Differential effects of serine proteases on the migration of normal and tumor cells: Implications for tumor microenvironment

Integrative Cancer Therapies

Volumn 7, Issue 4, 2008, Pages 282-294

  Elzer, Kirsten L ^a   Heitzman, Deborah A ^b   Chernin, Mitchell I ^b   Novak, Josef F ^b  

^a Cornell University ^*  (United States)

^b BUCKNELL UNIVERSITY   (United States)

Author keywords

Cancer; Cell migration; Protease activated receptors; Thrombin; Trypsin

Indexed keywords

PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; SERINE PROTEINASE; TRYPSIN;

ARTICLE; CANCER CELL CULTURE; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROMA CELL; TUMOR CELL; WESTERN BLOTTING;

ANIMALS; CATTLE; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CHYMOTRYPSIN; DOGS; ENZYME PRECURSORS; GENE EXPRESSION; HUMANS; NEOPLASMS; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; RATS; RECEPTOR, PAR-1; RECEPTOR, PAR-2; SERINE ENDOPEPTIDASES; THROMBIN; TRYPSIN;

EID: 58149177394     PISSN: 15347354     EISSN: 1552695X     Source Type: Journal    
DOI: 10.1177/1534735408327250     Document Type: Article

References (81)

1. Del Rosso M., Fibbi G., Pucci M., et al. Multiple pathways of cell invasion are regulated by multiple families of serine proteases. Clin Exp Metastasis. 2002 ; 19: 193-207.
2. Sorsa T., Salo T., Koivunen E., et al. Activation of type IV procollagenases by human tumor-associated trypsin-2. J Biol Chem. 1997 ; 272: 21067-21074.
3. Sadir R., Imberty A., Baleux F., Lortat-Jacob H. Heparan sulfate/ heparin oligosaccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV. J Biol Chem. 2004 ; 279: 43854-43860.
4. Hornebeck W., Maquart FX Proteolyzed matrix as a template for the regulation of tumor progression. Biomed Pharmacother. 2003 ; 57: 223-230.
5. Ghosh MC, Grass L., Soosaipillai A., Sotiropoulou G., Diamandis EP Human kallikrein 6 degrades extracellular matrix proteins and may enhance the metastatic potential of tumor cells. Tumor Biol. 2004 ; 25: 193-199.
6. Nyberg P., Xie L., Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res. 2005 ; 65: 3967-3979.
7. Nierodzik ML, Karpatkin S. Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell. 2006 ; 10: 355-362.
8. Arora P., Ricks TK, Trejo J. Protease-activated receptor signaling, endocytic sorting and dysregulation in cancer. J Cell Sci. 2007 ; 120: 921-928.
9. Darmoul D., Gratio V., Devaud H., Lehy T., Laburthe M. Aberrant expression and activation of the thrombin receptor protease-activated receptor-1 induces cell proliferation and motility in human colon cancer cells. Am J Pathol. 2003 ; 162: 1503-1513.
10. Hollenberg MD Protease-mediated signalling: new paradigms for cell regulation and drug development. Trends Pharmacol Sci. 1966 ; 17: 3-6.
11. Dery O., Corvera CU, Steinhoff M., Bunnett NW Proteinase-activated receptors: novel mechanisms of signaling by serine proteases. Am J Physiol. 1998 ; 274: C1429 - C1452.
12. O'Brien PJ, Molino M., Kahn M., Brass LF Protease activated receptors: theme and variations. Oncogene. 2001 ; 20: 1570-1581.
13. Ossovskaya VS, Bunnett NW Protease-activated receptors: contribution to physiology and disease. Physiol Rev. 2003 ; 84: 579-621.
14. Macfarlane SR, Seatter MJ, Kanke T., Hunter GD, Plevin R. Proteinase-activated receptors. Pharmacol Rev. 2001 ; 53: 245-282.
15. Kawabata A., Kawao N. Physiology and pathophysiology of proteinase-activated receptors (PARs): PARs in the respiratory system: cellular signaling and physiological/pathological roles. J Pharmacol Sci. 2005 ; 97: 20-24.
16. Novak JF, Trnka F. Proenzyme treatment of cancer. Anticancer Res. 2005 ; 25: 1157-1178.
17. Gaggioli C., Hooper S., Hidalgo-Carcedo C., et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol. 2007 ; 9: 1392-1400.
18. Even-Ram S., Uziely B., Cohen P., et al. Thrombin receptor over-expression in malignant and physiological invasion processes. Nat Med. 1998 ; 4: 909-914.
19. Henrikson KP, Salazar SL, Fenton JW II, Pentecost BT Role of thrombin receptor in breast cancer invasiveness. Br J Cancer. 1999 ; 79: 401-406.
20. Brass LF, Manning DR, Williams AG, Woolkalis MJ, Poncz M. Receptor and G-protein-mediated responses to thrombin in HEL cells. J Biol Chem. 1991 ; 266: 958-965.
21. Boire A., Covic L., Agarwal A., Jacques S., Sherifi S., Kuliopulos A. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell. 2005 ; 120: 303-313.
22. Majumdar M., Tarui T., Shi B., Akakura N., Ruf W., Takada Y. Plasmin-induced migration requires signaling through protease-activated receptor 1 and integrin α9β1. J Biol Chem. 2004 ; 279: 37528-37534.
23. Shi X., Gangadharan B., Brass, LF, Ruf W., Mueller BM Protease-activated receptors (PAR1 and PAR2) contribute to tumor cell motility and metastasis. Mol Cancer Res. 2004 ; 2: 395-402.
24. Morris DR, Ding Y., Ricks TK, Gullapalli A., Wolfe BL, Trejo J. Protease-activated receptor-2 is essential for factor VIIa and Xa-induced signaling, migration, and invasion of breast cancer cells. Cancer Res. 2006 ; 66, 307-314.
25. Kamath L., Meydani A., Foss F., Kuliopulos A. Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells. Cancer Res. 2001 ; 61: 5933-5940.
26. Beard J. The action of trypsin upon the living cells of Jensen's mouse-tumour. Br Med J. 1906 ; 1: 140-141.
27. Beard J. The Enzyme Treatment of Cancer and its Scientific Basis. London, UK. Chatto & Windus ; 1911.
28. Purushotham AD, Brown DC, McCulloch P., Choy A., George WD Streptokinase inhibits pulmonary tumor seeding in an animal experimental model. J Surg Oncol. 1994 ; 57: 3-7.
29. Beuth J., Ost B., Pakdaman A., et al. Impact of complementary oral enzyme application on the postoperative treatment results of breast cancer patients-results of an epidemiological multi-centre retrolective cohort study. Cancer Chemother Pharmacol. 2001 ; 47 (suppl): S45 - S54.
30. Popiela T., Kulig J., Hanisch J., Bock PR Influence of a complementary treatment with oral enzymes on patients with colorectal cancers-an epidemiological retrolective cohort study. Cancer Chemother Pharmacol. 2001 ; 47 (suppl): S55 - S63.
31. Sakalova A., Bock PR, Dedik L., et al. Retrolective cohort study of an additive therapy with an oral enzyme preparation in patients with multiple myeloma. Cancer Chemother Pharmacol. 2001 ; 47 (suppl): S38 - S44.
32. Desser L., Sakalova A., Zavadova E., Holomanova D., Mohr T. Oral enzyme therapy improves remission time, soluble TNFreceptors and β2-microglobulin concentration in chemotherapy treated multiple myeloma patients. Int J Tissue React. 1997 ; 19: 94.
33. Sebekova K., Dammrich J., Fierlbeck W., Krivosikova Z., Paczek L., Heidland A. Effect of chronic therapy with proteolytic enzymes on hypertension-induced renal injury in the rat model of Goldblatt hypertension. Am J Nephrol. 1998 ; 18: 570-576.
34. Gewert K., Holowachuk SA, Rippe C., et al. The enzyme levels in blood are not affected by oral administration of a pancreatic enzyme preparation (Creon 10,000) in pancreas-insufficient pigs. Pancreas. 2004 ; 28: 80-88.
35. Saifeddine M., Seymour ML, Xiao YP, et al. Proteinase-activated receptor-2 activating peptides: distinct canine coronary artery receptor systems. Am J Physiol. 2007 ; 293: H3279 - H3289.
36. Hollenberg MD, Compton SJ International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev. 2002 ; 54: 203-217.
37. Reijerkerk A., Voest EE, Gebbink MF No grip, no growth: the conceptual basis of excessive proteolysis in the treatment of cancer. Eur J Cancer. 2000 ; 36: 1695-1705.
38. Bohm SK, Khitin LM, Grady EF, Aponte G., Payan DG, Bunnett NW Mechanisms of desensitization and resensitization of proteinase-activated receptor-2. J Biol Chem. 1996 ; 271: 22003-22016.
39. Miyata S., Koshikawa N., Yasumitsu H., Miyazaki K. Trypsin stimulates integrin α5β1-dependent adhesion to fibronectin and proliferation of human gastric carcinoma cells through activation of proteinase-activated receptor-2. J Biol Chem. 2000 ; 275: 4592-4598.
40. Davies G., Jiang WG, Mason MD Cell-cell adhesion molecules and signaling intermediates and their role in the invasive potential of prostate cancer cells. J Urol. 2000 ; 163: 985-992.
41. DiMilla PA, Stone JA, Quinn JA, Albelda SM, Lauffenburger DA Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J Cell Biol. 1993 ; 122: 729-737.
42. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 1997 ; 385: 537-540.
43. Yin Y.-J., Salah Z., Grisaru-Granovsky S., et al. Human protease-activated receptor 1 expression in malignant epithelia: a role in invasiveness. Arterioscler Thromb Vasc Biol. 2003 ; 23: 940-944.
44. Bajou K., Masson V., Gerard RD, et al. The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin: implications for antiangiogenic strategies. J Cell Biol. 2001 ; 152: 777-784.
45. Ubl JJ, Sergeeva M., Reiser G. Desensitization of protease-activated receptor-1 (PAR-1) in rat astrocytes: evidence for a novel mechanism for terminating Ca2+ signaling evoked by the tethered ligand. J Physiol. 2000 ; 525: 319-330.
46. Altrogge LM, Monard D. An assay for high-sensitivity detection of thrombin activity and determination of proteases activating or inactivating protease-activated receptors. Anal Biochem. 2000 ; 277: 33-45.
47. Miao Q., Sun Y., Wei T., et al. Chymotrypsin B cached in rat liver lysosomes and involved in apoptotic regulation through a mitochondrial pathway. J Biol Chem. 2008 ; 283: 8218-8228.
48. Kim YV, Di Cello F., Hillaire CS, Kim KS Differential Ca2+ signaling by thrombin and protease-activated receptor-1-activating peptide in human brain microvascular endothelial cells. Am J Physiol. 2004 ; 286: C31 - C42.
49. Shintani Y., Hirano K., Nakayama T., Nishimura J., Nakano H., Kanaide H. Mechanism of trypsin-induced contraction in the rat myometrium: the possible involvement of a novel member of protease-activated receptor. Br J Pharmacol. 2001 ; 133: 1276-1285.
50. Loew D., Perrault C., Morales M., et al. Proteolysis of the exodomain of recombinant protease-activated receptors: prediction of receptor activation or inactivation by MALDI mass spectrometry. Biochemistry. 2000 ; 39: 10812-10822.
51. Cocks TM, Moffatt JD Protease-activated receptor-2 (PAR2) in the airways. Pulm Pharmacol Ther. 2001 ; 14: 183-191.
52. Kaneider NC, Leger AJ, Agarwal A., et al. "Role reversal" for the receptor PAR1 in sepsis-induced vascular damage. Nat Immunol. 2007 ; 8: 1303-1312.
53. Dery O., Thoma MS, Wong H., Grady EF, Bunnett NW Trafficking of proteinase-activated receptor-2 and β-arrestin-1 tagged with green fluorescent protein. β-Arrestin-dependent endocytosis of a proteinase receptor. J Biol Chem. 1999 ; 274: 18524-18535.
54. Brass LF, Pizarro S., Ahuja M., et al. Changes in the structure and function of the human thrombin receptor during receptor activation, internalization, and recycling. J Biol Chem. 1994 ; 269: 2943-2952.
55. Jacob C., Cottrell GS, Gehringer D., Schmidlin F., Grady EF, Bunnett NW c-Cbl mediates ubiquitination, degradation, and down-regulation of human protease-activated receptor 2. J Biol Chem. 2005 ; 280: 16076-16087.
56. Molino M., Woolkalis MJ, Reavey-Cantwell J., et al. Endothelial cell thrombin receptors and PAR-2. Two protease-activated receptors located in a single cellular environment. J Biol Chem. 1997 ; 272: 11133-11141.
57. Nakayama T., Hirano K., Shintani Y., et al. Unproductive cleavage and the inactivation of protease-activated receptor-1 by trypsin in vascular endothelial cells. Br J Pharmacol. 2003 ; 138: 121-130.
58. Woolkalis MJ, DeMelfi TM, Blanchard N., Hoxie JA, Brass LF Regulation of thrombin receptors on human umbilical vein endothelial cells. J Biol Chem. 1995 ; 270: 9868-9875.
59. Mirza H., Yatsula V., Bahou WF The proteinase activated receptor-2 (PAR-2) mediates mitogenic responses in human vascular endothelial cells. J Clin Invest. 1996 ; 97: 1705-1714.
60. Whitehead I., Kirk H., Kay R. Expression cloning of oncogenes by retroviral transfer of cDNA libraries. Mol Cell Biol. 1995 ; 15: 704-710.
61. Martin CB, Mahon GM, Klinger MB, et al. The thrombin receptor, PAR-1, causes transformation by activation of Rho-mediated signaling pathways. Oncogene. 2001 ; 20: 1953-1963.
62. Yamashita K., Mimori K., Inoue H., Mori M., Sidransky D. A tumor-suppressive role for trypsin in human cancer progression. Cancer Res. 2003 ; 63: 6575-6587.
63. Miller G., Bauer K., Howarth D., Cooper JA, Humphries SE, Rosenberg RD Increased incidence of neoplasia of the digestive tract in men with persistent activation of the coagulation pathway. J Thromb Haemost. 2004 ; 2: 2107-2114.
64. Booden MA, Eckert L., Der CJ, Trejo J. Persistent signaling by dysregulated thrombin receptor trafficking promotes breast carcinoma cell invasion. Mol Cell Biol. 2004 ; 24: 1990-1999.
65. Rudroff C., Striegler S., Schilli M., Scheele J. Thrombin enhances adhesion in pancreatic cancer in vitro through the activation of the thrombin receptor PAR1. Eur. J Surg Oncol. 2001 ; 27: 472-476.
66. Even-Ram SC, Maoz M., Pokroy E., et al. Tumor cell invasion is promoted by activation of protease activated receptor-1in cooperation with the αvβ5 integrin. J Biol Chem. 2001 ; 276: 10952-10962.
67. Huang YQ, Li JJ, Hu L., Lee M., Karpatkin S. Thrombin induces increased expression and secretion of angiopoietin-2 from human umbilical vein endothelial cells. Blood. 2002 ; 99: 1646-1650.
68. Innerfield I., Angrist A., Schwarz A. Parenteral administration of trypsin: clinical effect in 538 patients. J Am Med Assoc. 1953 ; 152: 597-605.
69. Napoli C., De Nigris F., Cicala C., et al. Protease-activated receptor-2 activation improves efficiency of experimental ischemic preconditioning. Am J Physiol. 2002 ; 282: H2004 - H2010.
70. Kawabata A., Kinoshita M., Nishikawa H., et al. The protease-activated receptor-2 agonist induces gastric mucus secretion and mucosal cytoprotection. J Clin Invest. 2001 ; 107: 1443-1450.
71. Moffatt JD, Jeffrey KL, Cocks TM Protease-activated receptor-2 activating peptide SLIGRL inhibits bacterial lipopolysaccharide-induced recruitment of polymorphonuclear leukocytes into the airways of mice. Am J Respir Cell Mol Biol. 2002 ; 26: 680-684.
72. Sharma A., Tao X., Gopal A., et al. Protection against acute pancreatitis activation of protease-activated receptor-2. Am J Physiol. 2005 ; 288: G388 - G395.
73. Steinhoff M., Buddenkotte J., Shpacovitch V., et al. Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr Rev. 2005 ; 26: 1-43.
74. Kaufmann R., Schafberg H., Nowak G. Proteinase-activated receptor-2-mediated signaling and inhibition of DNA synthesis in human pancreatic cancer cells. Int J Pancreatol. 1998 ; 24: 97-102.
75. Ikeda O., Egami H., Ishiko T., et al. Expression of proteinase-activated receptor-2 in human pancreatic cancer: a possible relation to cancer invasion and induction of fibrosis. Int J Oncol. 2003 ; 22: 295-300.
76. Hasebe T., Sasaki S., Imoto S., Ochiai A. Highly proliferative fibroblasts forming fibrotic focus govern metastasis of invasive ductal carcinoma if the breast. Mod Pathol. 2001 ; 14: 325-337.
77. VanSaun MN, Matrisian LM Matrix metalloproteinases and cellular motility in development and disease. Birth Defects Res C Embryo Today. 2006 ; 78: 69-79.
78. Radisky D., Hagios C., Bissell MJ Tumors are unique organs defined by abnormal signaling and context. Sem Cancer Biol. 2001 ; 11: 97-95.
79. Kassis J., Lauffenburger DA, Turner T., Wells A. Tumor invasion as dysregulated cell motility. Semin Cancer Biol. 2001 ; 11: 105-117.
80. Damjanovich L., Albelda SM, Mette SA, Buck CA Distribution of integrin cell adhesion receptors in normal and malignant lung tissue. Am J Respir Cell Mol Biol. 1992 ; 6: 197-206.
81. Omelchenko T., Fetisova E., Ivanova O., et al. Contact interactions between epitheliocytes and fibroblasts: formation of heterotypic cadherin-containing adhesion sites is accompanied by local cytoskeletal reorganization. Proc Nat Acad Sci U S A. 2001 ; 98: 8632-8637.