The neurofibromin recruitment factor Spred1 binds to the GAP related domain without affecting Ras inactivation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 27, 2016, Pages 7497-7502

  Dunzendorfer Matt, Theresia ^a   Mercado, Ellen L ^b   Maly, Karl ^a   McCormick, Frank ^b   Scheffzek, Klaus ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer; Nontruncating mutations; Protein protein interaction; RASopathy; Signal transduction

Indexed keywords

ENA VASP HOMOLOGY 1 PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATE; NEUROFIBROMIN; PEPTIDES AND PROTEINS; RAS PROTEIN; SPROUTY RELATED EVH1 DOMAIN CONTAINING 1 PROTEIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; SIGNAL PEPTIDE; SPRED1 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; INSECT CELL; LEGIUS SYNDROME; MISSENSE MUTATION; NEOPLASM; NEUROFIBROMA; NEUROFIBROMATOSIS TYPE 1; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; METABOLISM;

HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NEUROFIBROMIN 1; PROTEIN DOMAINS; RAS PROTEINS;

EID: 84977277330     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1607298113     Document Type: Article

References (51)

1. Riccardi VM (1992) Neurofibromatosis: Phenotype Natural History, and Pathogenesis (Johns Hopkins Univ Press, Baltimore), 2nd Ed.
2. Upadhyaya M, Cooper DN, eds (2012) Neurofibromatosis Type 1: Molecular and Cellular Biology (Springer, New York).
3. Ballester R, et al. (1990) The NF1 locus encodes a protein functionally related to mammalian GAP and yeast IRA proteins. Cell 63(4):851-859.
4. Martin GA, et al. (1990) The GAP-related domain of the neurofibromatosis type 1 gene product interacts with ras p21. Cell 63(4):843-849.
5. Xu GF, et al. (1990) The catalytic domain of the neurofibromatosis type 1 gene product stimulates ras GTPase and complements ira mutants of S. cerevisiae. Cell 63(4):835-841.
6. Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455(7216):1061-1068.
7. Ding L, et al. (2008) Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455(7216):1069-1075.
8. Sangha N, et al. (2008) Neurofibromin 1 (NF1) defects are common in human ovarian serous carcinomas and co-occur with TP53 mutations. Neoplasia (New York, N.Y.) 10(12):1362-1372.
9. Kan Z, et al. (2010) Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466(7308):869-873.
10. Boudry-Labis E, et al.; French ALFA group (2013) Neurofibromatosis-1 gene deletions and mutations in de novo adult acute myeloid leukemia. Am J Hematol 88(4):306-311.
11. Parsons DW, et al. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321(5897):1807-1812.
12. Hölzel M, et al. (2010) NF1 is a tumor suppressor in neuroblastoma that determines retinoic acid response and disease outcome. Cell 142(2):218-229.
13. Aravind L, Neuwald AF, Ponting CP (1999) Sec14p-like domains in NF1 and Dbl-like proteins indicate lipid regulation of Ras and Rho signaling. Curr Biol 9(6):R195-R197.
14. D'Angelo I, Welti S, Bonneau F, Scheffzek K (2006) A novel bipartite phospholipidbinding module in the neurofibromatosis type 1 protein. EMBO Rep 7(2):174-179.
15. WeltiS, D'Angelo I, Scheffzek K (2008) Neurofibromatoses (Karger, Würzburg, Germany), p192.
16. Ratner N, Miller SJ (2015) A RASopathy gene commonly mutated in cancer: The neurofibromatosis type 1 tumour suppressor. Nat Rev Cancer 15(5):290-301.
17. Brems H, et al. (2007) Germline loss-of-function mutations in SPRED1 cause a neurofibromatosis 1-like phenotype. Nat Genet 39(9):1120-1126.
18. Brems H, et al. (2012) Review and update of SPRED1 mutations causing Legius syndrome. Hum Mutat 33(11):1538-1546.
19. Wakioka T, et al. (2001) Spred is a Sprouty-related suppressor of Ras signalling. Nature 412(6847):647-651.
20. Miyoshi K, et al. (2004) The Sprouty-related protein, Spred, inhibits cell motility, metastasis, and Rho-mediated actin reorganization. Oncogene 23(33):5567-5576.
21. Nonami A, et al. (2005) The Sprouty-related protein, Spred-1, localizes in a lipid raft/ caveola and inhibits ERK activation in collaboration with caveolin-1. Genes Cells 10(9): 887-895.
22. Kim HJ, Bar-Sagi D (2004) Modulation of signalling by Sprouty: A developing story. Nat Rev Mol Cell Biol 5(6):441-450.
23. Pasmant E, et al. (2015) SPRED1, a RAS MAPK pathway inhibitor that causes Legius syndrome, is a tumour suppressor downregulated in paediatric acute myeloblastic leukaemia. Oncogene 34(5):631-638.
24. Harmer NJ, Sivak JM, Amaya E, Blundell TL (2005) 1.15 A crystal structure of the X. tropicalis Spred1 EVH1 domain suggests a fourth distinct peptide-binding mechanism within the EVH1 family. FEBS Lett 579(5):1161-1166.
25. Scheffzek K, Welti S (2012) Pleckstrin homology (PH) like domains - versatile modules in protein-protein interaction platforms. FEBS Lett 586(17):2662-2673.
26. Ball LJ, Jarchau T, Oschkinat H, Walter U (2002) EVH1 domains: Structure, function and interactions. FEBS Lett 513(1):45-52.
27. Peterson FC, Volkman BF (2009) Diversity of polyproline recognition by EVH1 domains. Front Biosci (Landmark Ed) 14:833-846.
28. Prehoda KE, Lee DJ, Lim WA (1999) Structure of the enabled/VASP homology 1 domain-peptide complex: A key component in the spatial control of actin assembly. Cell 97(4):471-480.
29. Bundschu K, Walter U, Schuh K (2007) Getting a first clue about SPRED functions. BioEssays 29(9):897-907.
30. Stowe IB, et al. (2012) A shared molecular mechanism underlies the human rasopathies Legius syndrome and Neurofibromatosis-1. Genes Dev 26(13):1421-1426.
31. McClatchey AI, Cichowski K (2012) SPRED proteins provide a NF-ty link to Ras suppression. Genes Dev 26(14):1515-1519.
32. Mittal R, Ahmadian MR, Goody RS, Wittinghofer A (1996) Formation of a transitionstate analog of the Ras GTPase reaction by Ras-GDP, tetrafluoroaluminate, and GTPase-activating proteins. Science 273(5271):115-117.
33. Scheffzek K, et al. (1998) Structural analysis of the GAP-related domain from neurofibromin and its implications. EMBO J 17(15):4313-4327.
34. Ahmadian MR, Hoffmann U, Goody RS, Wittinghofer A (1997) Individual rate constants for the interaction of Ras proteins with GTPase-activating proteins determined by fluorescence spectroscopy. Biochemistry 36(15):4535-4541.
35. Cichowski K, Jacks T (2001) NF1 tumor suppressor gene function: Narrowing the GAP. Cell 104(4):593-604.
36. Zhu Y, Parada LF (2001) Neurofibromin, a tumor suppressor in the nervous system. Exp Cell Res 264(1):19-28.
37. Ahmadian MR, Wiesmüller L, Lautwein A, Bischoff FR, Wittinghofer A (1996) Structural differences in the minimal catalytic domains of the GTPase-activating proteins p120GAP and neurofibromin. J Biol Chem 271(27):16409-16415.
38. Fahsold R, et al. (2000) Minor lesion mutational spectrum of the entire NF1 gene does not explain its high mutability but points to a functional domain upstream of the GAP-related domain. Am J Hum Genet 66(3):790-818.
39. Kaplan DR, Morrison DK, Wong G, McCormick F, Williams LT (1990) PDGF betareceptor stimulates tyrosine phosphorylation of GAP and association of GAP with a signaling complex. Cell 61(1):125-133.
40. Sivak JM, Petersen LF, Amaya E (2005) FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev Cell 8(5):689-701.
41. Sasaki A, Taketomi T, Wakioka T, Kato R, Yoshimura A (2001) Identification of a dominant negative mutant of Sprouty that potentiates fibroblast growth factor- but not epidermal growth factor-induced ERK activation. JBiolChem276(39):36804-36808.
42. Broach JR (1991) Ras-regulated signaling processes in Saccharomyces cerevisiae. Curr Opin Genet Dev 1(3):370-377.
43. Pena V, et al. (2008) The C2 domain of SynGAP is essential for stimulation of the Rap GTPase reaction. EMBO Rep 9(4):350-355.
44. Scheffzek K, Lautwein A, Kabsch W, Ahmadian MR, Wittinghofer A (1996) Crystal structure of the GTPase-activating domain of human p120GAP and implications for the interaction with Ras. Nature 384(6609):591-596.
45. Bonneau F, Lenherr ED, Pena V, Hart DJ, Scheffzek K (2009) Solubility survey of fragments of the neurofibromatosis type 1 protein neurofibromin. Protein Expr Purif 65(1):30-37.
46. Sugase K, Landes MA, Wright PE, Martinez-Yamout M (2008) Overexpression of posttranslationally modified peptides in Escherichia coli by co-expression with modifying enzymes. Protein Expr Purif 57(2):108-115.
47. Zhou P, Lugovskoy AA, Wagner G (2001) A solubility-enhancement tag (SET) for NMR studies of poorly behaving proteins. J Biomol NMR 20(1):11-14.
48. John J, Schlichting I, Schiltz E, Rösch P, Wittinghofer A (1989) C-terminal truncation of p21H preserves crucial kinetic and structural properties. J Biol Chem 264(22): 13086-13092.
49. Tucker J, et al. (1986) Expression of p21 proteins in Escherichia coli and stereochemistry of the nucleotide-binding site. EMBO J 5(6):1351-1358.
50. John J, et al. (1990) Kinetics of interaction of nucleotides with nucleotide-free H-ras p21. Biochemistry 29(25):6058-6065.
51. Ahmadian MR, et al. (1999) Guanosine triphosphatase stimulation of oncogenic Ras mutants. Proc Natl Acad Sci USA 96(12):7065-7070.