites for c-fms transcription in placental trophoblasts.

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Selected References

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

  1. Ben-Neriah Y., Bernards A., Paskind M., Daley G. Q., Baltimore D. Alternative 5' exons in c-abl mRNA. Cell. 1986 Feb 28;44(4):577–586. doi: 10.1016/0092-8674(86)90267-9. [DOI] [PubMed] [Google Scholar]
  2. Berk A. J., Sharp P. A. Structure of the adenovirus 2 early mRNAs. Cell. 1978 Jul;14(3):695–711. doi: 10.1016/0092-8674(78)90252-0. [DOI] [PubMed] [Google Scholar]
  3. Bernards A., Rubin C. M., Westbrook C. A., Paskind M., Baltimore D. The first intron in the human c-abl gene is at least 200 kilobases long and is a target for translocations in chronic myelogenous leukemia. Mol Cell Biol. 1987 Sep;7(9):3231–3236. doi: 10.1128/mcb.7.9.3231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Claesson-Welsh L., Eriksson A., Morén A., Severinsson L., Ek B., Ostman A., Betsholtz C., Heldin C. H. cDNA cloning and expression of a human platelet-derived growth factor (PDGF) receptor specific for B-chain-containing PDGF molecules. Mol Cell Biol. 1988 Aug;8(8):3476–3486. doi: 10.1128/mcb.8.8.3476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coussens L., Van Beveren C., Smith D., Chen E., Mitchell R. L., Isacke C. M., Verma I. M., Ullrich A. Structural alteration of viral homologue of receptor proto-oncogene fms at carboxyl terminus. Nature. 1986 Mar 20;320(6059):277–280. doi: 10.1038/320277a0. [DOI] [PubMed] [Google Scholar]
  7. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  8. Gronwald R. G., Grant F. J., Haldeman B. A., Hart C. E., O'Hara P. J., Hagen F. S., Ross R., Bowen-Pope D. F., Murray M. J. Cloning and expression of a cDNA coding for the human platelet-derived growth factor receptor: evidence for more than one receptor class. Proc Natl Acad Sci U S A. 1988 May;85(10):3435–3439. doi: 10.1073/pnas.85.10.3435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Haley J., Whittle N., Bennet P., Kinchington D., Ullrich A., Waterfield M. The human EGF receptor gene: structure of the 110 kb locus and identification of sequences regulating its transcription. Oncogene Res. 1987 Sep-Oct;1(4):375–396. [PubMed] [Google Scholar]
  10. Heisterkamp N., Groffen J., Stephenson J. R. Isolation of v-fms and its human cellular homolog. Virology. 1983 Apr 15;126(1):248–258. doi: 10.1016/0042-6822(83)90476-2. [DOI] [PubMed] [Google Scholar]
  11. Horiguchi J., Warren M. K., Ralph P., Kufe D. Expression of the macrophage specific colony-stimulating factor (CSF-1) during human monocytic differentiation. Biochem Biophys Res Commun. 1986 Dec 30;141(3):924–930. doi: 10.1016/s0006-291x(86)80131-0. [DOI] [PubMed] [Google Scholar]
  12. Izhar M., Siebert P. D., Oshima R. G., DeWolf W. C., Fukuda M. N. Trophoblastic differentiation of human teratocarcinoma cell line HT-H1. Dev Biol. 1986 Aug;116(2):510–518. doi: 10.1016/0012-1606(86)90151-x. [DOI] [PubMed] [Google Scholar]
  13. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  14. McKnight S. L., Gavis E. R., Kingsbury R., Axel R. Analysis of transcriptional regulatory signals of the HSV thymidine kinase gene: identification of an upstream control region. Cell. 1981 Aug;25(2):385–398. doi: 10.1016/0092-8674(81)90057-x. [DOI] [PubMed] [Google Scholar]
  15. Mitchell R. L., Zokas L., Schreiber R. D., Verma I. M. Rapid induction of the expression of proto-oncogene fos during human monocytic differentiation. Cell. 1985 Jan;40(1):209–217. doi: 10.1016/0092-8674(85)90324-1. [DOI] [PubMed] [Google Scholar]
  16. Müller R., Slamon D. J., Adamson E. D., Tremblay J. M., Müller D., Cline M. J., Verma I. M. Transcription of c-onc genes c-rasKi and c-fms during mouse development. Mol Cell Biol. 1983 Jun;3(6):1062–1069. doi: 10.1128/mcb.3.6.1062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Müller R., Tremblay J. M., Adamson E. D., Verma I. M. Tissue and cell type-specific expression of two human c-onc genes. Nature. 1983 Aug 4;304(5925):454–456. doi: 10.1038/304454a0. [DOI] [PubMed] [Google Scholar]
  18. Nienhuis A. W., Bunn H. F., Turner P. H., Gopal T. V., Nash W. G., O'Brien S. J., Sherr C. J. Expression of the human c-fms proto-oncogene in hematopoietic cells and its deletion in the 5q- syndrome. Cell. 1985 Sep;42(2):421–428. doi: 10.1016/0092-8674(85)90099-6. [DOI] [PubMed] [Google Scholar]
  19. Perlino E., Cortese R., Ciliberto G. The human alpha 1-antitrypsin gene is transcribed from two different promoters in macrophages and hepatocytes. EMBO J. 1987 Sep;6(9):2767–2771. doi: 10.1002/j.1460-2075.1987.tb02571.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pollard J. W., Bartocci A., Arceci R., Orlofsky A., Ladner M. B., Stanley E. R. Apparent role of the macrophage growth factor, CSF-1, in placental development. Nature. 1987 Dec 3;330(6147):484–486. doi: 10.1038/330484a0. [DOI] [PubMed] [Google Scholar]
  21. Propst F., Rosenberg M. P., Iyer A., Kaul K., Vande Woude G. F. c-mos proto-oncogene RNA transcripts in mouse tissues: structural features, developmental regulation, and localization in specific cell types. Mol Cell Biol. 1987 May;7(5):1629–1637. doi: 10.1128/mcb.7.5.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rambaldi A., Young D. C., Griffin J. D. Expression of the M-CSF (CSF-1) gene by human monocytes. Blood. 1987 May;69(5):1409–1413. [PubMed] [Google Scholar]
  23. Rettenmier C. W., Chen J. H., Roussel M. F., Sherr C. J. The product of the c-fms proto-oncogene: a glycoprotein with associated tyrosine kinase activity. Science. 1985 Apr 19;228(4697):320–322. doi: 10.1126/science.2580348. [DOI] [PubMed] [Google Scholar]
  24. Rettenmier C. W., Roussel M. F., Quinn C. O., Kitchingman G. R., Look A. T., Sherr C. J. Transmembrane orientation of glycoproteins encoded by the v-fms oncogene. Cell. 1985 Apr;40(4):971–981. doi: 10.1016/0092-8674(85)90357-5. [DOI] [PubMed] [Google Scholar]
  25. Roberts W. M., Look A. T., Roussel M. F., Sherr C. J. Tandem linkage of human CSF-1 receptor (c-fms) and PDGF receptor genes. Cell. 1988 Nov 18;55(4):655–661. doi: 10.1016/0092-8674(88)90224-3. [DOI] [PubMed] [Google Scholar]
  26. Roussel M. F., Rettenmier C. W., Look A. T., Sherr C. J. Cell surface expression of v-fms-coded glycoproteins is required for transformation. Mol Cell Biol. 1984 Oct;4(10):1999–2009. doi: 10.1128/mcb.4.10.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sariban E., Mitchell T., Kufe D. Expression of the c-fms proto-oncogene during human monocytic differentiation. Nature. 1985 Jul 4;316(6023):64–66. doi: 10.1038/316064a0. [DOI] [PubMed] [Google Scholar]
  28. Sherr C. J., Rettenmier C. W., Sacca R., Roussel M. F., Look A. T., Stanley E. R. The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell. 1985 Jul;41(3):665–676. doi: 10.1016/s0092-8674(85)80047-7. [DOI] [PubMed] [Google Scholar]
  29. Stanley E. R., Guilbert L. J., Tushinski R. J., Bartelmez S. H. CSF-1--a mononuclear phagocyte lineage-specific hemopoietic growth factor. J Cell Biochem. 1983;21(2):151–159. doi: 10.1002/jcb.240210206. [DOI] [PubMed] [Google Scholar]
  30. Stanton L. W., Bishop J. M. Alternative processing of RNA transcribed from NMYC. Mol Cell Biol. 1987 Dec;7(12):4266–4272. doi: 10.1128/mcb.7.12.4266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wahl G. M., Lewis K. A., Ruiz J. C., Rothenberg B., Zhao J., Evans G. A. Cosmid vectors for rapid genomic walking, restriction mapping, and gene transfer. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2160–2164. doi: 10.1073/pnas.84.8.2160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Watson R. J., Dyson P. J., McMahon J. Multiple c-myb transcript cap sites are variously utilized in cells of mouse haemopoietic origin. EMBO J. 1987 Jun;6(6):1643–1651. doi: 10.1002/j.1460-2075.1987.tb02413.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Woolford J., Rothwell V., Rohrschneider L. Characterization of the human c-fms gene product and its expression in cells of the monocyte-macrophage lineage. Mol Cell Biol. 1985 Dec;5(12):3458–3466. doi: 10.1128/mcb.5.12.3458. [DOI] [PMC free article] [PubMed] [Google Scholar]

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