Structural insights into the interaction between the Cripto CFC domain and the ALK4 receptor

Journal of Peptide Science

Volumn 15, Issue 3, 2009, Pages 175-183

  Calvanese, Luisa ^a   Saporito, Angela ^b   Oliva, Romina ^c   D'Auria, Gabriella ^a,b   Pedone, Carlo ^b   Paolillo, Livio ^a,b   Ruvo, Menotti ^b   Marasco, Daniela ^b   Falcigno, Lucia ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF NAPLES PARTHENOPE   (Italy)

Author keywords

Conformational analysis; Docking; EGF CFC family; Homology modelling; NMR; SPR

Indexed keywords

ACTIVIN; ACTIVIN RECEPTOR; ACTIVIN RECEPTOR 4; CYSTEINE; DISULFIDE; EPIDERMAL GROWTH FACTOR; GROWTH FACTOR; PROTEIN; PROTEIN CRIPTO; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ACTIVIN RECEPTOR 1; ACVR1B PROTEIN, HUMAN; MEMBRANE PROTEIN; TDGF1 PROTEIN, HUMAN; TUMOR PROTEIN;

BINDING AFFINITY; CARCINOGENESIS; CONFERENCE PAPER; CONTROLLED STUDY; EMBRYO DEVELOPMENT; MOLECULAR DOCKING; MOLECULAR INTERACTION; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; SYNTHESIS; AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ACTIVIN RECEPTORS, TYPE I; AMINO ACID SEQUENCE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EPIDERMAL GROWTH FACTOR; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 63449092615     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.1091     Document Type: Conference Paper

References (59)

1. Schiffer SG, Foley S, Kaffashan A, Hronowski X, Zichittella AE, Yeo CY, Miatkowski K, Adkins HB, Damon B, Whitman M, Salomon D, Sanicola M, Williams KP. Fucosylation of Cripto is required for its ability to facilitate nodal signaling. J. Biol. Chem. 2001; 276(41): 37769-37778.
2. Yan YT, Liu JJ, Luo YEC, Haltiwanger RS, Abate-Shen C, Shen MM. Dual roles of Cripto as a ligand and coreceptor in the nodal signaling pathway. Mol. Cell Biol. 2002; 22(13): 4439-4449.
3. Adkins HB, Bianco C, Schiffer SG, Rayhorn P, Zafari M, Cheung AE, Orozco O, Olson D, De Luca A, Chen LL, Miatkowski K, Benjamin C, Normanno N, Williams KP, Jarpe M, LePage D, Salomon D, Sanicola M. Antibody blockade of the Cripto CFC domain suppresses tumor cell growth in vivo. J. Clin. Invest. 2003; 112(4): 575-587.
4. Saloman DS, Bianco C, Ebert AD, Khan NI, De Santis M, Normanno N, Wechselberger C, Seno M, Williams K, Sanicola M, Foley S, Gullick WJ, Persico G. The EGF-CFC family: novel epidermal growth factor-related proteins in development and cancer. Endocr. Relat. Cancer 2000; 7(4): 199-226.
5. Shen MM. Decrypting the role of Cripto in tumorigenesis. J. Clin. Invest. 2003; 112(4): 500-502.
6. Parisi S, D'Andrea D, Lago CT, Adamson ED, Persico MG, Minchiotti G. Nodal-dependent Cripto signaling promotes cardiomyogenesis and redirects the neural fate of embryonic stem cells. J. Cell Biol. 2003; 163(2): 303-314.
7. Sakuma R, Ohnishi Yi Y, Meno C, Fujii H, Juan H, Takeuchi J, Ogura T, Li E, Miyazono K, Hamada H. Inhibition of Nodal signalling by Lefty mediated through interaction with common receptors and efficient diffusion. Genes Cells 2002; 7(4): 401-412.
8. Schier AF. Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 2003; 19: 589-621.
9. Yeo C, Whitman M. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol. Cells 2001; 7(5): 949-957.
10. Chen C, Ware SM, Sato A, Houston-Hawkins DE, Habas R, Matzuk MM, Shen MM, Brown CW. The Vg1-related protein Gdf3 acts in a Nodal signaling pathway in the pre-gastrulation mouse embryo. Development 2006; 133(2): 319-329.
11. Cheng SK, Olale F, Bennett JT, Brivanlou AH, Schier AF. EGF-CFC proteins are essential coreceptors for the TGF-beta signals Vg1 and GDF1. Genes Dev. 2003; 17(1): 31-36.
12. Gray PC, Harrison CA, Vale W. Cripto forms a complex with activin and type II activin receptors and can block activin signaling. Proc. Natl. Acad. Sci. U.S.A. 2003; 100(9): 5193-5198.
13. Cheng SK, Olale F, Brivanlou AH, Schier AF. Lefty blocks a subset of TGFbeta signals by antagonizing EGF-CFC coreceptors. PLoS Biol. 2004; 2(2): E30.
14. Marasco D, Saporito A, Ponticelli S, Chambery A, De Falco S, Pedone C, Minchiotti G, Ruvo M. Chemical synthesis ofmouse cripto CFC variants. Proteins 2006; 64(3): 779-788.
15. Risbridger GP, Schmitt JF, Robertson DM. Activins and inhibins in endocrine and other tumors. Endocr. Rev. 2001; 22(6): 836-858.
16. Shani G, Fischer WH, Justice NJ, Kelber JA, Vale W, Gray PC. GRP78 and Cripto form a complex at the cell surface and collaborate to inhibit transforming growth factor beta signalling and enhance cell growth. Mol. Cell Biol. 2008; 28(2): 666-677.
17. Bianco C, Normanno N, Salomon DS, Ciardiello F. Role of the cripto (EGF-CFC) family in embryogenesis and cancer. Growth Factors 2004; 22(3): 133-139.
18. Gray PC, Shani G, Aung K, Kelber J, Vale W. Cripto binds transforming growth factor beta (TGF-beta) and inhibits TGF-beta signalling. Mol. Cell Biol. 2006; 26(24): 9268-9278.
19. Lin SJ, Lerch TF, Cook RW, Jardetzky TS, Woodruff TK. The structural basis of TGF-beta, bone morphogenetic protein, and activin ligand binding. Reproduction 2006; 132(2): 179-190.
20. Calvanese L, Saporito A, Marasco D, D'Auria G, Minchiotti G, Pedone C, Paolillo L, Falcigno L, Ruvo M. Solution structure of mouse Cripto CFC domain and its inactive variant Trp107Ala. J. Med. Chem. 2006; 49(24): 7054-7062.
21. Kirsch T, Sebald W, Dreyer MK. Crystal structure of the BMP-2-BRIA ectodomain complex. Nat. Struct. Biol. 2000; 7(6): 492-496.
22. Fields GB, Noble RL. Solid phase peptide synthesis utilizing 9- fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 1990; 35(3): 161-214.
23. Bax A, Davis DG. MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 1985; 65: 355-360.
24. Bax A. Practical aspects of two-dimensional transverse NOE spectroscopy. J. Magn. Reson. 1985; 63: 207-213.
25. States DJ, Haberhorn RA, Ruben DJ. A two-dimensional nuclear Overhauser experiment with pure absorption phase in four quadrants. J. Magn. Reson. 1982; 48: 286-292.
26. Piotto M, Saudek V, Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 1992; 2(6): 661-665.
27. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 1995; 6(3): 277-293.
28. Johnson BA. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 2004; 278: 313-352.
29. Wuthrich K. NMR of Proteins and Nucleic Acids. Wiley: New York, 1986.
30. Guntert P, Braun W, Wuthrich K. Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol. 1991; 217(3): 517-530.
31. Guntert P, Mumenthaler C, Wuthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 1997; 273: 283-298.
32. Guntert P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 2004; 278: 353-378.
33. Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TE, III, DeBolt S, Ferguson D, Seibel G, Kollman P. AMBER, a package of computer program for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comp Phys Commun 1995; 91: 1-41.
34. Koradi R, Billeter M, Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 1996; 14(1): 51-55, 29-32.
35. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997; 25(17): 3389-3402.
36. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A. Pfam: clans, web tools and services. Nucleic Acids Res. 2006; 34: (Database issue): D247-D251.
37. Soding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005; 21(7): 951-960.
38. Soding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005; 33: (Web Server issue): W244-W248.
39. Jones DT. GenTHREADER: an efficient and reliable protein fold recognition method for genomic sequences. J. Mol. Biol. 1999; 287(4): 797-815.
40. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22): 4673-4680.
41. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993; 234(3): 779-815.
42. Hooft RW, Vriend G, Sander C, Abola EE. Errors in protein structures. Nature 1996; 381(6580): 272.
43. Vriend G. WHAT IF: a molecular modelling and drug design program. J. Mol. Graphics 1990; 8(1): 52-56, 29.
44. Bowie JU, Luthy R, Eisenberg D. A method to identify protein sequences that fold into a known three-dimensional structure. Science 1991; 253(5016): 164-170.
45. Luthy R, Bowie JU, Eisenberg D. Assessment of protein models with three-dimensional profiles. Nature 1992; 356(6364): 83-85.
46. Wallner B, Elofsson A. Can correct protein models be identified? Protein Sci. 2003; 12(5): 1073-1086.
47. Wallner B, Elofsson A. Identification of correct regions in protein models using structural, alignment, and consensus information. Protein Sci. 2006; 15(4): 900-913.
48. Gabb HA, Jackson RM, Sternberg MJ. Modelling protein docking using shape complementarity, electrostatics and biochemical information. J. Mol. Biol. 1997; 272(1): 106-120.
49. Moont G, Gabb HA, Sternberg MJ. Use of pair potentials across protein interfaces in screening predicted docked complexes. Proteins 1999; 35(3): 364-373.
50. Jackson RM, Gabb HA, Sternberg MJ. Rapid refinement of protein interfaces incorporating solvation: application to the docking problem. J. Mol. Biol. 1998; 276(1): 265-285.
51. Minchiotti G, Manco G, Parisi S, Lago CT, Rosa F, Persico MG. Structure-function analysis of the EGF-CFC family member Cripto identifies residues essential for nodal signalling. Development 2001; 128(22): 4501-4510.
52. Wishart DS, Sykes BD, Richards FM. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 1991; 222(2): 311-333.
53. Foley SF, van Vlijmen HW, Boynton RE, Adkins HB, Cheung AE, Singh J, Sanicola M, Young CN, Wen D. The CRIPTO/FRL-1/CRYPTIC (CFC) domain of human Cripto. Functional and structural insights through disulfide structure analysis. Eur. J. Biochem. 2003; 270(17): 3610-3618.
54. Kingsley DM. The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 1994; 8(2): 133-146.
55. Harrison CA, Gray PC, Koerber SC, Fischer W, Vale W. Identification of a functional binding site for activin on the type I receptor ALK4. J. Biol. Chem. 2003; 278(23): 21129-21135.
56. Innis CA, Shi J, Blundell TL. Evolutionary trace analysis of TGF-beta and related growth factors: implications for site-directed mutagenesis. Protein Eng. 2000; 13(12): 839-847.
57. Sternberg MJ, Gabb HA, Jackson RM, Moont G. Protein-protein docking. Generation and filtering of complexes. Methods Mol. Biol. 2000; 143: 399-415.
58. Fernandez-Recio J, Romero A, Sancho J. Energetics of a hydrogen bond (charged and neutral) and of a cation-pi interaction in apoflavodoxin. J. Mol. Biol. 1999; 290(1): 319-330.
59. Meurisse R, Brasseur R, Thomas A. Aromatic side-chain interactions in proteins. Near- and far-sequence His-X pairs. Biochim. Biophys. Acta 2003; 1649(1): 85-96.