Genetic suppression of inflammation blocks the tumor- promoting effects of tgf-βin gastric tissue

Cancer Research

Volumn 74, Issue 9, 2014, Pages 2642-2651

  Ota, Mitsuhiko ^a   Horiguchi, Masahito ^a   Fang, Victoria ^a   Shibahara, Kotaro ^a   Kadota, Kyuichi ^f   Loomis, Cynthia ^a,b,d,e   Cammer, Michael ^b,e   Rifkin, Daniel B ^a,c  

^a Departments of Pathology and Cell Biology and Pharmacology   (United States)

^b Departments of Pathology and Urology   (United States)

^c Departments of Preventive Medicine   (United States)

^d Departments of Dermatology   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f KAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; PHOSPHOPROTEIN; SCATTER FACTOR; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ADAPTIVE IMMUNITY; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CONTROLLED STUDY; EPITHELIUM; GASTROINTESTINAL TUMOR; GENE REPRESSION; INFLAMMATION; LYMPHOCYTE; MOUSE; MOUSE STRAIN; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; STOMACH MUCOSA; STROMA; TISSUE LEVEL; TUMOR GROWTH; TUMOR PROMOTION; WILD TYPE;

ANIMALS; CARCINOGENESIS; CYTOKINES; GASTRIC MUCOSA; GASTRITIS; HEPATOCYTE GROWTH FACTOR; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PARACRINE COMMUNICATION; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84900007855     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3404     Document Type: Article

References (38)

1. de Larco JE, Todaro GJ. Growth factors from murine sarcoma virustransformed cells. Proc Natl Acad Sci U S A 1978;75:4001-5.
2. Bierie B, Moses HL. TGF-beta and cancer. Cytokine Growth Factor Rev 2006;17:29-40.
3. Bachman KE, Park BH. Duel nature of TGF-beta signaling: tumor suppressor vs. tumor promoter. Curr Opin Oncol 2005;17:49-54.
4. Derynck R, Akhurst RJ, Balmain A. TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 2001;29:117-29.
5. Tang B, Vu M, Booker T, Santner SJ, Miller FR, Anver MR, et al. TGFbeta switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. J Clin Invest 2003;112:1116-24.
6. Wakefield LM, Roberts AB. TGF-beta signaling: positive and negative effects on tumorigenesis. Curr Opin Genet Dev 2002;12:22-9.
7. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009;119:1420-8.
8. Burstein B, Libby E, Calderone A, Nattel S. Differential behaviors of atrial versus ventricular fibroblasts: a potential role for platelet-derived growth factor in atrial-ventricular remodeling differences. Circulation 2008;117:1630-41.
9. Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, et al. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A 1993;90:770-4.
10. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, et al. Targeted disruption of the mouse transforming growth factor-b1 gene results in mulitfocal inflammatory disease. Nature 1992;359:693-9.
11. Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N, et al. Abnormal lung development and cleft palate in mice lacking TGF-b3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 1995;11:415-21.
12. Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, et al. Transforming growth factor-b3 is required for secondary palate fusion. Nat Genet 1995;11:409-14.
13. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, et al. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 1997;124:2659-70.
14. Yoshinaga K, Obata H, Jurukovski V, Mazzieri R, Chen Y, Zilberberg L, et al. Perturbation of transforming growth factor (TGF)-beta1 association with latent TGF-beta binding protein yields inflammation and tumors. Proc Natl Acad Sci U S A 2008;105:18758-63.
15. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003;116:217-24.
16. Rifkin DB. Latent transforming growth factor-beta (TGF-beta) binding proteins: orchestrators of TGF-beta availability. J Biol Chem 2005;280:7409-12.
17. Annes JP, Chen Y, Munger JS, Rifkin DB. Integrin alphaVbeta6- mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J Cell Biol 2004;165:723-34.
18. Munger JS, Huang XZ, Kawakatsu H, Griffiths MJD, Dalton SL, Wu JF, et al. The integrin avb6 binds and activates latent TGFb1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1998;96: 319-28.
19. Mazzieri R, Jurukovski V, Obata H, Sung J, Platt A, Annes E, et al. Expression of truncated latent TGF-beta-binding protein modulates TGF-beta signaling. J Cell Sci 2005;118:2177-87.
20. Yang Z, Mu Z, Dabovic B, Jurukovski V, Yu D, Sung J, et al. Absence of integrin-mediated TGFbeta1 activation in vivo recapitulates the phenotype of TGFbeta1-null mice. J Cell Biol 2007;176:787-93.
21. Shibahara K, Ota M, Horiguchi M, Yoshinaga K, Melamed J, Rifkin DB. Production of gastrointestinal tumors in mice by modulating latent TGF-beta1 activation. Cancer Res 2013;73:459-68.
22. Engle SJ, Hoying JB, Boivin GP, Ormsby I, Gartside PS, Doetschman T. Transforming growth factor beta1 suppresses nonmetastatic colon cancer at an early stage of tumorigenesis. Cancer Res 1999;59: 3379-86.
23. Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, Mendelsohn M, et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 1992;68:855-67.
24. Rasband WS. ImageJ. Bethesda, Maryland: NIH; 1997-2014 [cited 2014 Jan 17]. Available from:http://imagej.nih.gov/ij/
25. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
26. Kang Y, Chen CR, Massague J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell 2003;11:915-26.
27. Seamons A, Treuting PM, Brabb T, Maggio-Price L. Characterization of dextran sodium sulfate-induced inflammation and colonic tumorigenesis in Smad3 (-/-) mice with dysregulated TGFbeta. PLoS ONE 2013;8:e79182.
28. Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008;4:337-49.
29. Apte RN, Dotan S, Elkabets M, White MR, Reich E, Carmi Y, et al. The involvement of IL-1 in tumorigenesis, tumor invasiveness, metastasis and tumor-host interactions. Cancer Metastasis Rev 2006;25: 387-408.
30. Hodge DR, Hurt EM, Farrar WL. The role of IL-6 and STAT3 in inflammation and cancer. Eur J Cancer 2005;41:2502-12.
31. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 1998;334 (Pt 2):297-314.
32. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell 1999;98:295-303.
33. Kanda N, Seno H, Konda Y, Marusawa H, Kanai M, Nakajima T, et al. STAT3 is constitutively activated and supports cell survival in association with survivin expression in gastric cancer cells. Oncogene 2004;23:4921-9.
34. Solis-Herruzo JA, Rippe RA, Schrum LW, de La Torre P, Garcia I, Jeffrey JJ, et al. Interleukin-6 increases rat metalloproteinase-13 gene expression through stimulation of activator protein 1 transcription factor in cultured fibroblasts. J Biol Chem 1999;274:30919-26.
35. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S, et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004;303:848-51.
36. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, Rowley DR. Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res 2002;8:2912-23.
37. Cheng N, Bhowmick NA, Chytil A, Gorksa AE, Brown KA, Muraoka R, et al. Loss of TGF-beta type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-alpha-, MSP- and HGF-mediated signaling networks. Oncogene 2005;24:5053-68.
38. Cheng N, Chytil A, Shyr Y, Joly A, Moses HL. Transforming growth factor-beta signaling-deficient fibroblasts enhance hepatocyte growth factor signaling in mammary carcinoma cells to promote scattering and invasion. Mol Cancer Res 2008;6:1521-33