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. 1993 Aug;13(8):4986–4998. doi: 10.1128/mcb.13.8.4986

Alpha 2-chimerin, an SH2-containing GTPase-activating protein for the ras-related protein p21rac derived by alternate splicing of the human n-chimerin gene, is selectively expressed in brain regions and testes.

C Hall 1, W C Sin 1, M Teo 1, G J Michael 1, P Smith 1, J M Dong 1, H H Lim 1, E Manser 1, N K Spurr 1, T A Jones 1, et al.
PMCID: PMC360144  PMID: 8336731

Abstract

n-Chimerin (alpha 1-chimerin) is a brain GTPase-activating protein (GAP) for the ras-related p21rac. We now report the occurrence of another form of chimerin, termed alpha 2-chimerin. This is the product of an alternately spliced transcript of the human n-chimerin gene encoding an N-terminal SH2 (src homology 2) domain in addition to the phorbol ester receptor and GAP domains. alpha 1- and alpha 2-chimerin mRNAs were expressed differently. In the rat brain, only alpha 1-chimerin mRNA was expressed in cerebellar Purkinje cells, although both alpha 1- and alpha 2-chimerin mRNAs occurred in neurons in the cerebral cortex, hippocampus, and thalamus. Only alpha 2-chimerin RNA was expressed in rat testes, in early pachytene spermatocytes. A 45-kDa SH2-containing chimerin corresponding to the alpha 2 form was purified from rat brain. As with Escherichia coli 45-kDa recombinant alpha 2-chimerin, purified brain alpha 2-chimerin exhibited racGAP activity which was stimulated by phosphatidylserine. The recombinant SH2 domain bound several 32P-labelled phosphoproteins of PC12 cells, whose phosphorylation increased in response to trophic factors, including nerve growth factor. To examine the relationships of alpha 1- and alpha 2-chimerin transcripts, human genomic DNA clones were characterized. In alpha 2-chimerin mRNA, a 3' splice acceptor site within exon 1 of alpha 1-chimerin mRNA was used, replacing its 5' untranslated region and N-terminal coding sequence. The single human n-chimerin gene was mapped to chromosome 2q31-q32.1, colocalizing with the CRE-BP1 transcription factor gene (2q32). It contained several splice junctions conserved with the sequence-related protein kinase C and bcr genes. alpha 2-Chimerin is only the second SH2-containing GAP and the first example of an SH2 domain generated by alternate splicing.

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  1. Agnel M., Röder L., Vola C., Griffin-Shea R. A Drosophila rotund transcript expressed during spermatogenesis and imaginal disc morphogenesis encodes a protein which is similar to human Rac GTPase-activating (racGAP) proteins. Mol Cell Biol. 1992 Nov;12(11):5111–5122. doi: 10.1128/mcb.12.11.5111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ahmed S., Kozma R., Lee J., Monfries C., Harden N., Lim L. The cysteine-rich domain of human proteins, neuronal chimaerin, protein kinase C and diacylglycerol kinase binds zinc. Evidence for the involvement of a zinc-dependent structure in phorbol ester binding. Biochem J. 1991 Nov 15;280(Pt 1):233–241. doi: 10.1042/bj2800233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ahmed S., Kozma R., Monfries C., Hall C., Lim H. H., Smith P., Lim L. Human brain n-chimaerin cDNA encodes a novel phorbol ester receptor. Biochem J. 1990 Dec 15;272(3):767–773. doi: 10.1042/bj2720767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ahmed S., Lee J., Kozma R., Best A., Monfries C., Lim L. A novel functional target for tumor-promoting phorbol esters and lysophosphatidic acid. The p21rac-GTPase activating protein n-chimaerin. J Biol Chem. 1993 May 25;268(15):10709–10712. [PubMed] [Google Scholar]
  5. Andersen L. B., Ballester R., Marchuk D. A., Chang E., Gutmann D. H., Saulino A. M., Camonis J., Wigler M., Collins F. S. A conserved alternative splice in the von Recklinghausen neurofibromatosis (NF1) gene produces two neurofibromin isoforms, both of which have GTPase-activating protein activity. Mol Cell Biol. 1993 Jan;13(1):487–495. doi: 10.1128/mcb.13.1.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  7. Bollag G., McCormick F. Differential regulation of rasGAP and neurofibromatosis gene product activities. Nature. 1991 Jun 13;351(6327):576–579. doi: 10.1038/351576a0. [DOI] [PubMed] [Google Scholar]
  8. Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature. 1990 Nov 8;348(6297):125–132. doi: 10.1038/348125a0. [DOI] [PubMed] [Google Scholar]
  9. Brown W. R., MacKinnon P. J., Villasanté A., Spurr N., Buckle V. J., Dobson M. J. Structure and polymorphism of human telomere-associated DNA. Cell. 1990 Oct 5;63(1):119–132. doi: 10.1016/0092-8674(90)90293-n. [DOI] [PubMed] [Google Scholar]
  10. Cantley L. C., Auger K. R., Carpenter C., Duckworth B., Graziani A., Kapeller R., Soltoff S. Oncogenes and signal transduction. Cell. 1991 Jan 25;64(2):281–302. doi: 10.1016/0092-8674(91)90639-g. [DOI] [PubMed] [Google Scholar]
  11. Carlock L. R., Smith D., Wasmuth J. J. Genetic counterselective procedure to isolate interspecific cell hybrids containing single human chromosomes: construction of cell hybrids and recombinant DNA libraries specific for human chromosomes 3 and 4. Somat Cell Mol Genet. 1986 Mar;12(2):163–174. doi: 10.1007/BF01560663. [DOI] [PubMed] [Google Scholar]
  12. Cicchetti P., Mayer B. J., Thiel G., Baltimore D. Identification of a protein that binds to the SH3 region of Abl and is similar to Bcr and GAP-rho. Science. 1992 Aug 7;257(5071):803–806. doi: 10.1126/science.1379745. [DOI] [PubMed] [Google Scholar]
  13. Cocquerelle C., Daubersies P., Majérus M. A., Kerckaert J. P., Bailleul B. Splicing with inverted order of exons occurs proximal to large introns. EMBO J. 1992 Mar;11(3):1095–1098. doi: 10.1002/j.1460-2075.1992.tb05148.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cooper J. A., Kashishian A. In vivo binding properties of SH2 domains from GTPase-activating protein and phosphatidylinositol 3-kinase. Mol Cell Biol. 1993 Mar;13(3):1737–1745. doi: 10.1128/mcb.13.3.1737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Croce C. M., Huebner K., Isobe M., Fainstain E., Lifshitz B., Shtivelman E., Canaani E. Mapping of four distinct BCR-related loci to chromosome region 22q11: order of BCR loci relative to chronic myelogenous leukemia and acute lymphoblastic leukemia breakpoints. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7174–7178. doi: 10.1073/pnas.84.20.7174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Diekmann D., Brill S., Garrett M. D., Totty N., Hsuan J., Monfries C., Hall C., Lim L., Hall A. Bcr encodes a GTPase-activating protein for p21rac. Nature. 1991 May 30;351(6325):400–402. doi: 10.1038/351400a0. [DOI] [PubMed] [Google Scholar]
  17. Duchesne M., Schweighoffer F., Parker F., Clerc F., Frobert Y., Thang M. N., Tocqué B. Identification of the SH3 domain of GAP as an essential sequence for Ras-GAP-mediated signaling. Science. 1993 Jan 22;259(5094):525–528. doi: 10.1126/science.7678707. [DOI] [PubMed] [Google Scholar]
  18. Ellis C., Moran M., McCormick F., Pawson T. Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature. 1990 Jan 25;343(6256):377–381. doi: 10.1038/343377a0. [DOI] [PubMed] [Google Scholar]
  19. Fainstein E., Einat M., Gokkel E., Marcelle C., Croce C. M., Gale R. P., Canaani E. Nucleotide sequence analysis of human abl and bcr-abl cDNAs. Oncogene. 1989 Dec;4(12):1477–1481. [PubMed] [Google Scholar]
  20. Fantl W. J., Escobedo J. A., Martin G. A., Turck C. W., del Rosario M., McCormick F., Williams L. T. Distinct phosphotyrosines on a growth factor receptor bind to specific molecules that mediate different signaling pathways. Cell. 1992 May 1;69(3):413–423. doi: 10.1016/0092-8674(92)90444-h. [DOI] [PubMed] [Google Scholar]
  21. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. George J. M., Clayton D. F. Differential regulation in the avian song control circuit of an mRNA predicting a highly conserved protein related to protein kinase C and the bcr oncogene. Brain Res Mol Brain Res. 1992 Feb;12(4):323–329. doi: 10.1016/0169-328x(92)90134-w. [DOI] [PubMed] [Google Scholar]
  23. Hall A. Signal transduction through small GTPases--a tale of two GAPs. Cell. 1992 May 1;69(3):389–391. doi: 10.1016/0092-8674(92)90441-e. [DOI] [PubMed] [Google Scholar]
  24. Hall A. The cellular functions of small GTP-binding proteins. Science. 1990 Aug 10;249(4969):635–640. doi: 10.1126/science.2116664. [DOI] [PubMed] [Google Scholar]
  25. Hall C., Monfries C., Smith P., Lim H. H., Kozma R., Ahmed S., Vanniasingham V., Leung T., Lim L. Novel human brain cDNA encoding a 34,000 Mr protein n-chimaerin, related to both the regulatory domain of protein kinase C and BCR, the product of the breakpoint cluster region gene. J Mol Biol. 1990 Jan 5;211(1):11–16. doi: 10.1016/0022-2836(90)90006-8. [DOI] [PubMed] [Google Scholar]
  26. Hart M. J., Eva A., Evans T., Aaronson S. A., Cerione R. A. Catalysis of guanine nucleotide exchange on the CDC42Hs protein by the dbl oncogene product. Nature. 1991 Nov 28;354(6351):311–314. doi: 10.1038/354311a0. [DOI] [PubMed] [Google Scholar]
  27. Harvey R. J., Darlison M. G. Random-primed cDNA synthesis facilitates the isolation of multiple 5'-cDNA ends by RACE. Nucleic Acids Res. 1991 Jul 25;19(14):4002–4002. doi: 10.1093/nar/19.14.4002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Heisterkamp N., Groffen J. Duplication of the bcr and gamma-glutamyl transpeptidase genes. Nucleic Acids Res. 1988 Aug 25;16(16):8045–8056. doi: 10.1093/nar/16.16.8045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Heisterkamp N., Morris C., Groffen J. ABR, an active BCR-related gene. Nucleic Acids Res. 1989 Nov 11;17(21):8821–8831. doi: 10.1093/nar/17.21.8821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Heisterkamp N., Stam K., Groffen J., de Klein A., Grosveld G. Structural organization of the bcr gene and its role in the Ph' translocation. 1985 Jun 27-Jul 3Nature. 315(6022):758–761. doi: 10.1038/315758a0. [DOI] [PubMed] [Google Scholar]
  31. Kaplan D. R., Morrison D. K., Wong G., McCormick F., Williams L. T. PDGF beta-receptor stimulates tyrosine phosphorylation of GAP and association of GAP with a signaling complex. Cell. 1990 Apr 6;61(1):125–133. doi: 10.1016/0092-8674(90)90220-9. [DOI] [PubMed] [Google Scholar]
  32. Kashishian A., Kazlauskas A., Cooper J. A. Phosphorylation sites in the PDGF receptor with different specificities for binding GAP and PI3 kinase in vivo. EMBO J. 1992 Apr;11(4):1373–1382. doi: 10.1002/j.1460-2075.1992.tb05182.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kazlauskas A., Ellis C., Pawson T., Cooper J. A. Binding of GAP to activated PDGF receptors. Science. 1990 Mar 30;247(4950):1578–1581. doi: 10.1126/science.2157284. [DOI] [PubMed] [Google Scholar]
  34. Klippel A., Escobedo J. A., Fantl W. J., Williams L. T. The C-terminal SH2 domain of p85 accounts for the high affinity and specificity of the binding of phosphatidylinositol 3-kinase to phosphorylated platelet-derived growth factor beta receptor. Mol Cell Biol. 1992 Apr;12(4):1451–1459. doi: 10.1128/mcb.12.4.1451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. LeFranc M. P., Forster A., Baer R., Stinson M. A., Rabbitts T. H. Diversity and rearrangement of the human T cell rearranging gamma genes: nine germ-line variable genes belonging to two subgroups. Cell. 1986 Apr 25;45(2):237–246. doi: 10.1016/0092-8674(86)90388-0. [DOI] [PubMed] [Google Scholar]
  36. Leung T. K., Hall C., Rajendran M., Spurr N. K., Lim L. The human heat-shock genes HSPA6 and HSPA7 are both expressed and localize to chromosome 1. Genomics. 1992 Jan;12(1):74–79. doi: 10.1016/0888-7543(92)90409-l. [DOI] [PubMed] [Google Scholar]
  37. Leung T., How B. E., Manser E., Lim L. Germ cell beta-chimaerin, a new GTPase-activating protein for p21rac, is specifically expressed during the acrosomal assembly stage in rat testis. J Biol Chem. 1993 Feb 25;268(6):3813–3816. [PubMed] [Google Scholar]
  38. Lifshitz B., Fainstein E., Marcelle C., Shtivelman E., Amson R., Gale R. P., Canaani E. bcr genes and transcripts. Oncogene. 1988 Feb;2(2):113–117. [PubMed] [Google Scholar]
  39. Lim H. H., Michael G. J., Smith P., Lim L., Hall C. Developmental regulation and neuronal expression of the mRNA of rat n-chimaerin, a p21rac GAP:cDNA sequence. Biochem J. 1992 Oct 15;287(Pt 2):415–422. doi: 10.1042/bj2870415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Maekawa T., Sakura H., Kanei-Ishii C., Sudo T., Yoshimura T., Fujisawa J., Yoshida M., Ishii S. Leucine zipper structure of the protein CRE-BP1 binding to the cyclic AMP response element in brain. EMBO J. 1989 Jul;8(7):2023–2028. doi: 10.1002/j.1460-2075.1989.tb03610.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Manser E., Leung T., Monfries C., Teo M., Hall C., Lim L. Diversity and versatility of GTPase activating proteins for the p21rho subfamily of ras G proteins detected by a novel overlay assay. J Biol Chem. 1992 Aug 15;267(23):16025–16028. [PubMed] [Google Scholar]
  42. Margolis B., Li N., Koch A., Mohammadi M., Hurwitz D. R., Zilberstein A., Ullrich A., Pawson T., Schlessinger J. The tyrosine phosphorylated carboxyterminus of the EGF receptor is a binding site for GAP and PLC-gamma. EMBO J. 1990 Dec;9(13):4375–4380. doi: 10.1002/j.1460-2075.1990.tb07887.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Martin G. A., Yatani A., Clark R., Conroy L., Polakis P., Brown A. M., McCormick F. GAP domains responsible for ras p21-dependent inhibition of muscarinic atrial K+ channel currents. Science. 1992 Jan 10;255(5041):192–194. doi: 10.1126/science.1553544. [DOI] [PubMed] [Google Scholar]
  44. Martinez R., Mathey-Prevot B., Bernards A., Baltimore D. Neuronal pp60c-src contains a six-amino acid insertion relative to its non-neuronal counterpart. Science. 1987 Jul 24;237(4813):411–415. doi: 10.1126/science.2440106. [DOI] [PubMed] [Google Scholar]
  45. Maru Y., Witte O. N. The BCR gene encodes a novel serine/threonine kinase activity within a single exon. Cell. 1991 Nov 1;67(3):459–468. doi: 10.1016/0092-8674(91)90521-y. [DOI] [PubMed] [Google Scholar]
  46. Mayer B. J., Jackson P. K., Van Etten R. A., Baltimore D. Point mutations in the abl SH2 domain coordinately impair phosphotyrosine binding in vitro and transforming activity in vivo. Mol Cell Biol. 1992 Feb;12(2):609–618. doi: 10.1128/mcb.12.2.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Medema R. H., de Laat W. L., Martin G. A., McCormick F., Bos J. L. GTPase-activating protein SH2-SH3 domains induce gene expression in a Ras-dependent fashion. Mol Cell Biol. 1992 Aug;12(8):3425–3430. doi: 10.1128/mcb.12.8.3425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Melo J. V., Gordon D. E., Cross N. C., Goldman J. M. The ABL-BCR fusion gene is expressed in chronic myeloid leukemia. Blood. 1993 Jan 1;81(1):158–165. [PubMed] [Google Scholar]
  49. Molgaard H. V., Spurr N. K., Greaves M. F. The hemopoietic stem cell antigen, CD34, is encoded by a gene located on chromosome 1. Leukemia. 1989 Nov;3(11):773–776. [PubMed] [Google Scholar]
  50. Mulley J. C., Callen D. F. New regional localisations for HAGH and PGP on human chromosome 16. Hum Genet. 1986 Dec;74(4):423–424. doi: 10.1007/BF00280498. [DOI] [PubMed] [Google Scholar]
  51. Nathans J., Thomas D., Hogness D. S. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science. 1986 Apr 11;232(4747):193–202. doi: 10.1126/science.2937147. [DOI] [PubMed] [Google Scholar]
  52. Nishi T., Lee P. S., Oka K., Levin V. A., Tanase S., Morino Y., Saya H. Differential expression of two types of the neurofibromatosis type 1 (NF1) gene transcripts related to neuronal differentiation. Oncogene. 1991 Sep;6(9):1555–1559. [PubMed] [Google Scholar]
  53. Ohmichi M., Decker S. J., Saltiel A. R. Nerve growth factor stimulates the tyrosine phosphorylation of a 38-kDa protein that specifically associates with the src homology domain of phospholipase C-gamma 1. J Biol Chem. 1992 Oct 25;267(30):21601–21606. [PubMed] [Google Scholar]
  54. Otsu M., Hiles I., Gout I., Fry M. J., Ruiz-Larrea F., Panayotou G., Thompson A., Dhand R., Hsuan J., Totty N. Characterization of two 85 kd proteins that associate with receptor tyrosine kinases, middle-T/pp60c-src complexes, and PI3-kinase. Cell. 1991 Apr 5;65(1):91–104. doi: 10.1016/0092-8674(91)90411-q. [DOI] [PubMed] [Google Scholar]
  55. Ozawa K., Sudo T., Soeda E., Yoshida M. C., Ishii S. Assignment of the human CREB2 (CRE-BP1) gene to 2q32. Genomics. 1991 Aug;10(4):1103–1104. doi: 10.1016/0888-7543(91)90210-6. [DOI] [PubMed] [Google Scholar]
  56. Pawson T., Gish G. D. SH2 and SH3 domains: from structure to function. Cell. 1992 Oct 30;71(3):359–362. doi: 10.1016/0092-8674(92)90504-6. [DOI] [PubMed] [Google Scholar]
  57. Pendergast A. M., Muller A. J., Havlik M. H., Maru Y., Witte O. N. BCR sequences essential for transformation by the BCR-ABL oncogene bind to the ABL SH2 regulatory domain in a non-phosphotyrosine-dependent manner. Cell. 1991 Jul 12;66(1):161–171. doi: 10.1016/0092-8674(91)90148-r. [DOI] [PubMed] [Google Scholar]
  58. Raziuddin A., Sarkar F. H., Dutkowski R., Shulman L., Ruddle F. H., Gupta S. L. Receptors for human alpha and beta interferon but not for gamma interferon are specified by human chromosome 21. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5504–5508. doi: 10.1073/pnas.81.17.5504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Ridley A. J., Hall A. 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):389–399. doi: 10.1016/0092-8674(92)90163-7. [DOI] [PubMed] [Google Scholar]
  60. Ridley A. J., Paterson H. F., Johnston C. L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 1992 Aug 7;70(3):401–410. doi: 10.1016/0092-8674(92)90164-8. [DOI] [PubMed] [Google Scholar]
  61. Ron D., Zannini M., Lewis M., Wickner R. B., Hunt L. T., Graziani G., Tronick S. R., Aaronson S. A., Eva A. A region of proto-dbl essential for its transforming activity shows sequence similarity to a yeast cell cycle gene, CDC24, and the human breakpoint cluster gene, bcr. New Biol. 1991 Apr;3(4):372–379. [PubMed] [Google Scholar]
  62. Rosenthal A., Rhee L., Yadegari R., Paro R., Ullrich A., Goeddel D. V. Structure and nucleotide sequence of a Drosophila melanogaster protein kinase C gene. EMBO J. 1987 Feb;6(2):433–441. doi: 10.1002/j.1460-2075.1987.tb04773.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Settleman J., Albright C. F., Foster L. C., Weinberg R. A. Association between GTPase activators for Rho and Ras families. Nature. 1992 Sep 10;359(6391):153–154. doi: 10.1038/359153a0. [DOI] [PubMed] [Google Scholar]
  65. Settleman J., Narasimhan V., Foster L. C., Weinberg R. A. Molecular cloning of cDNAs encoding the GAP-associated protein p190: implications for a signaling pathway from ras to the nucleus. Cell. 1992 May 1;69(3):539–549. doi: 10.1016/0092-8674(92)90454-k. [DOI] [PubMed] [Google Scholar]
  66. Shtivelman E., Lifshitz B., Gale R. P., Roe B. A., Canaani E. Alternative splicing of RNAs transcribed from the human abl gene and from the bcr-abl fused gene. Cell. 1986 Oct 24;47(2):277–284. doi: 10.1016/0092-8674(86)90450-2. [DOI] [PubMed] [Google Scholar]
  67. Takeda J., Maekawa T., Sudo T., Seino Y., Imura H., Saito N., Tanaka C., Ishii S. Expression of the CRE-BP1 transcriptional regulator binding to the cyclic AMP response element in central nervous system, regenerating liver, and human tumors. Oncogene. 1991 Jun;6(6):1009–1014. [PubMed] [Google Scholar]
  68. Trahey M., Wong G., Halenbeck R., Rubinfeld B., Martin G. A., Ladner M., Long C. M., Crosier W. J., Watt K., Koths K. Molecular cloning of two types of GAP complementary DNA from human placenta. Science. 1988 Dec 23;242(4886):1697–1700. doi: 10.1126/science.3201259. [DOI] [PubMed] [Google Scholar]
  69. Waksman G., Kominos D., Robertson S. C., Pant N., Baltimore D., Birge R. B., Cowburn D., Hanafusa H., Mayer B. J., Overduin M. Crystal structure of the phosphotyrosine recognition domain SH2 of v-src complexed with tyrosine-phosphorylated peptides. Nature. 1992 Aug 20;358(6388):646–653. doi: 10.1038/358646a0. [DOI] [PubMed] [Google Scholar]
  70. Williams S. V., Jones T. A., Cottrell S., Zehetner G., Varesco L., Ward T., Thomas H., Lawson P. A., Solomon E., Bodmer W. F. Fine mapping of probes in the adenomatous polyposis coli region of chromosome 5 by in situ hybridization. Genes Chromosomes Cancer. 1991 Sep;3(5):382–389. doi: 10.1002/gcc.2870030509. [DOI] [PubMed] [Google Scholar]
  71. Yatani A., Okabe K., Polakis P., Halenbeck R., McCormick F., Brown A. M. ras p21 and GAP inhibit coupling of muscarinic receptors to atrial K+ channels. Cell. 1990 Jun 1;61(5):769–776. doi: 10.1016/0092-8674(90)90187-j. [DOI] [PubMed] [Google Scholar]

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