Proteomic identification of the cerebral cavernous malformation signaling complex

Journal of Proteome Research

Volumn 6, Issue 11, 2007, Pages 4343-4355

  Hilder, Thomas L ^a   Malone, Michael H ^a   Bencharit, Sompop ^a,b   Colicelli, John ^c   Haystead, Timothy A ^d   Johnson, Gary L ^a   Wu, Christine C ^e  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

CCM3; Cerebral cavernous malformation; KRIT1; MudPIT; OSM; PDCD10

Indexed keywords

PHOSPHATIDYLINOSITIDE; PROTEIN KRIT1; PROTEIN OSM; PROTEIN PDCD10; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BRAIN MALFORMATION; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME BINDING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEOMICS; UNINDEXED SEQUENCE;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETON; HEMANGIOMA, CAVERNOUS, CENTRAL NERVOUS SYSTEM; HUMANS; IMMUNOPRECIPITATION; MAP KINASE KINASE KINASE 3; MEMBRANE PROTEINS; MICE; PHOSPHATES; PHOSPHATIDYLINOSITOLS; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; PROTO-ONCOGENE PROTEINS; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 36348946966     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr0704276     Document Type: Article

References (56)

1. Zabramski, J. M.; Henn, J. S.; Coons, S. Pathology of cerebral vascular malformations. Neurosurg. Clin. N. Am. 1999, 10 (3), 395-410.
2. Moriarity, J. L.; Clatterbuck, R. E.; Rigamonti, D. The natural history of cavernous malformations. Neurosurg. Clin. N. Am. 1999, 10 (3), 411-417.
3. Clatterbuck, R. E.; Eberhart, C. G.; Crain, B. J.; Rigamonti, D. Ultrastructural and immunocytochemical evidence that an incompetent blood-brain barrier is related to the pathophysiology of cavernous malformations. J. Neurol. Neurosurg. Psychiatry 2001, 71 (2), 188-192.
4. Zabramski, J. M.; Wascher, T. M.; Spetzler, R. F.; Johnson, B.; Golfinos, J.; Drayer, B. P.; Brown, B.; Rigamonti, D.; Brown, G. The natural history of familial cavernous malformations: results of an ongoing study. J. Neurosurg. 1994, 80 (3), 422-432.
5. Kondziolka, D.; Lunsford, L. D.; Kestle, J. R. The natural history of cerebral cavernous malformations. J. Neurosurg. 1995, 83 (5), 820-824.
6. Dubovsky, J.; Zabramski, J. M.; Kurth, J.; Spetzler, R. F.; Rich, S. S.; Orr, H. T.; Weber, J. L. A gene responsible for cavernous malformations of the brain maps to chromosome 7q. Hum. Mol. Genet. 1995, 4 (3), 453-458.
7. Craig, H. D.; Gunel, M.; Cepeda, O.; Johnson, E. W.; Ptacek, L.; Steinberg, G. K.; Ogilvy, C. S.; Berg, M. J.; Crawford, S. C.; Scott, R. M.; Steichen-Gersdorf, E.; Sabroe, R.; Kennedy, C. T.; Mettler, G.; Beis, M. J.; Fryer, A.; Awad, I. A.; Lifton, R. P. Multilocus linkage identifies two new loci for a mendelian form of stroke, cerebral cavernous malformation, at 7p15-13 and 3q25.2-27. Hum. Mol. Genet. 1998, 7 (12), 1851-1858.
8. Gunel, M.; Awad, I. A.; Anson, J.; Lifton, R. P. Mapping a gene causing cerebral cavernous malformation to 7q11.2-q21. Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (14), 6620-6624.
9. Marchuk, D. A.; Gallione, C. J.; Morrison, L. A.; Clericuzio, C. L.; Hart, B. L.; Kosofsky, B. E.; Louis, D. N.; Gusella, J. F.; Davis, L. E.; Prenger, V. L. A locus for cerebral cavernous malformations maps to chromosome 7q in two families. Genomics 1995, 28 (2), 311-314.
10. Laberge-le Couteulx, S.; Jung, H. H.; Labauge, P.; Houtteville, J. P.; Lescoat, C.; Cecillon, M.; Marechal, E.; Joutel, A.; Bach, J. F.; Tournier-Lasserve, E. Truncating mutations in CCM1, encoding KRIT1, cause hereditary cavernous angiomas. Nat. Genet. 1999, 23 (2), 189-193.
11. Sahoo, T.; Johnson, E. W.; Thomas, J. W.; Kuehl, P. M.; Jones, T. L.; Dokken, C. G.; Touchman, J. W.; Gallione, C. J.; Lee-Lin, S. Q.; Kosofsky, B.; Kurth, J. H.; Louis, D. N.; Mettler, G.; Morrison, L.; Gil-Nagel, A.; Rich, S. S.; Zabramski, J. M.; Boguski, M. S.; Green, E. D.; Marchuk, D. A. Mutations in the gene encoding KRIT1, a Krev-1/rap1a binding protein, cause cerebral cavernous malformations (CCM1). Hum. Mol. Genet. 1999, 8 (12), 2325-2333.
12. Liquori, C. L.; Berg, M. J.; Siegel, A. M.; Huang, E.; Zawistowski, J. S.; Stoffer, T.; Verlaan, D.; Balogun, F.; Hughes, L.; Leedom, T. P.; Plummer, N. W.; Cannella, M.; Maglione, V.; Squitieri, F.; Johnson, E. W.; Rouleau, G. A.; Ptacek, L.; Marchuk, D. A. Mutations in a gene encoding a novel protein containing a phosphotyrosine-binding domain cause type 2 cerebral cavernous malformations. Am. J. Hum. Genet. 2003, 73 (6), 1459-1464.
13. Denier, C.; Goutagny, S.; Labauge, P.; Krivosic, V.; Arnoult, M.; Cousin, A.; Benabid, A. L.; Comoy, J.; Frerebeau, P.; Gilbert, B.; Houtteville, J. P.; Jan, M.; Lapierre, F.; Loiseau, H.; Menei, P.; Mercier, P.; Moreau, J. J.; Nivelon-Chevallier, A.; Parker, F.; Redondo, A. M.; Scarabin, J. M.; Tremoulet, M.; Zerah, M.; Maciazek, J.; Tournier-Lasserve, E. Mutations within the MGC4607 gene cause cerebral cavernous malformations. Am. J. Hum. Genet. 2004, 74 (2), 326-337.
14. Bergametti, F.; Denier, C.; Labauge, P.; Arnoult, M.; Boetto, S.; Clanet, M.; Coubes, P.; Echenne, B.; Ibrahim, R.; Irthum, B.; Jacquet, G.; Lonjon, M.; Moreau, J. J.; Neau, J. P.; Parker, F.; Tremoulet, M.; Tournier-Lasserve, E. Mutations within the programmed cell death 10 gene cause cerebral cavernous malformations. Am. J. Hum. Genet. 2005, 76 (1), 42-51.
15. Bretscher, A.; Edwards, K.; Fehon, R. G. ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 2002, 3 (8), 586-599.
16. Mosavi, L. K.; Cammett, T. J.; Desrosiers, D. C.; Peng, Z. Y. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 2004, 13 (6), 1435-1448.
17. Zawistowski, J. S.; Stalheim, L.; Uhlik, M. T.; Abell, A. N.; Ancrile, B. B.; Johnson, G. L.; Marchuk, D. A. CCM1 and CCM2 protein interactions in cell signaling: implications for cerebral cavernous malformations pathogenesis. Hum. Mol. Genet. 2005, 14 (17), 2521-2531.
18. Zawistowski, J. S.; Serebriiskii, I. G.; Lee, M. F.; Golemis, E. A.; Marchuk, D. A. KRIT1 association with the integrin-binding protein ICAP-1: a new direction in the elucidation of cerebral cavernous malformations (CCM1) pathogenesis. Hum. Mol. Genet. 2002, 11 (4), 389-396.
19. Uhlik, M. T.; Abell, A. N.; Johnson, N. L.; Sun, W.; Cuevas, B. D.; Lobel-Rice, K. E.; Horne, E. A.; Dell'Acqua, M. L.; Johnson, G. L., Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat. Cell Biol. 2003, 5 (12), 1104-1110.
20. Laurans, M. S.; DiLuna, M. L.; Shin, D.; Niazi, F.; Voorhees, J. R.; Nelson-Williams, C.; Johnson, E. W.; Siegel, A. M.; Steinberg, G. K.; Berg, M. J.; Scott, R. M.; Tedeschi, G.; Enevoldson, T. P.; Anson, J.; Rouleau, G. A.; Ogilvy, C.; Awad, I. A.; Lifton, R. P.; Gunel, M. Mutational analysis of 206 families with cavernous malformations. J. Neurosurg. 2003, 99 (1), 38-43.
21. Sun, W.; Kesavan, K.; Schaefer, B. C.; Garrington, T. P.; Ware, M.; Johnson, N. L.; Gelfand, E. W.; Johnson, G. L. MEKK2 associates with the adapter protein Lad/RIBP and regulates the MEK5-BMK1/ERK5 pathway. J. Biol. Chem. 2001, 276 (7), 5093-5100.
22. Lennon, G.; Auffray, C.; Polymeropoulos, M.; Soares, M. B. The I. M. A. G. E. Consortium: an integrated molecular analysis of genomes and their expression. Genomics 1996, 33 (1), 151-152.
23. Nolan, G. P.; Shatzman, A. R. Expression vectors and delivery systems. Curr. Opin. Biotechnol. 1998, 9 (5), 447-450.
24. Pear, W. S.; Nolan, G. P.; Scott, M. L.; Baltimore, D. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. U.S.A. 1993, 90 (18), 8392-8396.
25. Jin, J.; Smith, F. D.; Stark, C.; Wells, C. D.; Fawcett, J. P.; Kulkarni, S.; Metalnikov, P.; O'Donnell, P.; Taylor, P.; Taylor, L.; Zougman, A.; Woodgett, J. R.; Langeberg, L. K.; Scott, J. D.; Pawson, T., Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 2004, 14 (16), 1436-1450.
26. Wessel, D.; Flugge, U. I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 1984, 138 (1), 141-143.
27. Washburn, M. P.; Wolters, D.; Yates, J. R., 3rd. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19 (3), 242-247.
28. Gatlin, C. L.; Kleemann, G. R.; Hays, L. G.; Link, A. J.; Yates, J. R., 3rd. Protein identification at the low femtomole level from silver-stained gels using a new fritless electrospray interface for liquid chromatography-microspray and nanospray mass spectrometry. Anal. Biochem. 1998, 263 (1), 93-101.
29. McDonald, W. H.; Tabb, D. L.; Sadygov, R. G.; MacCoss, M. J.; Venable, J.; Graumann, J.; Johnson, J. R.; Cociorva, D.; Yates, J. R., 3rd. MS1, MS2, and SQT-three unified, compact, and easily parsed file formats for the storage of shotgun proteomic spectra and identifications. Rapid Commun. Mass Spectrom. 2004, 18 (18), 2162-2168.
30. Blackler, A. R.; Klammer, A. A.; MacCoss, M. J.; Wu, C. C. Quantitative comparison of proteomic data quality between a 2D and 3D quadrupole ion trap. Anal. Chem. 2006, 78 (4), 1337-1344.
31. MacCoss, M. J.; Wu, C. C.; Yates, J. R., 3rd. Probability-based validation of protein identifications using a modified SEQUEST algorithm. Anal. Chem. 2002, 74 (21), 5593-5599.
32. Yates, J. R., 3rd.; Eng, J. K.; McCormack, A. L.; Schieltz, D. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 1995, 67 (8), 1426-1436.
33. Tabb, D. L.; McDonald, W. H.; Yates, J. R., 3rd. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 2002, 1 (1), 21-26.
34. Uhlik, M. T.; Temple, B.; Bencharit, S.; Kimple, A. J.; Siderovski, D. P.; Johnson, G. L. Structural and evolutionary division of phosphotyrosine binding (PTB) domains. J. Mol. Biol. 2005, 345 (1), 1-20.
35. Condeelis, J. Elongation factor 1 alpha, translation and the cytoskeleton. Trends Biochem. Sci. 1995, 20 (5), 169-170.
36. Liu, G.; Grant, W. M.; Persky, D.; Latham, V. M., Jr.; Singer, R. H.; Condeelis, J. Interactions of elongation factor 1alpha with F-actin and beta-actin mRNA: implications for anchoring mRNA in cell protrusions. Mol. Biol. Cell 2002, 13 (2), 579-592.
37. Browne, G. J.; Proud, C. G. Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 2002, 269 (22), 5360-5368.
38. Gross, S. R.; Kinzy, T. G. Translation elongation factor 1A is essential for regulation of the actin cytoskeleton and cell morphology. Nat. Struct. Mol. Biol. 2005, 12 (9), 772-778.
39. Koch, H. B.; Zhang, R.; Verdoodt, B.; Bailey, A.; Zhang, C. D.; Yates, J. R., 3rd.; Menssen, A.; Hermeking, H. Large-scale identification of c-MYC-associated proteins using a combined TAP/MudPIT approach. Cell Cycle 2007, 6 (2), 205-217.
40. Sun, W.; Wei, X.; Kesavan, K.; Garrington, T. P.; Fan, R.; Mei, J.; Anderson, S. M.; Gelfand, E. W.; Johnson, G. L. MEK kinase 2 and the adaptor protein Lad regulate extracellular signal-regulated kinase 5 activation by epidermal growth factor via Src. Mol. Cell. Biol. 2003, 23 (7), 2298-2308.
41. Liu, H.; Sadygov, R. G.; Yates, J. R., 3rd. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 2004, 76 (14), 4193-4201.
42. Munshi, R.; Kandl, K. A.; Carr-Schmid, A.; Whitacre, J. L.; Adams, A. E.; Kinzy, T. G. Overexpression of translation elongation factor 1A affects the organization and function of the actin cytoskeleton in yeast. Genetics 2001, 157 (4), 1425-1436.
43. Murray, J. W.; Edmonds, B. T.; Liu, G.; Condeelis, J. Bundling of actin filaments by elongation factor 1 alpha inhibits polymerization at filament ends. J. Cell Biol. 1996, 135 (5), 1309-1321.
44. Owen, C. H.; DeRosier, D. J.; Condeelis, J. Actin crosslinking protein EF-1a of Dictyostelium discoideum has a unique bonding rule that allows square-packed bundles. J. Struct. Biol. 1992, 109 (3), 248-254.
45. Yang, F.; Demma, M.; Warren, V.; Dharmawardhane, S.; Condeelis, J. Identification of an actin-binding protein from Dictyostelium as elongation factor 1a. Nature 1990, 347 (6292), 494-496.
46. Bliss, J. M.; Venkatesh, B.; Colicelli, J. The RIN Family of Ras Effectors. Methods Enzymol. 2005, 407, 335-344.
47. Yang, J.; Boerm, M.; McCarty, M.; Bucana, C.; Fidler, I. J.; Zhuang, Y.; Su, B. Mekk3 is essential for early embryonic cardiovascular development. Nat. Genet. 2000, 24 (3), 309-313.
48. Gunel, M.; Laurans, M. S.; Shin, D.; DiLuna, M. L.; Voorhees, J.; Choate, K.; Nelson-Williams, C.; Lifton, R. P. KRIT1, a gene mutated in cerebral cavernous malformation, encodes a microtubule-associated protein. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (16), 10677-10682.
49. Goldfinger, L. E.; Ptak, C.; Jeffery, E. D.; Shabanowitz, J.; Han, J.; Haling, J. R.; Sherman, N. E.; Fox, J. W.; Hunt, D. F.; Ginsberg, M. H. An Experimentally Derived Database of Candidate Ras-Interacting Proteins. J. Proteome Res. 2007, 6 (5), 1806-1811.
50. Dunn, A. Y.; Melville, M. W.; Frydman, J. Review: cellular substrates of the eukaryotic chaperonin TRiC/CCT. J. Struct. Biol. 2001, 135 (2), 176-184.
51. Spiess, C.; Meyer, A. S.; Reissmann, S.; Frydman, J. Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol. 2004, 14 (11), 598-604.
52. Sternlicht, H.; Farr, G. W.; Sternlicht, M. L.; Driscoll, J. K.; Willison, K.; Yaffe, M. B. The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc. Natl. Acad. Sci. U.S.A. 1993, 90 (20), 9422-9426.
53. Rodriguez-Viciana, P.; Sabatier, C.; McCormick, F. Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol. Cell. Biol. 2004, 24 (11), 4943-4954.
54. Wohlgemuth, S.; Kiel, C.; Kramer, A.; Serrano, L.; Wittinghofer, F.; Herrmann, C. Recognizing and defining true Ras binding domains I: biochemical analysis. J. Mol. Biol. 2005, 348 (3), 741-758.
55. Kimura, T.; Sakisaka, T.; Baba, T.; Yamada, T.; Takai, Y. Involvement of the Ras-Ras-activated Rab5 guanine nucleotide exchange factor RIN2-Rab5 pathway in the hepatocyte growth factor-induced endocytosis of E-cadherin. J. Biol. Chem. 2006, 281 (15), 10598-10609.
56. Zhang, J.; Clatterbuck, R. E.; Rigamonti, D.; Chang, D. D.; Dietz, H. C. Interaction between krit1 and icap1alpha infers perturbation of integrin beta1-mediated angiogenesis in the pathogenesis of cerebral cavernous malformation. Hum. Mol. Genet. 2001, 10 (25), 2953-2960.