Molecular docking simulations provide insights in the substrate binding sites and possible substrates of the ABCC6 transporter

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Hosen, Mohammad Jakir ^a,b   Zubaer, Abdullah ^c   Thapa, Simrika ^c   Khadka, Bijendra ^c   De Paepe, Anne ^a   Vanakker, Olivier M ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b SHAHJALAL UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Bangladesh)

^c DataSoft Systems Bangladesh Limited   (Bangladesh)

Author keywords

[No Author keywords available]

Indexed keywords

LEUKOTRIENE C4; LIGAND; MENADIONE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 6; MULTIDRUG RESISTANCE PROTEIN 1; N ETHYLMALEIMIDE; ABCC6 PROTEIN, HUMAN; MULTIDRUG RESISTANCE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CLOSED CONFORMATION; COMPUTER MODEL; CONTROLLED STUDY; METABOLITE; MOLECULAR DOCKING; MOLECULAR MODEL; OPEN CONFORMATION; PREDICTION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN SUBSTRATE INTERACTION; PROTEIN TRANSPORT; PSEUDOXANTHOMA ELASTICUM; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; SUBSTRATE BINDING SITE; VIRTUAL REALITY; VIRTUAL SCREENING; CHEMICAL DATABASE; CHEMISTRY; CONFORMATION; ENZYME SPECIFICITY; GENETICS; HUMAN; METABOLISM; METABOLOME; PATHOLOGY;

BINDING SITES; DATABASES, CHEMICAL; HUMANS; METABOLOME; MOLECULAR CONFORMATION; MOLECULAR DOCKING SIMULATION; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROTEIN CONFORMATION; PSEUDOXANTHOMA ELASTICUM; SUBSTRATE SPECIFICITY;

EID: 84904904244     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102779     Document Type: Article

References (93)

1. Le Saux O, Urban Z, Tschuch C, Csiszar K, Bacchelli B, et al. (2000) Mutations in a gene encoding an ABC transporter cause pseudoxanthoma elasticum. Nat Genet 25: 223-227. (Pubitemid 30394998)
2. Uitto J, Bercovitch L, Terry SF, Terry P (2011) Pseudoxanthoma elasticum: Progress in diagnostics and research towards treatment. Summary of the 2010 PXE International Research Meeting. Am J Med Genet Part A 155: 1517-1526.
3. Le Saux O, Fülöp K, Yamaguchi Y, Iliás A, Szabó Z, et al. (2011) Expression and In Vivo Rescue of Human ABCC6 Disease-Causing Mutants in Mouse Liver. PLoS One 6: e24738.
4. Le Saux O, Bunda S, VanWart CM, Douet V, Got L, et al. (2006) Serum factors from pseudoxanthoma elasticum patients alter elastic fiber formation in vitro. J Invest Dermatol 126: 1497-505.
5. Uitto J, Pulkkinen L, Ringpfeil F (2001) Molecular genetics of Pseudoxanthoma elasticum: a metabolic disorder at the environment-genome interface? Trends Mol Med 7: 13-7. (Pubitemid 33718077)
6. Madon J, Hagenbuch B, Landmann L, Meier PJ, Stieger B (2000) Transport function and hepatocellular localization of mrp6 in rat liver. Mol Pharmacol 57: 634-41. (Pubitemid 30140896)
7. Belinsky MG, Chen ZS, Shchaveleva I, Zeng H, Kruh GD (2002) Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res 62: 6172-6177. (Pubitemid 35244468)
8. Ilias A, Urban Z, Seidl TL, Le Saux O, Sinko E, Boyd CD, et al. (2002) Loss of ATP-dependent transport activity in pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J Biol Chem 277: 16860-16867. (Pubitemid 34967710)
9. Le Saux O, Martin L, Aherrahrou Z, Leftheriotis G, Váradi A, et al. (2012) The molecular and physiological roles of ABCC6: more than meets the eye. Front Genet 3: 1-9.
10. Dawson RJ, Locher KP (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett 581: 935-8. (Pubitemid 46282725)
11. Fülöp K, Barna L, Symmons O, Závodszky P, Váradi A (2009) Clustering of disease-causing mutations on the domain-domain interfaces of ABCC6. Biochem. Biophys Res Commun 379: 706-9.
12. Váradi A, Szabó Z, Pomozi V, Boussac de H, Fülöp K, et al. (2011) ABCC6 as a target in Pseudoxanthoma Elasticum. Curr Drug Targets 12: 671-682.
13. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
14. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
15. Kurowski MA, Bujnicki JM (2003) GeneSilico protein structure prediction metaserver. Nucleic Acids Res 31: 3305-3307. (Pubitemid 37442145)
16. Wallner B, Elofsson A (2005) Pcons5: combining consensus, structural evaluation and fold recognition scores. Bioinformatics 21: 4248-4254. (Pubitemid 41724304)
17. Fiser A, Sali A (2003) Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol 374: 461-491. (Pubitemid 37531821)
18. Fiser A, Sali A (2003) ModLoop: automated modeling of loops in protein structures. Bioinformatics 19: 2500-2501. (Pubitemid 38016660)
19. Krieger E, Joo K, Lee J, Lee J, Raman S, et al. (2009) Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 9: 114-22.
20. DeGorter MK, Conseil G, Deeley RG, Campbell RL, Cole SP (2008) Molecular modeling of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochem Biophys Res Commun 365: 29-34. (Pubitemid 350102450)
21. Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2: 1511-1519. (Pubitemid 23262844)
22. Lovell SC, Davis IW, Arendall WB, de Bakker PI, Word JM, et al. (2003) Structure validation by C-alpha geometry: phi, psi and beta deviation. Proteins 50: 437-450.
23. Wallner B, Elofsson A (2003) Can correct protein models be identified? Protein Sci 12: 1073-1086. (Pubitemid 36505441)
24. Maiti R, Domselaar GHV, Zang H, Wishart DS (2004) SuperPose: a simple server for sophisticated structural superposition. Nuclic Acid Res 1: 32.
25. Amico M, Finelli M, Rossi I, Zauli A, Elofsson A, et al. (2006) PONGO: a web server for multiple predictions of all-alpha transmembrane proteins. Nucleic Acids Res 34: W169-W172. (Pubitemid 44529757)
26. Krogh A, Larsson B, Heijne GV, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J Mol Biol 305: 567-580. (Pubitemid 33032862)
27. Lukasz P, Kozlowski, Janusz M, Bujnicki (2012) MetaDisorder: a meta-server for the prediction of intrinsic disorder in proteins. BMC Bioinformatics 13: 1-11.
28. Wishart DS, Knox C, Guo AC, Cheng D, Shrivastava S, et al. (2008) DrugBank: a knowledgebase for drugs, drug actions and drug targets. Nucleic Acids Res 36: D901-D906. (Pubitemid 351149842)
29. Irwin JJ, Shoichet BK (2005) ZINC - A Free Database of Commercially Available Compounds for Virtual Screening. J Chem Inf Model 45: 177-182. (Pubitemid 40736970)
30. Fülöp K, Jiang Q, Wetering KV, Pomozi V, Szabó PT, et al. (2011) ABCC6 does not transport vitamin K3-glutathione conjugate from the liver: relevance to pathomechanisms of pseudoxanthoma elasticum. Biochem Biophys Res Commun 415: 468-71.
31. Li Z, Wan H, Shi Y, Ouyang P (2004) Personal experience with four kinds of chemical structure drawing software: review on ChemDraw, ChemWindow, ISIS/Draw, and ChemSketch. J Chem Inf Comput Sci 44: 1886-1890.
32. Rappe AK, Casewit CJ, Colwell KS, Goddard WA III, Skiff WM (1992) UFF, a Full Periodic Table Force Field for Molecular Mechanics and Molecular Dynamics Simulations. J A Chem Soc 114: 10024-10035.
33. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, et al. (2009) Autodock4 and AutoDockTools4: automated docking with selective receptor flexiblity. J Comput Chem 30: 2785-91.
34. Trott O, Olson AJ (2010) AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31: 455-61.
35. Forrest LR, Tang CL, Honig B (2006) On the accuracy of homology modeling and sequence alignment methods applied to membrane proteins. Biophys J 91: 508-517.
36. Gao C (2010) Computational studies on membrane protein structures and protein-ligand binding affinities. PhD Thesis, University of Rochester. Dept. of Chemistry, ISBN-10: 1243713143. Available: http://hdl.handle.net/1802/10585.
37. Reddy ChS, Vijayasarathy K, Srinivas E, Sastry GM, Sastry GN (2006) Homology modeling of membrane proteins: A critical assessment. Computational Biology and Chemistry 30: 120-126.
38. Xue P, Crum CM, Thibodeau PH (2014) Regulation of ABCC6 trafficking and stability by a conserved C-terminal PDZ-like sequence. PLoS ONE 9: e97360.
39. Gibrat JF, Higo J, Collura V, Garnier J (1992) A simulated annealing method for modeling the antigen combining site of antibodies. Immunomethods 1: 107-125.
40. Tusnády GE, Sarkadi B, Simon I, Váradi A (2006) Membrane topology of human ABC proteins. FEBS Letters 580: 1017-1022.
41. Mészáros B, Simon I, Dosztányi Z (2009) Prediction of protein binding regions in disordered proteins. PLoS Comput Biol 5: e1000376.
42. Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, et al. (2009) Structure of Pglycoprotein reveals a molecular basis for poly-specific drug binding. Science 323: 1718-1722.
43. Liu M, Hou T, Feng Z, Li Y (2013) The flexiblility of P-glycoprotein for its polyspecific drug binding from molecular dynamics simulations. J Biomol Struct Dyn 31: 612-29.
44. Koike K, Conseil G, Leslie EM, Deeply RG, et al. (2004) Identification of proline residues in the core cytoplasmic and transmembrane regions of multidrug resistance protein 1 (MRP1/ABCC1) important for transport function, substrate specificity, and nucleotide interactions. J Biol Chem 279: 12325-36. (Pubitemid 38445799)
45. Zang DW, Nunoya K, Vasa M, Gu HM, Theis A, et al. (2004) Transmembrane helix 11 of multidrug resistance protein 1 (MRP1/ABCC1): identification of polar amino acids important for substrate specificity and binding of ATP at nucleotide binding domain 1. Biochemistry 43: 9413-25. (Pubitemid 38955474)
46. Ito K, Oleschuk CJ, Westlake C, Vasa MZ, Deeley RG, et al. (2001) Mutation of Trp1254 in the multispecific organic anion transporter, MRP2 (ABCC2), alters substrate specificity and results in loss of methotrexate transport activity. J Biol Chem 276: 38108-14.
47. Williamson G, Aeberli I, Miguet L, Zhang Z, Sanchez MB, et al. (2007) Interaction of positional isomers of quercetin glucuronides with the transporter ABCC2 (cMOAT, MRP2). Drug Metab Dispos 35: 1262-8. (Pubitemid 47121765)
48. Wu P, Oleschuk CJ, Mao Q, Keller BO, Deeley RG, et al. (2005) Analysis of human multidrug resistance protein 1 (ABCC1) by matrix-assisted laser desorption ionization/time of flight mass spectrometry: toward identification of leukotriene C4 binding sites. Mol Pharmacol 68: 1455-65. (Pubitemid 41540001)
49. Zhang DW, Cole SP, Deeley RG (2002) Determinants of the substrate specificity of multidrug resistance protein 1: role of amino acid residues with hydrogen bonding potential in predicted transmembrane helix 17. J Biol Chem 277: 20934-41. (Pubitemid 34967403)
50. Ryu S, Kawabe T, Nada S, Yamaguchi A (2000) Identification of basic residues involved in drug export function of human multidrug resistance-associated protein 2. J Biol Chem 275: 39617-24. (Pubitemid 32058988)
51. Karwatsky JM, Georges E (2004) Drug binding domains of MRP1 (ABCC1) as revealed by photoaffinity labeling. Curr Med Chem Anticancer Agents 4: 19-30. (Pubitemid 38081747)
52. Holland IB, Cole SPC, Kuchler K, Higgins CF (2003) ABC Proteins: From Bacteria to Man. I. Barry Holland, Susan P.C. Cole, Karl Kuchler and Christopher F. Higgins, editors. Academic Press. pp. 82-97.
53. Ravna AW, Sylte I, Sager G (2009) Binding site of ABC transporter homology models confirmed by ABCB1 crystal structure. Theor Biol Med Model 4: 6-20.
54. Putman M, Van Veen HW, Konings WN (2000) Molecular Properties of Bacterial Multidrug Transporters. Microbiol Mol Biol Rev 64: 672-693. (Pubitemid 32475926)
55. Edgar R, Bibi E (1999) A single membrane-embedded negative charge is critical for recognizing positively charged drugs by the Escherichia coli multidrug resistance protein MdfA. EMBO J 18: 822-832. (Pubitemid 29082262)
56. Zhang DW, Cole SP, Deeley RG (2001) Identification of an amino acid residue in multidrug resistance protein 1 critical for conferring resistance to anthracyclines. J Biol Chem 20: 13231-9.
57. Razzaque MS (2011) The dualistic role of vitamin D in vascular calcifications. Kidney Int 79: 708-714.
58. Mallette LE, Mechanick JI (1987) Heritable syndrome of pseudoxanthoma elasticum with abnormal phosphorus and vitamin D metabolism. Am J Med 83: 1157-62. (Pubitemid 18098893)
59. Wishart DS, Jewison T, Guo AC, Wilson M, Knox C, et al. (2013) HMDB 3.0-The Human Metabolome Database in 2013. Nucleic Acids Res 41: D801-7.
60. Dobnig H, Pilz S, Scharnagl H, Renner W, Seelhorst U, et al. (2008) Independent association of low serum 25-hydroxyvitamin d and 1, 25-dihydroxyvitamin d levels with all-cause and cardiovascular mortality. Arch Intern Med 168: 1340-9 (Pubitemid 351930842)
61. Hume EM, Smith HH (1931) Calcification of the bones of rats on a diet low in ergosterol. Biochem J 25: 292-9.
62. Ishihara F, Hiramatsu K, Shigematsu S, Aizawa T, Niwa A, et al. (1992) Role of adrenal androgens in the development of arteriosclerosis as judged by pulse wave velocity and calcification of the aorta. Cardiology 80: 332-8.
63. Nishiwaki-Yasuda K, Suzuki A, Kakita A, Sekiguchi S, Asano S, et al. (2007) Vasopressin stimulates Na-dependent phosphate transport and calcification in rat aortic smooth muscle cells. Endocr J 54: 103-12. (Pubitemid 46481678)
64. Norazlina M, Chua CW, Ima-Nirwana S (2004) Vitamin E deficiency reduced lumbar bone calcium content in female rats. Med J Malaysia 59: 623-30.
65. Zimniak P, Little JM, Radominska A, Oelberg DG, Anwer MS, et al. (1991) Taurine-conjugated bile acids act as Ca2+ ionophores. Biochemistry 30: 8598-604.
66. Schiller PC, D'Ippolito G, Balkan W, Roos BA, Howard GA (2001) Gapjunctional communication mediates parathyroid hormone stimulation of mineralization in osteoblastic cultures. Bone 28: 38-44. (Pubitemid 32112060)
67. Progesterone and Tendon calcification. Available: http://www.ehealthme. com/ds/progesterone/.
68. Reichrath J (2012) Unravelling of hidden secrets: The role of vitamin D in skin aging. Dermatoendocrinol 4: 241-4.
69. Kim SJ, Lee J, Jee SH, Nam CM, Chun K, et al. (2010) Cardiovascular risk factors for incident hypertension in the prehypertensive population. Epidemiol Health 32: e2010003.
70. Shih DM, Shaposhnik Z, Meng Y, Rosales M, Wang X, et al. (2013) Hyodeoxycholic acid improves HDL function and inhibits atherosclerotic lesion formation in LDLR-knockout mice. FASEB J 27: 3805-17.
71. Wang Y, Sun Z (2009) Current understanding of klotho. Ageing Res Rev 8: 43-51.
72. Folic acid and calcification metastatic, http://www.ehealthme.com/ds/ folic+acid/calcification.
73. Mansell JP, Shorez D, Farrar D, Nowghani M (2009) Lithocholate-a promising non-calcaemic calcitriol surrogate for promoting human osteoblast maturation upon biomaterials. Steroids 74: 963-70.
74. Harmand PO, Duval R, Delage C, Simon A (2005) Ursolic acid induces apoptosis through mitochondrial intrinsic pathway and caspase-3 activation in M4Beu melanoma cells. Int J Cancer 114: 1-11. (Pubitemid 40194303)
75. Balmer ML, Siegrist K, Zimmermann A, Dufour JF (2009) Effects of ursodeoxycholic acid in combination with vitamin E on adipokines and apoptosis in patients with nonalcoholic steatohepatitis. Liver Int 29: 1184-8.
76. Straub RH, Tankó LB, Christiansen C, Larsen PJ, Jessop DS (2008) Higher physical activity is associated with increased androgens, low interleukin 6 and less aortic calcification in peripheral obese elderly women. J Endocrinol 199: 61-8.
77. The Editors (2012) Circulation research thermatic synopsis: Atherosclerosis. Circ Res 111: e123-162.
78. Blau N, Bonafé L, Krägeloh-Mann I, Thöny B, Kierat L, et al. (2003) Cerebrospinal fluid pterins and folates in Aicardi-Goutières syndrome: a new phenotype. Neurology 61: 642-7. (Pubitemid 37082601)
79. Woody RC, Brewster MA, Glasier C (1989) Progressive intracranial calcification in dihydropteridine reductase deficiency prior to folinic acid therapy. Neurology 39: 673-5. (Pubitemid 19126965)
80. Klesges LM, Murray DM, Brown JE, Cliver SP, Goldenberg RL (1998) Relations of cigarette smoking and dietary antioxidants with placental calcification. Am J Epidemiol 147: 127-35. (Pubitemid 28060482)
81. Pacini S, Morucci G, Branca JJ, Aterini S, Amato M, et al. (2013) Effects of vitamin D3 and paricalcitol on immature cardiomyocytes: a novel role for vitamin d analogs in the prevention of cardiovascular diseases. Nutrients 5: 2076-92.
82. Ziedén B, Kaminskas A, Kristenson M, Kucinskienê Z, Vessby B, et al. (1999) Increased plasma 7 beta-hydroxycholesterol concentrations in a population with a high risk for cardiovascular disease. Arterioscler Thromb Vasc Biol 19: 967-71. (Pubitemid 29177344)
83. Bird FH (1978) The effect of aflatoxin B1 on the utilization of cholecalciferol by chicks. Poult Sci 57: 1293-6.
84. http://www.ebay.com/itm/Cholesterol-Guard-high-quality-Beta-Sitosterol- Cayenne-Garlic-100-tablets-/330875462368.
85. Pacini S, Morucci G, Branca JJ, Aterini S, Amato M, et al. (2013). Effects of vitamin D3 and paricalcitol on immature cardiomyocytes: a novel role for vitamin D analogs i the prevention of cardiovascular diseases. Nutrients 5: 2076-92.
86. Oshima T, Sakamoto M, Tatsuta H, Arita H (1998) GABAergic inhibition of hiccup-like reflex induced by electrical stimulation in medulla of cats. Neurosci Res 30: 287-93. (Pubitemid 28291777)
87. Broulik PD, Stárka L (1997) Effect of antiandrogens casodex and epitestosterone on bone composition in mice. Bone 20: 473-5. (Pubitemid 27230452)
88. Thiers H, Pelloux H, Fayolle J, Brunat M (1960) Polymyositis with secondary calcification. Influence of stigmasterol on phosphorus-calcium elimination. Bull Soc Fr Dermatol Syphiligr 67: 359-60.
89. Ward JJ, McGuffin LJ, Bryson K, Buxton BF, Jones DT (2004) The DISOPRED server for the prediction of protein disorder. Bioinformatics 20: 2138-9. (Pubitemid 39236567)
90. Ishida T, Kinoshita K (2007) PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res 35: W460-4.
91. Dosztányi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21: 3433-4. (Pubitemid 41222453)
92. Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS, et al. (2007) DisProt: the Database of Disordered Proteins. Nucleic Acids Res 35: D786-93. (Pubitemid 46056310)
93. Linding R, Russell RB, Neduva V, Gibson TJ (2003) GlobPlot: Exploring protein sequences for globularity and disorder. Nucleic Acids Res 31: 3701-8. (Pubitemid 37442227)