Increased invasiveness of MMP-9-deficient tumors in two mouse models of neuroendocrine tumorigenesis

Oncogene

Volumn 32, Issue 4, 2013, Pages 502-513

  Shchors, K ^a,b   Nozawa, H ^b   Xu, J ^b   Rostker, F ^b   Swigart Brown, L ^b   Evan, G ^b   Hanahan, D ^a,b  

^a EPFL   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cathepsin; interleukin 1 ; invasion; metalloproteinase; Myc; tumor

Indexed keywords

CATHEPSIN B; CD11B ANTIGEN; GELATINASE B; INTERLEUKIN 1BETA;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INVASION; CARCINOGENESIS; CELL HOMING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DELETION; GENE EXPRESSION; GENOTYPE; HISTOPATHOLOGY; INFLAMMATION; INFLAMMATORY CELL; LEUKOCYTE; MOUSE; NEUROENDOCRINE TUMOR; NONHUMAN; ONCOGENE MYC; PANCREAS ISLET CELL; PANCREAS ISLET CELL TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD11B; BCL-X PROTEIN; CATHEPSIN B; CELL TRANSFORMATION, NEOPLASTIC; CYSTEINE; DISEASE MODELS, ANIMAL; GTPASE-ACTIVATING PROTEINS; INFLAMMATION; INTERLEUKIN-1BETA; LEUKOCYTES; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASE INHIBITORS; MICE; MICE, INBRED C57BL; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC;

MUS;

EID: 84873057030     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.60     Document Type: Article

References (71)

1. Moore MJ, Hamm J, Dancey J, Eisenberg PD, Dagenais M, Fields A et al. Comparison of gemcitabine versus the matrix metalloproteinase inhibitor BAY 12-9566 in patients with advanced or metastatic adenocarcinoma of the pancreas: A phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 2003; 21: 3296-3302.
2. Levin VA, Phuphanich S, Yung WK, Forsyth PA, Maestro RD, Perry JR et al. Randomized, double-blind, placebo-controlled trial of marimastat in glioblastoma multiforme patients following surgery and irradiation. J Neurooncol 2006; 78: 295-302.
3. Bissett D, O'Byrne KJ, von Pawel J, Gatzemeier U, Price A, Nicolson M et al. Phase III study of matrix metalloproteinase inhibitor prinomastat in non-small-cell lung cancer. J Clin Oncol 2005; 23: 842-849.
4. Zucker S, Cao J, Chen WT. Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene 2000; 19: 6642-6650.
5. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: Trials and tribulations. Science 2002; 295: 2387-2392.
6. Pavlaki M, Zucker S. Matrix metalloproteinase inhibitors (MMPIs): The beginning of phase I or the termination of phase III clinical trials. Cancer Metastasis Rev 2003; 22: 177-203.
7. Pellikainen JM, Ropponen KM, Kataja VV, Kellokoski JK, Eskelinen MJ, Kosma VM. Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis. Clin Cancer Res 2004; 10: 7621-7628.
8. Sillanpaa S, Anttila M, Voutilainen K, Ropponen K, Turpeenniemi-Hujanen T, Puistola U et al. Prognostic significance of matrix metalloproteinase-9 (MMP-9) in epithelial ovarian cancer. Gynecol Oncol 2007; 104: 296-303.
9. Kamat AA, Fletcher M, Gruman LM, Mueller P, Lopez A, Landen Jr CN et al. The clinical relevance of stromal matrix metalloproteinase expression in ovarian cancer. Clin Cancer Res 2006; 12: 1707-1714.
10. Melchiori A, Albini A, Ray JM, Stetler-Stevenson WG. Inhibition of tumor cell invasion by a highly conserved peptide sequence from the matrix metalloproteinase enzyme prosegment. Cancer Res 1992; 52: 2353-2356.
11. Himelstein BP, Canete-Soler R, Bernhard EJ, Dilks DW, Muschel RJ. Metalloproteinases in tumor progression: The contribution of MMP-9. Invasion Metastasis 1994; 14: 246-258.
12. Chintala SK, Tonn JC, Rao JS. Matrix metalloproteinases and their biological function in human gliomas. Int J Dev Neurosci 1999; 17: 495-502.
13. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000; 2: 737-744.
14. Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci USA 2006; 103: 12493-12498.
15. Giraudo E, Inoue M, Hanahan D. An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest 2004; 114: 623-633.
16. Pahler JC, Tazzyman S, Erez N, Chen YY, Murdoch C, Nozawa H et al. Plasticity in tumor-promoting inflammation: Impairment of macrophage recruitment evokes a compensatory neutrophil response. Neoplasia 2008; 10: 329-340.
17. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008; 13: 206-220.
18. Jodele S, Chantrain CF, Blavier L, Lutzko C, Crooks GM, Shimada H et al. The contribution of bone marrow-derived cells to the tumor vasculature in neuroblastoma is matrix metalloproteinase-9 dependent. Cancer Res 2005; 65: 3200-3208.
19. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004; 6: 409-421.
20. Pelengaris S, Khan M, Evan GI. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 2002; 109: 321-334.
21. Shchors K, Shchors E, Rostker F, Lawlor ER, Brown-Swigart L, Evan GI. The Mycdependent angiogenic switch in tumors is mediated by interleukin 1beta. Genes Dev 2006; 20: 2527-2538.
22. Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 1989; 339: 58-61.
23. Inoue M, Hager JH, Ferrara N, Gerber HP, Hanahan D. VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. Cancer Cell 2002; 1: 193-202.
24. Lawlor ER, Soucek L, Brown-Swigart L, Shchors K, Bialucha CU, Evan GI. Reversible kinetic analysis of Myc targets in vivo provides novel insights into Myc-mediated tumorigenesis. Cancer Res 2006; 66: 4591-4601.
25. Apte RN, Krelin Y, Song X, Dotan S, Recih E, Elkabets M et al. Effects of micro-environment- and malignant cell-derived interleukin-1 in carcinogenesis, tumour invasiveness and tumour-host interactions. Eur J Cancer 2006; 42: 751-759.
26. Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev 2010; 24: 241-255.
27. Joyce JA, Baruch A, Chehade K, Meyer-Morse N, Giraudo E, Tsai FY et al. Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 2004; 5: 443-453.
28. Stetler-Stevenson WG, Aznavoorian S, Liotta LA. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol 1993; 9: 541-573.
29. van Kempen LC, de Visser KE, Coussens LM. Inflammation, proteases and cancer. Eur J Cancer 2006; 42: 728-734.
30. Campbell EJ, Cury JD, Shapiro SD, Goldberg GI, Welgus HG. Neutral proteinases of human mononuclear phagocytes. Cellular differentiation markedly alters cell phenotype for serine proteinases, metalloproteinases, and tissue inhibitor of metalloproteinases. J Immunol 1991; 146: 1286-1293.
31. Ahn GO, Brown JM. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell 2008; 13: 193-205.
32. Dalet-Fumeron V, Guinec N, Pagano M. In vitro activation of pro-cathepsin B by three serine proteinases: Leucocyte elastase, cathepsin G, and the urokinase-type plasminogen activator. FEBS Lett 1993; 332: 251-254.
33. Geraghty P, Rogan MP, Greene CM, Boxio RM, Poiriert T, O'Mahony M et al. Neutrophil elastase up-regulates cathepsin B and matrix metalloprotease-2 expression. J Immunol 2007; 178: 5871-5878.
34. Kruger A, Soeltl R, Sopov I, Kopitz C, Arlt M, Magdolen V et al. Hydroxamate-type matrix metalloproteinase inhibitor batimastat promotes liver metastasis. Cancer Res 2001; 61: 1272-1275.
35. Overall CM, Kleifeld O. Tumour microenvironment-opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 2006; 6: 227-239.
36. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrowderived cells contributes to skin carcinogenesis. Cell 2000; 103: 481-490.
37. Littlepage LE, Sternlicht MD, Rougier N, Phillips J, Gallo E, Yu Y et al. Matrix metalloproteinases contribute distinct roles in neuroendocrine prostate carcinogenesis, metastasis, and angiogenesis progression. Cancer Res 2010; 70: 2224-2234.
38. Himelstein BP, Lee EJ, Sato H, Seiki M, Muschel RJ. Transcriptional activation of the matrix metalloproteinase-9 gene in an H-ras and v-myc transformed rat embryo cell line. Oncogene 1997; 14: 1995-1998.
39. Chesler L, Goldenberg DD, Seales IT, Satchi-Fainaro R, Grimmer M, Collins R et al. Malignant progression and blockade of angiogenesis in a murine transgenic model of neuroblastoma. Cancer Res 2007; 67: 9435-9442.
40. Sekhon HS, London CA, Sekhon M, Iversen PL, Devi GR. c-MYC antisense phosphosphorodiamidate morpholino oligomer inhibits lung metastasis in a murine tumor model. Lung Cancer 2008; 60: 347-354.
41. Elaraj DM, Weinreich DM, Varghese S, Puhlmann M, Hewitt SM, Carroll NM et al. The role of interleukin 1 in growth and metastasis of human cancer xenografts. Clin Cancer Res 2006; 12: 1088-1096.
42. Voronov E, Shouval DS, Krelin Y, Cagnano E, Benharroch D, Iwakura Y et al. IL-1 is required for tumor invasiveness and angiogenesis. Proc Natl Acad Sci USA 2003; 100: 2645-2650.
43. Lee HT, Lee JG, Na M, Kay EP. FGF-2 induced by interleukin-1 beta through the action of phosphatidylinositol 3-kinase mediates endothelial mesenchymal transformation in corneal endothelial cells. J Biol Chem 2004; 279: 32325-32332.
44. Lockwood CJ, Matta P, Krikun G, Koopman LA, Masch R, Toti P et al. Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor-alpha and interleukin-1beta in first trimester human decidual cells: Implications for preeclampsia. Am J Pathol 2006; 168: 445-452.
45. Raymond L, Eck S, Mollmark J, Hays E, Tomek I, Kantor S et al. Interleukin-1 beta induction of matrix metalloproteinase-1 transcription in chondrocytes requires ERK-dependent activation of CCAAT enhancer-binding protein-beta. J Cell Physiol 2006; 207: 683-688.
46. Mountain DJ, Singh M, Menon B, Singh K. Interleukin-1beta increases expression and activity of matrix metalloproteinase-2 in cardiac microvascular endothelial cells: role of PKCalpha/beta1 and MAPKs. Am J Physiol Cell Physiol 2007; 292: C867-C875.
47. Deryugina EI, Quigley JP. Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: Contrasting, overlapping and compensatory functions. Biochim Biophys Acta 2010; 1803: 103-120.
48. Tazawa H, Okada F, Kobayashi T, Tada M, Mori Y, Une Y et al. Infiltration of neutrophils is required for acquisition of metastatic phenotype of benign murine fibrosarcoma cells: Implication of inflammation-associated carcinogenesis and tumor progression. Am J Pathol 2003; 163: 2221-2232.
49. Shojaei F, Wu X, Malik AK, Zhong C, Baldwin ME, Schanz S et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol 2007; 25: 911-920.
50. Yang L, Huang J, Ren X, Gorska AE, Chytil A, Aakre M et al. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 2008; 13: 23-35.
51. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009; 15: 232-239.
52. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15: 220-231.
53. Balbin M, Fueyo A, Tester AM, Pendas AM, Pitiot AS, Astudillo A et al. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet 2003; 35: 252-257.
54. McCawley LJ, Wright J, LaFleur BJ, Crawford HC, Matrisian LM. Keratinocyte expression of MMP3 enhances differentiation and prevents tumor establishment. Am J Pathol 2008; 173: 1528-1539.
55. Turk V, Turk B, Guncar G, Turk D, Kos J. Lysosomal cathepsins: Structure, role in antigen processing and presentation, and cancer. Adv Enzyme Regul 2002; 42: 285-303.
56. Turk V, Turk B, Turk D. Lysosomal cysteine proteases: facts and opportunities. EMBO J 2001; 20: 4629-4633.
57. Gocheva V, Joyce JA. Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 2007; 6: 60-64.
58. Grimm J, Kirsch DG, Windsor SD, Kim CF, Santiago PM, Ntziachristos V et al. Use of gene expression profiling to direct in vivo molecular imaging of lung cancer. Proc Natl Acad Sci USA 2005; 102: 14404-14409.
59. Gocheva V, Zeng W, Ke D, Klimstra D, Reinheckel T, Peters C et al. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev 2006; 20: 543-556.
60. Lah TT, Buck MR, Honn KV, Crissman JD, Rao NC, Liotta LA et al. Degradation of laminin by human tumor cathepsin B. Clin Exp Metastasis 1989; 7: 461-468.
61. Buck MR, Karustis DG, Day NA, Honn KV, Sloane BF. Degradation of extracellularmatrix proteins by human cathepsin B from normal and tumour tissues. Biochem J 1992; 282 (Part 1):273-278.
62. Creemers LB, Hoeben KA, Jansen DC, Buttle DJ, Beertsen W, Everts V. Participation of intracellular cysteine proteinases, in particular cathepsin B, in degradation of collagen in periosteal tissue explants. Matrix Biol 1998; 16: 575-584.
63. Levicar N, Nuttall RK, Lah TT. Proteases in brain tumour progression. Acta Neurochir 2003; 145: 825-838.
64. Czyzewska J, Guzinska-Ustymowicz K, Kemona A, Bandurski R. The expression of matrix metalloproteinase 9 and cathepsin B in gastric carcinoma is associated with lymph node metastasis, but not with postoperative survival. Folia Histochem Cytobiol 2008; 46: 57-64.
65. Kirschke H, Clausen T, Gohring B, Gunther D, Heucke E, Laube F et al. Concentrations of lysosomal cysteine proteases are decreased in renal cell carcinoma compared with normal kidney. J Cancer Res Clin Oncol 1997; 123: 402-406.
66. Batist G, Patenaude F, Champagne P, Croteau D, Levinton C, Hariton C et al. Neovastat (AE-941) in refractory renal cell carcinoma patients: report of a phase II trial with two dose levels. Ann Oncol 2002; 13: 1259-1263.
67. Lopez T, Hanahan D. Elevated levels of IGF-1 receptor convey invasive and metastatic capability in a mouse model of pancreatic islet tumorigenesis. Cancer Cell 2002; 1: 339-353.
68. Chun MG, Mao JH, Chiu CW, Balmain A, Hanahan D. Polymorphic genetic control of tumor invasion in a mouse model of pancreatic neuroendocrine carcinogenesis. Proc Natl Acad Sci USA 2010; 107: 17268-17273.
69. Sounni NE, Dehne K, van Kempen L, Egeblad M, Affara NI, Cuevas I et al. Stromal regulation of vessel stability by MMP14 and TGFbeta. Dis Model Mech 2010; 3: 317-332.
70. Herron GS, Banda MJ, Clark EJ, Gavrilovic J, Werb Z. Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J Biol Chem 1986; 261: 2814-2818.
71. Herron GS, Werb Z, Dwyer K, Banda MJ. Secretion of metalloproteinases by stimulated capillary endothelial cells. I. Production of procollagenase and prostromelysin exceeds expression of proteolytic activity. J Biol Chem 1986; 261: 2810-2813.