MT1-MMP cooperates with Kras G12D to promote pancreatic fibrosis through increased TGF-β signaling

Molecular Cancer Research

Volumn 9, Issue 10, 2011, Pages 1294-1304

  Krantz, Seth B ^a   Shields, Mario A ^a   Dangi Garimella, Surabhi ^a   Cheon, Eric C ^a   Barron, Morgan R ^a   Hwang, Rosa F ^c   Rao, M Sambasiva ^a   Grippo, Paul J ^a   Bentrem, David J ^a,b   Munshi, Hidayatullah G ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; K RAS PROTEIN; MATRIX METALLOPROTEINASE 14; MUCIN; PROTEIN KRAS G12D; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE EXPRESSION; GENE MUTATION; IN VITRO STUDY; MOUSE; MYOFIBROBLAST; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREATIC DUCT ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STELLATE CELL; STROMA CELL; TUMOR MICROENVIRONMENT;

ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; FIBROSIS; HUMANS; IMMUNOHISTOCHEMISTRY; MATRIX METALLOPROTEINASE 14; MICE; MICE, TRANSGENIC; PANCREAS; PANCREATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS P21(RAS); RAS PROTEINS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION;

MUS;

EID: 80054687133     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0023     Document Type: Article

References (50)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Chu GC, Kimmelman AC, Hezel AF, Depinho RA. Stromal biology of pancreatic cancer. J Cell Biochem 2007;101:887-907. (Pubitemid 47040870)
3. Keleg S, Büchler P, Ludwig R, Büchler MW, Friess H. Invasion and metastasis in pancreatic cancer. Mol Cancer 2003;2:14.
4. Hidalgo M. Pancreatic cancer. N Engl J Med 2010;362:1605-17.
5. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009;324:1457-61.
6. Radisky DC, Kenny PA, Bissell MJ. Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem 2007;101:830-9. (Pubitemid 47040865)
7. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005;121:335-48. (Pubitemid 40692295)
8. Yen TWf, Aardal NP, Bronner MP, Thorning DR, Savard CE, Lee SP, et al. Myofibroblasts are responsible for the desmoplastic reaction surrounding human pancreatic carcinomas. Surgery 2002;131:129-34.
9. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 2008;68:918-26. (Pubitemid 351206771)
10. Vonlaufen A, Phillips PA, Xu Z, Goldstein D, Pirola RC, Wilson JS, et al. Pancreatic stellate cells and pancreatic cancer cells: an unholy alliance. Cancer Res 2008;68:7707-10.
11. Ottaviano AJ, Sun L, Ananthanarayanan V, Munshi HG. Extracellular matrix-mediated membrane-type 1 matrix metalloproteinase expression in pancreatic ductal cells is regulated by transforming growth factor-beta1. Cancer Res 2006;66:7032-40. (Pubitemid 44197679)
12. Friess H, Yamanaka Y, Büchler M, Ebert M, Beger HG, Gold LI, et al. Enhanced expression of transforming growth factor beta isoforms in pancreatic cancer correlates with decreased survival. Gastroenterology 1993;105:1846-56. (Pubitemid 24002804)
13. Apte MV, Park S, Phillips PA, Santucci N, Goldstein D, Kumar RK, et al. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas 2004;29:179-87. (Pubitemid 39304974)
14. Aoyagi Y, Oda T, Kinoshita T, Nakahashi C, Hasebe T, Ohkohchi N, et al. Overexpression of TGF-beta by infiltrated granulocytes correlates with the expression of collagen mRNA in pancreatic cancer. Br J Cancer 2004;91:1316-26. (Pubitemid 39424793)
15. Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E, et al. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 1994;370:61-5. (Pubitemid 24216953)
16. Okada A, Bellocq JP, Rouyer N, Chenard MP, Rio MC, Chambon P, et al. Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas. Proc Natl Acad Sci USA 1995;92:2730-4.
17. Iacobuzio-Donahue CA, Ryu B, Hruban RH, Kern SE. Exploring the host desmoplastic response to pancreatic carcinoma: gene expression of stromal and neoplastic cells at the site of primary invasion. Am J Pathol 2002;160:91-9. (Pubitemid 34052270)
18. Bramhall SR, Neoptolemos JP, Stamp GW, Lemoine NR. Imbalance of expression of matrix metalloproteinases (MMPs) and tissue inhibitors of the matrix metalloproteinases (TIMPs) in human pancreatic carcinoma. J Pathol 1997;182:347-55. (Pubitemid 27285789)
19. Imamura T, Ohshio G, Mise M, Harada T, Suwa H, Okada N, et al. Expression of membrane-type matrix metalloproteinase-1 in human pancreatic adenocarcinomas. J CancerRes ClinOncol 1998;124:65-72. (Pubitemid 28161282)
20. Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY, Rauser RW, et al. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci U S A 2000;97:4052-7. (Pubitemid 30226085)
21. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M, Kuznetsov SA, et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999;99:81-92. (Pubitemid 29468632)
22. Hotary KB, Allen ED, Brooks PC, Datta NS, Long MW, Weiss SJ. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 2003;114:33-45. (Pubitemid 36859839)
23. Ha HY, Moon HB, Nam MS, Lee JW, Ryoo ZY, Lee TH, et al. Overexpression of membrane-type matrix metalloproteinase-1 gene induces mammary gland abnormalities and adenocarcinoma in transgenic mice. Cancer Res 2001;61:984-90.
24. Dangi-Garimella S, Redig AJ, Shields MA, Siddiqui MA, Munshi HG. Rho-ROCK-myosin signaling mediates membrane type 1 matrix metalloproteinase- induced cellular aggregation of keratinocytes. J Biol Chem 2010;285:28363-72.
25. Soulié P, Carrozzino F, Pepper MS, Strongin AY, Poupon M-F, Montesano R. Membrane-type-1 matrix metalloproteinase confers tumorigenicity on nonmalignant epithelial cells. Oncogene 2005;24:1689-97. (Pubitemid 40467524)
26. Grippo PJ, Nowlin PS, Demeure MJ, Longnecker DS, Sandgren EP. Preinvasive pancreatic neoplasia of ductal phenotype induced by acinar cell targeting of mutant Kras in transgenic mice. Cancer Res 2003;63:2016-9. (Pubitemid 36538599)
27. Guerra C, Schuhmacher AJ, Cañamero M, Grippo PJ, Verdaguer L, Pérez-Gallego L, et al. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 2007;11:291-302. (Pubitemid 46349841)
28. Strouch MJ, Cheon EC, Salabat MR, Krantz SB, Gounaris E, Melstrom LG, et al. Crosstalk between mast cells and pancreatic cancer cells contributes to pancreatic tumor progression. Clin Cancer Res 2010; 16:2257-65.
29. Diamond ME, Sun L, Ottaviano AJ, Joseph MJ, Munshi HG. Differential growth factor regulation of N-cadherin expression and motility in normal and malignant oral epithelium. J Cell Sci 2008;121:2197-207.
30. Klimstra DS, Longnecker DS. K-ras mutations in pancreatic ductal proliferative lesions. Am J Pathol 1994;145:1547-50. (Pubitemid 24378508)
31. Almoguera C, Shibata D, Forrester K, Martin J, Arnheim N, Perucho M. Most human carcinomas of the exocrine pancreas contain mutant c-K-ras genes. Cell 1988;53:549-54.
32. Bardeesy N, Cheng K-H, Berger JH, Chu GC, Pahler J, Olson P, et al. Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer. Genes Dev 2006;20:3130-46. (Pubitemid 44790628)
33. Izeradjene K, Combs C, Best M, Gopinathan A, Wagner A, Grady WM, et al. Kras(G12D) and Smad4/Dpc4 haploinsufficiency cooperate to induce mucinous cystic neoplasms and invasive adenocarcinoma of the pancreas. Cancer Cell 2007;11:229-43. (Pubitemid 46349845)
34. Hruban RH, Takaori K, Klimstra DS, Adsay NV, Albores-Saavedra J, Biankin AV, et al. An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms. Am J Surg Pathol 2004;28:977-87. (Pubitemid 38971421)
35. Kojima K, Vickers SM, Adsay NV, Jhala NC, Kim H-G, Schoeb TR, et al. Inactivation of Smad4 accelerates Kras(G12D)-mediated pancreatic neoplasia. Cancer Res 2007;67:8121-30. (Pubitemid 47395147)
36. Rustgi AK. The molecular pathogenesis of pancreatic cancer: clarifying a complex circuitry. Genes Dev 2006;20:3049-53. (Pubitemid 44790620)
37. Hezel AF, Kimmelman AC, Stanger BZ, Bardeesy N, Depinho RA. Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev 2006;20:1218-49. (Pubitemid 43727584)
38. Ijichi H, Chytil A, Gorska AE, Aakre ME, Fujitani Y, Fujitani S, et al. Aggressive pancreatic ductal adenocarcinoma in mice caused by pancreas-specific blockade of transforming growth factor-beta signaling in cooperation with active Kras expression. Genes Dev 2006;20:3147-60. (Pubitemid 44790629)
39. Hruban RH, Adsay NV, Albores-Saavedra J, Anver MR, Biankin AV, Boivin GP, et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res 2006;66:95-106. (Pubitemid 43166014)
40. Gidekel Friedlander SY, Chu GC, Snyder EL, Girnius N, Dibelius G, Crowley D, et al. Context-dependent transformation of adult pancreatic cells by oncogenic K-Ras. Cancer Cell 2009;16:379-89.
41. De La O J-P, Emerson LL, Goodman JL, Froebe SC, Illum BE, Curtis AB, et al. Notch and Kras reprogram pancreatic acinar cells to ductal intraepithelial neoplasia. Proc Natl Acad Sci USA 2008;105:18907-12.
42. Habbe N, Shi G, Meguid RA, Fendrich V, Esni F, Chen H, et al. Spontaneous induction of murine pancreatic intraepithelial neoplasia (mPanIN) by acinar cell targeting of oncogenic Kras in adult mice. Proc Natl Acad Sci USA 2008;105:18913-8.
43. Deshmukh HS, McLachlan A, Atkinson JJ, Hardie WD, Korfhagen TR, Dietsch M, et al. Matrix metalloproteinase-14 mediates a phenotypic shift in the airways to increase mucin production. Am J Respir Crit Care 2009;180:834-45.
44. Thathiah A, Carson DD. MT1-MMP mediates MUC1 shedding independent of TACE/ADAM17. Biochem J 2004;382:363-73. (Pubitemid 39141600)
45. Spinale FG, Escobar GP, Mukherjee R, Zavadzkas JA, Saunders SM, Jeffords LB, et al. Cardiac-restricted overexpression of membrane type-1 matrix metalloproteinase in mice: effects on myocardial remodeling with aging. Circ Heart Fail 2009;2:351-60.
46. Karsdal MA, Larsen L, Engsig MT, Lou H, Ferreras M, Lochter A, et al. Matrix metalloproteinase-dependent activation of latent transforming growth factor-beta controls the conversion of osteoblasts into osteocytes by blockingosteoblast apoptosis. JBiolChem2002;277:44061-7. (Pubitemid 36157833)
47. Freudenberg J, Chen W. Induction of Smad1 by MT1-MMP contributes to tumor growth. Int J Cancer 2007;121:966-77. (Pubitemid 47101631)
48. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010;141:52-67.
49. Tatti O, Vehviläinen P, Lehti K, Keski-Oja J. MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp Cell Res 2008;314:2501-14.
50. Böttinger EP, Factor VM, Tsang ML, Weatherbee JA, Kopp JB, Qian SW, et al. The recombinant proregion of transforming growth factor beta1 (latency-associated peptide) inhibits active transforming growth factor beta1 in transgenic mice. Proc Natl Acad Sci USA 1996;93:5877-82.