Virtual screening for LPA2-specific agonists identifies a nonlipid compound with antiapoptotic actions

Molecular Pharmacology

Volumn 82, Issue 6, 2012, Pages 1162-1173

  Kiss, Gyöngyi N ^a,b   Fells, James I ^a   Gupte, Renuka ^a   Lee, Sue Chin ^a   Liu, Jianxiong ^a   Nusser, Nóra ^a   Lim, Keng G ^a   Ray, Ramesh M ^a   Lin, Fang Tsyr ^c   Parrill, Abby L ^d   Sümegi, Balázs ^b   Miller, Duane D ^a   Tigyi, Gabor ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF PÉCS   (Hungary)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d University of Memphis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [(9 OXO 9H FLUOREN 2 YL) CARBAMOYL]BENZOIC ACID; 2 [(9,10 DIOXO 9,10 DIHYDROANTHRACEN 2 YL)CARBAMOYL]BENZOIC ACID; 2 [[3 [1,3 DIOXO 1H BENZO [DE]ISOQUINOLIN 2(3H)YL]PROPYL]THIO]BENZOIC ACID; 4,5 DICHLORO 2 [(9 OXO 9H FLUOREN 2 YL)CARBAMOYL]BENZOIC ACID; APOPTOSIS INHIBITOR; CASPASE 3; CASPASE 7; CASPASE 9; GRI 977143; H 2 L 554924; H 2 L 5828102; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID AGONIST; LYSOPHOSPHATIDIC ACID RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NSC 12404; THYROID RECEPTOR INTERACTING PROTEIN 6; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CASPASE; G PROTEIN COUPLED RECEPTOR; LIM PROTEIN; LYSOPHOSPHOLIPID; PHOSPHOPROTEIN; PROTEIN BAX; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SODIUM HYDROGEN EXCHANGER REGULATORY FACTOR; SODIUM PROTON EXCHANGE PROTEIN; SODIUM-HYDROGEN EXCHANGER REGULATORY FACTOR; THYROID HORMONE RECEPTOR INTERACTING PROTEIN; THYROID-HORMONE-RECEPTOR INTERACTING PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG SCREENING; EMBRYO; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; UMBILICAL VEIN ENDOTHELIAL CELL; VIRTUAL REALITY; ANIMAL; CANCER INVASION; CELL LINE; CELL PROLIFERATION; CHO CELL; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; EPITHELIUM CELL; FIBROBLAST; HAMSTER; METABOLISM; MOUSE MUTANT; RAT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASES; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CHO CELLS; CRICETINAE; DNA FRAGMENTATION; EPITHELIAL CELLS; FIBROBLASTS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIM DOMAIN PROTEINS; LYSOPHOSPHOLIPIDS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; NEOPLASM INVASIVENESS; PHOSPHOPROTEINS; POLY(ADP-RIBOSE) POLYMERASES; RATS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LYSOPHOSPHATIDIC ACID; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER; TRANSCRIPTION FACTORS;

EID: 84869786660     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.079699     Document Type: Article

References (46)

1. Ballesteros JA and Weinstein H (1995) Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors. Methods Neurosci 25:366-425.
2. Brinkmann V, Billich A, Baumruker T, Heining P, Schmouder R, Francis G, Aradhye S, and Burtin P (2010) Fingolimod (FTY720): discovery and development of an oral drug to treat multiple sclerosis. Nat Rev Drug Discov 29:883-897.
3. Chen J, Han Y, Zhu W, Ma R, Han B, Cong X, Hu S, and Chen X (2006) Specific receptor subtype mediation of LPA-induced dual effects in cardiac fibroblasts. FEBS Lett 580:4737-4745. (Pubitemid 44209256)
4. Deng W, Balazs L, Wang DA, Van Middlesworth L, Tigyi G, and Johnson LR (2002) Lysophosphatidic acid protects and rescues intestinal epithelial cells from radiation- and chemotherapy-induced apoptosis. Gastroenterology 123:206-216. (Pubitemid 34747541)
5. Deng W, Poppleton H, Yasuda S, Makarova N, Shinozuka Y, Wang DA, Johnson LR, Patel TB, and Tigyi G (2004) Optimal lysophosphatidic acid-induced DNA synthesis and cell migration but not survival require intact autophosphorylation sites of the epidermal growth factor receptor. J Biol Chem 279:47871-47880. (Pubitemid 39540938)
6. Deng W, Shuyu E, Tsukahara R, Valentine WJ, Durgam G, Gududuru V, Balazs L, Manickam V, Arsura M, VanMiddlesworth L, et al. (2007) The lysophosphatidic acid type 2 receptor is required for protection against radiation-induced intestinal injury. Gastroenterology 132:1834-1851. (Pubitemid 46691269)
7. Deng W, Wang DA, Gosmanova E, Johnson LR, and Tigyi G (2003) LPA protects intestinal epithelial cells from apoptosis by inhibiting the mitochondrial pathway. Am J Physiol Gastrointest Liver Physiol 284:G821-G829. (Pubitemid 36437983)
8. Durgam GG, Tsukahara R, Makarova N, Walker MD, Fujiwara Y, Pigg KR, Baker DL, Sardar VM, Parrill AL, Tigyi G, et al. (2006) Synthesis and pharmacological evaluation of second-generation phosphatidic acid derivatives as lysophosphatidic acid receptor ligands. Bioorg Med Chem Lett 16:633-640. (Pubitemid 43014849)
9. E S, Lai YJ, Tsukahara R, Chen CS, Fujiwara Y, Yue J, Yu JH, Guo H, Kihara A, Tigyi G, et al. (2009) Lysophosphatidic acid 2 receptor-mediated supramolecular complex formation regulates its antiapoptotic effect. J Biol Chem 284:14558-14571.
10. Fischer DJ, Nusser N, Virag T, Yokoyama K, Wang Da, Baker DL, Bautista D, Parrill AL, and Tigyi G (2001) Short-chain phosphatidates are subtype-selective antagonists of lysophosphatidic acid receptors. Mol Pharmacol 60:776-784. (Pubitemid 32900260)
11. Fujiwara Y, Osborne DA, Walker MD, Wang DA, Bautista DA, Liliom K, Van Brocklyn JR, Parrill AL, and Tigyi G (2007) Identification of the hydrophobic ligand binding pocket of the S1P1 receptor. J Biol Chem 282:2374-2385. (Pubitemid 47076755)
12. Fujiwara Y, Sardar V, Tokumura A, Baker D, Murakami-Murofushi K, Parrill A, and Tigyi G (2005) Identification of residues responsible for ligand recognition and regioisomeric selectivity of lysophosphatidic acid receptors expressed in mammalian cells. J Biol Chem 280:35038-35050. (Pubitemid 41504639)
13. Funke M, Zhao Z, Xu Y, Chun J, and Tager AM (2012) The lysophosphatidic acid receptor LPA1 promotes epithelial cell apoptosis after lung injury. Am J Respir Cell Mol Biol 46:355-364.
14. Furui T, LaPushin R, Mao M, Khan H, Watt SR, Watt MA, Lu Y, Fang X, Tsutsui S, Siddik ZH, et al. (1999) Overexpression of edg-2/vzg-1 induces apoptosis and anoikis in ovarian cancer cells in a lysophosphatidic acid-independent manner. Clin Cancer Res 5:4308-4318. (Pubitemid 30013820)
15. Gupte R, Patil R, Liu J, Wang Y, Lee SC, Fujiwara Y, Fells J, Bolen AL, Emmons-Thompson K, Yates CR, et al. (2011) Benzyl and naphthalene methylphosphonic acid inhibitors of autotaxin with anti-invasive and anti-metastatic activity. ChemMedChem 6:922-935.
16. Hanson MA, Roth CB, Jo E, Griffith MT, Scott FL, Reinhart G, Desale H, Clemons B, Cahalan SM, Schuerer SC, et al. (2012) Crystal structure of a lipid G protein-coupled receptor. Science 335:851-855.
17. Lai YJ, Chen CS, Lin WC, and Lin FT (2005) c-Src-mediated phosphorylation of TRIP6 regulates its function in lysophosphatidic acid-induced cell migration. Mol Cell Biol 25:5859-5868.
18. Lai YJ, Lin WC, and Lin FT (2007) PTPL1/FAP-1 negatively regulates TRIP6 function in lysophosphatidic acid-induced cell migration. J Biol Chem 282:24381-24387.
19. Li C, Dandridge KS, Di A, Marrs KL, Harris EL, Roy K, Jackson JS, Makarova NV, Fujiwara Y, Farrar PL, et al. (2005) Lysophosphatidic acid inhibits cholera toxin-induced secretory diarrhea through CFTR-dependent protein interactions. J Exp Med 202:975-986. (Pubitemid 41396897)
20. Lin FT, Lai YJ, Makarova N, Tigyi G, and Lin WC (2007) The lysophosphatidic acid 2 receptor mediates down-regulation of Siva-1 to promote cell survival. J Biol Chem 282:37759-37769.
21. Lipinski CA (2003) Chris Lipinski discusses life and chemistry after the Rule of Five. Drug Discov Today 8:12-16.
22. Chemical Computing Group (2002) Molecular Operating Environment, Chemical Computing Group, Montreal, QC, Canada.
23. Mukai M and Akedo H (1999) Induction of tumor invasion by lysophosphatidic acid and inhibition of tumor invasion by cyclic phosphatidic acid. Tanpakushitsu Kakusan Koso 44 (8 suppl):1126-1131.
24. Mukai M, Iwasaki T, Tatsuta M, Togawa A, Nakamura H, Murakami-Murofushi K, Kobayashi S, Imamura F, and Inoue M (2003) Cyclic phosphatidic acid inhibits RhoA-mediated autophosphorylation of FAK at Tyr-397 and subsequent tumor-cell invasion. Int J Oncol 22:1247-1256.
25. Mukai M, Kusama T, Hamanaka Y, Koga T, Endo H, Tatsuta M, and Inoue M (2005) Cross talk between apoptosis and invasion signaling in cancer cells through caspase-3 activation. Cancer Res 65:9121-9125. (Pubitemid 41507970)
26. Mukai M, Nakamura H, Tatsuta M, Iwasaki T, Togawa A, Imamura F, and Akedo H (2000) Hepatoma cell migration through a mesothelial cell monolayer is inhibited by cyclic AMP-elevating agents via a Rho-dependent pathway. FEBS Lett 484:69-73.
27. 10 receptor as the sphingosine-1-phosphate and lysophosphatidic acid receptor. Biochem Biophys Res Commun 371:707-712.
28. Ohta H, Sato K, Murata N, Damirin A, Malchinkhuu E, Kon J, Kimura T, Tobo M, Yamazaki Y, Watanabe T, et al. (2003) Ki16425, a subtype-selective antagonist for EDG-family lysophosphatidic acid receptors. Mol Pharmacol 64:994-1005. (Pubitemid 37153068)
29. Parrill AL, Wang D, Bautista DL, Van Brocklyn JR, Lorincz Z, Fischer DJ, Baker DL, Liliom K, Spiegel S, and Tigyi G (2000) Identification of Edg1 receptor residues that recognize sphingosine 1-phosphate. J Biol Chem 275:39379-39384. (Pubitemid 32058961)
30. Perygin DH (2010) Identification of non-lipid LPA receptor agonists and antagonists through in silico screening, in Chemistry, p 130, University of Memphis, Memphis, TN.
31. Ray RM, Bhattacharya S, and Johnson LR (2011) Mdm2 inhibition induces apoptosis in p53 deficient human colon cancer cells by activating p73- and E2F1-mediated expression of PUMA and Siva-1. Apoptosis 16:35-44.
32. Sardar VM, Bautista DL, Fischer DJ, Yokoyama K, Nusser N, Virag T, Wang DA, Baker DL, Tigyi G, and Parrill AL (2002) Molecular basis for lysophosphatidic acid receptor antagonist selectivity. Biochim Biophys Acta 1582:309-317. (Pubitemid 34634143)
33. Sun Y, Nam JS, Han DH, Kim NH, Choi HK, Lee JK, Rhee HJ, and Huh SO (2010) Lysophosphatidic acid induces upregulation of Mcl-1 and protects apoptosis in a PTX-dependent manner in H19-7 cells. Cell Signal 22:484-494.
34. Swaney JS, Chapman C, Correa LD, Stebbins KJ, Broadhead AR, Bain G, Santini AM, Darlington J, King CD, Baccei CS, et al. (2011) Pharmacokinetic and pharmacodynamic characterization of an oral lysophosphatidic acid type 1 receptor-selective antagonist. J Pharmacol Exp Ther 336:693-700.
35. Tabata K, Baba K, Shiraishi A, Ito M, and Fujita N (2007) The orphan GPCR GPR87 was deorphanized and shown to be a lysophosphatidic acid receptor. Biochem Biophys Res Commun 363:861-866. (Pubitemid 47516713)
36. Taghavi P, Verhoeven E, Jacobs JJ, Lambooij JP, Stortelers C, Tanger E, Moolenaar WH, and van Lohuizen M (2008) In vitro genetic screen identifies a cooperative role for LPA signaling and c-Myc in cell transformation. Oncogene 27:6806-6816.
37. Tigyi G (2010) Aiming drug discovery at lysophosphatidic acid targets. Br J Pharmacol 161:241-270.
38. Tigyi G, Dyer DL, and Miledi R (1994) Lysophosphatidic acid possesses dual action in cell proliferation. Proc Natl Acad Sci USA 91:1908-1912. (Pubitemid 24080315)
39. Trott O and Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31:455-461.
40. Uchiyama A, Mukai M, Fujiwara Y, Kobayashi S, Kawai N, Murofushi H, Inoue M, Enoki S, Tanaka Y, Niki T, et al. (2007) Inhibition of transcellular tumor cell migration and metastasis by novel carba-derivatives of cyclic phosphatidic acid. Biochim Biophys Acta 1771:103-112. (Pubitemid 46073879)
41. Valentine WJ, Fells JI, Perygin DH, Mujahid S, Yokoyama K, Fujiwara Y, Tsukahara R, Van Brocklyn JR, Parrill AL, and Tigyi G (2008) Subtype-specific residues involved in ligand activation of the endothelial differentiation gene family lysophosphatidic acid receptors. J Biol Chem 283:12175-12187.
42. Valentine WJ, Kiss GN, Liu J, E S, Gotoh M, Murakami-Murofushi K, Pham TC, Baker DL, Parrill AL, Lu X, et al. (2010) (S)-FTY720-vinylphosphonate, an analogue of the immunosuppressive agent FTY720, is a pan-antagonist of sphingosine 1-phosphate GPCR signaling and inhibits autotaxin activity. Cell Signal 22:1543-1553.
43. Wang DA, Lorincz Z, Bautista DL, Liliom K, Tigyi G, and Parrill AL (2001) A single amino acid determines lysophospholipid specificity of the S1P1 (EDG1) and LPA1 (EDG2) phospholipid growth factor receptors. J Biol Chem 276:49213-49220.
44. Williams JR, Khandoga AL, Goyal P, Fells JI, Perygin DH, Siess W, Parrill AL, Tigyi G, and Fujiwara Y (2009) Unique ligand selectivity of the GPR92/LPA5 lysophosphatidate receptor indicates role in human platelet activation. J Biol Chem 284:17304-17319.
45. Xu J, Lai YJ, Lin WC, and Lin FT (2004) TRIP6 enhances lysophosphatidic acid-induced cell migration by interacting with the lysophosphatidic acid 2 receptor. J Biol Chem 279:10459-10468. (Pubitemid 38372655)
46. Yu S, Murph MM, Lu Y, Liu S, Hall HS, Liu J, Stephens C, Fang X, and Mills GB (2008) Lysophosphatidic acid receptors determine tumorigenicity and aggressiveness of ovarian cancer cells. J Natl Cancer Inst 100:1630-1642.