The solution structure and dynamics of the DH-PH module of PDZRhoGEF in isolation and in complex with nucleotide-free RhoA

Protein Science

Volumn 18, Issue 10, 2009, Pages 2067-2079

  Cierpicki, Tomasz ^a   Bielnicki, Jakub ^a   Zheng, Meiying ^a   Gruszczyk, Jakub ^a   Kasterka, Marta ^a   Petoukhov, Maxim ^b   Zhang, Aming ^c   Fernandez, Erik J ^c   Svergun, Dmitri I ^b   Derewenda, Urszula ^a   Bushweller, John H ^a   Derewenda, Zygmunt S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c University of Virginia   (United States)

Author keywords

Deuterium hydrogen exchange mass spectrometry; Guanine nucleotide exchange factors; Nuclear magnetic resonance; Protein dynamics; Protein structure; RhoA; Small angle X ray scattering

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HYDROGEN; NUCLEOTIDE; PDZ PROTEIN; PLEKSTRIN; PROTEIN; PROTEIN DBL; RHO FACTOR; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; ERROR; HUMAN; IN VIVO STUDY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VALIDITY; X RAY CRYSTALLOGRAPHY;

GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MULTIPROTEIN COMPLEXES; PDZ DOMAINS; PROTEIN CONFORMATION; RHOA GTP-BINDING PROTEIN;

EID: 70349448687     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.219     Document Type: Article

References (55)

1. Jaffe AB, Hall A (2005) RHO GTPASES: biochemistry and biology. Annu Rev Cell Dev Biol 21:247-269.
2. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629-635.
3. Bishop AL, Hall A (2000) Rho GTPases and their effector proteins. Biochem J 348 (Part 2):241-255.
4. Rossman KL, Der CJ, Sondek J (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6:167-180. (Pubitemid 40215811)
5. Erickson JW, Cerione RA (2004) Structural elements, mechanism, and evolutionary convergence of Rho protein-guanine nucleotide exchange factor complexes. Biochemistry 43:837-842.
6. Whitehead IP, Campbell S, Rossman KL, Der CJ (1997) Dbl family proteins. Biochim Biophys Acta 1332:F1-F23.
7. Kandpal RP (2006) Rho GTPase activating proteins in cancer phenotypes. Curr Protein Pept Sci 7:355-365.
8. Hart MJ, Jiang X, Kozasa T, Roscoe W, Singer WD, Gilman AG, Sternweis PC, Bollag G (1998) Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by galpha13. Science 280:2112-2114. (Pubitemid 28366203)
9. Kourlas PJ, Strout MP, Becknell B, Veronese ML, Croce CM, Theil KS, Krahe R, Ruutu T, Knuutila S, Bloomfield CD, Caligiuri MA (2000) Identification of a gene at 11q23 encoding a guanine nucleotide exchange factor: evidence for its fusion with MLL in acute myeloid leukemia. Proc Natl Acad Sci USA 97:2145-2150. (Pubitemid 30134036)
10. Reuther GW, Lambert QT, Booden MA, Wennerberg K, Becknell B, Marcucci G, Sondek J, Caligiuri MA, Der CJ (2001) Leukemia-associated Rho guanine nucleotide exchange factor, a Dbl family protein found mutated in leukemia, causes transformation by activation of RhoA. J Biol Chem 276:27145-27151.
11. Fukuhara S, Murga C, Zohar M, Igishi T, Gutkind JS (1999) A novel PDZ domain containing guanine nucleotide exchange factor links heterotrimeric G proteins to Rho. J Biol Chem 274:5868-5879. (Pubitemid 29109244)
12. Sternweis PC, Carter AM, Chen Z, Danesh SM, Hsiung YF, Singer WD (2007) Regulation of Rho guanine nucleotide exchange factors by G proteins. Adv Protein Chem 74:189-228. (Pubitemid 47369751)
13. Teixeira CE, Jin L, Priviero FB, Ying Z, Webb RC (2007) Comparative pharmacological analysis of Rho-kinase inhibitors and identification of molecular components of Ca2+ sensitization in the rat lower urinary tract. Biochem Pharmacol 74:647-658. (Pubitemid 47042014)
14. Hilgers RH, Todd J, Webb RC (2007) Increased PDZRhoGEF/RhoA/Rho kinase signaling in small mesenteric arteries of angiotensin II-induced hypertensive rats. J Hypertens 25:1687-1697. (Pubitemid 47056577)
15. Gong MC, Iizuka K, Nixon G, Browne JP, Hall A, Eccleston JF, Sugai M, Kobayashi S, Somlyo AV, Somlyo AP (1996) Role of guanine nucleotide-binding proteins - ras-family or trimeric proteins or both - in Ca2+ sensitization of smooth muscle. Proc Natl Acad Sci USA 93:1340-1345. (Pubitemid 26052891)
16. Kristelly R, Gao G, Tesmer JJ (2004) Structural determinants of RhoA binding and nucleotide exchange in leukemia-associated Rho guanine-nucleotide exchange factor. J Biol Chem 279:47352-47362. (Pubitemid 39518392)
17. Derewenda U, Oleksy A, Stevenson AS, Korczynska J, Dauter Z, Somlyo AP, Otlewski J, Somlyo AV, Derewenda ZS (2004) The crystal structure of RhoA in complex with the DH/PH fragment of PDZRhoGEF, an activator of the Ca(2+) sensitization pathway in smooth muscle. Structure 12:1955-1965. (Pubitemid 39469393)
18. Worthylake DK, Rossman KL, Sondek J (2004) Crystal structure of the DH/PH fragment of Dbs without bound GTPase. Structure 12:1078-1086.
19. Snyder JT, Worthylake DK, Rossman KL, Betts L, Pruitt WM, Siderovski DP, Der CJ, Sondek J (2002)Structural basis for the selective activation of Rho GTPases by Dbl exchange factors. Nat Struct Biol 9:468-475. (Pubitemid 34568794)
20. Rossman KL, Worthylake DK, Snyder JT, Siderovski DP, Campbell SL, Sondek J (2002) A crystallographic view of interactions between Dbs and Cdc42: PH domain-assisted guanine nucleotide exchange. EMBO J 21:1315-1326.
21. Worthylake DK, Rossman KL, Sondek J (2000) Crystal structure of Rac1 in complex with the guanine nucleotide exchange region of Tiam1. Nature 408:682-688.
22. Soisson SM, Nimnual AS, Uy M, Bar-Sagi D, Kuriyan J (1998) Crystal structure of the Dbl and pleckstrin homology domains from the human Son of sevenless protein. Cell 95:259-268. (Pubitemid 28473786)
23. Cierpicki T, Bushweller JH, Derewenda ZS (2005) Probing the supramodular architecture of a multidomain protein: the structure of syntenin in solution. Structure 13:319-327. (Pubitemid 40247707)
24. Karnoub AE, Worthylake DK, Rossman KL, Pruitt WM, Campbell SL, Sondek J, Der CJ (2001) Molecular basis for Rac1 recognition by guanine nucleotide exchange factors. Nat Struct Biol 8:1037-1041.
25. Berjanskii MV, Wishart DS (2005) A simple method to predict protein flexibility using secondary chemical shifts. J Am Chem Soc 127:14970-14971.
26. Zheng M, Cierpicki T, Momotani K, Artamonov MV, Derewenda U, Bushweller JH, Somlyo AV, Derewenda ZS (2009) On the mechanism of autoinhibition of the RhoA-specific nucleotide exchange factor PDZRhoGEF. BMC Struct Biol 9:36.
27. Bax A (2003) Weak alignment offers new NMR opportunities to study protein structure and dynamics. Protein Sci 12:1-16.
28. Bax A, Kontaxis G, Tjandra N (2001) Dipolar couplings in macromolecular structure determination. Methods Enzymol 339:127-174. (Pubitemid 32666560)
29. Prestegard JH, Al-Hashimi HM, Tolman JR (2000) NMR structures of biomolecules using field oriented media and residual dipolar couplings. Q Rev Biophys 33:371-424.
30. Cornilescu G, Marquardt JL, Ottiger M, Bax A (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120:6836-6837. (Pubitemid 28347351)
31. Zweckstetter M, Bax A (2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J Am Chem Soc 122:3791-3792. (Pubitemid 30233459)
32. Svergun DI (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76:2879-2886.
33. Volkov VV, Svergun DI (2003) Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 36:860-864.
34. Svergun DI, Barberato C, Koch MHJ (1995) CRYSOL - a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr 28:768-773. (Pubitemid 3014671)
35. Takahashi H, Nakanishi T, Kami K, Arata Y, Shimada I (2000) A novel NMR method for determining the interfaces of large protein-protein complexes. Nat Struct Biol 7:220-223. (Pubitemid 30140768)
36. Oleksy A, Opalinski L, Derewenda U, Derewenda ZS, Otlewski J (2006) The molecular basis of RhoA specificity in the guanine nucleotide exchange factor PDZ-Rho-GEF. J Biol Chem 281:32891-32897. (Pubitemid 46036844)
37. Zhou B, Zhang JL, Liu SJ, Reddy S, Wang F, Zhang ZY (2006) Mapping ERK2-MKP3 binding interfaces by hydrogen/deuterium exchange mass spectrometry. J Biol Chem 281:38834-38844. (Pubitemid 46042010)
38. Mandell JG, Falick AM, Komives EA (1998) Identification of protein-protein interfaces by decreased amide proton solvent accessibility. Proc Natl Acad Sci USA 95:14705-14710.
39. Zhang B, Zhang Y, Shacter E, Zheng Y (2005) Mechanism of the guanine nucleotide exchange reaction of Ras GTPase-evidence for a GTP/GDP displacement model. Biochemistry 44:2566-2576. (Pubitemid 40279560)
40. Barbato G, Ikura M, Kay LE, Pastor RW, Bax A (1992) Backbone dynamics of calmodulin studied by 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry 31:5269-5278.
41. Chhatriwala MK, Betts L, Worthylake DK, Sondek J (2007) The DH and PH domains of Trio coordinately engage Rho GTPases for their efficient activation. J Mol Biol 368:1307-1320. (Pubitemid 46617588)
42. Rapley J, Tybulewicz VL, Rittinger K (2008) Crucial structural role for the PH and C1 domains of the Vav1 exchange factor. EMBO Report 9:655-661. (Pubitemid 351927686)
43. Chrencik JE, Brooun A, Zhang H, Mathews II, Hura GL, Foster SA, Perry JJ, Streiff M, Ramage P, Widmer H, Bokoch GM, Tainer JA, Weckbecker G, Kuhn P (2008) Structural basis of guanine nucleotide exchange mediated by the T-cell essential Vav1. J Mol Biol 380:828-843.
44. Itzen A, Pylypenko O, Goody RS, Alexandrov K, Rak A (2006) Nucleotide exchange via local protein unfolding - structure of Rab8 in complex with MSS4. EMBO J 25:1445-1455.
45. Sue SC, Cervantes C, Komives EA, Dyson HJ (2008) Transfer of flexibility between ankyrin repeats in IkappaB* upon formation of the NF-kappaB complex. J Mol Biol 380:917-931.
46. Oleksy A, Barton H, Devedjiev Y, Purdy M, Derewenda U, Otlewski J, Derewenda ZS (2004) Preliminary crystallographic analysis of the complex of the human GTPase RhoA with the DH/PH tandem of PDZ-RhoGEF. Acta Cryst 60:740-742. (Pubitemid 41184833)
47. Sheffield P, Garrard S, Derewenda Z (1999) Overcoming expression and purification problems of RhoGDI using a family of "Parallel" expression vectors. Protein Expr Purif 15:34-39.
48. Cierpicki T, Bushweller JH (2004) Charged gels as orienting media for measurement of residual dipolar couplings in soluble and integral membrane proteins. J Am Chem Soc 126:16259-16266. (Pubitemid 39627638)
49. Tugarinov V, Kay LE (2003) Quantitative NMR studies of high molecular weight proteins: application to domain orientation and ligand binding in the 723 residue enzyme malate synthase G. J Mol Biol 327:1121-1133. (Pubitemid 36363717)
50. Roessle MW, Klaering R, Ristau U, Robrahn B, Jahn D, Gehrmann T, Konarev P, Round A, Fiedler S, Hermes C, Svergun D (2007) Upgrade of the small-angle X-ray scattering beamline X33 at the European Molecular Biology Laboratory, Hamburg. J Appl Cryst 40:s190-s194. (Pubitemid 46732685)
51. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Cryst 36:1277-1282.
52. Petoukhov MV, Konarev PV, Kikhney AG, Svergun DI (2007) ATSAS 2.1 - towards automated and web-supported small-angle scattering data analysis. J Appl Cryst 40:s223-s228.
53. Porod G, General theory. In:Glatter O, Kratky O, Eds. (1982) Small-angle X-ray scattering. London: Academic Press, pp 17-51.
54. Svergun DI (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 25:495-503.
55. Kozin MB, Svergun DI (2001) Automated matching of high- and low-resolution structural models. J Appl Cryst 34:33-41. (Pubitemid 32151714)