Oncogenic K-Ras Binds to an Anionic Membrane in Two Distinct Orientations: A Molecular Dynamics Analysis

Biophysical Journal

Volumn 110, Issue 5, 2016, Pages 1125-1138

  Prakash, Priyanka ^a   Zhou, Yong ^a   Liang, Hong ^a   Hancock, John F ^a   Gorfe, Alemayehu A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANION; LIPID BILAYER; PROTEIN BINDING; RAS PROTEIN;

AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; ENZYME ACTIVE SITE; HUMAN; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR MODEL; ONCOGENE RAS;

AMINO ACID SEQUENCE; ANIONS; CATALYTIC DOMAIN; CELL MEMBRANE; GENES, RAS; HUMANS; LIPID BILAYERS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; RAS PROTEINS;

EID: 84960850844     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2016.01.019     Document Type: Article

References (57)

1. A.D. Cox, and C.J. Der Ras history: the saga continues Small GTPases 1 2010 2 27
2. J.L. Bos Ras oncogenes in human cancer: a review Cancer Res. 49 1989 4682 4689
3. I.A. Prior, P.D. Lewis, and C. Mattos A comprehensive survey of Ras mutations in cancer Cancer Res. 72 2012 2457 2467
4. M. Schmick, A. Kraemer, and P.I. Bastiaens Ras moves to stay in place Trends Cell Biol. 25 2015 190 197
5. J.A. Parker, and C. Mattos The Ras-membrane interface: isoform-specific differences in the catalytic domain Mol. Cancer Res. 13 2015 595 603
6. I.M. Ahearn, and K. Haigis M.R. Philips Regulating the regulator: post-translational modification of RAS Nat. Rev. Mol. Cell Biol. 13 2012 39 51
7. D. Abankwa, A.A. Gorfe, and J.F. Hancock Ras nanoclusters: molecular structure and assembly Semin. Cell Dev. Biol. 18 2007 599 607
8. J.F. Hancock Ras proteins: different signals from different locations Nat. Rev. Mol. Cell Biol. 4 2003 373 384
9. Y. Zhou, and J.F. Hancock Ras nanoclusters: versatile lipid-based signaling platforms Biochim. Biophys. Acta 1853 2015 841 849
10. P. Prakash, and A.A. Gorfe Overview of simulation studies on the enzymatic activity and conformational dynamics of the GTPase Ras Mol. Simul. 40 2014 839 847
11. P. Prakash, and A.A. Gorfe Lessons from computer simulations of Ras proteins in solution and in membrane Biochim. Biophys. Acta 1830 2013 5211 5218
12. A. Ehrhardt, and G.R. Ehrhardt J.W. Schrader Ras and relatives - job sharing and networking keep an old family together Exp. Hematol. 30 2002 1089 1106
13. I.A. Prior, and J.F. Hancock Compartmentalization of Ras proteins J. Cell Sci. 114 2001 1603 1608
14. D. Abankwa, and A.A. Gorfe J.F. Hancock Ras membrane orientation and nanodomain localization generate isoform diversity Proc. Natl. Acad. Sci. USA 107 2010 1130 1135
15. D. Abankwa, and M. Hanzal-Bayer J.F. Hancock A novel switch region regulates H-ras membrane orientation and signal output EMBO J. 27 2008 727 735
16. A.A. Gorfe, and M. Hanzal-Bayer J.A. McCammon Structure and dynamics of the full-length lipid-modified H-Ras protein in a 1,2-dimyristoylglycero-3-phosphocholine bilayer J. Med. Chem. 50 2007 674 684
17. S. Kapoor, and G. Triola R. Winter Revealing conformational substates of lipidated N-Ras protein by pressure modulation Proc. Natl. Acad. Sci. USA 109 2012 460 465
18. S. Kapoor, and K. Weise R. Winter The role of G-domain orientation and nucleotide state on the Ras isoform-specific membrane interaction Eur. Biophys. J. 41 2012 801 813
19. M.T. Mazhab-Jafari, and C.B. Marshall M. Ikura Oncogenic and RASopathy-associated K-RAS mutations relieve membrane-dependent occlusion of the effector-binding site Proc. Natl. Acad. Sci. USA 112 2015 6625 6630
20. S. Lukman, and B.J. Grant J.A. McCammon The distinct conformational dynamics of K-Ras and H-Ras A59G PLOS Comput. Biol. 6 2010 e1000922
21. M. Buck, and S. Bouguet-Bonnet A.D. MacKerell Jr. Importance of the CMAP correction to the CHARMM22 protein force field: dynamics of hen lysozyme Biophys. J. 90 2006 L36 L38
22. P. Prakash, J.F. Hancock, and A.A. Gorfe Binding hotspots on K-ras: consensus ligand binding sites and other reactive regions from probe-based molecular dynamics analysis Proteins 83 2015 898 909
23. T. Maurer, and L.S. Garrenton G. Fang Small-molecule ligands bind to a distinct pocket in Ras and inhibit SOS-mediated nucleotide exchange activity Proc. Natl. Acad. Sci. USA 109 2012 5299 5304
24. L. Janosi, and A.A. Gorfe Segregation of negatively charged phospholipids by the polycationic and farnesylated membrane anchor of Kras Biophys. J. 99 2010 3666 3674
25. Y. Zhou, and H. Liang J.F. Hancock Signal integration by lipid-mediated spatial cross talk between Ras nanoclusters Mol. Cell. Biol. 34 2014 862 876
26. J.P.C. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 15
27. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an N×log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
28. A.D. MacKerell, and D. Bashford M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
29. J.B. Klauda, and R.M. Venable R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
30. A.D. Mackerell Jr., M. Feig, and C.L. Brooks 3rd Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
31. A.A. Gorfe, R. Pellarin, and A. Caflisch Membrane localization and flexibility of a lipidated ras peptide studied by molecular dynamics simulations J. Am. Chem. Soc. 126 2004 15277 15286
32. J.C. Phillips, and R. Braun K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
33. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 27 38
34. M.A. Kiskowski, J.F. Hancock, and A.K. Kenworthy On the use of Ripley's K-function and its derivatives to analyze domain size Biophys. J. 97 2009 1095 1103
35. S.J. Plowman, and C. Muncke J.F. Hancock H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton Proc. Natl. Acad. Sci. USA 102 2005 15500 15505
36. I.A. Prior, and C. Muncke J.F. Hancock Direct visualization of Ras proteins in spatially distinct cell surface microdomains J. Cell Biol. 160 2003 165 170
37. P.J. Diggle, J. Mateu, and H.E. Clough A comparison between parametric and non-parametric approaches to the analysis of replicated spatial point patterns Adv. Appl. Probab. 32 2000 13
38. L. Janosi, and Z. Li A.A. Gorfe Organization, dynamics, and segregation of Ras nanoclusters in membrane domains Proc. Natl. Acad. Sci. USA 109 2012 8097 8102
39. Z. Li, L. Janosi, and A.A. Gorfe Formation and domain partitioning of H-ras peptide nanoclusters: effects of peptide concentration and lipid composition J. Am. Chem. Soc. 134 2012 17278 17285
40. H. Li, and A.A. Gorfe Membrane remodeling by surface-bound protein aggregates: insights from coarse-grained molecular dynamics simulation J. Phys. Chem. Lett. 5 2014 1457 1462
41. A.A. Gorfe, B.J. Grant, and J.A. McCammon Mapping the nucleotide and isoform-dependent structural and dynamical features of Ras proteins Structure 16 2008 885 896
42. B.J. Grant, A.A. Gorfe, and J.A. McCammon Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics PLOS Comput. Biol. 5 2009 e1000325
43. J. Güldenhaupt, and T. Rudack K. Gerwert N-Ras forms dimers at POPC membranes Biophys. J. 103 2012 1585 1593
44. B.J. Grant, A.A. Gorfe, and J.A. McCammon Large conformational changes in proteins: signaling and other functions Curr. Opin. Struct. Biol. 20 2010 142 147
45. B.J. Grant, J.A. McCammon, and A.A. Gorfe Conformational selection in G-proteins: lessons from Ras and Rho Biophys. J. 99 2010 L87 L89
46. G.M. Lee, and C.S. Craik Trapping moving targets with small molecules Science 324 2009 213 215
47. G. Kar, and O. Keskin R. Nussinov Allostery and population shift in drug discovery Curr. Opin. Pharmacol. 10 2010 715 722
48. G. Buhrman, and G. Holzapfel C. Mattos Allosteric modulation of Ras positions Q61 for a direct role in catalysis Proc. Natl. Acad. Sci. USA 107 2010 4931 4936
49. F. Raimondi, M. Orozco, and F. Fanelli Deciphering the deformation modes associated with function retention and specialization in members of the Ras superfamily Structure 18 2010 402 414
50. M.T. Mazhab-Jafari, and C.B. Marshall M. Ikura Membrane-dependent modulation of the mTOR activator Rheb: NMR observations of a GTPase tethered to a lipid-bilayer nanodisc J. Am. Chem. Soc. 135 2013 3367 3370
51. Y. Liu, R.A. Kahn, and J.H. Prestegard Dynamic structure of membrane-anchored Arf∗GTP Nat. Struct. Mol. Biol. 17 2010 876 881
52. X. Nan, and T.M. Tamgüney S. Chu Ras-GTP dimers activate the mitogen-activated protein kinase (MAPK) pathway Proc. Natl. Acad. Sci. USA 112 2015 7996 8001
53. S. Muratcioglu, and T.S. Chavan R. Nussinov GTP-dependent K-Ras dimerization Structure 23 2015 1325 1335
54. W.C. Lin, and L. Iversen J.T. Groves H-Ras forms dimers on membrane surfaces via a protein-protein interface Proc. Natl. Acad. Sci. USA 111 2014 2996 3001
55. S.K. Fetics, and H. Guterres C. Mattos Allosteric effects of the oncogenic RasQ61L mutant on Raf-RBD Structure 23 2015 505 516
56. A.A. Gorfe, and J.A. McCammon Similar membrane affinity of mono- and Di-S-acylated ras membrane anchors: a new twist in the role of protein lipidation J. Am. Chem. Soc. 130 2008 12624 12625
57. P. Prakash, A. Sayyed-Ahmad, and A.A. Gorfe pMD-membrane: a method for ligand binding site identifcation in membrane-bound proteins PLOS Comput. Biol. 11 2015 e1004469