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PMID: 7479904 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mutant forms of growth factor-binding protein-2 reverse BCR-ABL-induced transformation.

Gishizky ML, Cortez D, Pendergast AM

Abstract

Growth factor-binding protein 2 (Grb2) is an adaptor protein that links tyrosine kinases to Ras. BCR-ABL is a tyrosine kinase oncoprotein that is implicated in the pathogenesis of Philadelphia chromosome (Ph1)-positive leukemias. Grb2 forms a complex with BCR-ABL and the nucleotide exchange factor Sos that leads to the activation of the Ras protooncogene. In this report we demonstrate that Grb2 mutant proteins lacking amino- or carboxyl-terminal src homology SH3 domains suppress BCR-ABL-induced Ras activation and reverse the oncogenic phenotype. The Grb2 SH3-deletion mutant proteins bind to BCR-ABL and do not impair tyrosine kinase activity. Expression of the Grb2 SH3-deletion mutant proteins in BCR-ABL-transformed Rat-1 fibroblasts and in the human Ph1-positive leukemic cell line K562 inhibits their ability to grow as foci in soft agar and form tumors in nude mice. Furthermore, expression of the Grb2 SH3-deletion mutants in K562 cells induced their differentiation. Because Ras plays an important role in signaling by receptor and nonreceptor tyrosine kinases, the use of interfering mutant Grb2 proteins may be applied to block the proliferation of other cancers that depend in part on activated tyrosine kinases for growth.

MeSH Terms
Adaptor Proteins, Signal Transducing Animals Cell Differentiation Cell Division Cell Transformation, Neoplastic/metabolism Fusion Proteins, bcr-abl/metabolism GRB2 Adaptor Protein Humans Leukemia, Myelogenous, Chronic, BCR-ABL Positive/metabolism Mice Mice, Nude Protein Serine-Threonine Kinases/physiology Protein-Tyrosine Kinases/metabolism Proteins/metabolism Proto-Oncogene Proteins/physiology Proto-Oncogene Proteins c-raf Proto-Oncogene Proteins p21(ras)/metabolism Rats Signal Transduction Structure-Activity Relationship Tumor Cells, Cultured src Homology Domains
Chemicals
Adaptor Proteins, Signal Transducing GRB2 Adaptor Protein GRB2 protein, human Grb2 protein, mouse Grb2 protein, rat Proteins Proto-Oncogene Proteins Protein-Tyrosine Kinases Fusion Proteins, bcr-abl Protein Serine-Threonine Kinases Proto-Oncogene Proteins c-raf HRAS protein, human Proto-Oncogene Proteins p21(ras)
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gishizky M L
Department of Hematology/Oncology, SUGEN, Inc., Redwood City, CA 94063, USA.
Cortez D
Pendergast A M
References (40)
40 references, click to expand
  1. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors.
    Cell. 1992 Aug 7;70(3):389-99 PMID: 1643657
  2. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling.
    Cell. 1992 Aug 7;70(3):431-42 PMID: 1322798
  3. BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias.
    Mol Cell Biol. 1991 Apr;11(4):1785-92 PMID: 2005881
  4. Serum-, TPA-, and Ras-induced expression from Ap-1/Ets-driven promoters requires Raf-1 kinase.
    Genes Dev. 1992 Apr;6(4):545-56 PMID: 1313769
  5. The viral and cellular forms of the Abelson (abl) oncogene.
    Adv Virus Res. 1988;35:39-81 PMID: 2852893
  6. Bcr-Abl oncoproteins bind directly to activators of the Ras signalling pathway.
    EMBO J. 1994 Feb 15;13(4):764-73 PMID: 8112292
  7. Raf functions downstream of Ras1 in the Sevenless signal transduction pathway.
    Nature. 1992 Dec 10;360(6404):600-3 PMID: 1461284
  8. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling.
    Cell. 1992 Aug 7;70(3):401-10 PMID: 1643658
  9. The human leukemia oncogene bcr-abl abrogates the anchorage requirement but not the growth factor requirement for proliferation.
    Mol Cell Biol. 1995 Mar;15(3):1286-93 PMID: 7862122
  10. Binding of the Grb2 SH2 domain to phosphotyrosine motifs does not change the affinity of its SH3 domains for Sos proline-rich motifs.
    EMBO J. 1994 Sep 1;13(17):4011-21 PMID: 7521298
  11. A temperature sensitive p210 BCR-ABL mutant defines the primary consequences of BCR-ABL tyrosine kinase expression in growth factor dependent cells.
    EMBO J. 1994 Dec 15;13(24):5887-95 PMID: 7813429
  12. Structural and signaling requirements for BCR-ABL-mediated transformation and inhibition of apoptosis.
    Mol Cell Biol. 1995 Oct;15(10):5531-41 PMID: 7565705
  13. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3443-7 PMID: 7512734
  14. Dynamin binds to SH3 domains of phospholipase C gamma and GRB-2.
    J Biol Chem. 1994 Jun 10;269(23):16009-14 PMID: 8206897
  15. Tyrphostin-induced inhibition of p210bcr-abl tyrosine kinase activity induces K562 to differentiate.
    Blood. 1993 Dec 15;82(12):3524-9 PMID: 7505115
  16. BCR-ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB-2 adaptor protein.
    Cell. 1993 Oct 8;75(1):175-85 PMID: 8402896
  17. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome.
    Blood. 1975 Mar;45(3):321-34 PMID: 163658
  18. Specific inhibition of cytoplasmic protein tyrosine kinases by herbimycin A in vitro.
    Biochem Pharmacol. 1991 Oct 9;42(9):1661-71 PMID: 1656993
  19. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains.
    Nature. 1992 Mar 26;356(6367):340-4 PMID: 1372395
  20. Differential complementation of Bcr-Abl point mutants with c-Myc.
    Science. 1994 Apr 15;264(5157):424-6 PMID: 8153630
  21. SH2-containing phosphotyrosine phosphatase Syp is a target of p210bcr-abl tyrosine kinase.
    J Biol Chem. 1994 May 27;269(21):15381-7 PMID: 8195176
  22. An alteration of the human c-abl protein in K562 leukemia cells unmasks associated tyrosine kinase activity.
    Cell. 1984 Jul;37(3):1035-42 PMID: 6204766
  23. Requirement for Raf and MAP kinase function during the meiotic maturation of Xenopus oocytes.
    J Cell Biol. 1993 Aug;122(3):645-52 PMID: 8335690
  24. How receptor tyrosine kinases activate Ras.
    Trends Biochem Sci. 1993 Aug;18(8):273-5 PMID: 8236435
  25. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation.
    Cell. 1990 Feb 9;60(3):375-86 PMID: 2302733
  26. Growth factor-induced binding of dynamin to signal transduction proteins involves sorting to distinct and separate proline-rich dynamin sequences.
    EMBO J. 1994 Jun 1;13(11):2574-82 PMID: 8013457
  27. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP.
    Mol Cell Biol. 1988 Aug;8(8):3235-43 PMID: 3145408
  28. The BCR-ABL oncogene transforms Rat-1 cells and cooperates with v-myc.
    Mol Cell Biol. 1989 Mar;9(3):1263-70 PMID: 2725497
  29. Cloning of a Grb2 isoform with apoptotic properties.
    Science. 1994 May 13;264(5161):971-4 PMID: 8178156
  30. C. elegans lin-45 raf gene participates in let-60 ras-stimulated vulval differentiation.
    Nature. 1993 May 13;363(6425):133-40 PMID: 8483497
  31. Mammalian Ras interacts directly with the serine/threonine kinase Raf.
    Cell. 1993 Jul 16;74(1):205-14 PMID: 8334704
  32. Expression of raf oncogenes activates the PEA1 transcription factor motif.
    Mol Cell Biol. 1989 May;9(5):2247-50 PMID: 2501665
  33. SH2 and SH3 domains.
    Curr Biol. 1993 Jul 1;3(7):434-42 PMID: 15335710
  34. Expression of the normal p53 gene induces differentiation of K562 cells.
    Oncogene. 1992 Sep;7(9):1853-7 PMID: 1501893
  35. Apoptosis (the 1992 Frank Rose Memorial Lecture).
    Br J Cancer. 1993 Feb;67(2):205-8 PMID: 8431353
  36. Signalling through SH2 and SH3 domains.
    Trends Cell Biol. 1993 Jan;3(1):8-13 PMID: 14731533
  37. Genetic requirement for Ras in the transformation of fibroblasts and hematopoietic cells by the Bcr-Abl oncogene.
    J Exp Med. 1995 Jan 1;181(1):307-13 PMID: 7807010
  38. SH3 domains of the adapter molecule Grb2 complex with two proteins in T cells: the guanine nucleotide exchange protein Sos and a 75-kDa protein that is a substrate for T cell antigen receptor-activated tyrosine kinases.
    J Biol Chem. 1994 May 13;269(19):14081-7 PMID: 8188688
  39. Role of p21 RAS in p210 bcr-abl transformation of murine myeloid cells.
    Blood. 1993 Sep 15;82(6):1838-47 PMID: 7691239
  40. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins.
    Science. 1986 Sep 5;233(4768):1061-8 PMID: 3090687
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-11-21
Pages
10889-93
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC40536
Subset
IM
Grants
NCI NIH HHS · CA61033 · United States
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