Targeting protease-activated receptor-1 with cell-penetrating pepducins in lung cancer

American Journal of Pathology

Volumn 179, Issue 1, 2011, Pages 513-523

  Cisowski, Jaroslaw ^a   O'Callaghan, Katie ^a   Kuliopulos, Athan ^a,b   Yang, John ^a   Nguyen, Nga ^a   Deng, Qing ^c   Yang, Eric ^a,b   Fogel, Michael ^a   Tressel, Sarah ^a   Foley, Caitlin ^b   Agarwal, Anika ^a   Hunt III, Stephen W ^c   McMurry, Tom ^c   Brinckerhoff, Larry ^a   Covic, Lidija ^a,b  

^a TUFTS MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Anchor Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BEVACIZUMAB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PEPDUCIN INHIBITOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ALVEOLUS EPITHELIUM; LUNG CARCINOMA; MOLECULARLY TARGETED THERAPY; MONOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING;

ADENOCARCINOMA; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CYTOPLASM; EPITHELIAL CELLS; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; LIPOPEPTIDES; LUNG; LUNG NEOPLASMS; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; RECEPTOR, PAR-1; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

EID: 80052443569     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.03.025     Document Type: Article

References (53)

1. A. Jemal, R. Siegel, E. Ward, T. Murray, J. Xu, and M.J. Thun Cancer statistics, 2007 CA Cancer J Clin 57 2007 43 66
2. W.C. Dempke, T. Suto, and M. Reck Targeted therapies for non-small cell lung cancer Lung Cancer 67 2010 257 274
3. R.S. Herbst, T.J. Lynch, and A.B. Sandler Beyond doublet chemotherapy for advanced non-small-cell lung cancer: combination of targeted agents with first-line chemotherapy Clin Lung Cancer 10 2009 20 27
4. A. Boire, L. Covic, A. Agarwal, S. Jacques, S. Sherifi, and A. Kuliopulos PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells Cell 120 2005 303 313
5. N. Nguyen, A. Kuliopulos, R.A. Graham, and L. Covic Tumor-derived Cyr61 (CCN1) promotes stromal matrix metalloproteinase-1 production and protease-activated receptor 1-dependent migration of breast cancer cells Cancer Res 66 2006 2658 2665
6. A. Agarwal, L. Covic, L.M. Sevigny, N.C. Kaneider, K. Lazarides, G. Azabdaftari, S. Sharifi, and A. Kuliopulos Targeting a metalloprotease-PAR1 signaling system with cell-penetrating pepducins inhibits angiogenesis, ascites, and progression of ovarian cancer Mol Cancer Ther 7 2008 2746 2757
7. E. Yang, A. Boire, A. Agarwal, N. Nguyen, K. O'Callaghan, P. Tu, A. Kuliopulos, and L. Covic Blockade of PAR1 signaling with cell-penetrating pepducins inhibits Akt survival pathways in breast cancer cells and suppresses tumor survival and metastasis Cancer Res 69 2009 6223 6231
8. T.-K.H. Vu, D.T. Hung, V.I. Wheaton, and S.R. Coughlin Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor action Cell 64 1991 1057 1068
9. S. Nystedt, K. Emilsson, C. Wahlestedt, and J. Sundelin Molecular cloning of a potential proteinase activated receptor Proc Natl Acad Sci U S A 91 1994 9208 9212
10. H. Ishihara, A.J. Connolly, D. Zeng, M.L. Kahn, Y.W. Zheng, C. Timmons, T. Tram, and S.R. Coughlin Protease-activated receptor 3 is a second thrombin receptor in humans Nature 386 1997 502 506
11. W.-F. Xu, H. Andersen, T.E. Whitmore, S.R. Presnell, D.P. Yee, A. Ching, T. Gilbert, E.W. Davie, and D.C. Foster Cloning and characterization of human protease-activated receptor 4 Proc Natl Acad Sci U S A 95 1998 6642 6646
12. V.A. Schmidt, W.C. Nierman, D.R. Maglott, L.D. Cupit, K.A. Moskowitz, J.A. Wainer, and W.F. Bahou The human proteinase-activated receptor-3 (PAR-3) gene Identification within a Par gene cluster and characterization in vascular endothelial cells and platelets J Biol Chem 273 1998 15061 15068
13. M.L. Kahn, Y.-W. Zheng, W. Huang, V. Bigornia, D. Zheng, S. Moff, R.V. Farese, C. Tam, and S.R. Coughlin A dual thrombin receptor system for platelet activation Nature 394 1998 690 694
14. S.K. Bohm, W. Kong, D. Bromme, S.P. Smeekens, D.C. Anderson, A. Connolly, M. Kahn, N.A. Nelken, S.R. Coughlin, D.G. Payan, and N.W. Bunnett Molecular cloning, expression and potential functions of the human proteinase-activated receptor-2 Biochem J 314 1996 1009 1016
15. V. Trivedi, A. Boire, B. Tchernychev, N.C. Kaneider, A.J. Leger, K. O'Callaghan, L. Covic, and A. Kuliopulos Platelet matrix metalloprotease-1 mediates thrombogenesis by activating PAR1 at a cryptic ligand site Cell 137 2009 332 343
16. R.R. Vassallo, T. Kieber-Emmons, K. Cichowski, and L.R. Brass Structure-function relationships in the activation of platelet thrombin receptors by receptor-derived peptides J Biol Chem 267 1992 6081 6085
17. B. al-Ani, M. Saifeddine, and M.D. Hollenberg Detection of functional receptors for the proteinase-activated-receptor-2-activating polypeptide SLIGRL-NH2, in rat vascular and gastric smooth muscle Can J Physiol Pharmacol 73 1995 1203 1207
18. V.S. Ossovskaya, and N.W. Bunnett Protease-activated receptors: contribution to physiology and disease Physiol Rev 84 2004 579 621
19. C.T. Griffin, Y. Srinivasan, Y.-W. Zheng, W. Huang, and S.R. Coughlin A role for thrombin receptor signaling in endothelial cells during embryonic development Science 293 2001 1666 1670
20. K. Borensztajn, J.H. von der Thusen, M.P. Peppelenbosch, and C.A. Spek The coagulation factor Xa/protease activated receptor-2 axis in the progression of liver fibrosis: a multifaceted paradigm J Cell Mol Med 14 2010 143 153
21. A.J. Leger, S.L. Jacques, J. Badar, N.C. Kaneider, C.K. Derian, P. Andrade-Gordon, L. Covic, and A. Kuliopulos Blocking the protease-activated receptor 14 heterodimer in platelet-mediated thrombosis Circulation 113 2006 1244 1254
22. N.C. Kaneider, A.J. Leger, A. Agarwal, N. Nguyen, G. Perides, C. Derian, L. Covic, and A. Kuliopulos 'Role reversal' for the receptor PAR1 in sepsis-induced vascular damage Nat Immunol 8 2007 1303 1312
23. M.L. Nierodzik, K. Chen, K. Takeshita, J.J. Li, Y.Q. Huang, X.S. Feng, M.R. D'Andrea, P. Andrade-Gordon, and S. Karpatkin Protease-activated receptor 1 (PAR-1) is required and rate-limiting for thrombin-enhanced experimental pulmonary metastasis Blood 92 1998 3694 3700
24. C. Tellez, and M. Bar-Eli Role and regulation of the thrombin receptor (PAR-1) in human melanoma Oncogene 22 2003 3130 3137
25. S. Even-Ram, B. Uziely, P. Cohen, S. Grisaru-Granovsky, M. Maoz, Y. Ginzburg, R. Reich, I. Vlodavsky, and R. Bar-Shavit Thrombin receptor overexpression in malignant and physiological invasion processes Nat Med 4 1998 909 914
26. K.P. Henrikson, S.L. Salazar, J.W. Fenton, and B.T. Pentecost Role of thrombin receptor in breast cancer invasiveness Br J Cancer 79 1999 401 406
27. C. Rudroff, S. Seibold, R. Kaufmann, C.C. Zetina, K. Reise, U. Schafer, A. Schneider, M. Brockmann, J. Scheele, and E.A. Neugebauer Expression of the thrombin receptor PAR-1 correlates with tumour cell differentiation of pancreatic adenocarcinoma in vitro Clin Exp Metastasis 19 2002 181 189
28. I. Whitehead, H. Kirk, and R. Kay Expression cloning of oncogenes by retroviral transfer of cDNA libraries Mol Cell Biol 15 1995 704 710
29. C.B. Martin, G.M. Mahon, M.B. Klinger, R.J. Kay, M. Symons, C.J. Der, and I.P. Whitehead The thrombin receptor, PAR-1, causes transformation by activation of Rho-mediated signaling pathways Oncogene 20 2001 1953 1963
30. P. Ghio, S. Cappia, G. Selvaggi, S. Novello, P. Lausi, G. Zecchina, M. Papotti, P. Borasio, and G.V. Scagliotti Prognostic role of protease-activated receptors 1 and 4 in resected stage IB non-small-cell lung cancer Clin Lung Cancer 7 2006 395 400
31. L. Covic, A.L. Gresser, J. Talavera, S. Swift, and A. Kuliopulos Activation and inhibition of G protein-coupled receptors by cell-penetrating membrane-tethered peptides Proc Natl Acad Sci U S A 99 2002 643 648
32. N.C. Kaneider, A. Agarwal, A.J. Leger, and A. Kuliopulos Reversing systemic inflammatory response syndrome with chemokine receptor pepducins Nat Med 11 2005 661 665
33. M.D. Hollenberg, M. Saifeddine, S. Sandhu, S. Houle, and N. Vergnolle Proteinase-activated receptor-4: evaluation of tethered ligand-derived peptides as probes for receptor function and as inflammatory agonists in vivo Br J Pharmacol 143 2004 443 454
34. S.H. Slofstra, M.F. Bijlsma, A.P. Groot, P.H. Reitsma, T. Lindhout, H. ten Cate, and C.A. Spek Protease-activated receptor-4 inhibition protects from multiorgan failure in a murine model of systemic inflammation Blood 110 2007 3176 3182
35. L. Covic, M. Misra, J. Badar, C. Singh, and A. Kuliopulos Pepducin-based intervention of thrombin receptor signaling and systemic platelet activation Nat Med 8 2002 1161 1165
36. L. Kamath, A. Meydani, F. Foss, and A. Kuliopulos Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells Cancer Res 61 2001 5933 5940
37. M. Hatziapostolou, C. Polytarchou, D. Panutsopulos, L. Covic, and P.N. Tsichlis Proteinase-activated receptor-1-triggered activation of tumor progression locus-2 promotes actin cytoskeleton reorganization and cell migration Cancer Res 68 2008 1851 1861
38. A. Agarwal, S.L. Tressel, R. Kaimal, M. Balla, F.H. Lam, L. Covic, and A. Kuliopulos Identification of a metalloprotease-chemokine signaling system in the ovarian cancer microenvironment: implications for antiangiogenic therapy Cancer Res 70 2010 5880 5890
39. K. Palczewski, T. Kumasaka, T. Hori, C.A. Behnke, H. Motoshima, B.A. Fox, I.L. Trong, D.C. Teller, T. Okada, R.E. Stenkamp, M. Yamamoto, and M. Miyano Crystal structure of rhodopsin: a G protein-coupled receptor Science 289 2000 739 745
40. S. Swift, A.J. Leger, J. Talavera, L. Zhang, A. Bohm, and A. Kuliopulos Role of the PAR1 receptor 8th helix in signaling: the 7-8-1 receptor activation mechanism J Biol Chem 281 2006 4109 4116
41. q in a patient with abnormal platelet responses Proc Natl Acad Sci U S A 94 1997 8750 8755
42. L. Covic, A.L. Gresser, and A. Kuliopulos Biphasic kinetics of activation and signaling for PAR1 and PAR4 thrombin receptors in platelets Biochemistry 39 2000 5458 5467
43. P.J. Roberts, and C.J. Der Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer Oncogene 26 2007 3291 3310
44. H. Wang, F. Moreau, C.L. Hirota, and W.K. Macnaughton Proteinase-activated receptors induce interleukin-8 expression by intestinal epithelial cells through ERK/RSK90 activation and histone acetylation FASEB J 24 2010 1971 1980
45. C.H. Shih, M.Y. Bien, L.L. Chiang, C.L. Su, C.H. Lin, and B.C. Chen Thrombin induces cyclooxygenase-2 expression via the ERK and NF-kappaB pathways in human lung fibroblasts Eur J Pharmacol 618 2009 70 75
46. R. Wadgaonkar, K. Somnay, and J.G. Garcia Thrombin induced secretion of macrophage migration inhibitory factor (MIF) and its effect on nuclear signaling in endothelium J Cell Biochem 105 2008 1279 1288
47. H. Wang, J.J. Ubl, R. Stricker, and G. Reiser Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways Am J Physiol Cell Physiol 283 2002 C1351 C1364
48. P. Andrade-Gordon, B.E. Maryanoff, C.K. Derian, H.-C. Zhang, M.F. Addo, A.L. Darrow, A.J. Eckardt, W.J. Hoekstra, D.F. McComsey, D. Oksenberg, E.E. Reynolds, R.J. Santulli, R.M. Scarborough, C.E. Smith, and K.B. White Design, synthesis, and biological characterization of a peptide-mimetic antagonist for a tethered-ligand receptor Proc Natl Acad Sci U S A 96 1999 12257 12262
49. Y.Q. Huang, J.J. Li, L. Hu, M. Lee, and S. Karpatkin Thrombin induces increased expression and secretion of VEGF from human FS4 fibroblasts DU145 prostate cells and CHRF megakaryocytes Thromb Haemost 86 2001 1094 1098
50. L. Covic, B. Tchernychev, S. Jacques, and A. Kuliopulos Pharmacology and in vivo efficacy of pepducins in hemostasis and arterial thrombosis Handbook of Cell-Penetrating Peptides 14 2006 245 257
51. S.J. Wielders, A. Bennaghmouch, C.P. Reutelingsperger, E.M. Bevers, and T. Lindhout Anticoagulant and antithrombotic properties of intracellular protease-activated receptor antagonists J Thromb Haemost 5 2007 571 576
52. M.D. Hollenberg PARs in the stars: proteinase-activated receptors and astrocyte function Focus on "Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways." Am J Physiol Cell Physiol 283 2002 C1347 C1350
53. A. Kuliopulos, L. Covic, S.K. Seeley, P.J. Sheridan, J. Helin, and C.E. Costello Plasmin desensitization of the PAR1 thrombin receptor: kinetics Sites of truncation, and implications for thrombolytic therapy Biochemistry 38 1999 4572 4585