Interleukin-like epithelial-to-mesenchymal transition inducer activity is controlled by proteolytic processing and plasminogen-urokinase plasminogen activator receptor system-regulated secretion during breast cancer progression

Breast Cancer Research

Volumn 16, Issue 5, 2014, Pages

  Csiszar, Agnes ^a,f   Kutay, Betül ^a   Wirth, Silvia ^a,e   Schmidt, Ulrike ^a   Macho Maschler, Sabine ^b   Schreiber, Martin ^c   Alacakaptan, Memetcan ^a   Vogel, Georg F ^d   Aumayr, Karin ^a   Huber, Lukas A ^d   Beug, Hartmut ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e EPFL   (Switzerland)

^f MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

APROTININ; CATHEPSIN B; CYTOKINE; FIBRONECTIN; INTERLEUKIN LIKE EPITHELIAL TO MESENCHYMAL TRANSITION INDUCER; LEUKOCYTE ELASTASE; PLASMA KALLIKREIN; PLASMIN; PLASMINOGEN; PROTEINASE; PROTEINASE INHIBITOR; SERINE PROTEINASE; SHORT HAIRPIN RNA; THROMBIN; UNCLASSIFIED DRUG; UROKINASE RECEPTOR; FAM3C PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER SURVIVAL; CELLULAR DISTRIBUTION; CYTOKINE RELEASE; FEMALE; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; METASTASIS FREE SURVIVAL; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; DISEASE COURSE; EPITHELIAL MESENCHYMAL TRANSITION; KAPLAN MEIER METHOD; LUNG TUMOR; METABOLISM; MORTALITY; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TRANSPORT; SECONDARY; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CYTOKINES; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FIBRINOLYSIN; HUMANS; KAPLAN-MEIER ESTIMATE; LEUKOCYTE ELASTASE; LUNG NEOPLASMS; MICE, NUDE; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; PLASMA KALLIKREIN; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR;

EID: 84908501082     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-014-0433-7     Document Type: Article

References (55)

1. Gupta GP, Massagué J. Cancer metastasis: building a framework. Cell 2006, 127:679-695. 10.1016/j.cell.2006.11.001, 17110329.
2. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011, 331:1559-1564. 10.1126/science.1203543, 21436443.
3. Tlsty TD, Coussens LM. Tumor stroma and regulation of cancer development. Annu Rev Pathol 2006, 1:119-150. 10.1146/annurev.pathol.1.110304.100224, 18039110.
4. Sheu BC, Chang WC, Cheng CY, Lin HH, Chang DY, Huang SC. Cytokine regulation networks in the cancer microenvironment. Front Biosci 2008, 13:6255-6268. 10.2741/3152, 18508658.
5. Jechlinger M, Sommer A, Moriggl R, Seither P, Kraut N, Capodiecci P, Donovan M, Cordon-Cardo C, Beug H, Grünert S. Autocrine PDGFR signaling promotes mammary cancer metastasis. J Clin Invest 2006, 116:1561-1570. 10.1172/JCI24652, 16741576.
6. Oft M, Heider KH, Beug H. TGFβ signaling is necessary for carcinoma cell invasiveness and metastasis. Curr Biol 1998, 8:1243-1252. 10.1016/S0960-9822(07)00533-7, 9822576.
7. Waerner T, Alacakaptan M, Tamir I, Oberauer R, Gal A, Brabletz T, Schreiber M, Jechlinger M, Beug H. ILEI: a cytokine essential for EMT, tumor formation, and late events in metastasis in epithelial cells. Cancer Cell 2006, 10:227-239. 10.1016/j.ccr.2006.07.020, 16959614.
8. Jechlinger M, Grunert S, Tamir IH, Janda E, Lüdemann S, Waerner T, Seither P, Weith A, Beug H, Kraut N. Expression profiling of epithelial plasticity in tumor progression. Oncogene 2003, 22:7155-7169. 10.1038/sj.onc.1206887, 14562044.
9. Hussey GS, Chaudhury A, Dawson AE, Lindner DJ, Knudsen CR, Wilce MC, Merrick WC, Howe PH. Identification of an mRNP complex regulating tumorigenesis at the translational elongation step. Mol Cell 2011, 41:419-431. 10.1016/j.molcel.2011.02.003, 21329880.
10. Chaudhury A, Hussey GS, Ray PS, Jin G, Fox PL, Howe PH. TGF-β-mediated phosphorylation of hnRNP E1 induces EMT via transcript-selective translational induction of Dab2 and ILEI. Nat Cell Biol 2010, 12:286-293. 20154680.
11. Lahsnig C, Mikula M, Petz M, Zulehner G, Schneller D, van Zijl F, Huber H, Csiszar A, Beug H, Mikulits W. ILEI requires oncogenic Ras for the epithelial to mesenchymal transition of hepatocytes and liver carcinoma progression. Oncogene 2009, 28:638-650. 10.1038/onc.2008.418, 19015638.
12. Zhu Y, Xu G, Patel A, McLaughlin MM, Silverman C, Knecht K, Sweitzer S, Li X, McDonnell P, Mirabile R, Zimmerman D, Boyce R, Tierney LA, Hu E, Livi GP, Wolf B, Abdel-Mequid SS, Rose GD, Aurora R, Hensley P, Briggs M, Young PR. Cloning, expression, and initial characterization of a novel cytokine-like gene family. Genomics 2002, 80:144-150. 10.1006/geno.2002.6816, 12160727.
13. Johansson P, Bernström J, Gorman T, Oster L, Bäckström S, Schweikart F, Xu B, Xue Y, Schiavone LH. FAM3B PANDER and FAM3C ILEI represent a distinct class of signaling molecules with a non-cytokine-like fold. Structure 2013, 21:306-313. 10.1016/j.str.2012.12.009, 23333428.
14. Mason SD, Joyce JA. Proteolytic networks in cancer. Trends Cell Biol 2011, 21:228-237. 10.1016/j.tcb.2010.12.002, 21232958.
15. Lyons RM, Gentry LE, Purchio AF, Moses HL. Mechanism of activation of latent recombinant transforming growth factor β1 by plasmin. J Cell Biol 1990, 110:1361-1367. 10.1083/jcb.110.4.1361, 2139036.
16. Bergsten E, Uutela M, Li X, Pietras K, Ostman A, Heldin CH, Alitalo K, Eriksson U. PDGF-D is a specific, protease-activated ligand for the PDGF β-receptor. Nat Cell Biol 2001, 3:512-516. 10.1038/35074588, 11331881.
17. Li X, Pontén A, Aase K, Karlsson L, Abramsson A, Uutela M, Bäckström G, Hellström M, Boström H, Li H, Soriano P, Betsholtz C, Heldin CH, Alitalo K, Ostman A, Eriksson U. PDGF-C is a new protease-activated ligand for the PDGF α-receptor. Nat Cell Biol 2000, 2:302-309. 10.1038/35010579, 10806482.
18. Ustach CV, Kim HR. Platelet-derived growth factor D is activated by urokinase plasminogen activator in prostate carcinoma cells. Mol Cell Biol 2005, 25:6279-6288. 10.1128/MCB.25.14.6279-6288.2005, 15988036.
19. Smith HW, Marshall CJ. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 2010, 11:23-36. 10.1038/nrm2821, 20027185.
20. Andreasen PA, Egelund R, Petersen HH. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell Mol Life Sci 2000, 57:25-40. 10.1007/s000180050497, 10949579.
21. Lund LR, Green KA, Stoop AA, Ploug M, Almholt K, Lilla J, Nielsen BS, Christensen IJ, Craik CS, Werb Z, Danø K, Rømer J. Plasminogen activation independent of uPA and tPA maintains wound healing in gene-deficient mice. EMBO J 2006, 25:2686-2697. 10.1038/sj.emboj.7601173, 16763560.
22. Sotiropoulou G, Pampalakis G, Diamandis EP. Functional roles of human kallikrein-related peptidases. J Biol Chem 2009, 284:32989-32994. 10.1074/jbc.R109.027946, 19819870.
23. Binder BR, Mihaly J. The plasminogen activator inhibitor " paradox" in cancer. Immunol Lett 2008, 118:116-124. 10.1016/j.imlet.2008.03.017, 18495253.
24. D'Alessio S, Blasi F. The urokinase receptor as an entertainer of signal transduction. Front Biosci 2009, 14:4575-4587. 10.2741/3550.
25. Maas C, Renné T. Regulatory mechanisms of the plasma contact system. Thromb Res 2012, 129:S73-S76. 10.1016/j.thromres.2012.02.039, 22398015.
26. Moroy G, Alix AJ, Sapi J, Hornebeck W, Bourguet E. Neutrophil elastase as a target in lung cancer. Anticancer Agents Med Chem 2012, 12:565-579. 10.2174/187152012800617696, 22263788.
27. Ulisse S, Baldini E, Sorrenti S, D'Armiento M. The urokinase plasminogen activator system: a target for anti-cancer therapy. Curr Cancer Drug Targets 2009, 9:32-71. 10.2174/156800909787314002, 19200050.
28. Oft M, Peli J, Rudaz C, Schwarz H, Beug H, Reichmann E. TGF-β1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev 1996, 10:2462-2477. 10.1101/gad.10.19.2462, 8843198.
29. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J, Beug H, Grünert S. Ras and TGFβ cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 2002, 156:299-313. 10.1083/jcb.200109037, 11790801.
30. Janda E, Litos G, Grünert S, Downward J, Beug H. Oncogenic Ras/Her-2 mediate hyperproliferation of polarized epithelial cells in 3D cultures and rapid tumor growth via the PI3K pathway. Oncogene 2002, 21:5148-5159. 10.1038/sj.onc.1205661, 12140765.
31. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939. 10.1016/j.cell.2004.06.006, 15210113.
32. Dandachi N, Hauser-Kronberger C, Moré E, Wiesener B, Hacker GW, Dietze O, Wirl G. Co-expression of tenascin-C and vimentin in human breast cancer cells indicates phenotypic transdifferentiation during tumour progression: correlation with histopathological parameters, hormone receptors, and oncoproteins. J Pathol 2001, 193:181-189. 10.1002/1096-9896(2000)9999:9999<::AID-PATH752>3.0.CO;2-V, 11180164.
33. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997, 15:871-875. 10.1038/nbt0997-871, 9306402.
34. Orecchia A, Lacal PM, Schietroma C, Morea V, Zambruno G, Failla CM. Vascular endothelial growth factor receptor-1 is deposited in the extracellular matrix by endothelial cells and is a ligand for the α5β1 integrin. J Cell Sci 2003, 116:3479-3489. 10.1242/jcs.00673, 12865438.
35. qPrimerDepot., http://primerdepot.nci.nih.gov
36. Vinatzer U, Dampier B, Streubel B, Pacher M, Seewald MJ, Stratowa C, Kaserer K, Schreiber M. Expression of HER2 and the coamplified genes GRB7 and MLN64 in human breast cancer: quantitative real-time reverse transcription-PCR as a diagnostic alternative to immunohistochemistry and fluorescence in situ hybridization. Clin Cancer Res 2005, 11:8348-8357. 10.1158/1078-0432.CCR-05-0841, 16322295.
37. Harrington DP, Fleming TR. A class of rank test procedures for censored survival data. Biometrika 1982, 69:553-566. 10.1093/biomet/69.3.553.
38. Akizuki M, Fukutomi T, Takasugi M, Takahashi S, Sato T, Harao M, Mizumoto T, Yamashita J. Prognostic significance of immunoreactive neutrophil elastase in human breast cancer: long-term follow-up results in 313 patients. Neoplasia 2007, 9:260-264. 10.1593/neo.06808, 17401466.
39. Rakic JM, Maillard C, Jost M, Bajou K, Masson V, Devy L, Lambert V, Foidart JM, Noël A. Role of plasminogen activator-plasmin system in tumor angiogenesis. Cell Mol Life Sci 2003, 60:463-473. 10.1007/s000180300039, 12737307.
40. Maschler S, Gebeshuber CA, Wiedemann EM, Alacakaptan M, Schreiber M, Custic I, Beug H. Annexin A1 attenuates EMT and metastatic potential in breast cancer. EMBO Mol Med 2010, 2:401-414. 10.1002/emmm.201000095, 20821804.
41. Xiang X, Zhuang X, Ju S, Zhang S, Jiang H, Mu J, Zhang L, Miller D, Grizzle W, Zhang HG. miR-155 promotes macroscopic tumor formation yet inhibits tumor dissemination from mammary fat pads to the lung by preventing EMT. Oncogene 2011, 30:3440-3453. 10.1038/onc.2011.54, 21460854.
42. Gumireddy K, Li A, Gimotty PA, Klein-Szanto AJ, Showe LC, Katsaros D, Coukos G, Zhang L, Huang Q. KLF17 is a negative regulator of epithelial-mesenchymal transition and metastasis in breast cancer. Nat Cell Biol 2009, 11:1297-1304. 10.1038/ncb1974, 19801974.
43. Kirstein JM, Graham KC, MacKenzie LT, Johnston DE, Martin LJ, Tuck AB, MacDonald IC, Chambers AF. Effect of anti-fibrinolytic therapy on experimental melanoma metastasis. Clin Exp Metastasis 2009, 26:121-131. 10.1007/s10585-008-9221-z, 19082867.
44. Santiago-Tirado FH, Bretscher A. Membrane-trafficking sorting hubs: cooperation between PI4P and small GTPases at the trans-Golgi network. Trends Cell Biol 2011, 21:515-525. 10.1016/j.tcb.2011.05.005, 21764313.
45. Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 1993, 123:35-45. 10.1083/jcb.123.1.35, 8408203.
46. Kotzsch M, Bernt K, Friedrich K, Luther E, Albrecht S, Gatzweiler A, Magdolen V, Baretton G, Zietz C, Luther T. Prognostic relevance of tumour cell-associated uPAR expression in invasive ductal breast carcinoma. Histopathology 2010, 57:461-471. 10.1111/j.1365-2559.2010.03644.x, 20840675.
47. de Bock CE, Wang Y. Clinical significance of urokinase-type plasminogen activator receptor (uPAR) expression in cancer. Med Res Rev 2004, 24:13-39. 10.1002/med.10054, 14595671.
48. Bertos NR, Park M. Breast cancer-one term, many entities?. J Clin Invest 2011, 121:3789-3796. 10.1172/JCI57100, 21965335.
49. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielses TO, Moorman PG, Earp HS, Millikan RC. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 2006, 295:2492-2502. 10.1001/jama.295.21.2492, 16757721.
50. Parise CA, Bauer KR, Brown MM, Caggiano V. Breast cancer subtypes as defined by the estrogen receptor (ER), progesterone receptor (PR), and the human epidermal growth factor receptor 2 (HER2) among women with invasive breast cancer in California, 1999-2004. Breast J 2009, 15:593-602. 10.1111/j.1524-4741.2009.00822.x, 19764994.
51. Avgeris M, Mavridis K, Scorilas A. Kallikrein-related peptidases in prostate, breast, and ovarian cancers: from pathobiology to clinical relevance. Biol Chem 2012, 393:301-317. 10.1515/hsz-2011-0260, 22505514.
52. Wachtfogel YT, Kucich U, James HL, Scott CF, Schapira M, Zimmerman M, Cohen AB, Colman RW. Human plasma kallikrein releases neutrophil elastase during blood coagulation. J Clin Invest 1983, 72:1672-1677. 10.1172/JCI111126, 6556194.
53. Beaufort N, Leduc D, Rousselle JC, Magdolen V, Luther T, Namane A, Chignard M, Pidard D. Proteolytic regulation of the urokinase receptor/CD87 on monocytic cells by neutrophil elastase and cathepsin G. J Immunol 2004, 172:540-549. 10.4049/jimmunol.172.1.540, 14688365.
54. Wu K, Urano T, Ihara H, Takada Y, Fujie M, Shikimori M, Hashimoto K, Takada A. The cleavage and inactivation of plasminogen activator inhibitor type 1 by neutrophil elastase: the evaluation of its physiologic relevance in fibrinolysis. Blood 1995, 86:1056-1061. 7620159.
55. Han B, Nakamura M, Mori I, Nakamura Y, Kakudo K. Urokinase-type plasminogen activator system and breast cancer. Oncol Rep 2005, 14:105-112. 15944776.