Proteases and their receptors as mediators of inflammation-associated colon cancer

Current Pharmaceutical Design

Volumn 21, Issue 21, 2015, Pages 2983-2992

  Trusevych, Elizabeth H ^a   MacNaughton, Wallace K ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Colitis associated cancer; Colorectal cancer; Cyclooxygenase 2; Inflammatory bowel disease; Protease activated receptors; Serine proteases

Indexed keywords

CYCLOOXYGENASE 2; HEMOSTATIC PROTEASE; ICOSANOID; IMMUNE CELL PROTEASE; KALLIKREIN; MATRIPTASE; MATRIX METALLOPROTEINASE; PLASMA KALLIKREIN; PROSTAGLANDIN D2; PROSTAGLANDIN E2; PROTEINASE; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; TISSUE KALLIKREIN; UNCLASSIFIED DRUG; PEPTIDE HYDROLASE;

ARTICLE; COLORECTAL CANCER; DISEASE ASSOCIATION; ENTERITIS; HUMAN; MAST CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CHRONIC DISEASE; COLITIS; COLONIC NEOPLASMS; COLORECTAL NEOPLASMS; COMPLICATION; ENZYMOLOGY; GASTROENTERITIS; GENETICS; PHYSIOLOGY;

ANIMALS; CHRONIC DISEASE; COLITIS; COLONIC NEOPLASMS; COLORECTAL NEOPLASMS; CYCLOOXYGENASE 2; GASTROENTERITIS; HUMANS; PEPTIDE HYDROLASES; RECEPTORS, PROTEINASE-ACTIVATED;

EID: 84931846533     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612821666150514104800     Document Type: Article

References (156)

1. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001; 357(9255): 539-45.
2. Heidland A, Klassen A, Rutkowski P, Bahner U. The contribution of Rudolf Virchow to the concept of inflammation: what is still of importance? J Nephrol 2006; 19(S10): S102-9.
3. Hirota CL, Moreau F, Iablokov V, et al. Epidermal growth factor receptor transactivation is required for proteinase-activated receptor- 2-induced COX-2 expression in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2012; 303(1): G111-9.
4. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100(1): 57-70.
5. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144(5): 646-74.
6. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420: 860-7.
7. Karin M, Greten FR. NF-κB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005; 5(10): 749-59.
8. Lu H, Ouyang W, Huang C. Inflammation, a key event in cancer development. Mol Cancer Res 2006; 4(4): 221-33.
9. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454(7203): 436-44.
10. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140(6): 883-99.
11. Pal S, Bhattacharjee A, Ali A, Mandal NC, Mandal SC, Pal M. Chronic inflammation and cancer: potential chemoprevention through nuclear factor kappa B and p53 mutual antagonism. J Inflamm 2014; 11(1): 23.
12. Palazon A, Goldrath AW, Nizet V, Johnson RS. HIF transcription factors, inflammation, and immunity. Immunity 2014; 41(4): 518- 28.
13. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancer. Science 1991; 253: 49-53.
14. Powell SM, Zilz N, Beazer-Barclay Y, et al. APC mutations occur early during colorectal tumorigenesis. Nature 1992; 359(6392): 235-7.
15. Su L-K, Vogelstein B, Kinzler KW. Association of the APC tumorsuppressor protein with catenins. Science 1993; 262(5140): 1734-7.
16. Vogelstein B, Fearon ER, Hamilton SR, et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988; 319(9): 525-32.
17. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61(5): 759-67.
18. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA-Cancer J Clin 2014; 64(1): 9-29.
19. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996; 87(2): 159-70.
20. Fearnhead NS, Britton MP, Bodmer WF. The ABC of APC. Hum Mol Genet 2001; 10(7): 721-33.
21. Morin PJ, Sparks AB, Korinek V, et al. Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science 1997; 275(5307): 1787-90.
22. Xie J, Itzkowitz SH. Cancer in inflammatory bowel disease. World J Gastroenterol 2008; 14(3): 378-89.
23. Ekbom A, Helmick C, Zack M, Adami HO. Increased risk of largebowel cancer in crohns-disease with colonic involvement. Lancet 1990; 336(8711): 357-9.
24. Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer - a population-based study. N Engl J Med 1990; 323(18): 1228-33.
25. Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 2001; 48(4): 526-35
26. Jess T, Gamborg M, Matzen P, Munkholm P, Sorensen TIA. Increased risk of intestinal cancer in Crohn's disease: a meta-analysis of population-based cohort ttudies. Am J Gastroenterol 2005; 100(12): 2724-9.
27. Jess T, Simonsen J, Jørgensen KT, Pedersen BV, Nielsen NM, Frisch M. Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years. Gastroenterology 2012; 143(2): 375-81.
28. Lutgens MWMD, van Oijen MGH, van der Heijden GJMG, Vleggaar FP, Siersema PD, Oldenburg B. Declining risk of colorectal cancer in inflammatory bowel disease. Inflamm Bowel Dis 2013; 19(4): 789-99.
29. Ren LL, Fang JY. Should we sound the alarm? Dysplasia and colitis- associated colorectal cancer. Asian Pac J Cancer Prev 2011; 12(8): 1881-6.
30. Zhao P, Metcalf M, Bunnett NW. Biased signaling of proteaseactivated receptors. Front Endocrinol 2014; 5: 67.
31. Hollenberg MD, Mihara K, Polley D, et al. Biased signalling and proteinase-activated receptors (PARs): targeting inflammatory disease. Br J Pharmacol 2014; 171: 1180-94.
32. Soh UJ, Dores MR, Chen B, Trejo J. Signal transduction by protease- activated receptors. Br J Pharmacol 2010; 160(2): 191-203.
33. Ramachandran R, Hollenberg MD. Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br J Pharmacol 2009; 153(S1): S263-82.
34. Arora P, Ricks TK, Trejo J. Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J Cell Sci 2007; 120(6): 921-8.
35. Schaffner F, Ruf W. Tissue factor and protease-activated receptor signaling in cancer. Semin Thromb Hemost 2008; 34(2): 147-53.
36. Nguyen GC, Bernstein CN, Bitton A, et al. Consensus statements on the risk, prevention, and treatment of venous thromboembolism in inflammatory bowel disease. Gastroenterology 2014; 146(3): 835-6.
37. Twig G, Zandman-Goddard G, Szyper-Kravitz M, Shoenfeld Y. Systemic thromboembolism in inflammatory bowel disease: mechanisms and clinical applications. Ann N Y Acad Sci 2005; 1051: 166-73.
38. Turpin B, Miller W, Rosenfeldt L, et al. Thrombin drives tumorigenesis in colitis-associated colon cancer. Cancer Res 2014; 74(11): 3020-30.
39. Anthoni C, Russell J, Wood KC, et al. Tissue factor: a mediator of inflammatory cell recruitment, tissue injury, and thrombus formation in experimental colitis. J Exp Med 2007; 204(7): 1595-601.
40. van den Berg YW, Osanto S, Reitsma PH, Versteeg HH. The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood 2012; 119(4): 924-32.
41. Yu JL. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood 2005; 105(4): 1734-41.
42. Rao B, Gao Y, Huang J, et al. Mutations of p53 and K-ras correlate TF expression in human colorectal carcinomas: TF downregulation as a marker of poor prognosis. Int J Colorectal Dis 2011; 26(5): 593-601.
43. Raspi G. Kallikrein and kallikrein-like proteinases: purification and determination by chromatographic and electrophoretic methods. J Chromatogr Biomed Appl 1996; 684: 265-87.
44. Costa-Neto CM, Dillenburg-Pilla P, Heinrich TA, et al. Participation of kallikrein-kinin system in different pathologies. Int Immunopharmacol 2008; 8(2): 135-42.
45. Elliott DF, Horton EW, Lewis GP. Actions of pure bradykinin. J Physiol 1960; 153(3): 473-80.
46. Stadnicki A. Immunolocalization and expression of kinin B1R and B2R receptors in human inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 2005; 289(2): G361-6.
47. Marceau F, Regoli D. Therapeutic options in inflammatory bowel disease: experimental evidence of a beneficial effect of kinin B1 receptor blockade. Br J Pharmacol 2008; 154(6): 1163-5.
48. Yoo J, Perez CER, Nie W, Sinnett-Smith J, Rozengurt E. Protein kinase D1 mediates synergistic MMP-3 expression induced by TNF-alpha and bradykinin in human colonic myofibroblasts. Biochem Biophys Res Commun 2011; 413(1): 30-5.
49. Bradley JR. TNF-mediated inflammatory disease. J Pathol 2008; 214(2): 149-60.
50. Wilson JAP. Tumor necrosis factor alpha and colitis-associated colon cancer. N Engl J Med 2008; 358(25): 2733-4.
51. Louis E, Ribbens C, Godon A, et al. Increased production of matrix metalloproteinase-3 and tissue inhibitor of metalloproteinase-1 by inflamed mucosa in inflammatory bowel disease. Clin Exp Immunol 2000; 120(2): 241-6.
52. Roeb E, Arndt M, Jansen B, Schumpelick V, Matern S. Simultaneous determination of matrix metalloproteinase (MMP)-7, MMP-1, - 3, and -13 gene expression by multiplex PCR in colorectal carcinomas. Int J Colorectal Dis 2004; 19(6): 518-24.
53. Abdallah RT, Keum JS, Lee MH, et al. Plasma kallikrein promotes epidermal growth factor receptor transactivation and signaling in vascular smooth muscle through direct activation of proteaseactivated receptors. J Biol Chem 2010; 285(45): 35206-15.
54. Oikonomopoulou K, Hansen KK, Saifeddine M, et al. Proteinaseactivated receptors, targets for kallikrein signaling. J Biol Chem 2006; 281(43): 32095-112.
55. Stadnicki A. Intestinal tissue kallikrein-kinin system in inflammatory bowel disease. Inflamm Bowel Dis 2011; 17(2): 645-54.
56. Hollenberg MD, Oikonomopoulou K, Hansen KK, Saifeddine M, Ramachandran R, Diamandis EP. Kallikreins and proteinasemediated signaling: proteinase-activated receptors (PARs) and the pathophysiology of inflammatory diseases and cancer. Biol Chem 2008; 389(6): 1-9.
57. Kontos CK, Mavridis K, Talieri M, Scorilas A. Kallikrein-related peptidases (KLKs) in gastrointestinal cancer: mechanistic and clinical aspects. Thromb Haemost 2013; 110(3): 450-7.
58. Ramachandran R, Eissa A, Mihara K, et al. Proteinase-activated receptors (PARs): differential signalling by kallikrein-related peptidases KLK8 and KLK14. Biol Chem 2012; 393(5): 421-7.
59. Hamilton MJ, Frei SM, Stevens RL. The multifaceted mast cell in inflammatory bowel disease. Inflamm Bowel Dis 2014; 20(12): 2364-78.
60. Ribatti D, Ranieri G, Nico B, Benagiano V, Crivellato E. Tryptase and chymase are angiogenic in vivo in the chorioallantoic membrane assay. Int J Dev Biol 2011; 55(1): 99-102.
61. Gelbmann CM, Mestermann S, Gross V, Köllinger M, Schölmerich J, Falk W. Strictures in Crohn's disease are characterised by an accumulation of mast cells colocalised with laminin but not with fibronectin or vitronectin. Gut 1999; 45(2): 210-7.
62. Raithel M, Winterkamp S, Pacurar A. Release of mast cell tryptase from human colorectal mucosa in inflammatory bowel disease. Scand J Gastroenterol 2001; 36(2): 174-9.
63. Kurosawa M, Nagai H. Accumulation of mast cells in the lesions and effects of antiallergic drugs on the patients with inflammatory bowel disease. Ulcers 2013; 2013(8074): 1-7.
64. Hamilton MJ, Sinnamon MJ, Lyng GD. Essential role for mast cell tryptase in acute experimental colitis. Proc Natl Acad Sci 2011; 108: 290-5.
65. Khan MW, Keshavarzian A, Gounaris E, et al. PI3K/AKT signaling is essential for communication between tissue-infiltrating mast cells, macrophages, and epithelial cells in colitis-induced cancer. Clin Cancer Res 2013; 19(9): 2342-54.
66. Gounaris E, Erdman SE, Restaino C, et al. Mast cells are an essential hematopoietic component for polyp development. Proc Natl Acad Sci 2007; 104(50): 19977-82.
67. Malfettone A, Silvestris N, Saponaro C, et al. High density of tryptase- positive mast cells in human colorectal cancer: a poor prognostic factor related to protease-activated receptor 2 expression. J Cell Mol Med 2013; 17(8): 1025-37.
68. Gulubova M, Vlaykova T. Prognostic significance of mast cell number and microvascular density for the survival of patients with primary colorectal cancer. J Gastroenterol Hepatol 2009; 24(7): 1265-75.
69. Ammendola M, Leporini C, Marech I, et al. Targeting mast cells tryptase in tumor microenvironment: a potential antiangiogenetic strategy. Biomed Res Int 2014; 2014(16): 154702-16.
70. Marech I, Ammendola M, Gadaleta C, et al. Possible biological and translational significance of mast cells density in colorectal cancer 2014; 20(27): 8910-20.
71. Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol 2012; 5(4): 354-66.
72. Dhaliwal A, Zeino Z, Tomkins C, et al. Utility of faecal calprotectin in inflammatory bowel disease (IBD): what cut-offs should we apply? Frontline Gastroenterol 2015; 6(1): 14-9.
73. Hofman PM. Pathobiology of the neutrophil-intestinal epithelial cell interaction: Role in carcinogenesis. World J Gastroenterol 2010; 16(46): 5790.
74. Shang K, Bai YP, Wang C, et al. Crucial involvement of tumorassociated neutrophils in the regulation of chronic colitis-associated carcinogenesis in mice. PLoS One 2012; 7(12): e51848.
75. Wang Y, Wang K, Han GC, et al. Neutrophil infiltration favors colitis-associated tumorigenesis by activating the interleukin-1 (IL- 1)/IL-6 axis. Mucosal Immunol 2014; 7(5): 1106-15.
76. Guma M, Ronacher L, Liu-Bryan R, Takai S, Karin M, Corr M. Caspase 1 independent activation of interleukin-1β in neutrophilpredominant inflammation. Arthritis Rheum 2009; 60(12): 3642-50.
77. Ramachandran R, Mihara K, Chung H, et al. Neutrophil elastase acts as a biased agonist for proteinase-activated receptor-2 (PAR2). J Biol Chem 2011; 286(28): 24638-48.
78. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92(8): 827-39.
79. Baugh MD, Perry MJ, Hollander AP, et al. Matrix metalloproteinase levels are elevated in inflammatory bowel disease. Gastroenterology 1999; 117(4): 814-22.
80. Meijer MJW, Mieremet-Ooms MAC, van der Zon AM, et al. Increased mucosal matrix metalloproteinase-1, -2, -3 and -9 activity in patients with inflammatory bowel disease and the relation with Crohn's disease phenotype. Dig Liver Dis 2007; 39(8): 733-9.
81. Garg P, Vijay-Kumar M, Wang L, Gewirtz AT, Merlin D, Sitaraman SV. Matrix metalloproteinase-9-mediated tissue injury overrides the protective effect of matrix metalloproteinase-2 during colitis. Am J Physiol Gastrointest Liver Physiol 2008; 296(2): G175- 84.
82. Garg P, Sarma D, Jeppsson S, et al. Matrix metalloproteinase-9 functions as a tumor suppressor in colitis-associated cancer. Cancer Res 2010; 70(2): 792-801.
83. Garg P, Jeppsson S, Dalmasso G, et al. Notch1 regulates the effects of matrix metalloproteinase-9 on colitis-associated cancer in mice. Gastroenterology 2011; 141(4): 1381-92.
84. Vaalamo M, Karjalainen-Lindsberg ML, Puolakkainen P, Kere J, Saarialho-Kere U. Distinct expression profiles of stromelysin-2 (MMP-10), collagenase-3 (MMP-13), macrophage metalloelastase (MMP-12), and tissue inhibitor of metalloproteinases-3 (TIMP-3) in intestinal ulcerations. Am J Pathol 1998; 152(4): 1005-14.
85. Koller FL, Dozier EA, Nam KT, et al. Lack of MMP10 exacerbates experimental colitis and promotes development of inflammationassociated colonic dysplasia. Lab Invest 2012; 92(12): 1749-59.
86. Monteleone I, Federici M, Sarra M, et al. Tissue inhibitor of metalloproteinase- 3 regulates inflammation in human and mouse intestine. Gastroenterology 2012; 143(5): 1277-87
87. Shi YE, Torri J, Yieh L, Wellstein A, Lippman ME, Dickson RB. Identification and characterization of a novel matrix-degrading protease from hormone-dependent human breast cancer cells. Cancer Res 1993; 53(6): 1409-15.
88. Lin CY, Anders J, Johnson M, Dickson RB. Purification and characterization of a complex containing matriptase and a Kunitz-type serine protease inhibitor from human milk. J Biol Chem 1999; 274(26): 18237-42.
89. Buzza MS, Martin EW, Driesbaugh KH, Desilets A, Leduc R, Antalis TM. Prostasin is required for matriptase activation in intestinal epithelial cells to regulate closure of the paracellular pathway. J Biol Chem 2013; 288(15): 10328-37.
90. Friis S, Uzzun Sales K, Godiksen S, et al. A Matriptase-Prostasin reciprocal zymogen activation complex with unique features. J Biol Chem 2013; 288(26): 19028-39.
91. List K, Kosa P, Szabo R, et al. Epithelial integrity is maintained by a matriptase- dependent proteolytic pathway. Am J Pathol 2010; 175(4): 1453-63.
92. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448(7152): 427-34.
93. Netzel-Arnett S, Buzza MS, Shea-Donohue T, et al. Matriptase protects against experimental colitis and promotes intestinal barrier recovery. Inflamm Bowel Dis 2012; 18(7): 1303-14.
94. Kosa P, Szabo R, Molinolo AA, Bugge TH. Suppression of Tumorigenicity- 14, encoding matriptase, is a critical suppressor of colitis and colitis-associated colon carcinogenesis. Oncogene 2011; 31(32): 3679-95.
95. Oberst M, Anders J, Bin Xie, et al. Matriptase and HAI-1 are expressed by normal and malignant epithelial cells in vitro and in vivo. Am J Pathol 2010; 158(4): 1301-11.
96. Zeng L, Cao J, Zhang X. Expression of serine protease SNC19/ matriptase and its inhibitor hepatocyte growth factor activator inhibitor type 1 in normal and malignant tissues of gastrointestinal tract. World J Gastroenterol 2005; 11(39): 6202-7.
97. Galandrin S, Oligny-Longpré G, Bouvier M. The evasive nature of drug efficacy: implications for drug discovery. Trends in Pharmacol Sci 2007; 28(8): 423-30.
98. Rasmussen UB, Vouret-Craviari V, Jallat S, et al. cDNA cloning and expression of a hamster alpha-thrombin receptor coupled to Ca2+ mobilization. FEBS Lett 1991; 288(1-2): 123-8.
99. Nystedt S, Emilsson K, Wahlestedt C, Sundelin J. Molecularcloning of a potential proteinase activated receptor. Proc Natl Acad Sci 1994; 91(20): 9208-12.
100. Ishihara H, Connolly AJ, Zeng DW, et al. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature 1997; 386(6624): 502-6.
101. Kahn ML, Zheng YW, Huang W, et al. A dual thrombin receptor system for platelet activation. Nature 1998; 394(6694): 690-4.
102. Xu WF, Andersen H, Whitmore TE, et al. Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci 1998; 95(12): 6642-6.
103. Camerer E, Huang W, Coughlin SR. Tissue factor- and factor Xdependent activation of protease-activated receptor 2 by factor VIIa. Proc Natl Acad Sci 2000; 97(10): 5255-60.
104. Vu T-K, Hung DT, Wheaton VI, Coughlin SR. Molecular-cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 1991; 64(6): 1057-68.
105. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000; 407(6801): 258-64.
106. Cenac N, Cellars L, Steinhoff M, et al. Proteinase-activated receptor- 1 is an anti-inflammatory signal for colitis mediated by a type 2 immune response. Inflamm Bowel Dis 2005; 11(9): 792-8.
107. Darmoul D, Gratio V, Devaud H, Lehy T, Laburthe M. Aberrant expression and activation of the thrombin receptor proteaseactivated receptor-1 induces cell proliferation and motility in human colon cancer cells. Am J Pathol 2003; 162(5): 1503-13.
108. Darmoul D, Gratio V, Devaud H, Peiretti F, Laburthe M. Activation of proteinase-activated receptor 1 promotes human colon cancer cell proliferation through epidermal growth factor receptor transactivation. Mol Cancer Res 2004; 2(9): 514-22.
109. Nierodzik ML, Karpatkin S. Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 2006; 10(5): 355-62.
110. Borensztajn K, Bijlsma MF, Reitsma PH, Peppelenbosch MP, Spek CA. Coagulation Factor Xa inhibits cancer cell migration via protease- activated receptor-1 activation. Thrombosis Res 2009; 124(2): 219-25.
111. Molino M, Barnathan ES, Numerof R, et al. Interactions of mast cell tryptase with thrombin receptors and PAR-2. J Biol Chem 1997; 272(7): 4043-9.
112. Riewald M, Ruf W. Mechanistic coupling of protease signaling and initiation of coagulation by tissue factor. Proc Natl Acad Sci 2001; 98(14): 7742-7.
113. McCoy KL, Traynelis SF, Hepler JR. PAR1 and PAR2 couple to overlapping and distinct sets of G proteins and linked signaling pathways to differentially regulate cell physiology. Mol Pharmacol 2010; 77(6): 1005-15.
114. Maeda S, Ohno K, Uchida K, et al. Intestinal protease-activated receptor-2 and fecal serine protease activity are increased in canine inflammatory bowel disease and may contribute to intestinal cytokine expression. J Vet Med Sci 2014; 76(8): 1119-27.
115. Cenac N, Coelho A-M, Nguyen C, et al. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor- 2. Am J Pathol 2002; 161(5): 1903-15.
116. Hyun E, Andrade-Gordon P, Steinhoff M, Vergnolle N. Proteaseactivated receptor-2 activation: a major actor in intestinal inflammation. Gut 2008; 57(9): 1222-9.
117. Kakarala KK, Jamil K. Protease activated receptor (PAR2): Possible target of phytochemicals. J Biomol Struct Dyn 2014; 1-57.
118. Chang JH, Park JM, Kim SW, Jung CK, Kang WK, Oh ST. Expression of protease activated receptor-2 in human colorectal cancer and its association with tumor progression. Dis Colon Rectum 2010; 53(8): 1202-8.
119. Ma Y, Bao-Han W, Lu X, et al. MicroRNA-34a mediates the autocrine signaling of PAR2-activating proteinase and its role in colonic cancer cell proliferation. PLoS One 2013; 8(8): e72383.
120. Zhou H, Hu H, Shi W, Ling S, Wang T, Wang H. The expression and the functional roles of tissue factor and protease-activated receptor- 2 on SW620 cells. Oncol Rep 2008; 20: 1069-76.
121. Hu L, Xia L, Zhou H, et al. TF/FVIIa/PAR2 promotes cell proliferation and migration via PKCα and ERK-dependent c-Jun/AP-1 pathway in colon cancer cell line SW620. Tumor Biol 2013; 34(5): 2573-81.
122. Darmoul D, Marie JC, Devaud H, Gratio V, Laburthe M. Initiation of human colon cancer cell proliferation by trypsin acting at protease- activated receptor-2. Br J Cancer 2001; 85(5): 772-9.
123. Iablokov V, Hirota CL, Peplowski MA, et al. Proteinase-activated receptor 2 decreases apoptosis in colonic epithelial cells. J Biol Chem 2014; 289(49): 34366-77
124. Arora P, Cuevas BD, Russo A, Johnson GL, Trejo J. Persistent transactivation of EGFR and ErbB2/HER2 by protease-activated receptor-1 promotes breast carcinoma cell invasion. Oncogene 2008; 27(32): 4434-45.
125. Caruso R, Pallone F, Fina D, et al. Protease-activated receptor-2 activation in gastric cancer cells promotes epidermal growth factor receptor trans-activation and proliferation. Am J Pathol 2006; 169(1): 268-78.
126. De Stefano A, Carlomagno C. Beyond KRAS: Predictive factors of the efficacy of anti-EGFR monoclonal antibodies in the treatment of metastatic colorectal cancer. World J Gastroenterol 2014; 20(29): 9732-43.
127. Stein A, Bokemeyer C. How to select the optimal treatment for first line metastatic colorectal cancer. World J Gastroenterol 2014; 20(4): 899-907.
128. Pagán B, Isidro AA, Cruz ML, et al. Erlotinib inhibits progression to dysplasia in a colitis-associated colon cancer model. World J Gastroenterol 2011; 17(44): 4858-66.
129. Elste AP, Petersen I. Expression of proteinase-activated receptor 1- 4 (PAR 1-4) in human cancer. J Mol Hist 2010; 41(2-3): 89-99.
130. Sambrano GR, Huang W, Faruqi T, Mahrus S, Craik C, Coughlin SR. Cathepsin G activates protease-activated receptor-4 in human platelets. J Biol Chem 2000; 275(10): 6819-23.
131. Dabek M, Ferrier L, Roka R, et al. Luminal cathepsin G and protease- activated receptor 4. Am J Pathol 2010; 175(1): 207-14.
132. Schmid W, Vogelsang H, Papay P, et al. Increased responsiveness to thrombin through protease-activated receptors (PAR)-1 and -4 in active Crohn's disease. J Crohns Colitis 2014; 8(6): 495-503.
133. Gratio V, Walker F, Lehy T, Laburthe M, Darmoul D. Aberrant expression of proteinase-activated receptor 4 promotes colon cancer cell proliferation through a persistent signaling that involves Src and ErbB-2 kinase. Int J Cancer 2009; 124(7): 1517-25.
134. Wallace JL. COX-2: A pivotal enzyme in mucosal protection and resolution of inflammation. Sci World J 2006; 6: 577-88.
135. Peek R Jr. Prevention of colorectal cancer through the use of COX- 2 selective inhibitors. Cancer Chemother Pharmacol 2004; 54(1): S50-6.
136. Setia S, Nehru B, Sanyal SN. The PI3K/Akt pathway in colitis associated colon cancer and its chemoprevention with celecoxib, a Cox-2 selective inhibitor. Biomed Pharmacother 2014; 68(6): 721- 7.
137. Kim S-H, Margalit O, Katoh H, et al. CG100649, a novel COX-2 inhibitor, inhibits colorectal adenoma and carcinoma growth in mouse models. Invest New Drugs 2014; 32(6): 1105-12.
138. Ishikawa T-O, Herschman HR. Tumor formation in a mouse model of colitis-associated colon cancer does not require COX-1 or COX- 2 expression. Carcinogenesis 2010; 31(4): 729-36.
139. Thun MJ, Namboodiri MM, Heath CW Jr. Asprin use and reduced risk of fatal colon cancer. N Engl J Med 1991; 325(23): 1593-6.
140. Yang YH, Yang Y-HK, Cheng CL, Ho PS, Ko YC. The role of chemoprevention by selective cyclooxygenase-2 inhibitors in colorectal cancer patients - a population-based study. BMC Cancer 2012; 12(1): 582.
141. Almhanna K, El-Rayes B, Sethi S, et al. Association between COX- 2 expression and effectiveness of COX-2 inhibitors in a phase II trial in patients with metastatic colorectal adenocarcinoma. Anticancer Res 2012; 32(8): 3559-63.
142. Sheibanie AF, Yen J-H, Khayrullina T, et al. The proinflammatory effect of prostaglandin E2 in experimental inflammatory bowel disease is mediated through the IL-23-->IL-17 axis. J Immunol 2007; 178(12): 8138-47.
143. Jiang G-L, Nieves A, Im WB, Old DW, Dinh DT, Wheeler L. The prevention of colitis by E prostanoid receptor 4 agonist through enhancement of epithelium survival and regeneration. J Pharmacol Exp Ther 2007; 320(1): 22-8.
144. Wang D, DuBois RN. Eicosanoids and cancer. Nat Rev Cancer 2010; 10(3): 181-93.
145. Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS. Prostaglandin E2 promotes colon cancer cell growth through a Gsaxin- beta-catenin signaling axis. Science 2005; 310(5753): 1504- 10.
146. Xu L, Stevens J, Hilton MB, et al. COX-2 inhibition potentiates antiangiogenic cancer therapy and prevents metastasis in preclinical models. Sci Transl Med 2014; 6(242): 242ra84.
147. Scher JU, Pillinger MH. 15d-PGJ2: The anti-inflammatory prostaglandin? Clin Immunol 2005; 114(2): 100-9.
148. Ajuebor MN, Singh A, Wallace JL. Cyclooxygenase-2-derived prostaglandin D-2 is an early anti-inflammatory signal in experimental colitis. Am J Physiol Gastrointest Liver Physiol 2000; 279(1): G238-44.
149. Vong L, Ferraz JGP, Panaccione R, Beck PL, Wallace JL. A proresolution mediator, prostaglandin D2, is specifically up-regulated in individuals in long-term remission from ulcerative colitis. Proc Natl Acad Sci 2010; 107(26): 12023-7.
150. Zamuner SR, Bak AW, Devchand PR, Wallace JL. Predisposition to colorectal cancer in rats with resolved colitis. Am J Pathol 2005; 167(5): 1293-300.
151. Iwanaga K, Nakamura T, Maeda S, et al. Mast cell-derived prostaglandin D2 inhibits colitis and colitis-associated colon cancer in mice. Cancer Res 2014; 74(11): 3011-9.
152. Houliston RA, Keogh RJ, Sugden D, Dudhia J, Carter TD, Wheeler-Jones CPD. Protease-activated receptors upregulate cyclooxygenase- 2 expression in human endothelial cells. Thromb Haemost 2002; 88: 321-8.
153. Kawao N, Nagataki M, Nagasawa K, et al. Signal transduction for proteinase-activated receptor-2-triggered prostaglandin E2 formation in human lung epithelial cells. J Pharmacol Exp Ther 2005; 315(2): 576-89.
154. Wang H, Wen S, Bunnett NW, Leduc R, Hollenberg MD, MacNaughton WK. Proteinase-activated receptor-2 induces cyclooxygenase- 2 expression through 22-catenin and cyclic AMPresponse element-binding protein. J Biol Chem 2008; 283(2): 809- 15.
155. van der Merwe JQ, Hollenberg MD, MacNaughton WK. EGF receptor transactivation and MAP kinase mediate proteinase-activated receptor-2-induced chloride secretion in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2007; 294(2): G441-51.
156. van der Merwe JQ, Ohland CL, Hirota CL, MacNaughton WK. Prostaglandin E2 derived from cyclooxygenases 1 and 2 mediates intestinal epithelial ion transport stimulated by the activation of protease- activated receptor 2. J Pharmacol Exp Ther 2009; 329(2): 747-52.