The binding affinities of proteins interacting with the PDZ domain of PICK1

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 5, 2012, Pages 1393-1408

  Bolia, Ashini ^a   Gerek, Z Nevin ^a   Keskin, Ozlem ^b   Banu Ozkan, Sefika ^a   Dev, Kumlesh K ^c  

^a ARIZONA STATE UNIVERSITY   (United States)

^b KOÇ UNIVERSITY   (Turkey)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Binding affinity; Modeling; Molecular docking; PICK1

Indexed keywords

GLUTAMATE RECEPTOR 2; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN KINASE C ALPHA;

ARTICLE; BINDING AFFINITY; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CARRIER PROTEINS; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PDZ DOMAINS; PROTEIN BINDING; SEQUENCE ALIGNMENT;

EID: 84859444323     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24034     Document Type: Article

References (65)

1. Ponting CP. Evidence for PDZ domains in bacteria, yeast, and plants. Protein Sci 1997; 6: 464-468.
2. Jemth P, Gianni S. PDZ domains: folding and binding. Biochemistry 2007; 46: 8701-8708.
3. Sheng M, Sala C. PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 2001; 24: 1-29.
4. Dev KK, Nakajima Y, Kitano J, Braithwaite SP, Henley JM, Nakanishi S. PICK1 interacts with and regulates PKC phosphorylation of mGLUR7. J Neurosci 2000; 20: 7252-7257.
5. Gardner SM, Takamiya K, Xia J, Suh JG, Johnson R, Yu S, Huganir RL. Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 2005; 45: 903-915.
6. Hanley JG, Henley JM. PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking. EMBO J 2005; 24: 3266-3278.
7. Jin W, Ge WP, Xu J, Cao M, Peng L, Yung W, Liao D, Duan S, Zhang M, Xia J. Lipid binding regulates synaptic targeting of PICK1, AMPA receptor trafficking, and synaptic plasticity. J Neurosci 2006; 26: 2380-2390.
8. Kim CH, Chung HJ, Lee HK, Huganir RL. Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc Natl Acad Sci USA 2001; 98: 11725-11730.
9. Lin DT, Huganir RL. PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization. J Neurosci 2007; 27: 13903-13908.
10. Terashima A, Pelkey KA, Rah JC, Suh YH, Roche KW, Collingridge GL, McBain CJ, Isaac JT. An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity. Neuron 2008; 57: 872-882.
11. Xia J, Zhang X, Staudinger J, Huganir RL. Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 1999; 22: 179-187.
12. Xia J, Chung HJ, Wihler C, Huganir RL, Linden DJ. Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron 2000; 28: 499-510.
13. Rocca DL, Martin S, Jenkins EL, Hanley JG. Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis. Nat Cell Biol 2008; 10: 259-271.
14. Wang WL, Yeh SF, Huang EY, Lu YL, Wang CF, Huang CY, Lin WJ. Mitochondrial anchoring of PKCα by PICK1 confers resistance to etoposide-induced apoptosis. Apoptosis 2007; 12: 1857-1871.
15. Staudinger J, Lu J, Olson EN. Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha. J Biol Chem 1997; 272: 32019-32024.
16. Bertaso F, Zhang C, Scheschonka A, de Bock F, Fontanaud P, Marin P, Huganir RL, Betz H, Bockaert J, Fagni L, Lerner-Natoli M. PICK1 uncoupling from mGluR7a causes absence-like seizures. Nat Neurosci 2008; 11: 940-948.
17. Zhang CS, Bertaso F, Eulenburg V, Lerner-Natoli M, Herin GA, Bauer L, Bockaert J, Fagni L, Betz H, Scheschonka A. Knock-in mice lacking the PDZ-ligand motif of mGluR7a show impaired PKC-dependent autoinhibition of glutamate release, spatial working memory deficits, and increased susceptibility to pentylenetetrazol. J Neurosci 2008; 28: 8604-8614.
18. Baron A, Deval E, Salinas M, Lingueglia E, Voilley N, Lazdunski M. Protein kinase C stimulates the acid-sensing ion channel ASIC2a via the PDZ domain-containing protein PICK1. J Biol Chem 2002; 277: 50463-50468.
19. Garry EM, Moss A, Rosie R, Delaney A, Mitchell R, Fleetwood-Walker SM. Specific involvement in neuropathic pain of AMPA receptors and adapter proteins for the GluR2 subunit. Mol Cell Neurosci 2003; 24: 10-22.
20. Bell JD, Park E, Ai J, Baker AJ. PICK1-mediated GluR2 endocytosis contributes to cellular injury after neuronal trauma. Cell Death Differ 2009; 16: 1665-1680.
21. Dixon RM, Mellor JR, Hanley JG. PICK1-mediated glutamate receptor subunit 2 (GluR2) trafficking contributes to cell death in oxygen/glucose-deprived hippocampal neurons. J Biol Chem 2009; 284: 14230-14235.
22. Joch M, Ase AR, Chen CX, MacDonald PA, Kontogiannea M, Corera AT, Brice A, Seguela P, Fon EA. Parkin-mediated monoubiquitination of the PDZ protein PICK1 regulates the activity of acid-sensing ion channels. Mol Biol Cell 2007; 18: 3105-3118.
23. Beneyto M, Meador-Woodruff JH. Lamina-specific abnormalities of AMPA receptor trafficking and signaling molecule transcripts in the prefrontal cortex in schizophrenia. Synapse 2006; 60: 585-598.
24. Bousman CA, Glatt SJ, Everall IP, Tsuang MT. Genetic association studies of methamphetamine use disorders: a systematic review and synthesis. Am J Med Genet B Neuropsychiatr 2009; 150: 1025-1049.
25. Dev KK, Henley JM. The schizophrenic faces of PICK1. Trends Pharmacol Sci 2006; 27: 574-579.
26. Dracheva S, McGurk SR, Haroutunian V. mRNA expression of AMPA receptors and AMPA receptor binding proteins in the cerebral cortex of elderly schizophrenics. J Neurosci Res 2005; 79: 868-878.
27. Fujii K, Maeda K, Hikida T, Mustafa AK, Balkissoon R, Xia J, Yamada T, Ozeki Y, Kawahara R, Okawa M, Huganir RL, Ujike H, Snyder SH, Sawa A. Serine racemase binds to PICK1: potential relevance to schizophrenia. Mol Psychiatry 2006: 11: 150-157.
28. Ghasemzadeh MB, Vasudevan P, Mueller C, Seubert C, Mantsch JR. Region specific alterations in glutamate receptor expression and subcellular distribution following extinction of cocaine self-administration. Brain Res 2009; 1267: 89-102.
29. Hong CJ, Liao DL, Shih HL, Tsai SJ. Association study of PICK1 rs3952 polymorphism and schizophrenia. Neuroreport 2004; 15: 1965-1967.
30. Ishiguro H, Koga M, Horiuchi Y, Inada T, Iwata N, Ozaki N, Ujike H, Muratake T, Someya T, Arinami T. PICK1 is not a susceptibility gene for schizophrenia in a Japanese population: association study in a large case-control population. Neurosci Res 2007; 58: 145-148.
31. Matsuzawa D, Hashimoto K, Miyatake R, Shirayama Y, Shimizu E, Maeda K, Suzuki Y, Mashimo Y, Sekine Y, Inada T, Ozaki N, Iwata N, Harano M, Komiyama T, Yamada M, Sora I, Ujike H, Hata A, Sawa A, Iyo M. Identification of functional polymorphisms in the promoter region of the human PICK1 gene and their association with methamphetamine psychosis. Am J Psychiatry 2007; 164: 1105-1114.
32. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, Doerks T, Julien P, Roth A, Simonovic M, Bork P, von Mering C. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009; 37: D412-D416.
33. Elkins JM, Papagrigoriou E, Berridge G, Yang X, Phillips C, Gileadi C, Savitsky P, Doyle DA. Structure of PICK1 and other PDZ domains obtained with the help of self-binding C-terminal extensions. Protein Sci. 2007; 16: 683-694.
34. Madsen KL, Beuming T, Niv MY, Chang CW, Dev KK, Weinstein H, Gether U. Molecular determinants for the complex binding specificity of the PDZ domain in PICK1. J Biol Chem 2005; 280: 20539-20548.
35. Perez JL, Khatri L, Chang C, Srivastava S, Osten P, Ziff EB. PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J Neurosci 2001; 21: 5417-5428.
36. Dev KK, Nakanishi S, Henley JM. The PDZ domain of PICK1 differentially accepts protein kinase C-alpha and GluR2 as interacting ligands. J Biol Chem 2004; 279: 41393-41397.
37. Thorsen TS, Madsen KL, Rebola N, Rathje M, Anggono V, Bach A, Moreira IS, Stuhr-Hansen N, Dyhring T, Peters D, Beuming T, Huganir R, Weinstein H, Mulle C, Stromgaard K, Ronn, LC, Gether U. Identification of a small-molecule inhibitor of the PICK1 PDZ domain that inhibits hippocampal LTP and LTD. Proc Natl Acad Sci USA 2010; 107: 413-418.
38. Bach A, Stuhr-Hansen N, Thorsen TS, Bork N, Moreira IS, Frydenvang K, Padrah S, Christensen SB, Madsen KL, Weinstein H, Gether U, Strømgaard K. Structure-activity relationships of a small-molecule inhibitor of the PDZ domain of PICK1. Org Biomol Chem 2010; 8: 4281-4288.
39. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000; 28: 235-242.
40. Guex N, Peitsch MC. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997; 18: 2714-2723.
41. Atilgan C, Gerek ZN, Ozkan SB, Atilgan AR. Manipulation of conformational change in proteins by single-residue perturbations. Biophys J 2010; 99: 933-943.
42. Tsui V, Case DA. Molecular dynamics simulations of nucleic acids with a generalized born solvation model. J Am Chem Soc 2000; 122: 2489-2498.
43. Davis IW, Baker D. RosettaLigand docking with full ligand and receptor flexibility. J Mol Biol 2009; 385: 381-392.
44. Meiler J, Baker D. ROSETTALIGAND: protein-small molecule docking with full side-chain flexibility. Proteins 2006; 65: 538-548.
45. Gohlke H, Hendlich M, Klebe G. Knowledge-based scoring function to predict protein-ligand interactions. J Mol Biol 2000; 29: 337-356.
46. Tuncbag N, Gursoy A, Keskin O. Identification of computational hot spots in protein interfaces: combining solvent accessibility and inter-residue potentials improves the accuracy. Bioinformatics 2009; 25: 1513-1520.
47. Tuncbag N, Keskin O, Gursoy A. HotPoint: hot spot prediction server for protein interfaces. Nucleic Acids Res 2010; 38: W402-W406.
48. Aytuna AS, Gursoy A, Keskin O. Prediction of protein-protein interactions by combining structure and sequence conservation in protein interfaces. Bioinformatics 2005; 21: 2850-2855.
49. Ogmen U, Keskin O, Aytuna AS, Nussinov R, Gursoy A. PRISM: protein interactions by structural matching. Nucleic Acids Res 2005; 33: W331-W336.
50. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004; 25: 1605-1612.
51. Madsen KL, Eriksen J, Milan-Lobo L, Han DS, Niv MY, Ammendrup-Johnsen I, Henriksen U, Bhatia VK, Stamou D, Sitte HH, McMahon HT, Weinstein H, Gether U. Membrane localization is critical for activation of the PICK1 BAR domain. Traffic 2008; 9: 1327-1343.
52. Pan L, Wu H, Shen C, Shi Y, Jin W, Xia J, Zhang M. Clustering and synaptic targeting of PICK1 requires direct interaction between the PDZ domain and lipid membranes. EMBO J 2007; 26: 4576-4587.
53. Shi Y, Zhang L, Yuan J, Xiao H, Yang X, Niu L. Zinc binding site in PICK1 is dominantly located at the CPC motif of its PDZ domain. J Neurochem 2008; 106: 1027-1034.
54. Clackson T, Wells JA. A hot spot of binding energy in a hormone-receptor interface. Science 1995; 267: 383-386.
55. Bassan M, Liu H, Madsen KL, Armsen W, Zhou J, Desilva T, Chen W, Paradise A, Brasch MA, Staudinger J, Gether U, Irwin N, Rosenberg PA. Interaction between the glutamate transporter GLT1b and the synaptic PDZ domain protein PICK1. Eur J Neurosci 2008; 27: 66-82.
56. Wells S, Menor S, Hespenheide B, Thorpe MF. Constrained geometric simulation of diffusive motion in proteins. Phys Biol 2005; 2: S127-S136.
57. Lockless SW, Ranganathan R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 1999; 286: 295-299.
58. Dhulesia A, Gsponer J, Vendruscolo M. Mapping of two networks of residues that exhibit structural and dynamical changes upon binding in a PDZ domain protein. J Am Chem Soc 2008; 130: 8931-8939.
59. Ho BK, Agard DA. Conserved tertiary couplings stabilize elements in the PDZ fold, leading to characteristic patterns of domain conformational flexibility. Protein Sci 2010; 19: 398-411.
60. Kong Y, Karplus M. Signaling pathways of PDZ2 domain: a molecular dynamics interaction correlation analysis. Proteins 2009; 74: 145-154.
61. Gerek ZN, Keskin O, Ozkan SB. Identification of specificity and promiscuity of PDZ domain interactions through their dynamic behavior. Proteins 2009; 77: 796-811.
62. Gerek ZN, Ozkan SB. A flexible docking scheme to explore the binding selectivity of PDZ domains. Protein Sci 2010; 19: 914-928.
63. Smith CA, Kortemme T. Structure-based prediction of the peptide sequence space recognized by natural and synthetic PDZ domains. J Mol Biol 2010; 402: 460-474.
64. Ikeguchi M, Ueno J, Sato M, Kidera A. Protein structural change upon ligand binding: linear response theory. Phys Rev Lett 2005; 94: 078102.
65. Dev KK. Making protein interactions druggable: targeting PDZ domains. Nat Rev Drug Dis 2004; 3: 1047-1056.