Small molecule inhibitors target the tissue transglutaminase and fibronectin interaction

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Yakubov, Bakhtiyor ^a   Chen, Lan ^b   Belkin, Alexey M ^b   Zhang, Sheng ^b   Chelladurai, Bhadrani ^a   Zhang, Zhong Yin ^b,c   Matei, Daniela ^a,b,c  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 (GAMMA GLUTAMYL)LYSINE; ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; FIBRONECTIN; HISTIDINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 288; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 37; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 40; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 49; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 50; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 52; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 53; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 58; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 59; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 62; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 63; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 64; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 65; SMALL MOLECULE INHIBITOR; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN; MOLECULAR LIBRARY;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOTINYLATION; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; COMPETITIVE INHIBITION; COMPLEX FORMATION; CONTROLLED STUDY; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME STRUCTURE; FEMALE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IC 50; METASTASIS; METASTASIS INHIBITION; OVARY CANCER; PERITONEUM; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; STRUCTURE ANALYSIS; TISSUE DISTRIBUTION; ANTAGONISTS AND INHIBITORS; CELL MOTION; DRUG EFFECTS; METABOLISM; MOLECULAR LIBRARY; OVARIAN NEOPLASMS; PATHOLOGY; PHARMACOLOGY; TUMOR CELL CULTURE; WESTERN BLOTTING; WOUND HEALING;

BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FIBRONECTINS; GTP-BINDING PROTEINS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; OVARIAN NEOPLASMS; PROTEIN INTERACTION MAPS; SMALL MOLECULE LIBRARIES; TRANSGLUTAMINASES; TUMOR CELLS, CULTURED; WOUND HEALING;

EID: 84895879476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089285     Document Type: Article

References (31)

1. Hang J, Zemskov EA, Lorand L, Belkin AM (2005) Identification of a novel recognition sequence for fibronectin within the NH2-terminal beta-sandwich domain of tissue transglutaminase. J Biol Chem 280: 23675-23683. (Pubitemid 40884849)
2. Akimov SS, Belkin AM (2001) Cell-surface transglutaminase promotes fibronectin assembly via interaction with the gelatin-binding domain of fibronectin: a role in TGFbeta-dependent matrix deposition. J Cell Sci 114: 2989-3000. (Pubitemid 32821537)
3. Radek JT, Jeong JM, Murthy SN, Ingham KC, Lorand L (1993) Affinity of human erythrocyte transglutaminase for a 42-kDa gelatin-binding fragment of human plasma fibronectin. Proc Natl Acad Sci U S A 90: 3152-3156. (Pubitemid 23111323)
4. Zemskov EA, Janiak A, Hang J, Waghray A, Belkin AM (2006) The role of tissue transglutaminase in cell-matrix interactions. Front Biosci 11: 1057-1076. (Pubitemid 43253460)
5. Satpathy M, Cao L, Pincheira R, Emerson R, Bigsby R, et al. (2007) Enhanced peritoneal ovarian tumor dissemination by tissue transglutaminase. Cancer Res 67: 7194-7202. (Pubitemid 47206547)
6. Verma A, Wang H, Manavathi B, Fok JY, Mann AP, et al. (2006) Increased expression of tissue transglutaminase in pancreatic ductal adenocarcinoma and its implications in drug resistance and metastasis. Cancer Res 66: 10525-10533. (Pubitemid 44799775)
7. Mann AP, Verma A, Sethi G, Manavathi B, Wang H, et al. (2006) Overexpression of Tissue Transglutaminase Leads to Constitutive Activation of Nuclear Factor-{kappa}B in Cancer Cells: Delineation of a Novel Pathway. Cancer Res 66: 8788-8795. (Pubitemid 44449196)
8. Kumar A, Xu J, Brady S, Gao H, Yu D, et al. (2010) Tissue transglutaminase promotes drug resistance and invasion by inducing mesenchymal transition in mammary epithelial cells. PLoS One 5: e13390.
9. Verma A, Guha S, Diagaradjane P, Kunnumakkara AB, Sanguino AM, et al. (2008) Therapeutic significance of elevated tissue transglutaminase expression in pancreatic cancer. Clin Cancer Res 14: 2476-2483. (Pubitemid 351551083)
10. Satpathy M, Shao M, Emerson R, Donner DB, Matei D (2009) Tissue transglutaminase regulates matrix metalloproteinase-2 in ovarian cancer by modulating cAMP-response element-binding protein activity. The Journal of biological chemistry 284: 15390-15399.
11. Shao M, Cao L, Shen C, Satpathy M, Chelladurai B, et al. (2009) Epithelial-to-mesenchymal transition and ovarian tumor progression induced by tissue transglutaminase. Cancer Res 69: 9192-9201.
12. Cao L, Shao M, Schilder J, Guise T, Mohammad KS, et al. (2012) Tissue transglutaminase links TGF-beta, epithelial to mesenchymal transition and a stem cell phenotype in ovarian cancer. Oncogene 31: 2521-2534.
13. Condello S, Cao L, Matei D (2013) Tissue transglutaminase regulates beta-catenin signaling through a c-Src-dependent mechanism. FASEB J
14. Akimov SS, Krylov D, Fleischman LF, Belkin AM (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 148: 825-838.
15. Herman JF, Mangala LS, Mehta K (2006) Implications of increased tissue transglutaminase (TG2) expression in drug-resistant breast cancer (MCF-7) cells. Oncogene 25: 3049-3058. (Pubitemid 43780469)
16. Fok JY, Ekmekcioglu S, Mehta K (2006) Implications of tissue transglutaminase expression in malignant melanoma. Mol Cancer Ther 5: 1493-1503. (Pubitemid 44070486)
17. Yuan L, Siegel M, Choi K, Khosla C, Miller CR, et al. (2007) Transglutaminase 2 inhibitor, KCC009, disrupts fibronectin assembly in the extracellular matrix and sensitizes orthotopic glioblastomas to chemotherapy. Oncogene 26: 2563-2573. (Pubitemid 46632005)
18. Liu S, Cerione RA, Clardy J (2002) Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc Natl Acad Sci U S A 99: 2743-2747. (Pubitemid 34240531)
19. Borsi L, Castellani P, Balza E, Siri A, Pellecchia C, et al. (1986) Large-scale procedure for the purification of fibronectin domains. Anal Biochem 155: 335-345. (Pubitemid 16060163)
20. Zhang JH, Chung TD, Oldenburg KR (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4: 67-73. (Pubitemid 29278954)
21. Folk JE, Cole PW (1966) Transglutaminase: mechanistic features of the active site as determined by kinetic and inhibitor studies. Biochim Biophys Acta 122: 244-264.
22. Pfluger M, Kapuscik A, Lucas R, Koppensteiner A, Katzlinger M, et al. (2013) A combined impedance and AlphaLISA-based approach to identify anti-inflammatory and barrier-protective compounds in human endothelium. J Biomol Screen 18: 67-74.
23. Han BG, Cho JW, Cho YD, Jeong KC, Kim SY, et al. (2010) Crystal structure of human transglutaminase 2 in complex with adenosine triphosphate. International Journal of Biological Macromolecules 47: 190-195.
24. Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. Plos Biology 5: 2788-2796. (Pubitemid 351159708)
25. Khanna M, Chelladurai B, Gavini A, Li L, Shao M, et al. (2011) Targeting ovarian tumor cell adhesion mediated by tissue transglutaminase. Molecular cancer therapeutics 10: 626-636.
26. Muegge I, Heald SL, Brittelli D (2001) Simple selection criteria for drug-like chemical matter. J Med Chem 44: 1841-1846. (Pubitemid 32884510)
27. Gertz M, Harrison A, Houston JB, Galetin A (2010) Prediction of human intestinal first-pass metabolism of 25 CYP3A substrates from in vitro clearance and permeability data. Drug Metab Dispos 38: 1147-1158.
28. Belkin AM, Tsurupa G, Zemskov E, Veklich Y, Weisel JW, et al. (2005) Transglutaminase-mediated oligomerization of the fibrin(ogen) {alpha}C-domains promotes integrin-dependent cell adhesion and signaling. Blood.
29. Belkin AM, Zemskov EA, Hang J, Akimov SS, Sikora S, et al. (2004) Cell-surface-associated tissue transglutaminase is a target of MMP-2 proteolysis. Biochemistry 43: 11760-11769. (Pubitemid 39277621)
30. Falasca L, Iadevaia V, Ciccosanti F, Melino G, Serafino A, et al. (2005) Transglutaminase type II is a key element in the regulation of the anti-inflammatory response elicited by apoptotic cell engulfment. J Immunol 174: 7330-7340. (Pubitemid 40705703)
31. Fesus L, Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27: 534-539. (Pubitemid 35279599)