Loss of Trop2 causes ErbB3 activation through a neuregulin-1-dependent mechanism in the mesenchymal subtype of HNSCC

Oncotarget

Volumn 5, Issue 19, 2014, Pages 9281-9294

  Zhang, Kaihua ^a   Jones, Lamont ^a   Lim, Sora ^a   Maher, Christopher A ^a,b   Adkins, Douglas ^a,b   Lewis, James ^a,b   Kimple, Randall J ^c   Fertig, Elana J ^d   Chung, Christine H ^d   Van Tine, Brian A ^a,b   Ellis, Matthew J ^a,b   Herrlich, Andreas ^e   Michel, Loren S ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b USA   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

ErbB3; Head and Neck Squamous Cell Carcinoma (HNSCC); Neuregulin 1; Therapy; Trop2

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 3; MEMBRANE PROTEIN; NEU DIFFERENTIATION FACTOR; CANCER ANTIBODY; CELL ADHESION MOLECULE; ERBB3 PROTEIN, HUMAN; SMALL INTERFERING RNA; TACSTD2 PROTEIN, HUMAN; TUMOR ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER GROWTH; CELL GROWTH; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; DISEASE MARKER; FEMALE; GROWTH INHIBITION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; ANIMAL; CANCER TRANSPLANTATION; CLASSIFICATION; ENZYME ACTIVATION; GENETICS; HEAD AND NECK TUMOR; HUMAN; IMMUNOLOGY; METABOLISM; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTIBODIES, NEOPLASM; ANTIGENS, NEOPLASM; CARCINOMA, SQUAMOUS CELL; CELL ADHESION MOLECULES; CELL LINE, TUMOR; ENZYME ACTIVATION; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEUREGULIN-1; RECEPTOR, ERBB-3; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSPLANTATION, HETEROLOGOUS;

EID: 84910030857     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2423     Document Type: Article

References (44)

1. Rothenberg SM and Ellisen LW. The molecular pathogenesis of head and neck squamous cell carcinoma. J Clin Invest. 2012; 122(6):1951-1957.
2. Chung CH, Parker JS, Karaca G, Wu J, Funkhouser WK, Moore D, Butterfoss D, Xiang D, Zanation A, Yin X, Shockley WW, Weissler MC, Dressler LG, Shores CG, Yarbrough WG and Perou CM. Molecular classification of head and neck squamous cell carcinomas using patterns of gene expression. Cancer Cell. 2004; 5(5):489-500.
3. Walter V, Yin X, Wilkerson MD, Cabanski CR, Zhao N, Du Y, Ang MK, Hayward MC, Salazar AH, Hoadley KA, Fritchie K, Sailey CG, Weissler MC, Shockley WW, Zanation AM, Hackman T, et al. Molecular subtypes in head and neck cancer exhibit distinct patterns of chromosomal gain and loss of canonical cancer genes. PLoS One. 2013; 8(2):e56823.
4. Hayes DN, Grandis, J.R., El-Naggar, A.K. The Cancer Genome Atlas: Integrated analysis of genome alterations in squamous cell carcinoma of the head and neck. J Clin Oncol. 2013; 31(suppl):abstract 6009.
5. Prat A and Perou CM. Deconstructing the molecular portraits of breast cancer. Mol Oncol. 2011; 5(1):5-23.
6. Karapetis CS, Khambata-Ford S, Jonker DJ, O'Callaghan CJ, Tu D, Tebbutt NC, Simes RJ, Chalchal H, Shapiro JD, Robitaille S, Price TJ, Shepherd L, Au HJ, Langer C, Moore MJ and Zalcberg JR. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med. 2008; 359(17):1757-1765.
7. Wang J, Zhang K, Grabowska D, Li A, Dong Y, Day R, Humphrey P, Lewis J, Kladney RD, Arbeit JM, Weber JD, Chung CH and Michel LS. Loss of Trop2 promotes carcinogenesis and features of epithelial to mesenchymal transition in squamous cell carcinoma. Mol Cancer Res. 2011; 9(12):1686-1695.
8. Wang J, Day R, Dong Y, Weintraub SJ and Michel L. Identification of Trop-2 as an oncogene and an attractive therapeutic target in colon cancers. Mol Cancer Ther. 2008; 7(2):280-285.
9. Cubas R, Zhang S, Li M, Chen C and Yao Q. Trop2 expression contributes to tumor pathogenesis by activating the ERK MAPK pathway. Mol Cancer. 2010; 9:253.
10. Lin JC, Wu YY, Wu JY, Lin TC, Wu CT, Chang YL, Jou YS, Hong TM and Yang PC. TROP2 is epigenetically inactivated and modulates IGF-1R signalling in lung adenocarcinoma. EMBO Mol Med. 2012; 4(6):472-485.
11. Bei R, Budillon A, Masuelli L, Cereda V, Vitolo D, Di Gennaro E, Ripavecchia V, Palumbo C, Ionna F, Losito S, Modesti A, Kraus MH and Muraro R. Frequent overexpression of multiple ErbB receptors by head and neck squamous cell carcinoma contrasts with rare antibody immunity in patients. J Pathol. 2004; 204(3):317-325.
12. Wilson TR, Lee DY, Berry L, Shames DS and Settleman J. Neuregulin-1-mediated autocrine signaling underlies sensitivity to HER2 kinase inhibitors in a subset of human cancers. Cancer Cell. 2011; 20(2):158-172.
13. Xia W, Lau YK, Zhang HZ, Xiao FY, Johnston DA, Liu AR, Li L, Katz RL and Hung MC. Combination of EGFR, HER-2/neu, and HER-3 is a stronger predictor for the outcome of oral squamous cell carcinoma than any individual family members. Clin Cancer Res. 1999; 5(12):4164-4174.
14. Yarden Y. The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. Eur J Cancer. 2001; 37 Suppl 4:S3-8.
15. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF, 3rd and Hynes NE. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci U S A. 2003; 100(15):8933-8938.
16. Muller WJ, Sinn E, Pattengale PK, Wallace R and Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell. 1988; 54(1):105-115.
17. Berger MB, Mendrola JM and Lemmon MA. ErbB3/HER3 does not homodimerize upon neuregulin binding at the cell surface. FEBS Lett. 2004; 569(1-3):332-336.
18. Amin DN, Campbell MR and Moasser MM. The role of HER3, the unpretentious member of the HER family, in cancer biology and cancer therapeutics. Semin Cell Dev Biol. 2010; 21(9):944-950.
19. Sergina NV, Rausch M, Wang D, Blair J, Hann B, Shokat KM and Moasser MM. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature. 2007; 445(7126):437-441.
20. Jaiswal BS, Kljavin NM, Stawiski EW, Chan E, Parikh C, Durinck S, Chaudhuri S, Pujara K, Guillory J, Edgar KA, Janakiraman V, Scholz RP, Bowman KK, Lorenzo M, Li H, Wu J, et al. Oncogenic ERBB3 mutations in human cancers. Cancer Cell. 2013; 23(5):603-617.
21. Carraway KL, 3rd, Sliwkowski MX, Akita R, Platko JV, Guy PM, Nuijens A, Diamonti AJ, Vandlen RL, Cantley LC and Cerione RA. The erbB3 gene product is a receptor for heregulin. J Biol Chem. 1994; 269(19):14303-14306.
22. Holmes WE, Sliwkowski MX, Akita RW, Henzel WJ, Lee J, Park JW, Yansura D, Abadi N, Raab H, Lewis GD and et al. Identification of heregulin, a specific activator of p185erbB2. Science. 1992; 256(5060):1205-1210.
23. Zhou BB, Peyton M, He B, Liu C, Girard L, Caudler E, Lo Y, Baribaud F, Mikami I, Reguart N, Yang G, Li Y, Yao W, Vaddi K, Gazdar AF, Friedman SM, et al. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell. 2006; 10(1):39-50.
24. Blobel CP. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol. 2005; 6(1):32-43.
25. Maretzky T, Zhou W, Huang XY and Blobel CP. A transforming Src mutant increases the bioavailability of EGFR ligands via stimulation of the cell-surface metalloproteinase ADAM17. Oncogene. 2011; 30(5):611-618.
26. Van Schaeybroeck S, Kyula JN, Fenton A, Fenning CS, Sasazuki T, Shirasawa S, Longley DB and Johnston PG. Oncogenic Kras promotes chemotherapy-induced growth factor shedding via ADAM17. Cancer Res. 2011; 71(3):1071-1080.
27. Dang M, Armbruster N, Miller MA, Cermeno E, Hartmann M, Bell GW, Root DE, Lauffenburger DA, Lodish HF and Herrlich A. Regulated ADAM17-dependent EGF family ligand release by substrate-selecting signaling pathways. Proc Natl Acad Sci U S A. 2013; 110(24):9776-9781.
28. Gilmour LM, Macleod KG, McCaig A, Sewell JM, Gullick WJ, Smyth JF and Langdon SP. Neuregulin expression, function, and signaling in human ovarian cancer cells. Clin Cancer Res. 2002; 8(12):3933-3942.
29. Yonesaka K, Zejnullahu K, Okamoto I, Satoh T, Cappuzzo F, Souglakos J, Ercan D, Rogers A, Roncalli M, Takeda M, Fujisaka Y, Philips J, Shimizu T, Maenishi O, Cho Y, Sun J, et al. Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci Transl Med. 2011; 3(99):99ra86.
30. Reschke M, Mihic-Probst D, van der Horst EH, Knyazev P, Wild PJ, Hutterer M, Meyer S, Dummer R, Moch H and Ullrich A. HER3 is a determinant for poor prognosis in melanoma. Clin Cancer Res. 2008; 14(16):5188-5197.
31. Zhang Z, Prentiss L, Heitzman D, Stahl RC, DiPino F, Jr. and Carey DJ. Neuregulin isoforms in dorsal root ganglion neurons: effects of the cytoplasmic domain on localization and membrane shedding of Nrg-1 type I. J Neurosci Res. 2006; 84(1):1-12.
32. Sheng Q, Liu X, Fleming E, Yuan K, Piao H, Chen J, Moustafa Z, Thomas RK, Greulich H, Schinzel A, Zaghlul S, Batt D, Ettenberg S, Meyerson M, Schoeberl B, Kung AL, et al. An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell. 2010; 17(3):298-310.
33. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, Onsum M, Burenkova O, Pace E, Walton Z, Nie L, Fulgham A, Song Y, Nielsen UB, Engelman JA and Wong KK. An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res. 2010; 70(6):2485-2494.
34. Higgins MJ and Baselga J. Targeted therapies for breast cancer. J Clin Invest. 2011; 121(10):3797-3803.
35. Chen LF, Cohen EE and Grandis JR. New strategies in head and neck cancer: understanding resistance to epidermal growth factor receptor inhibitors. Clin Cancer Res. 2010; 16(9):2489-2495.
36. Stoyanova T, Goldstein AS, Cai H, Drake JM, Huang J and Witte ON. Regulated proteolysis of Trop2 drives epithelial hyperplasia and stem cell self-renewal via beta-catenin signaling. Genes Dev. 2012; 26(20):2271-2285.
37. Nakanishi H, Taccioli C, Palatini J, Fernandez-Cymering C, Cui R, Kim T, Volinia S and Croce CM. Loss of miR-125b-1 contributes to head and neck cancer development by dysregulating TACSTD2 and MAPK pathway. Oncogene. 2013.
38. Murphy G. Regulation of the proteolytic disintegrin metalloproteinases, the 'Sheddases'. Semin Cell Dev Biol. 2009; 20(2):138-145.
39. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, Kosaka T, Holmes AJ, Rogers AM, Cappuzzo F, Mok T, Lee C, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007; 316(5827):1039-1043.
40. Shames DS, Carbon J, Walter K, Jubb AM, Kozlowski C, Januario T, AnDo, Fu L, Xiao Y, Raja R, Jiang B, Malekafzali A, Stern H, Settleman J, Wilson TR, Hampton GM, et al. High heregulin expression is associated with activated HER3 and may define an actionable biomarker in patients with squamous cell carcinomas of the head and neck. PLoS One. 2013; 8(2):e56765.
41. Fong D, Spizzo G, Gostner JM, Gastl G, Moser P, Krammel C, Gerhard S, Rasse M and Laimer K. TROP2: a novel prognostic marker in squamous cell carcinoma of the oral cavity. Mod Pathol. 2008; 21(2):186-191.
42. Stepan LP, Trueblood ES, Hale K, Babcook J, Borges L and Sutherland CL. Expression of Trop2 cell surface glycoprotein in normal and tumor tissues: potential implications as a cancer therapeutic target. J Histochem Cytochem. 2011; 59(7):701-710.
43. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, Cerami E, Sander C and Schultz N. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013; 6(269):pl1.
44. TCGA. Available from: https://tcga-data.nci.nih.gov.