Kinetic mechanisms of mutation-dependent harvey ras activation and their relevance for the development of costello syndrome

Biochemistry

Volumn 52, Issue 47, 2013, Pages 8465-8479

  Wey, Michael ^a   Lee, Jungwoon ^a,b   Jeong, Soon Seog ^c   Kim, Jungho ^b   Heo, Jongyun ^a  

^a UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

^b Sogang University   (South Korea)

^c HumanZyme   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROAD SPECTRUM; INTRINSIC KINETICS; KINETIC MECHANISM; MUTANT PROTEINS; UPPER-END;

CHEMICAL ACTIVATION; DISEASES;

KINETICS;

GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; MUTANT PROTEIN; PROTEIN P120; RAS PROTEIN;

ANIMAL CELL; ARTICLE; CALCULATION; CARCINOGENESIS; COSTELLO SYNDROME; GENE MUTATION; GENE SEQUENCE; KINETICS; MOUSE; NONHUMAN; ONCOGENE H RAS; PRIORITY JOURNAL; THEORETICAL STUDY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; BIOCATALYSIS; COSTELLO SYNDROME; ENZYME ACTIVATION; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HUMANS; HYDROLYSIS; KINETICS; MICE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; NIH 3T3 CELLS; P120 GTPASE ACTIVATING PROTEIN; PROTEIN STRUCTURE, SECONDARY; PROTO-ONCOGENE PROTEINS P21(RAS); RAS-GRF1; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84888586550     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400679q     Document Type: Article

References (56)

1. Oxford, G. and Theodorescu, D. (2003) Ras superfamily monomeric G proteins in carcinoma cell motility Cancer Lett. 189, 117-128
2. Marshall, C. B., Meiri, D., Smith, M. J., Mazhab-Jafari, M. T., Gasmi-Seabrook, G. M. C., Rottapel, R., Stambolic, V., and Ikura, M. (2012) Probing the GTPase cycle with real-time NMR: GAP and GEF activities in cell extracts Methods 57, 473-485
3. Geyer, M. and Wittinghofer, A. (1997) GEFs, GAPs, GDIs and effectors: Taking a closer (3D) look at the regulation of Ras-related GTP-binding proteins Curr. Opin. Struct. Biol. 7, 786-792
4. Bonfini, L., Karlovich, C. A., Dasgupta, C., and Banerjee, U. (1992) The Son of sevenless gene product: A putative activator of Ras Science 255, 603-606
5. Ebinu, J. O., Bottorff, D. A., Chan, E. Y., Stang, S. L., Dunn, R. J., and Stone, J. C. (1998) RasGRP, a Ras guanyl nucleotide-releasing protein with calcium- and diacylglycerol-binding motifs Science 280, 1082-1086
6. Bottorff, D., Ebinu, J., and Stone, J. C. (1999) RasGRP, a Ras activator: Mouse and human cDNA sequences and chromosomal positions Mamm. Genome 10, 358-361
7. Boriack-Sjodin, P. A., Margarit, S. M., Bar-Sagi, D., and Kuriyan, J. (1998) The structural basis of the activation of Ras by Sos Nature 394, 337-343
8. Traut, T. W. (1994) Physiological concentrations of purines and pyrimidines Mol. Cell. Biochem. 140, 1-22
9. Sprang, S. (2001) GEFs: Master regulators of G-protein activation Trends Biochem. Sci. 26, 266-267
10. Grewal, T., Koese, M., Tebar, F., and Enrich, C. (2011) Differential Regulation of RasGAPs in Cancer Genes Cancer 2, 288-297
11. Scheffzek, K., Ahmadian, M. R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997) The Ras-RasGAP complex: Structural basis for GTPase activation and its loss in oncogenic Ras mutants Science 277, 333-338
12. Boguski, M. S. and McCormick, F. (1993) Proteins regulating Ras and its relatives Nature 366, 643-654
13. Schubbert, S., Shannon, K., and Bollag, G. (2007) Hyperactive Ras in developmental disorders and cancer Nat. Rev. Cancer 7, 295-308
14. Roberts, P. J. and Der, C. J. (2007) Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer Oncogene 26, 3291-3310
15. Fasano, O., Aldrich, T., Tamanoi, F., Taparowsky, E., Furth, M., and Wigler, M. (1984) Analysis of the transforming potential of the human H-ras gene by random mutagenesis Proc. Natl. Acad. Sci. U.S.A. 81, 4008-4012
16. Matsuda, K., Shimada, A., Yoshida, N., Ogawa, A., Watanabe, A., Yajima, S., Iizuka, S., Koike, K., Yanai, F., Kawasaki, K., Yanagimachi, M., Kikuchi, A., Ohtsuka, Y., Hidaka, E., Yamauchi, K., Tanaka, M., Yanagisawa, R., Nakazawa, Y., Shiohara, M., Manabe, A., and Kojima, S. (2007) Spontaneous improvement of hematologic abnormalities in patients having juvenile myelomonocytic leukemia with specific RAS mutations Blood 109, 5477-5480
17. Jakubauskas, A. and Griskevicius, L. (2010) KRas and BRaf mutational status analysis from formalin-fixed, paraffin-embedded tissues using multiplex polymerase chain reaction-based assay Arch. Pathol. Lab. Med. 134, 620-624
18. Sahu, R. P., Batra, S., Kandala, P. K., Brown, T. L., and Srivastava, S. K. (2011) The role of K-ras gene mutation in TRAIL-induced apoptosis in pancreatic and lung cancer cell lines Cancer Chemother. Pharmacol. 67, 481-487
19. Seeburg, P. H., Colby, W. W., Capon, D. J., Goeddel, D. V., and Levinson, A. D. (1984) Biological properties of human c-Ha-ras1 genes mutated at codon 12 Nature 312, 71-75
20. 2+ on the guanine nucleotide exchange rate of p21N-ras J. Biol. Chem. 261, 10963-10965
21. Gideon, P., John, J., Frech, M., Lautwein, A., Clark, R., Scheffler, J. E., and Wittinghofer, A. (1992) Mutational and kinetic analyses of the GTPase-activating protein (GAP)-p21 interaction: The C-terminal domain of GAP is not sufficient for full activity Mol. Cell. Biol. 12, 2050-2056
22. Mm Biochemistry 37, 7420-7430
23. Cotton, F. A. and Wilkinson, G. (1988) Advanced Inorganic Chemistry, 5 th ed., John Wiley & Sons, New York.
24. Heo, J. and Campbell, S. L. (2005) Superoxide Anion Radical Modulates the Activity of Ras and Ras-related GTPases by a Radical-based Mechanism Similar to that of Nitric Oxide J. Biol. Chem. 280, 12438-12445
25. Leupold, C. M., Goody, R. S., and Wittinghofer, A. (1983) Stereochemistry of the elongation factor Tu X GTP complex Eur. J. Biochem. 135, 237-241
26. Eccleston, J. F., Moore, K. J., Morgan, L., Skinner, R. H., and Lowe, P. N. (1993) Kinetics of interaction between normal and proline 12 Ras and the GTPase-activating proteins, p120-GAP and neurofibromin. The significance of the intrinsic GTPase rate in determining the transforming ability of ras J. Biol. Chem. 268, 27012-27019
27. Downward, J., Graves, J. D., Warne, P. H., Rayter, S., and Cantrell, D. A. (1990) Stimulation of p21ras upon T-cell activation Nature 346, 719-723
28. Krengel, U., Schlichting, I., Scherer, A., Schumann, R., Frech, M., John, J., Kabsch, W., Pai, E. F., and Wittinghofer, A. (1990) Three-dimensional structures of H-ras p21 mutants: Molecular basis for their inability to function as signal switch molecules Cell 62, 539-548
29. John, J., Frech, M., and Wittinghofer, A. (1988) Biochemical properties of Ha-ras encoded p21 mutants and mechanism of the autophosphorylation reaction J. Biol. Chem. 263, 11792-11799
30. Maurer, T., Garrenton, L. S., Oh, A., Pitts, K., Anderson, D. J., Skelton, N. J., Fauber, B. P., Pan, B., Malek, S., Stokoe, D., Ludlam, M. J., Bowman, K. K., Wu, J., Giannetti, A. M., Starovasnik, M. A., Mellman, I., Jackson, P. K., Rudolph, J., Wang, W., and Fang, G. (2012) Small-molecule ligands bind to a distinct pocket in Ras and inhibit SOS-mediated nucleotide exchange activity Proc. Natl. Acad. Sci. U.S.A. 109, 5299-5304
31. Kuniba, H., Pooh, R. K., Sasaki, K., Shimokawa, O., Harada, N., Kondoh, T., Egashira, M., Moriuchi, H., Yoshiura, K., and Niikawa, N. (2009) Prenatal diagnosis of Costello syndrome using 3D ultrasonography amniocentesis confirmation of the rare HRAS mutation G12D Am. J. Med. Genet., Part A 149, 785-787
32. Gureasko, J., Galush, W. J., Boykevisch, S., Sondermann, H., Bar-Sagi, D., Groves, J. T., and Kuriyan, J. (2008) Membrane-dependent signal integration by the Ras activator Son of sevenless Nat. Struct. Mol. Biol. 15, 452-461
33. Bollag, G. and McCormick, F. (1991) Differential regulation of rasGAP and neurofibromatosis gene product activities Nature 351, 576-579
34. Scheele, J. S., Rhee, J. M., and Boss, G. R. (1995) Determination of absolute amounts of GDP and GTP bound to Ras in mammalian cells: Comparison of parental and Ras-overproducing NIH 3T3 fibroblasts Proc. Natl. Acad. Sci. U.S.A. 92, 1097-1100
35. Gelb, B. D. and Tartaglia, M. (2006) Noonan syndrome and related disorders: Dysregulated RAS-mitogen activated protein kinase signal transduction Hum. Mol. Genet. 15 (Special Issue 2) R220-R226
36. Aoki, Y., Niihori, T., Kawame, H., Kurosawa, K., Ohashi, H., Tanaka, Y., Filocamo, M., Kato, K., Suzuki, Y., Kure, S., and Matsubara, Y. (2005) Germline mutations in HRAS proto-oncogene cause Costello syndrome Nat. Genet. 37, 1038-1040
37. Gripp, K. W., Lin, A. E., Stabley, D. L., Nicholson, L., Scott, C. I., Jr., Doyle, D., Aoki, Y., Matsubara, Y., Zackai, E. H., Lapunzina, P., Gonzalez-Meneses, A., Holbrook, J., Agresta, C. A., Gonzalez, I. L., and Sol-Church, K. (2006) HRAS mutation analysis in Costello syndrome: Genotype and phenotype correlation Am. J. Med. Genet., Part A 140, 1-7
38. Estep, A. L., Tidyman, W. E., Teitell, M. A., Cotter, P. D., and Rauen, K. A. (2006) HRAS mutations in Costello syndrome: Detection of constitutional activating mutations in codon 12 and 13 and loss of wild-type allele in malignancy Am. J. Med. Genet., Part A 140, 8-16
39. Kerr, B., Delrue, M. A., Sigaudy, S., Perveen, R., Marche, M., Burgelin, I., Stef, M., Tang, B., Eden, O. B., O'Sullivan, J., De Sandre-Giovannoli, A., Reardon, W., Brewer, C., Bennett, C., Quarell, O., M'Cann, E., Donnai, D., Stewart, F., Hennekam, R., Cave, H., Verloes, A., Philip, N., Lacombe, D., Levy, N., Arveiler, B., and Black, G. (2006) Genotype-phenotype correlation in Costello syndrome: HRAS mutation analysis in 43 cases J. Med. Genet. 43, 401-405
40. Sol-Church, K., Stabley, D. L., Nicholson, L., Gonzalez, I. L., and Gripp, K. W. (2006) Paternal bias in parental origin of HRAS mutations in Costello syndrome Hum. Mutat. 27, 736-741
41. Zampino, G., Pantaleoni, F., Carta, C., Cobellis, G., Vasta, I., Neri, C., Pogna, E. A., De Feo, E., Delogu, A., Sarkozy, A., Atzeri, F., Selicorni, A., Rauen, K. A., Cytrynbaum, C. S., Weksberg, R., Dallapiccola, B., Ballabio, A., Gelb, B. D., Neri, G., and Tartaglia, M. (2007) Diversity, parental germline origin, and phenotypic spectrum of de novo HRAS missense changes in Costello syndrome Hum. Mutat. 28, 265-272
42. van der Burgt, I., Kupsky, W., Stassou, S., Nadroo, A., Barroso, C., Diem, A., Kratz, C. P., Dvorsky, R., Ahmadian, M. R., and Zenker, M. (2007) Myopathy caused by HRAS germline mutations: Implications for disturbed myogenic differentiation in the presence of constitutive HRas activation J. Med. Genet. 44, 459-462
43. Gripp, K. W., Innes, A. M., Axelrad, M. E., Gillan, T. L., Parboosingh, J. S., Davies, C., Leonard, N. J., Lapointe, M., Doyle, D., Catalano, S., Nicholson, L., Stabley, D. L., and Sol-Church, K. (2008) Costello syndrome associated with novel germline HRAS mutations: An attenuated phenotype? Am. J. Med. Genet., Part A 146, 683-690
44. Burkitt-Wright, E. M., Bradley, L., Shorto, J., McConnell, V. P., Gannon, C., Firth, H. V., Park, S. M., D'Amore, A., Munyard, P. F., Turnpenny, P. D., Charlton, A., Wilson, M., and Kerr, B. (2012) Neonatal lethal Costello syndrome and unusual dinucleotide deletion/insertion mutations in HRAS predicting p.Gly12Val Am. J. Med. Genet., Part A 158, 1102-1110
45. Niihori, T., Aoki, Y., Okamoto, N., Kurosawa, K., Ohashi, H., Mizuno, S., Kawame, H., Inazawa, J., Ohura, T., Arai, H., Nabatame, S., Kikuchi, K., Kuroki, Y., Miura, M., Tanaka, T., Ohtake, A., Omori, I., Ihara, K., Mabe, H., Watanabe, K., Niijima, S., Okano, E., Numabe, H., and Matsubara, Y. (2011) HRAS mutants identified in Costello syndrome patients can induce cellular senescence: Possible implications for the pathogenesis of Costello syndrome J. Hum. Genet. 56, 707-715
46. Digilio, M. C., Lepri, F., Baban, A., Dentici, M. L., Versacci, P., Capolino, R., Ferese, R., De Luca, A., Tartaglia, M., Marino, B., and Dallapiccola, B. (2011) RASopathies: Clinical Diagnosis in the First Year of Life Mol. Syndromol. 1, 282-289
47. Tidyman, W. E., Lee, H. S., and Rauen, K. A. (2011) Skeletal muscle pathology in Costello and cardio-facio-cutaneous syndromes: Developmental consequences of germline Ras/MAPK activation on myogenesis Am. J. Med. Genet., Part C 157, 104-114
48. Gripp, K. W., Hopkins, E., Sol-Church, K., Stabley, D. L., Axelrad, M. E., Doyle, D., Dobyns, W. B., Hudson, C., Johnson, J., Tenconi, R., Graham, G. E., Sousa, A. B., Heller, R., Piccione, M., Corsello, G., Herman, G. E., Tartaglia, M., and Lin, A. E. (2011) Phenotypic Analysis of Individuals With Costello Syndrome due to HRAS p.G13C Am. J. Med. Genet., Part A 155, 706-716
49. Piccione, M., Piro, E., Pomponi, M. G., Matina, F., Pietrobono, R., Candela, E., Gabriele, B., Neri, G., and Corsello, G. (2009) A Premature Infant With Costello Syndrome Due to a Rare G13C HRAS Mutation Am. J. Med. Genet., Part A 149, 487-489
50. Schulz, A. L., Albrecht, B., Arici, C., van der Burgt, I., Buske, A., Gillessen-Kaesbach, G., Heller, R., Horn, D., Hubner, C. A., Korenke, G. C., Konig, R., Kress, W., Kruger, G., Meinecke, P., Mucke, J., Plecko, B., Rossier, E., Schinzel, A., Schulze, A., Seemanova, E., Seidel, H., Spranger, S., Tuysuz, B., Uhrig, S., Wieczorek, D., Kutsche, K., and Zenker, M. (2008) Mutation and phenotypic spectrum in patients with cardio-facio-cutaneous and Costello syndrome Clin. Genet. 73, 62-70
51. Denayer, E., Parret, A., Chmara, M., Schubbert, S., Vogels, A., Devriendt, K., Frijns, J. P., Rybin, V., de Ravel, T. J., Shannon, K., Cools, J., Scheffzek, K., and Legius, E. (2008) Mutation analysis in Costello syndrome: Functional and structural characterization of the HRAS p.Lys117Arg mutation Hum. Mutat. 29, 232-239
52. Sinico, M., Bassez, G., Touboul, C., Cave, H., Vergnaud, A., Zirah, C., Fleury-Feith, J., Gettler, S., Vojtek, A. M., Chevalier, N., Amram, D., Alsamad, I. A., Haddad, B., and Encha-Razavi, F. (2011) Excess of neuromuscular spindles in a fetus with Costello syndrome: A clinicopathological report Pediatr. Dev. Pathol. 14, 218-223
53. Piispanen, A. E., Bonnefoi, O., Carden, S., Deveau, A., Bassilana, M., and Hogan, D. A. (2011) Roles of Ras1 membrane localization during Candida albicans hyphal growth and farnesol response Eukaryotic Cell 10, 1473-1484
54. Franken, S. M., Scheidig, A. J., Krengel, U., Rensland, H., Lautwein, A., Geyer, M., Scheffzek, K., Goody, R. S., Kalbitzer, H. R., and Pai, E. F. 1993, Three-dimensional structures and properties of a transforming and a nontransforming glycine-12 mutant of p21H-ras Biochemistry 32, 8411-8420
55. Gibbs, J. B., Schaber, M. D., Allard, W. J., Sigal, I. S., and Scolnick, E. M. (1988) Purification of ras GTPase activating protein from bovine brain Proc. Natl. Acad. Sci. U.S.A. 85, 5026-5030
56. Feig, L. A. and Cooper, G. M. (1988) Relationship among guanine nucleotide exchange, GTP hydrolysis, and transforming potential of mutated ras proteins Mol. Cell. Biol. 8, 2472-2478