ADP-ribosylated proteins as old and new drug targets for anticancer therapy: The example of ARF6

Current Pharmaceutical Design

Volumn 19, Issue 4, 2013, Pages 624-633

  Dani, Nadia ^a,c   Moura Barbosa, Arménio Jorge ^b   Del Rio, Alberto ^b   Di Girolamo, Maria ^a  

^a Laboratorio Angela Valenti dei Fattori Genetici e Ambientali di Rischio Trombotico   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c Bioclarma Srl   (Italy)

Author keywords

ADP ribosyltransferase; ARF6; ARTC; ARTD; Mono ADP ribosylation; NAD; NAD glycohydrolase; PARP; Poly ADP ribosylpolymerase; Post translational modification; Protein protein docking

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; ANTINEOPLASTIC AGENT; ARGININE; BMN 763; CEP 9722; CYSTEINE; GLUTAMIC ACID; GPI 21016; INIPARIB; INO 1001; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NIRAPARIB; OLAPARIB; POLY(ADENOSINE DIPHOSPHATE RIBOSE); RUCAPARIB; UNCLASSIFIED DRUG; VELIPARIB;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ALPHA HELIX; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER THERAPY; CRYSTAL STRUCTURE; DNA REPAIR; DRUG TARGETING; ENDOPLASMIC RETICULUM; GENOMIC INSTABILITY; HUMAN; MITOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 84876733507     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161213804581882     Document Type: Review

References (127)

1. Di Girolamo M, Dani N, Stilla A, Corda D. Physiological relevance of the endogenous mono(ADP-ribosyl)ation of cellular proteins. Febs J 2005; 272: 4565-75.
2. Slade D, Dunstan MS, Barkauskaite E, et al. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 2011; 477: 616-20.
3. Fathers C, Drayton RM, Solovieva S, Bryant HE. Inhibition of poly(ADP-ribose) glycohydrolase (PARG) specifically kills BRCA2-deficient tumor cells. Cell Cycle 2012; 11.
4. Kato J, Zhu J, Liu C, et al. ADP-ribosylarginine hydrolase regulates cell proliferation and tumorigenesis. Cancer Res 2011; 71: 5327-35.
5. Krueger KM, Barbieri JT. The family of bacterial ADPribosylating exotoxins. Clin Microbiol Rev 1995; 8: 34-47.
6. Seman M, Adriouch S, Haag F, Koch-Nolte F. Ecto-ADPribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr Med Chem 2004; 11: 857-72.
7. Domenighini M, Magagnoli C, Pizza M, Rappuoli R. Common features of the NAD-binding and catalytic site of ADP-ribosylating toxins. Mol Microbiol 1994; 14: 41-50.
8. Hottiger MO, Hassa PO, Luscher B, Schuler H, Koch-Nolte F. Toward a unified nomenclature for mammalian ADPribosyltransferases. Trends Biochem Sci 2010; 35: 208-19.
9. Glowacki G, Braren R, Firner K, et al. The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci 2002; 11: 1657-70.
10. Okazaki IJ, Moss J. Characterization of glycosylphosphatidylinositiol-anchored, secreted, and intracellular vertebrate mono-ADPribosyltransferases. Annu Rev Nutr 1999; 19: 485-509.
11. Stilla A, Di Paola S, Dani N, et al. Characterisation of a novel glycosylphosphatidylinositol-anchored mono-ADP-ribosyltransferase isoform in ovary cells. Eur J Cell Biol 2011; 90: 665-77.
12. Seman M, Adriouch S, Scheuplein F, Krebs C, Freese D, Glowacki G, Deterre P, Haag F, Koch-Nolte F. NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 2003; 19: 571-82.
13. Paone G, Wada A, Stevens LA, et al. ADP ribosylation of human neutrophil peptide-1 regulates its biological properties. Proc Natl Acad Sci U S A 2002; 99: 8231-5.
14. Zolkiewska A, Moss J. Integrin alpha 7 as substrate for a glycosylphosphatidylinositol-anchored ADP-ribosyltransferase on the surface of skeletal muscle cells. J Biol Chem 1993; 268: 25273-76.
15. Okazaki IJ, Moss J. Glycosylphosphatidylinositol-anchored and secretory isoforms of mono-ADP-ribosyltransferases. J Biol Chem 1998; 273: 23617-620.
16. Corda D, Di Girolamo M. Mono-ADP-ribosylation: a tool for modulating immune response and cell signaling. Sci STKE 2002; 2002: PE53.
17. Leno GH, Ledford BE. ADP-ribosylation of the 78-kDa glucoseregulated protein during nutritional stress. Eur. J. Biochem. 1989; 186: 205-11.
18. Lupi R, Corda D, Di Girolamo M. Endogenous ADP-ribosylation of the G protein beta subunit prevents the inhibition of type 1 adenylyl cyclase. J Biol Chem 2000; 275: 9418-24.
19. Herrero-Yraola A, Bakhit SM, Franke P, et al. Regulation of glutamate dehydrogenase by reversible ADP-ribosylation in mitochondria. Embo J 2001; 20: 2404-12.
20. Dani N, Stilla A, Marchegiani A, et al. Combining affinity purification by ADP-ribose-binding macro domains with mass spectrome try to define the mammalian ADP-ribosyl proteome. Proc Natl Acad Sci U S A 2009; 106: 4243-48.
21. Ame JC, Spenlehauer C, de Murcia G. The PARP superfamily. Bioessays 2004; 26: 882-93.
22. Hakme A, Wong HK, Dantzer F, Schreiber V. The expanding field of poly(ADP-ribosyl)ation reactions. 'Protein Modifications: Beyond the Usual Suspects' Review Series. EMBO Rep 2008; 9: 1094-100.
23. Wahlberg E, Karlberg T, Kouznetsova E, et al. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat Biotechnol 2012; 30: 283-88.
24. Cerbinskaite A, Mukhopadhyay A, Plummer ER, Curtin NJ, Edmondson RJ. Defective homologous recombination in human cancers. Cancer Treat Rev 2012; 38: 89-100.
25. Citarelli M, Teotia S, Lamb RS. Evolutionary history of the poly(ADP-ribose) polymerase gene family in eukaryotes. BMC Evol Biol 2010; 10: 308.
26. Miwa M, Masutani M. PolyADP-ribosylation and cancer. Cancer Sci 2007; 98: 1528-1535.
27. Boehler C, Dantzer F. PARP-3, a DNA-dependent PARP with emerging roles in double-strand break repair and mitotic progression. Cell Cycle 2011; 10: 1023-4.
28. Chang P, Coughlin M, Mitchison TJ. Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 2005; 7: 1133-9.
29. Kanai M, Tong WM, Sugihara E, Wang ZQ, Fukasawa K, Miwa M. Involvement of poly(ADP-Ribose) polymerase 1 and poly(ADP-Ribosyl)ation in regulation of centrosome function. Mol Cell Biol 2003; 23: 2451-62.
30. Kleine H, Poreba E, Lesniewicz K, et al. Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol Cell 2008; 32: 57-69.
31. Yu M, Schreek S, Cerni C, et al. PARP-10, a novel Mycinteracting protein with poly(ADP-ribose) polymerase activity, inhibits transformation. Oncogene 2005; 24: 1982-93.
32. Goenka S, Boothby M. Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. Proc Natl Acad Sci U S A 2006; 103: 4210-5.
33. Di Paola S, Micaroni M, Di Tullio G, Buccione R, Di Girolamo M. PARP16/ARTD15 Is a Novel Endoplasmic-Reticulum-Associated Mono-ADP-ribosyltransferase that interacts with, and modifies Karyopherin-β1. PLoS ONE 2012; in press.
34. Nachury MV, Maresca TJ, Salmon WC, Waterman-Storer CM, Heald R, Weis K. Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 2001; 104: 95-106.
35. Tanner KG, Landry J, Sternglanz R, Denu JM. Silent information regulator 2 family of NAD-dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc Natl Acad Sci U S A 2000; 97: 14178-82.
36. Frye RA. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun 2000; 273: 793-8.
37. Bruzzone S PM, Grozio A, Bauer I, Del Rio A, Nencioni A. Rejuvenating sirtuins: the rise of a new family of cancer drug targets. Curr Pharm Des 2013; 19(4): 614-23.
38. Andreoli F BA, Parenti MD, Del Rio A. Modulation of epigenetic targets for anticancer therapy: clinicopathological relevance, structural data and drug discovery perspectives. Curr Pharm Des 2013; 19(4): 578-613.
39. Liszt G, Ford E, Kurtev M, Guarente L. Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J Biol Chem 2005; 280: 21313-20.
40. Haigis MC, Mostoslavsky R, Haigis KM, et al. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell 2006; 126: 941-54.
41. Ferraris DV. Evolution of poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors. From concept to clinic. J Med Chem 2010; 53: 4561-84.
42. Narwal M, Venkannagari H, Lehtio L. Structural basis of selective inhibition of human tankyrases. J Med Chem 2012; 55: 1360-7.
43. Curtin NJ. Poly(ADP-ribose) polymerase (PARP) and PARP inhibitors. In Drug Discovery Today: Disease Models. Elsevier B.V., 2012: e51-e58.
44. Tentori L, Graziani G. Chemopotentiation by PARP inhibitors in cancer therapy. Pharmacol Res 2005; 52: 25-33.
45. Berman HM, Westbrook J, Feng Z, et al. The Protein Data Bank. Nucleic Acids Res 2000; 28: 235-42.
46. UniProtConsortium: Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 2012; 40: D71-75.
47. Plummer R, Jones C, Middleton M, et al. Phase I study of the poly(ADP-ribose) polymerase inhibitor, AG014699, in combination with temozolomide in patients with advanced solid tumors. Clin Cancer Res 2008; 14: 7917-23.
48. Virag L, Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 2002; 54: 375-429.
49. Jagtap P, Szabo C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 2005; 4: 421-40.
50. Leung M, Rosen D, Fields S, Cesano A, Budman DR. Poly(ADPribose) polymerase-1 inhibition: preclinical and clinical development of synthetic lethality. Mol Med 2011; 17: 854-62.
51. Guha M. PARP inhibitors stumble in breast cancer. Nat Biotechnol 2011; 29: 373-374.
52. O'Shaughnessy J, Osborne C, Pippen JE, et al. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med 2011; 364: 205-14.
53. Ohno K, Mitsui T, Tanida Y, et al. Docking study and binding free energy calculation of poly (ADP-ribose) polymerase inhibitors. J Mol Model 2011; 17: 383-9.
54. Costantino G, Macchiarulo A, Camaioni E, Pellicciari R. Modeling of poly(ADP-ribose)polymerase (PARP) inhibitors. Docking of ligands and quantitative structure-activity relationship analysis. J Med Chem 2001; 44: 3786-94.
55. Bellocchi D, Macchiarulo A, Costantino G, Pellicciari R. Docking studies on PARP-1 inhibitors: insights into the role of a binding pocket water molecule. Bioorg Med Chem 2005; 13: 1151-7.
56. Gandhi VB, Luo Y, Liu X, et al. Discovery and SAR of substituted 3-oxoisoindoline-4-carboxamides as potent inhibitors of poly(ADP-ribose) polymerase (PARP) for the treatment of cancer. Bioorg Med Chem Lett 2010; 20: 1023-6.
57. Hanai S, Kanai M, Ohashi S, et al. Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc Natl Acad Sci U S A 2004; 101: 82-6.
58. Fauzee NJ, Li Q, Wang YL, Pan J. Silencing Poly (ADP-Ribose) Glycohydrolase (PARG) Expression Inhibits Growth of Human Colon Cancer Cells In Vitro via PI3K/Akt/NFkappa-B Pathway. Pathol Oncol Res 2012; 18: 191-9.
59. Min W, Wang ZQ. Poly (ADP-ribose) glycohydrolase (PARG) and its therapeutic potential. Front Biosci 2009; 14: 1619-26.
60. Finch KE, Knezevic CE, Nottbohm AC, Partlow KC, Hergenrother PJ. Selective Small Molecule Inhibition of Poly(ADP-Ribose) Glycohydrolase (PARG). ACS Chem Biol 2012; 7: 563-70.
61. Lupi R, Dani N, Dietrich A, et al. Endogenous mono-ADPribosylation of the free Gbetagamma prevents stimulation of phosphoinositide 3 kinase-gamma and phospholipase C-beta2 and Is activated by G-protein-coupled receptors. Biochem J 2002; 30.
62. Chen Y, Weng G, Li J, et al. A surface on the G protein betasubunit involved in interactions with adenylyl cyclases. Proc Natl Acad Sci U S A 1997; 94: 2711-4.
63. Dani N, Mayo E, Stilla A, et al. Mono-ADP-ribosylation of the G Protein βα Dimer Is Modulated by Hormones and Inhibited by Arf6. J Biol Chem 2011; 286: 5995-6005.
64. Ledford BE, Leno GH. ADP-ribosylation of the molecular chaperone GRP78/BiP. Mol Cell Biochem 1994; 138: 141-8.
65. Maattanen P, Gehring K, Bergeron JJ, Thomas DY. Protein quality control in the ER: The recognition of misfolded proteins. Semin Cell Dev Biol 2010.
66. Dudek J, Benedix J, Cappel S, Greiner M, Jalal C, Muller L, Zimmermann R. Functions and pathologies of BiP and its interaction partners. Cell Mol Life Sci 2009; 66: 1556-69.
67. Pfaffenbach KT, Lee AS. The critical role of GRP78 in physiologic and pathologic stress. Curr Opin Cell Biol 2010.
68. Laitusis AL, Brostrom MA, Brostrom CO. The dynamic role of GRP78/BiP in the coordination of mRNA translation with protein processing. J Biol Chem 1999; 274: 486-93.
69. Dolle C, Niere M, Lohndal E, Ziegler M. Visualization of subcellular NAD pools and intra-organellar protein localization by poly-ADP-ribose formation. Cell Mol Life Sci 2010; 67: 433-43.
70. Du L, Zhang X, Han YY, et al. Intra-mitochondrial poly(ADPribosylation) contributes to NAD+ depletion and cell death induced by oxidative stress. J Biol Chem 2003; 278: 18426-33.
71. Du X, Matsumura T, Edelstein D, et al. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Invest 2003; 112: 1049-57.
72. De Matteis MA, Di Girolamo M, Colanzi A, et al. Stimulation of endogenous ADP-ribosylation by brefeldin A. Proc Natl Acad Sci U S A 1994; 91: 1114-8.
73. Di Girolamo M, Silletta MG, De Matteis MA, et al. Evidence that the 50-kDa substrate of brefeldin A-dependent ADP-ribosylation binds GTP and is modulated by the G-protein beta gamma subunit complex. Proc Natl Acad Sci U S A 1995; 92: 7065-9.
74. Weigert R, Colanzi A, Mironov A, et al. Characterization of chemical inhibitors of brefeldin A-activated mono-ADPribosylation. J Biol Chem 1997; 272: 14200-7.
75. Deveze-Alvarez M, Garcia-Soto J, Martinez-Cadena G. Glyceraldehyde-3-phosphate dehydrogenase is negatively regulated by ADP-ribosylation in the fungus Phycomyces blakesleeanus. Microbiology 2001; 147: 2579-84.
76. Fendrick JL, Iglewski WJ. Endogenous ADP-ribosylation of elongation factor 2 in polyoma virus-transformed baby hamster kidney cells. Proc Natl Acad Sci U S A 1989; 86: 554-7.
77. Fendrick JL, Iglewski WJ, Moehring JM, Moehring TJ. Characterization of the endogenous ADP-ribosylation of wild-type and mutant elongation factor 2 in eukaryotic cells. Eur J Biochem 1992; 205: 25-31.
78. Corda D, Di Girolamo M. Functional aspects of protein mono-ADP-ribosylation. EMBO J 2003; 22: 1953-8.
79. Aktories K, Lang AE, Schwan C, Mannherz HG. Actin as target for modification by bacterial protein toxins. Febs J 2011; 278: 4526-43.
80. Terashima M, Yamamori C, Shimoyama M. ADP-ribosylation of Arg28 and Arg206 on the actin molecule by chicken argininespecific ADP-ribosyltransferase. Eur J Biochem 1995; 231: 242-9.
81. Tsuyama S, Fujita H, Hijikata R, Okamoto H, Takenaka S. Effects of mono-ADP-ribosylation on cytoskeletal actin in chromaffin cells and their release of catecholamine. Int J Biochem Cell Biol 1999; 31: 601-11.
82. Lodhi IJ, Clift RE, Omann GM, Sweeney JF, McMahon KK, Hinshaw DB. Inhibition of mono-ADP-ribosyltransferase activity during the execution phase of apoptosis prevents apoptotic body formation. Arch Biochem Biophys 2001; 387: 66-77.
83. Terashima M, Shimoyama M, Tsuchiya M. Introduction of NAD decreases fMLP-induced actin polymerization in chicken polymorphonuclear leukocytes--the role of intracellular ADP-ribosylation of actin for cytoskeletal organization. Biochem Mol Biol Int 1999; 47: 615-20.
84. Honda A, Nogami M, Yokozeki T, et al. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 1999; 99: 521-32.
85. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006; 7: 347-58.
86. Donaldson JG. Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem 2003; 278: 41573-6.
87. Hashimoto S, Onodera Y, Hashimoto A, et al. Requirement for Arf6 in breast cancer invasive activities. Proc Natl Acad Sci U S A 2004; 101: 6647-52.
88. Tague SE, Muralidharan V, D'Souza-Schorey C. ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc Natl Acad Sci U S A 2004; 101: 9671-6.
89. Moss J, Vaughan M. Molecules in the ARF orbit. J Biol Chem 1998; 273: 21431-34.
90. Tsuchiya M, Price SR, Tsai SC, Moss J, Vaughan M. Molecular identification of ADP-ribosylation factor mRNAs and their expression in mammalian cells. J Biol Chem 1991; 266: 2772-7.
91. Hosaka M, Toda K, Takatsu H, Torii S, Murakami K, Nakayama K. Structure and intracellular localization of mouse ADPribosylation factors type 1 to type 6 (ARF1-ARF6). J Biochem 1996; 120: 813-9.
92. Tsai SC, Adamik R, Haun RS, Moss J, Vaughan M. Differential interaction of ADP-ribosylation factors 1, 3, and 5 with rat brain Golgi membranes. Proc Natl Acad Sci U S A 1992; 89: 9272-6.
93. Whitney JA, Gomez M, Sheff D, Kreis TE, Mellman I. Cytoplasmic coat proteins involved in endosome function. Cell 1995; 83: 703-13.
94. Kim SW, Hayashi M, Lo JF, Yang Y, Yoo JS, Lee JD. ADPribosylation factor 4 small GTPase mediates epidermal growth factor receptor-dependent phospholipase D2 activation. J Biol Chem 2003; 278: 2661-8.
95. Yang CZ, Heimberg H, D'Souza-Schorey C, Mueckler MM, Stahl PD. Subcellular distribution and differential expression of endogenous ADP-ribosylation factor 6 in mammalian cells. J Biol Chem 1998; 273: 4006-11.
96. Claing A. Regulation of G protein-coupled receptor endocytosis by ARF6 GTP-binding proteins. Biochem Cell Biol 2004; 82: 610-7.
97. Gillingham AK, Munro S. The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 2007; 23: 579-611.
98. D'Souza-Schorey C, van Donselaar E, Hsu VW, Yang C, Stahl PD, Peters PJ. ARF6 targets recycling vesicles to the plasma membrane: insights from an ultrastructural investigation. J Cell Biol 1998; 140: 603-16.
99. Radhakrishna H, Klausner RD, Donaldson JG. Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J Cell Biol 1996; 134: 935-47.
100. Macia E, Luton F, Partisani M, Cherfils J, Chardin P, Franco M. The GDP-bound form of Arf6 is located at the plasma membrane. J Cell Sci 2004; 117: 2389-98.
101. Menetrey J, Macia E, Pasqualato S, Franco M, Cherfils J. Structure of Arf6-GDP suggests a basis for guanine nucleotide exchange factors specificity. Nat Struct Biol 2000; 7: 466-9.
102. Pasqualato S, Menetrey J, Franco M, Cherfils J. The structural GDP/GTP cycle of human Arf6. EMBO Rep 2001; 2: 234-8.
103. Goldberg J. Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching. Cell 1998; 95: 237-8.
104. Goldberg J. Structural and functional analysis of the ARF1-ARFGAP complex reveals a role for coatomer in GTP hydrolysis. Cell 1999; 96: 893-902.
105. Welsh CF, Moss J, Vaughan M. ADP-ribosylation factors: a family of approximately 20-kDa guanine nucleotide-binding proteins that activate cholera toxin. Mol Cell Biochem 1994; 138: 157-66.
106. Moss J, Haun RS, Tsai SC, et al. Activation of cholera toxin by ADP-ribosylation factors: 20-kDa guanine nucleotide-binding proteins. Methods Enzymol 1994; 237: 44-63.
107. Moss J, Vaughan M. Activation of cholera toxin and Escherichia coli heat-labile enterotoxins by ADP-ribosylation factors, a family of 20 kDa guanine nucleotide-binding proteins. Mol Microbiol 1991; 5: 2621-7.
108. Cassel D, Pfeuffer T. Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc Natl Acad Sci U S A 1978; 75: 2669-73.
109. Di Girolamo M, Corda D. Mono-ADP-ribosylation of heterotrimeric G proteins. San Diego, Ralph Bradshaw and Edward Dennis, Academic Press, 2009.
110. O'Neal CJ, Jobling MG, Holmes RK, Hol WG. Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 2005; 309: 1093-6.
111. Mueller-Dieckmann C, Ritter H, Haag F, Koch-Nolte F, Schulz GE. Structure of the ecto-ADP-ribosyl transferase ART2.2 from rat. J Mol Biol 2002; 322: 687-96.
112. Ritter H, Koch-Nolte F, Marquez VE, Schulz GE. Substrate binding and catalysis of ecto-ADP-ribosyltransferase 2.2 from rat. Biochemistry 2003; 42: 10155-62.
113. Bazan JF, Koch-Nolte F. Sequence and structural links between distant ADP-ribosyltransferase families. Adv Exp Med Biol 1997; 419: 99-107.
114. Maestro v: 2011.
115. Schrödinger Suite 2011 Protein Preparation Wizard; Epik version 2.2 S, LLC, New York, NY, 2011; Impact version 5.7, Schrödinger, LLC, New York, NY, 2011; Prime version 3.0, Schrödinger, LLC, New York, NY, 2011.: 2011.
116. Tovchigrechko A, Vakser IA. Development and testing of an automated approach to protein docking. Proteins 2005; 60: 296-301.
117. Tovchigrechko A, Vakser IA. GRAMM-X public web server for protein-protein docking. Nucleic Acids Res 2006; 34: W310-4.
118. Muralidharan-Chari V, Clancy J, Plou C, et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 2009; 19: 1875-85.
119. Muralidharan-Chari V, Hoover H, Clancy J, et al. ADPribosylation factor 6 regulates tumorigenic and invasive properties in vivo. Cancer Res 2009; 69: 2201-9.
120. Sabe H. Requirement for Arf6 in cell adhesion, migration, and cancer cell invasion. J Biochem 2003; 134: 485-9.
121. Sabe H, Hashimoto S, Morishige M, et al. The EGFR-GEP100-Arf6-AMAP1 signaling pathway specific to breast cancer invasion and metastasis. Traffic 2009; 10: 982-93.
122. Knizhnik AV, Kovaleva OB, Laktionov KK, et al. [Arf6, RalA and BIRC5 protein expression in non small cell lung cancer]. Mol Biol (Mosk) 2011; 45: 307-15.
123. Sanders MP, Barbosa AJ, Zarzycka B, et al. Comparative Analysis of Pharmacophore Screening Tools. J Chem Inf Model 2012.
124. Moura Barbosa AJ, Del Rio A. Freely accessible databases of commercial compounds for high-throughput virtual screenings. Curr Top Med Chem 2012; 12: 866-77.
125. Caporuscio F, Rastelli G, Imbriano C, Del Rio A. Structure-based design of potent aromatase inhibitors by high-throughput docking. J Med Chem 2011; 54: 4006-17.
126. Del Rio A, Barbosa A, Caporuscio F. Use of large multiconformational databases with structure-based pharmacophore models for fast screening of commercial compound collections. Journal of Cheminformatics 2011.
127. Cousins KR. Computer review of Chem Draw Ultra 12.0. J Am Chem Soc 2011; 133: 8388.