Home LiteratureArticle Details
PMID: 1718742 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transient and locally restricted expression of the ros1 protooncogene during mouse development.

The EMBO journal ·Vol. 10 ·No. 12 ·1991-12-00 ·Pages 3693-702

Sonnenberg E, Gödecke A, Walter B, Bladt F, Birchmeier C

Abstract

The ros1 gene was detected originally by virtue of its transforming potential; the cDNA of the human protooncogene was isolated from a tumor cell line expressing the gene ectopically. It encodes a receptor-type tyrosine specific protein kinase which is closely related to sevenless in Drosophila. Here we report the novel and remarkable in vivo expression pattern of c-ros1, which was determined in the mouse. By a combination of RNase protection and in situ hybridization, we find transient c-ros1 expression during development in the kidney, intestine and lung, coinciding with major morphogenetic and differentiation events in these organs. This temporally restricted nature of expression is unusual for tyrosine kinase receptors and suggests a role for ros1 during development. Furthermore, in kidney development c-ros1 transcripts are confined to subgroups of ureter cells known to be involved directly in inductive interactions between ureter epithelium and metanephric mesenchyme. Thus, this study implicates for the first time a tyrosine kinase receptor in mesenchymal epithelial interactions and suggests a molecular basis for these important inductive events in development.

Related Genes
MeSH Terms
Animals Blotting, Northern DNA/genetics Gene Expression Intestinal Mucosa/metabolism Intestines/embryology Kidney/embryology,metabolism Ligands Lung/embryology,metabolism Male Mice Nucleic Acid Hybridization Protein Biosynthesis Proto-Oncogene Proteins/biosynthesis,genetics Proto-Oncogenes RNA/genetics Receptor Protein-Tyrosine Kinases Ribonucleases/chemistry Testis/embryology,metabolism Transcription, Genetic
Chemicals
Ligands Proto-Oncogene Proteins RNA DNA Receptor Protein-Tyrosine Kinases Ros1 protein, mouse Ribonucleases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Sonnenberg E
Max-Delbrück-Laboratorium, Max-Planck-Gesellschaft, Köln, Germany.
Gödecke A
Walter B
Bladt F
Birchmeier C
References (62)
62 references, click to expand
  1. N-myc proto-oncogene expression during organogenesis in the developing mouse as revealed by in situ hybridization.
    J Cell Biol. 1988 Oct;107(4):1325-35 PMID: 3049618
  2. Morphogenesis of the small intestine during fetal development.
    Ciba Found Symp. 1979 Jan 16-18;(70):3-29 PMID: 261525
  3. Characterization of the rat mas oncogene and its high-level expression in the hippocampus and cerebral cortex of rat brain.
    Proc Natl Acad Sci U S A. 1988 Jul;85(14):5339-42 PMID: 2455902
  4. Cytokeratin polypeptide patterns of different epithelia of the human male urogenital tract: immunofluorescence and gel electrophoretic studies.
    J Histochem Cytochem. 1985 May;33(5):415-26 PMID: 2580881
  5. In situ hybridization reveals temporal and spatial changes in cellular expression of mRNA for a laminin receptor, laminin, and basement membrane (type IV) collagen in the developing kidney.
    J Cell Biol. 1989 Sep;109(3):1351-62 PMID: 2527859
  6. Developmentally regulated conversion of mesenchyme to epithelium.
    FASEB J. 1989 Aug;3(10):2141-50 PMID: 2666230
  7. Vimentin cDNA clones covering the complete intermediate-filament protein are found in an EHS tumor cDNA library.
    Gene. 1989 Mar 15;76(1):171-5 PMID: 2744479
  8. Specific expression of the Hox 1.3 homeo box gene in murine embryonic structures originating from or induced by the mesoderm.
    EMBO J. 1987 Oct;6(10):2965-75 PMID: 2891502
  9. Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine.
    Development. 1988 Aug;103(4):785-90 PMID: 3248525
  10. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter.
    Nucleic Acids Res. 1984 Sep 25;12(18):7035-56 PMID: 6091052
  11. New human transforming genes detected by a tumorigenicity assay.
    Mol Cell Biol. 1984 Sep;4(9):1695-705 PMID: 6092933
  12. Characterization of an activated human ros gene.
    Mol Cell Biol. 1986 Sep;6(9):3109-16 PMID: 3785223
  13. The neu oncogene encodes an epidermal growth factor receptor-related protein.
    Nature. 1986 Jan 16-22;319(6050):226-30 PMID: 3945311
  14. Cell-adhesion molecule uvomorulin during kidney development.
    Dev Biol. 1985 Nov;112(1):213-21 PMID: 3902535
  15. Signal transduction by receptors with tyrosine kinase activity.
    Cell. 1990 Apr 20;61(2):203-12 PMID: 2158859
  16. Variations of cervical vertebrae after expression of a Hox-1.1 transgene in mice.
    Cell. 1990 Apr 20;61(2):301-8 PMID: 1970515
  17. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain.
    Cell. 1990 Sep 21;62(6):1073-85 PMID: 2205396
  18. Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development.
    Nature. 1990 Aug 30;346(6287):847-50 PMID: 2202907
  19. Transient and locally restricted expression of laminin A chain mRNA by developing epithelial cells during kidney organogenesis.
    Cell. 1990 Jan 26;60(2):337-46 PMID: 2404613
  20. Characterization of ROS1 cDNA from a human glioblastoma cell line.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4799-803 PMID: 2352949
  21. sevenless: Seven found?
    Cell. 1990 Apr 6;61(1):15-6 PMID: 2317871
  22. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells.
    Nature. 1984 May 31-Jun 6;309(5967):418-25 PMID: 6328312
  23. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences.
    Nature. 1984 Feb 9-15;307(5951):521-7 PMID: 6320011
  24. The erbB gene of avian erythroblastosis virus is a member of the src gene family.
    Cell. 1983 Nov;35(1):71-8 PMID: 6313229
  25. Sequence and gene organization of mouse mitochondrial DNA.
    Cell. 1981 Oct;26(2 Pt 2):167-80 PMID: 7332926
  26. Ligand-independent activation of the sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye.
    Cell. 1991 Mar 22;64(6):1069-81 PMID: 2004416
  27. Contrasting expression patterns of three members of the myc family of protooncogenes in the developing and adult mouse kidney.
    J Cell Biol. 1991 Jan;112(1):13-25 PMID: 1986001
  28. Molecular cloning of mast cell growth factor, a hematopoietin that is active in both membrane bound and soluble forms.
    Cell. 1990 Oct 5;63(1):235-43 PMID: 1698558
  29. Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5.
    Nature. 1991 Apr 11;350(6318):473-9 PMID: 1673020
  30. Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor.
    Nature. 1991 Jul 18;352(6332):207-12 PMID: 1857416
  31. Pax2, a new murine paired-box-containing gene and its expression in the developing excretory system.
    Development. 1990 Aug;109(4):787-95 PMID: 1977574
  32. Hox-2.3 upstream sequences mediate lacZ expression in intermediate mesoderm derivatives of transgenic mice.
    Development. 1990 Aug;109(4):775-86 PMID: 1977573
  33. Induction of cell fate in the Drosophila retina: the bride of sevenless protein is predicted to contain a large extracellular domain and seven transmembrane segments.
    Genes Dev. 1990 Nov;4(11):1835-47 PMID: 2276620
  34. Primary structure and functional expression of rat and human stem cell factor DNAs.
    Cell. 1990 Oct 5;63(1):203-11 PMID: 2208279
  35. The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development.
    Cell. 1989 Mar 24;56(6):1093-104 PMID: 2924351
  36. Profile scanning for three-dimensional structural patterns in protein sequences.
    Comput Appl Biosci. 1988 Mar;4(1):61-6 PMID: 3383004
  37. The Drosophila gene torso encodes a putative receptor tyrosine kinase.
    Nature. 1989 Apr 6;338(6215):478-83 PMID: 2927509
  38. The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF receptor homolog.
    Cell. 1989 Mar 24;56(6):1085-92 PMID: 2493993
  39. Cloning of a Drosophila cDNA encoding a polypeptide similar to the human insulin receptor precursor.
    Biochem Biophys Res Commun. 1986 Dec 15;141(2):474-81 PMID: 3099787
  40. Growth factor receptor tyrosine kinases.
    Annu Rev Biochem. 1988;57:443-78 PMID: 3052279
  41. The Drosophila EGF receptor gene homolog: conservation of both hormone binding and kinase domains.
    Cell. 1985 Mar;40(3):599-607 PMID: 2982499
  42. Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes.
    Nature. 1985 Feb 28-Mar 6;313(6005):756-61 PMID: 2983222
  43. The human insulin receptor cDNA: the structural basis for hormone-activated transmembrane signalling.
    Cell. 1985 Apr;40(4):747-58 PMID: 2859121
  44. Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA.
    Nature. 1987 Sep 24-30;329(6137):341-3 PMID: 3498123
  45. The murine and Drosophila homeobox gene complexes have common features of organization and expression.
    Cell. 1989 May 5;57(3):367-78 PMID: 2566383
  46. Do multigene families regulate vertebrate development?
    Trends Genet. 1988 Aug;4(8):214-9 PMID: 2907693
  47. A human oncogene formed by the fusion of truncated tropomyosin and protein tyrosine kinase sequences.
    Nature. 1986 Feb 27-Mar 5;319(6056):743-8 PMID: 2869410
  48. Homeo boxes in the study of development.
    Science. 1987 Jun 5;236(4806):1245-52 PMID: 2884726
  49. Expression and rearrangement of the ROS1 gene in human glioblastoma cells.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):9270-4 PMID: 2827175
  50. Control of photoreceptor cell fate by the sevenless protein requires a functional tyrosine kinase domain.
    Cell. 1988 Jul 29;54(3):299-311 PMID: 2840202
  51. A new acute transforming feline retrovirus and relationship of its oncogene v-kit with the protein kinase gene family.
    Nature. 1986 Apr 3-9;320(6061):415-21 PMID: 3007997
  52. Nucleotide sequence of avian sarcoma virus UR2 and comparison of its transforming gene with other members of the tyrosine protein kinase oncogene family.
    J Virol. 1985 Mar;53(3):879-84 PMID: 2983097
  53. Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-arc-1: mechanistic aspects and identification of the antigen as a component related to uvomorulin.
    J Cell Biol. 1985 Oct;101(4):1307-15 PMID: 2995405
  54. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless.
    Cell. 1987 Aug 14;50(4):649-57 PMID: 3111720
  55. Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins.
    Annu Rev Biochem. 1982;51:219-50 PMID: 6180679
  56. Differentiation of cell types in the mammalian kidney by immunofluorescence microscopy using antibodies to intermediate filament proteins and desmoplakins.
    Histochemistry. 1983;77(3):365-94 PMID: 6345481
  57. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  58. 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
  59. Junctional complexes in fetal rat small intestine during morphogenesis.
    Dev Biol. 1981 Aug;86(1):170-8 PMID: 7286391
  60. Hereditary anemias of the mouse: a review for geneticists.
    Adv Genet. 1979;20:357-459 PMID: 390999
  61. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  62. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains.
    Science. 1988 Jul 1;241(4861):42-52 PMID: 3291115
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1991-12-00
Pages
3693-702
Language
English
Region
England
NLM ID
8208664
PMCID
PMC453103
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com