Cholesterol interaction with the MAGUK protein family member, MPP1, via CRAC and CRAC-like motifs: An in silico docking analysis

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Listowski, Marcin A ^a   Leluk, Jacek ^b   Kraszewski, Sebastian ^c   Sikorski, Aleksander F ^a,b  

^a UNIVERSITY OF WROC AW   (Poland)

^b UNIVERSITY OF ZIELONA GÓRA   (Poland)

^c WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL; CHOLESTEROL; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; MEMBRANE PALMITOYLATED PROTEIN 1; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; MPP1 PROTEIN, HUMAN; PLASMA PROTEIN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BIOINFORMATICS; CHOLESTEROL RECOGNITION INTERACTION AMINO ACID CONSENSUS MOTIF; COMPUTER MODEL; CONTROLLED STUDY; CRAC LIKE MOTIF; MEMBRANE STRUCTURE; MOLECULAR DOCKING; ONLINE SYSTEM; PALMITOYLATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; CHEMICAL PHENOMENA; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BLOOD PROTEINS; CHOLESTEROL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84941368502     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133141     Document Type: Article

References (45)

1. Li H, Papadopoulos V (1998) Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139: 4991-4997. PMID: 9832438
2. Palmer M (2004) Cholesterol and the activity of bacterial toxins. FEMS Microbiol Lett 238: 281-289. PMID: 15358412
3. Epand RM (2006) Cholesterol and the interaction of proteins with membrane domains. Prog Lipid Res 45: 279-294. PMID: 16574236
4. Boesze-Battaglia K, Brown A, Walker L, Besack D, Zekavat A, Wrenn S, et al. (2009) Cytolethal distending toxin-induced cell cycle arrest of lymphocytes is dependent upon recognition and binding to cholesterol. J Biol Chem 284: 10650-10658. doi: 10.1074/jbc.M809094200 PMID: 19240023
5. Muñoz-Barroso I, Salzwedel K, Hunter E, Blumenthal R (1999) Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusion. J Virol 73: 6089-6092. PMID: 10364363
6. Vishwanathan SA, Thomas A, Brasseur R, Epand RF, Hunter E, Epand RM (2008) Large changes in the CRAC segment of the gp41 of HIV does not destroy fusion activity if the segment interacts with cholesterol. Biochemistry 47: 11869-11876. doi: 10.1021/bi8014828 PMID: 18937430
7. Liao Z, Graham DR, Hildreth JEK (2003) Lipid rafts and HIV pathogenesis: virion-associated cholesterol is required for fusion and infection of susceptible cells. AIDS Res Hum Retroviruses 19: 675-687. PMID: 13678470
8. Maddon PJ, Dalgleish AG, McDougal JS, Clapham PR, Weiss RA, Axel R (1986) The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47: 333-348. PMID: 3094962
9. Xavier R, Brennan T, Li Q, McCormack C, Seed B (1998) Membrane Compartmentation Is Required for Efficient T Cell Activation. Immunity 8: 723-732. PMID: 9655486
10. Mañes S, del Real G, Lacalle RA, Lucas P, Gómez-Moutón C, Sánchez-Palomino S, et al. (2000) Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep 1: 190-196. PMID: 11265761
11. Oddi S, Dainese E, Fezza F, Lanuti M, Barcaroli D, De Laurenzi V, et al. (2011) Functional characterization of putative cholesterol binding sequence (CRAC) in human type-1 cannabinoid receptor. J Neurochem 116: 858-865. doi: 10.1111/j.1471-4159.2010.07041.x PMID: 21214565
12. Baier CJ, Fantini J, Barrantes FJ (2011) Disclosure of cholesterol recognition motifs in transmembrane domains of the human nicotinic acetylcholine receptor. Sci Rep 1: 69. doi: 10.1038/srep00069 PMID: 22355588
13. Epand RF, Thomas A, Brasseur R, Vishwanathan SA, Epand RM (2006) Juxtamembrane Protein Segments that Contribute to Recruitment of Cholesterol into Domains. Biochemistry 45: 6105-6114. doi: 10.1021/bi060245 PMID: 16681383
14. Anderson JM (1996) Cell signalling: MAGUK magic. Curr Biol 6: 382-384. PMID: 8723338
15. Dimitratos SD, Woods DF, Stathakis DG, Bryant PJ (1999) Signaling pathways are focused at specialized regions of the plasma membrane by scaffolding proteins of the MAGUK family. Bioessays 21: 912-921. PMID: 10517864
16. Funke L, Dakoji S, Bredt DS (2005) Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu Rev Biochem 74: 219-245. PMID: 15952887
17. Ruff P, Speicher DW, Husain-Chishti A (1991) Molecular identification of a major palmitoylated erythrocyte membrane protein containing the src homology 3 motif. Proc Natl Acad Sci U S A 88: 6595-6599. PMID: 1713685
18. Hemming NJ, Anstee DJ, Staricoff MA, Tanner MJ MN (1995) Identification of the membrane attachment sites for protein 4.1 in the human erythrocyte. J Biol Chem 270: 5360-5366. doi: 10.1074/jbc. 270.10.5360 PMID: 7890649
19. Seo P-S, Quinn BJ, Khan AA, Zeng L, Takoudis CG, Hanada T, et al. (2009) Identification of erythrocyte p55/MPP1 as a binding partner of NF2 tumor suppressor protein/Merlin. Exp Biol Med (Maywood) 234: 255-262.
20. Łach A, Grzybek M, Heger E, Korycka J, Wolny M, Kubiak J, et al. (2012) Palmitoylation of MPP1 (membrane-palmitoylated protein 1)/p55 is crucial for lateral membrane organization in erythroid cells. J Biol Chem 287: 18974-18984. doi: 10.1074/jbc.M111.332981 PMID: 22496366
21. Biernatowska A, Podkalicka J, Majkowski M, Hryniewicz-Jankowska A, Augoff K, Kozak K, et al. (2013) The role of MPP1/p55 and its palmitoylation in resting state raft organization in HEL cells. Biochim Biophys Acta 1833: 1876-1884. doi: 10.1016/j.bbamcr.2013.03.009 PMID: 23507198
22. Kusunoki H, Kohno T (2006) Solution Structure of Human Erythroid p55 PDZ Domain. Proteins. 64: 804-807. doi: 10.1002/prot PMID: 16741958
23. Kusunoki H, Kohno T (2007) Structural insight into the interaction between the p55 PDZ domain and glycophorin C. Biochem Biophys Res Commun. 359: 972-978. doi: 10.1016/j.bbrc.2007.05.215 PMID: 17572384
24. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40. doi: 10.1186/1471-2105-9-40 PMID: 18215316
25. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738. doi: 10.1038/nprot.2010.5 PMID: 20360767
26. Roy A, Yang J, Zhang Y (2012) COFACTOR: an accurate comparative algorithm for structure-based protein function annotation. Nucleic Acids Res 40: W471-W477. doi: 10.1093/nar/gks372 PMID: 22570420
27. Zhang Y, Skolnick J (2005) TM-align: A protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 33: 2302-2309. doi: 10.1093/nar/gki524 PMID: 15849316
28. Jayasinghe S, Hristova K, White SH (2001) Energetics, stability, and prediction of transmembrane helices. J Mol Biol 312: 927-934. PMID: 11580239
29. Eisenberg D, Weiss RM, Terwilliger TC, Wilcox W (1982) Hydrophobic moments and protein structure. Faraday Symp Chem Soc 17: 109-120.
30. Wimley WC, Gawrisch K, Creamer TP, White SH (1996) Direct measurement of salt-bridge solvation energies using a peptide model system: implications for protein stability. Proc Natl Acad Sci U S A 93: 2985-2990. PMID: 8610155
31. Costantini S, Colonna G, Facchiano AM (2008) Bioinformation ESBRI : A web server for evaluating salt bridges in proteins. Bioinformation 3: 137-138. PMID: 19238252
32. Gasteiger E, Wilkins MR, Bairoch A, Sanchez JC, Williams KL, Appel RD, et al. (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112: 531-552. PMID: 10027275
33. Yang G, Xu H, Li Z, Li F (2014) Interactions of caveolin-1 scaffolding and intramembrane regions containing a CRAC motif with cholesterol in lipid bilayers. Biochim Biophys Acta 1838: 2588-2599. doi: 10.1016/j.bbamem.2014.06.018 PMID: 24998359
34. Sheng R, Chen Y, Gee HY, Stec E, Melowic HR, Blatner NR, et al. (2012) Cholesterol Modulates Cell Signaling and Protein Networking by Specifically Interacting with PDZ Domain-Containing Scaffold Proteins. Nat Commun 3: 1-20. doi: 10.1038/ncomms2221
35. Yang W, Di Vizio D, Kirchner M, Steen H, Freeman MR (2010) Proteome scale characterization of human S-acylated proteins in lipid raft-enriched and non-raft membranes. Mol Cell Proteomics 9: 54-70. doi: 10.1074/mcp.M800448-MCP200 PMID: 19801377
36. Zhou Q, Li J, Yu H, Zhai Y, Gao Z, Yanxin L, et al. (2014) Molecular insights into the membrane-associated phosphatidylinositol 4-kinase IIα. Nat Commun 5: 1-10.
37. Barylko B, Mao YS, Wlodarski P, Jung G, Binns DD, Sun HQ, Yin HL, et al. (2009) Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase IIα. J Biol Chem. 284: 9994-10003. doi: 10.1074/jbc.M900724200 PMID: 19211550
38. Swarthout JT, Lobo S, Farh L, Croke MR, Greentree WK, Deschenes RJ, et al. (2005) DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-Ras. J Biol Chem 280: 31141-31148. PMID: 16000296
39. Rosnizeck IC, Graf T, Spoerner M, Tränkle J, Filchtinski D, Herrmann C, et al. (2010) Stabilizing a weak binding state for effectors in the human ras protein by cyclen complexes. Angew Chem Int Ed Engl 49: 3830-3833. doi: 10.1002/anie.200907002 PMID: 20401883
40. Brannigan G, Hénin J, Law R, Eckenhoff R, Klein ML (2008) Embedded cholesterol in the nicotinic acetylcholine receptor. Proc Natl Acad Sci U S A. 105: 14418-14423. doi: 10.1073/pnas.0803029105 PMID: 18768796
41. Hamouda AK, Chiara DC, Sauls D, Cohen JB, Blanton MP (2006) Cholesterol interacts with transmembrane alpha-helices M1, M3, and M4 of the Torpedo nicotinic acetylcholine receptor: photolabeling studies using [3H]Azicholesterol. Biochemistry. 45: 976-986. doi: 10.1021/bi051978h PMID: 16411773
42. Picazo-Juárez G, Romero-Suárez S, Nieto-Posadas AS, Llorente I, Jara-Oseguera AS, Briggs M, Mclntosh TJ, et al. (2011) Identification of a binding motif in the S5 helix that confers cholesterol sensitivity to the TRPV1 ion channel. J Biol Chem. 286: 24966-24976. doi: 10.1074/jbc.M111.237537 PMID: 21555515
43. Niv H, Gutman O, Kloog Y, Henis YI (2002) Activated K-Ras and H-Ras display different interactions with saturable nonraft sites at the surface of live cells. J Cell Biol 157: 865-872. PMID: 12021258
44. Roy S, Luetterforst R, Harding A, Apolloni A, Etheridge M, Stang E, et al. (1999) Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat Cell Biol 1: 98-105. PMID: 10559881
45. Eggeling C, Ringemann C, Medda R, Schwarzmann G, Sandhoff K, Polyakova S, et al. (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457: 1159-1162. doi: 10.1038/nature07596 PMID: 19098897