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PMID: 3525854 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The amino-terminal domain of the v-fms oncogene product includes a functional signal peptide that directs synthesis of a transforming glycoprotein in the absence of feline leukemia virus gag sequences.

Journal of virology ·Vol. 59 ·No. 2 ·1986-08-00 ·Pages 224-33

Wheeler EF, Roussel MF, Hampe A, Walker MH, Fried VA, Look AT, Rettenmier CW, Sherr CJ

Abstract

The nucleotide sequence of a 5' segment of the human genomic c-fms proto-oncogene suggested that recombination between feline leukemia virus and feline c-fms sequences might have occurred in a region encoding the 5' untranslated portion of c-fms mRNA. The polyprotein precursor gP180gag-fms encoded by the McDonough strain of feline sarcoma virus was therefore predicted to contain 34 v-fms-coded amino acids derived from sequences of the c-fms gene that are not ordinarily translated from the proto-oncogene mRNA. The (gP180gag-fms) polyprotein was cotranslationally cleaved near the gag-fms junction to remove its gag gene-coded portion. Determination of the amino-terminal sequence of the resulting v-fms-coded glycoprotein, gp120v-fms, showed that the site of proteolysis corresponded to a predicted signal peptidase cleavage site within the c-fms gene product. Together, these analyses suggested that the linked gag sequences may not be necessary for expression of a biologically active v-fms gene product. The gag-fms sequences of feline sarcoma virus strain McDonough and the v-fms sequences alone were inserted into a murine retroviral vector containing a neomycin resistance gene. Both constructs were biologically active when transfected into NIH 3T3 cells and produced morphologically transformed foci at equivalent efficiencies. When transfected into a cell line (psi 2) expressing complementary viral gene functions, G418-resistant (Neor) cells containing either of these vector DNAs produced high titers of transforming viruses. Analysis of proteins produced in cells containing the vector lacking gag gene sequences showed that gP180gag-fms was not synthesized, whereas normal levels of both immature gp120v-fms and mature gp140v-fms were detected. The glycoprotein was efficiently transported to the cell surface, and it retained wild-type tyrosine kinase activity. We conclude that a cryptic hydrophobic signal peptide sequence in v-fms was unmasked by gag deletion, thereby allowing the correct orientation and transport of the v-fms gene product within membranous organelles. It seems likely that the proteolytic cleavage of gP180gag-fms is mediated by signal peptidase and that the amino termini of gp140v-fms and the c-fms gene product are identical.

MeSH Terms
Amino Acid Sequence Antigens, Polyomavirus Transforming Antigens, Surface/genetics Antigens, Viral, Tumor/genetics Cell Transformation, Viral Cloning, Molecular Gene Products, gag Humans Membrane Proteins/genetics Molecular Weight Oncogene Proteins, Viral/genetics Oncogenes Protein Sorting Signals/genetics Proto-Oncogene Mas Proto-Oncogene Proteins/genetics Retroviridae Proteins/genetics
Chemicals
Antigens, Polyomavirus Transforming Antigens, Surface Antigens, Viral, Tumor Gene Products, gag MAS1 protein, human Membrane Proteins Oncogene Proteins, Viral Protein Sorting Signals Proto-Oncogene Mas Proto-Oncogene Proteins Retroviridae Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Wheeler E F
Roussel M F
Hampe A
Walker M H
Fried V A
Look A T
Rettenmier C W
Sherr C J
References (37)
37 references, click to expand
  1. Enhancement and inhibition of avian sarcoma viruses by polycations and polyanions.
    Virology. 1969 Jul;38(3):414-26 PMID: 4308055
  2. Human-tumor-derived cell lines contain common and different transforming genes.
    Cell. 1981 Dec;27(3 Pt 2):467-76 PMID: 6101201
  3. The SM strain of feline sarcoma virus. Biologic and antigenic characterization of virus.
    Proc Soc Exp Biol Med. 1972 Sep;140(4):1365-8 PMID: 5057599
  4. Biological properties and translational products of three independent isolates of feline sarcoma virus.
    Virology. 1979 Jan 15;92(1):91-107 PMID: 217170
  5. Restriction endonuclease mapping of unintegrated proviral DNA of Snyder-Theilen feline sarcoma virus: localization of sarcoma-specific sequences.
    J Virol. 1979 Dec;32(3):860-75 PMID: 229270
  6. Biochemical and immunological characterization of polyproteins coded for by the McDonough, Gardner-Arnstein, and Snyder-Theilen strains of feline sarcoma virus.
    J Virol. 1980 Jan;33(1):196-207 PMID: 6154148
  7. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  8. Characterization of a 170,000-dalton polyprotein encoded by the McDonough strain of feline sarcoma virus.
    J Virol. 1980 Jul;35(1):165-75 PMID: 6251265
  9. Three independent isolates of feline sarcoma virus code for three distinct gag-x polyproteins.
    J Virol. 1980 Jul;35(1):259-64 PMID: 6251274
  10. Gene products of McDonough feline sarcoma virus have an in vitro-associated protein kinase that phosphorylates tyrosine residues: lack of detection of this enzymatic activity in vivo.
    J Virol. 1981 Dec;40(3):812-21 PMID: 6275118
  11. Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy.
    Cell. 1982 Jan;28(1):71-81 PMID: 6978185
  12. McDonough feline sarcoma virus: characterization of the molecularly cloned provirus and its feline oncogene (v-fms).
    J Virol. 1982 Feb;41(2):489-500 PMID: 6281462
  13. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter.
    J Mol Appl Genet. 1982;1(4):327-41 PMID: 6286831
  14. Monoclonal antibodies to the transformation-specific glycoprotein encoded by the feline retroviral oncogene v-fms.
    J Virol. 1982 Nov;44(2):696-702 PMID: 6292527
  15. Nucleotide sequences of feline sarcoma virus long terminal repeats and 5' leaders show extensive homology to those of other mammalian retroviruses.
    J Virol. 1983 Jan;45(1):466-72 PMID: 6296453
  16. Isolation of v-fms and its human cellular homolog.
    Virology. 1983 Apr 15;126(1):248-58 PMID: 6302985
  17. Isolation of microgram quantities of proteins from polyacrylamide gels for amino acid sequence analysis.
    Methods Enzymol. 1983;91:227-36 PMID: 6855576
  18. A fps gene without gag gene sequences transforms cells in culture and induces tumors in chickens.
    J Virol. 1983 Dec;48(3):744-51 PMID: 6605429
  19. Molecular cloning of the c-fms locus and its assignment to human chromosome 5.
    J Virol. 1983 Dec;48(3):770-3 PMID: 6632085
  20. Nucleotide sequence of the feline retroviral oncogene v-fms shows unexpected homology with oncogenes encoding tyrosine-specific protein kinases.
    Proc Natl Acad Sci U S A. 1984 Jan;81(1):85-9 PMID: 6582485
  21. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids.
    Anal Biochem. 1984 Apr;138(1):141-3 PMID: 6731838
  22. Construction and applications of a highly transmissible murine retrovirus shuttle vector.
    Cell. 1984 Jul;37(3):1053-62 PMID: 6331674
  23. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus.
    Cell. 1983 May;33(1):153-9 PMID: 6678608
  24. Subcellular localization of glycoproteins encoded by the viral oncogene v-fms.
    J Virol. 1984 Sep;51(3):730-41 PMID: 6381756
  25. Cell surface expression of v-fms-coded glycoproteins is required for transformation.
    Mol Cell Biol. 1984 Oct;4(10):1999-2009 PMID: 6390182
  26. Human c-fms proto-oncogene: comparative analysis with an abnormal allele.
    Mol Cell Biol. 1985 Feb;5(2):422-6 PMID: 3974576
  27. The product of the c-fms proto-oncogene: a glycoprotein with associated tyrosine kinase activity.
    Science. 1985 Apr 19;228(4697):320-2 PMID: 2580348
  28. Transmembrane orientation of glycoproteins encoded by the v-fms oncogene.
    Cell. 1985 Apr;40(4):971-81 PMID: 3986905
  29. The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1.
    Cell. 1985 Jul;41(3):665-76 PMID: 2408759
  30. Activation of the transformation potential of the cellular fps gene.
    Cell. 1985 Aug;42(1):105-15 PMID: 2990723
  31. Viral oncogenes.
    Cell. 1985 Aug;42(1):23-38 PMID: 2990725
  32. Deletion of the gag region from FBR murine osteosarcoma virus does not affect its enhanced transforming activity.
    J Virol. 1985 Sep;55(3):521-6 PMID: 2991577
  33. Expression of the human c-fms proto-oncogene in hematopoietic cells and its deletion in the 5q- syndrome.
    Cell. 1985 Sep;42(2):421-8 PMID: 4028159
  34. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes.
    Cell. 1986 Jan 31;44(2):283-92 PMID: 3943125
  35. Structural alteration of viral homologue of receptor proto-oncogene fms at carboxyl terminus.
    Nature. 1986 Mar 20-26;320(6059):277-80 PMID: 2421165
  36. Specific binding of the mononuclear phagocyte colony-stimulating factor CSF-1 to the product of the v-fms oncogene.
    Proc Natl Acad Sci U S A. 1986 May;83(10):3331-5 PMID: 3010289
  37. A transmissible feline fibrosarcoma of viral origin.
    Cancer Res. 1971 Jul;31(7):953-6 PMID: 4997847
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1986-08-00
Pages
224-33
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC253070
Subset
IM
Grants
NCI NIH HHS · CA 09346-6 · United States
NCI NIH HHS · CA 21765 · United States
NCI NIH HHS · CA 38187 · United States
Databases
GENBANK
M14002
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