ADAM17 is a tumor promoter and therapeutic target in western diet-Associated colon cancer

Clinical Cancer Research

Volumn 23, Issue 2, 2017, Pages 549-561

  Mustafi, Reba ^a   Dougherty, Urszula ^a   Mustafi, Devkumar ^a   Ayaloglu Butun, Fatma ^a   Fletcher, Michelle ^a   Adhikari, Sarbani ^a   Sadiq, Farhana ^a   Meckel, Katherine ^a   Haider, Haider I ^a   Khalil, Abdurahman ^a   Pekow, Joel ^a   Konda, Vani ^a   Joseph, Loren ^a   Hart, John ^a   Fichera, Alessandro ^a   Li, Yan Chun ^a   Bissonnette, Marc ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM10 ENDOPEPTIDASE; APC PROTEIN; AZOXYMETHANE; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR4 ANTAGONIST; CXCL2 CHEMOKINE; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR; MARIMASTAT; MYC PROTEIN; PLERIXAFOR; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR PROMOTER; ADAM17 PROTEIN, HUMAN; CXCL2 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; INCB3619; LIGAND; PIPERIDINE DERIVATIVE; SPIRO COMPOUND; TGFA PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; COLON CANCER; COLON CELL; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOLECULAR INTERACTION; MOUSE; MUTANT; NONHUMAN; SIGNAL TRANSDUCTION; STROMA CELL; TRANSACTIVATION; UPREGULATION; WESTERN DIET; ANIMAL; COLON TUMOR; GENETICS; PATHOLOGY; TUMOR CELL LINE;

ADAM17 PROTEIN; ANIMALS; CARCINOGENESIS; CELL LINE, TUMOR; CHEMOKINE CXCL2; COLONIC NEOPLASMS; DIET, WESTERN; HUMANS; LIGANDS; MICE; PIPERIDINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; SPIRO COMPOUNDS; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 85011303875     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-3140     Document Type: Article

References (52)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Weisburger JH. Dietary fat and risk of chronic disease:mechanistic insights from experimental studies. J Am Diet Assoc 1997;97:16-23.
3. La Vecchia C, Negri E, De Carli A, Franceschi S. Diabetes mellitus and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 1997; 6:1007-10.
4. Frezza EE, Wachtel MS, Chiriva-Internati M. Influence of obesity on the risk of developing colon cancer. Gut 2006;55:285-91.
5. Sung JJ, Lau JY, Goh KL, Leung WK. Asia Pacific Working Group on Colorectal C. Increasing incidence of colorectal cancer in Asia: implications for screening. Lancet Oncol 2005;6:871-6.
6. Kwong LN, Dove WF. APC and its modifiers in colon cancer. Adv Exp Med Biol 2009;656:85-106.
7. Takahashi M, Wakabayashi K. Gene mutations and altered gene expression in azoxymethane-induced colon carcinogenesis in rodents. Cancer Sci 2004;95:475-80.
8. Wasan HS, Novelli M, Bee J, Bodmer WF. Dietary fat influences on polyp phenotype in multiple intestinal neoplasia mice. Proc Natl Acad Sci U S A 1997;94:3308-13.
9. Dougherty U, Cerasi D, Taylor I, Tekin U, Badal S, Aluri L, et al. Epidermal growth factor receptor is required for colonic tumor promotion by dietary fat in the azoxymethane/dextran sulfate sodium model: Roles of transforming growth factor-{alpha} and PTGS2. Clin Cancer Res 2009;15:6780-9.
10. Zhu H, Dougherty U, Robinson V, Mustafi R, Pekow J, Kupfer S, et al. EGFR signals downregulate tumor suppressorsmiR-143 andmiR-145 in Western diet-promoted murine colon cancer: Role of G1 regulators. Mol Cancer Res 2011;9:960-75.
11. Fichera A, Little N, Jagadeeswaran S, Dougherty U, Sehdev A, Mustafi R, et al. EGFR signaling is required for microadenoma formation in the mouse azoxymethane model of colonic carcinogenesis. Cancer Res 2007;67:827-35.
12. Dougherty U, Sehdev A, Cerda S, Mustafi R, Little N, Yuan W, et al. Epidermal growth factor receptor controls flat dysplastic aberrant crypt foci development and colon cancer progression in the rat azoxymethane model. Clin Cancer Res 2008;14:2253-62.
13. Prenzel N, Fischer OM, Streit S, Hart S, Ullrich A. The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr Relat Cancer 2001; 8:11-31.
14. Kuwai T, Nakamura T, Sasaki T, Kim SJ, Fan D, Villares GJ, et al. Phosphorylated epidermal growth factor receptor on tumor-Associated endothelial cells is a primary target for therapy with tyrosine kinase inhibitors. Neoplasia 2008;10:489-500.
15. Yoo J, Rodriguez Perez CE, Nie W, Edwards RA, Sinnett-Smith J, Rozengurt E. TNF-Alpha induces upregulation of EGFR expression and signaling in human colonic myofibroblasts. Am J Physiol Gastrointest Liver Physiol 2012;302:805-14.
16. Barber TD, Vogelstein B, Kinzler KW, Velculescu VE. Somatic mutations of EGFR in colorectal cancers and glioblastomas. N Engl J Med 2004; 351:2883.
17. Blanchot-Jossic F, JarryA, MassonD, Bach-Ngohou K, Paineau J, Denis MG, et al. Up-regulated expression of ADAM17 in human colon carcinoma: coexpression with EGFR in neoplastic and endothelial cells. J Pathol 2005;207:156-63.
18. Fischer OM, Hart S, Gschwind A, Ullrich A. EGFR signal transactivation in cancer cells. Biochem Soc Trans 2003;31:1203-8.
19. Akishima-Fukasawa Y, Nakanishi Y, Ino Y, Moriya Y, Kanai Y, Hirohashi S. Prognostic significance of CXCL12 expression in patients with colorectal carcinoma. Am J Clin Pathol 2009;132:202-10.
20. de Meijer VE, Le HD, Meisel JA, Sharma AK, Popov Y, Puder M. Tumor necrosis factor alpha-converting enzyme inhibition reverses hepatic steatosis and improves insulin sensitivity markers and surgical outcome in mice. PLoS One 2011;6:e25587.
21. Rosenkilde MM, Gerlach LO, Jakobsen JS, Skerlj RT, Bridger GJ, Schwartz TW. Molecular mechanismof AMD3100 antagonism in the CXCR4 receptor: Transfer of binding site to the CXCR3 receptor. J Biol Chem 2004; 279:3033-41.
22. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J, et al. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 2004;164:769-79.
23. Liu X, Fridman JS, Wang Q, Caulder E, Yang G, Covington M, et al. Selective inhibition of ADAM metalloproteases blocks HER-2 extracellular domain (ECD) cleavage and potentiates the anti-Tumor effects of trastuzumab. Cancer Biol Ther 2006;5:648-56.
24. Roberts RB, Min L, Washington MK, Olsen SJ, Settle SH, Coffey RJ, et al. Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis. Proc Natl Acad Sci U S A 2002;99:1521-6.
25. Moran AE, Hunt DH, Javid SH, Redston M, Carothers AM, Bertagnolli MM. Apc deficiency is associated with increased Egfr activity in the intestinal enterocytes and adenomas of C57BL/6J-Min/ mice. J Biol Chem 2004;279:43261-72.
26. Rasmussen HS, McCann PP. Matrix metalloproteinase inhibition as a novel anticancer strategy: A review with special focus on batimastat and marimastat. Pharmacol Ther 1997;75:69-75..
27. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990; 247:322-4.
28. Hung KE, Maricevich MA, Richard LG, Chen WY, Richardson MP, Kunin A, et al. Development of a mouse model for sporadic and metastatic colon tumors and its use in assessing drug treatment. Proc Natl Acad Sci U S A 2010;107:1565-70.
29. Dougherty U, Mustafi R, Wang Y, Musch MW, Wang C-Z, Konda VJ, et al. American ginseng suppresses Western diet-promoted tumorigenesis in model of inflammation-Associated colon cancer: Role of EGFR. BMC Complement Altern Med 2011;11:111.
30. Seidelin JB, Horn T, Nielsen OH. Simple and efficient method for isolation and cultivation of endoscopically obtained human colonocytes. Am J Physiol Gastrointest Liver Physiol 2003;285: 1122-8.
31. Khalil H, Nie W, Edwards RA, Yoo J. Isolation of primary myofibroblasts from mouse and human colon tissue. J Vis Exp 2013;80:e50611.
32. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: An open-source platform for biological-image analysis. Nat Methods 2012;9:676-82.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-Time quantitative PCR and the 2(-Delta Delta C(T))method. Methods 2001;25:402-8.
34. Porcile C, Bajetto A, Barbieri F, Barbero S, Bonavia R, Biglieri M, et al. Stromal cell-derived factor-1alpha (SDF-1alpha/CXCL12) stimulates ovarian cancer cell growth through the EGF receptor transactivation. Exp Cell Res 2005;308:241-53.
35. Romee R, Foley B, Lenvik T, Wang Y, Zhang B, Ankarlo D, et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 2013;121:3599-608.
36. Tsai YH, VanDussen KL, Sawey ET, Wade AW, Kasper C, Rakshit S, et al. ADAM10 regulates Notch function in intestinal stem cells of mice. Gastroenterology 2014;147:822-34 e13.
37. Fre S, Pallavi SK, HuygheM, LaeM, Janssen K-P, Robine S, et al. Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc Natl Acad Sci U S A 2009;106:6309-14.
38. Horiuchi K, Kimura T, Miyamoto T, Takaishi H, Okada Y, Toyama Y, et al. Cutting edge: TNF-Alpha-converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J Immunol 2007;179:2686-9.
39. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 2002;277:33275-83.
40. Serino M, Menghini R, Fiorentino L, Amoruso R, Mauriello A, Lauro D, et al. Mice heterozygous for tumor necrosis factor-Alpha converting enzyme are protected from obesity-induced insulin resistance and diabetes. Diabetes 2007;56:2541-6.
41. Gelling RW, Yan W, Al-Noori S, Pardini A, Morton GJ, Ogimoto K, et al. Deficiency of TNFalpha converting enzyme (TACE/ADAM17) causes a lean, hypermetabolic phenotype in mice. Endocrinology 2008;149: 6053-64.
42. Kasina S, Scherle PA, Hall CL, Macoska JA. ADAM-mediated amphiregulin shedding and EGFR transactivation. Cell Prolif 2009;42:799-812.
43. Blobel CP. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol 2005;6:32-43.
44. Xia XM, Wang FY, Zhou J, Hu KF, Li SW, Zou BB. CXCR4 antagonist AMD3100 modulates claudin expression and intestinal barrier function in experimental colitis. PLoS One 2011;6:e27282.
45. Fridman JS, Caulder E, Hansbury M, Liu X, Yang G, Wang Q, et al. Selective inhibition of ADAM metalloproteases as a novel approach for modulating ErbB pathways in cancer. Clin Cancer Res 2007;13:1892-902.
46. Infante J, Burris H, Lewis N, Donehower R, Redman J, Friedman S, et al. A multicenter phase Ib study of the safety, pharmacokinetics, biological activity and clinical efficacy of INCB7839, a potent and selective inhibitor of ADAM10 and ADAM17. Breast Cancer Res Treat 2007;106:S269.
47. Newton R, Bradley E, Levy R, Doval D, Bondarde S, Sahoo TP, et al. Clinical benefit of INCB7839, a potent and selective ADAM inhibitor, in combination with trastuzumab in patients with metastatic HER2 breast cancer. J Clin Oncol 2010;28:15s, (suppl; abstr 3025).
48. Wang R, Ye X, Bhattacharya R, Boulbes DR, Fan F, Xia L, et al. A disintegrin and metalloproteinase domain 17 regulates colorectal cancer stem cells and chemosensitivity via notch1 signaling. Stem Cells Transl Med 2016; 5:331-8.
49. Lu J, Ye X, Fan F, Xia L, Bhattacharya R, Bellister S, et al. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 2013;23:171-85.
50. Feng Y, Tsai YH, Xiao W, Ralls MW, Stoeck A, Wilson CL, et al. Loss of ADAM17-mediated tumor necrosis factor alpha signaling in intestinal cells attenuates mucosal atrophy in a mouse model of parenteral nutrition. Mol Cell Biol 2015;35:3604-21.
51. Shimoda M, Horiuchi K, Sasaki A, Tsukamoto T, Okabayashi K, Hasegawa H, et al. Epithelial cell-derived a disintegrin and metalloproteinase-17 confers resistance to colonic inflammation through EGFR activation. E Bio Medicine 2016;5:114-24.
52. Rios-Doria J, Sabol D, Chesebrough J, Stewart D, Xu L, Tammali R, et al. A monoclonal antibody to ADAM17 inhibits tumor growth by inhibiting EGFR and Non-EGFR-Mediated pathways. Mol Cancer Ther 2015;14: 1637-49.