Cabozantinib (XL184) inhibits growth and invasion of preclinical TNBC models

Clinical Cancer Research

Volumn 22, Issue 4, 2016, Pages 923-934

  Sameni, Mansoureh ^a   Tovar, Elizabeth A ^b   Essenburg, Curt J ^b   Chalasani, Anita ^a   Linklater, Erik S ^b   Borgman, Andrew ^b   Cherba, David M ^b   Anbalagan, Arulselvi ^a   Winn, Mary E ^b   Graveel, Carrie R ^b   Sloane, Bonnie F ^a,c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

^c WAYNE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CABOZANTINIB; RECEPTOR SUBTYPE; TYROSINE KINASE RECEPTOR; ANILIDE; ANTINEOPLASTIC AGENT; MET PROTEIN, HUMAN; PYRIDINE DERIVATIVE; SCATTER FACTOR RECEPTOR;

ARTICLE; BREAST CANCER CELL LINE; CANCER GROWTH; CANCER INHIBITION; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; FIBROBLAST; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS; PARACRINE SIGNALING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TRIPLE NEGATIVE BREAST CANCER; TUMOR MICROENVIRONMENT; XENOGRAFT; ANIMAL; C3H MOUSE; COCULTURE; DRUG EFFECTS; DRUG SCREENING; FEMALE; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; SCID MOUSE; SECONDARY; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE; TUMOR INVASION; TUMOR VOLUME;

ANILIDES; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; COCULTURE TECHNIQUES; FEMALE; FIBROBLASTS; HUMANS; LUNG NEOPLASMS; MICE, INBRED C3H; MICE, SCID; NEOPLASM INVASIVENESS; PROTO-ONCOGENE PROTEINS C-MET; PYRIDINES; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84964293321     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-0187     Document Type: Article

References (48)

1. Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med 2010;363:1938-48.
2. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007;13:4429-34.
3. Lehmann BD, Bauer JA, Chen X, SandersME, Chakravarthy AB, Shyr Y, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011;121: 2750-67.
4. Burstein MD, Tsimelzon A, Poage GM, Covington KR, Contreras A, Fuqua SA, et al. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res 2015;21:1688-98.
5. Liedtke C, Mazouni C, Hess KR, Andre F, Tordai A, Mejia JA, et al. Response to neoadjuvant therapy and long-term survival in patients with triplenegative breast cancer. J Clin Oncol 2008;26:1275-81.
6. Xu AM, Huang PH. Receptor tyrosine kinase coactivation networks in cancer. Cancer Res 2010;70:3857-60.
7. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012;487:505-9.
8. JedeszkoC, Victor BC, Podgorski I, Sloane BF. Fibroblast hepatocyte growth factor promotes invasion of human mammary ductal carcinoma in situ. Cancer Res 2009;69:9148-55.
9. Tchou J, Conejo-Garcia J. Targeting the tumor stroma as a novel treatment strategy for breast cancer: shifting from the neoplastic cell-centric to a stroma-centric paradigm. Adv Pharmacol 2012;65:45-61.
10. Rudnick JA, Kuperwasser C. Stromal biomarkers in breast cancer development and progression. Clin Exp Metastasis 2012;29:663-72.
11. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003;4:915-25.
12. Ghoussoub RA, Dillon DA, D'Aquila T, Rimm EB, Fearon ER, Rimm DL. Expression of c-met is a strong independent prognostic factor in breast carcinoma. Cancer 1998;82:1513-20.
13. Camp RL, Rimm EB, Rimm DL. Met expression is associated with poor outcome in patients with axillary lymph node negative breast carcinoma. Cancer 1999;86:2259-65.
14. Ocal IT, Dollard-Filhart M, D'Aquila T, Camp RL, Rimm DL. Tissue microarray-based studies of patients with lymph node negative breast carcinoma show that met expression is associated with worse outcome but is not correlated with epidermal growth factor family receptors. Cancer 2003;97:1841-48.
15. Edakuni G, Sasatomi E, Satoh T, Tokunaga O, Miyazaki K. Expression of the hepatocyte growth factor/c-Met pathway is increased at the cancer front in breast carcinoma. Pathol Int 2001;51:172-8.
16. Lengyel E, Prechtel D, Resau JH, Gauger K, Welk A, Lindemann K, et al. CMet overexpression in node-positive breast cancer identifies patients with poor clinical outcome independent of Her2/neu. Int J Cancer 2005;113: 678-82.
17. Graveel CR, DeGroot JD, Su Y, Koeman J, Dykema K, Leung S, et al. Met induces diverse mammary carcinomas in mice and is associated with human basal breast cancer. Proc Natl Acad Sci U S A 2009;106:12909-14.
18. Ponzo MG, Lesurf R, Petkiewicz S, O'Malley FP, Pinnaduwage D, Andrulis IL, et al. Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Proc Natl Acad Sci U S A 2009;106:12903-8.
19. Ho-Yen CM, Green AR, Rakha EA, Brentnall AR, Ellis IO, Kermorgant S, et al. C-Met in invasive breast cancer: Is there a relationship with the basallike subtype? Cancer 2014;120:163-71.
20. Inanc M, Ozkan M, Karaca H, Berk V, Bozkurt O, Duran AO, et al. Cytokeratin 5/6, c-Met expressions, and PTEN loss prognostic indicators in triple-negative breast cancer. Med Oncol 2014;31:801.
21. Paulson AK, Linklater ES, Berghuis BD, App CA, Oostendorp LD, Paulson JE, et al. MET and ERBB2 are coexpressed in ERBB2+ breast cancer and contribute to innate resistance. Mol Cancer Res 2013;11:1112-21.
22. Camp JT, Elloumi F, Roman-Perez E, Rein J, Stewart DA, Harrell JC, et al. Interactions with fibroblasts are distinct in Basal-like and luminal breast cancers. Mol Cancer Res 2011;9:3-13.
23. Yakes FM, Chen J, Tan J, Yamaguchi K, Shi Y, Yu P, et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther 2011;10: 2298-308.
24. Lee RJ, Saylor PJ, Michaelson MD, Rothenberg SM, Smas ME, Miyamoto DT, et al. A dose-ranging study of cabozantinib in men with castrationresistant prostate cancer and bone metastases. Clin Cancer Res 2013;19: 3088-94.
25. Smith DC, Smith MR, Sweeney C, Elfiky AA, Logothetis C, Corn PG, et al. Cabozantinib in patients with advanced prostate cancer: results of a phase II randomized discontinuation trial. J Clin Oncol 2013;31:412-9.
26. Bengsch F, Buck A, Gunther SC, Seiz JR, Tacke M, Pfeifer D, et al. Cell typedependent pathogenic functions of overexpressed human cathepsin B in murine breast cancer progression. Oncogene 2014;33:4474-84.
27. Moin K, Sameni M, Victor BC, Rothberg JM, Mattingly RR, Sloane BF. 3D/4D functional imaging of tumor-associated proteolysis: impact of microenvironment. Methods Enzymol 2012;506:175-94.
28. Rong S, Bodescot M, Blair D, Dunn J, Nakamura T, Mizuno K, et al. Tumorigenicity of the met proto-oncogene and the gene for hepatocyte growth factor. Mol Cell Biol 1992;12:5152-8.
29. Zhang YW, Su Y, Lanning N, Gustafson M, Shinomiya N, Zhao P, et al. Enhanced growth of human met-expressing xenografts in a new strain of immunocompromised mice transgenic for human hepatocyte growth factor/scatter factor. Oncogene 2005;24:101-6.
30. Zhang YW, Staal B, Essenburg C, Su Y, Kang L, West R, et al. MET kinase inhibitor SGX523 synergizes with epidermal growth factor receptor inhibitor erlotinib in a hepatocyte growth factor-dependent fashion to suppress carcinoma growth. Cancer Res 2010;70:6880-90.
31. Pauley RJ, Santner SJ, Tait LR, Bright RK, Santen RJ. Regulated CYP19 aromatase transcription in breast stromal fibroblasts. J Clin Endocrinol Metab 2000;85:837-46.
32. Koblinski JE, Dosescu J, SameniM, Moin K, Clark K, Sloane BF. Interaction of human breast fibroblasts with collagen I increases secretion of procathepsin B. J Biol Chem 2002;277:32220-7.
33. Kuperwasser C, Chavarria T, Wu M, Magrane G, Gray JW, Carey L, et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci U S A 2004;101:4966-71.
34. Sameni M, Anbalagan A, Olive MB, Moin K, Mattingly RR, Sloane BF. MAME models for 4D live-cell imaging of tumor: microenvironment interactions that impact malignant progression. J Vis Exp 2012; pii:3661.
35. Mullins SR, Sameni M, Blum G, Bogyo M, Sloane BF, Moin K. Threedimensional cultures modeling premalignant progression of human breast epithelial cells: role of cysteine cathepsins. Biol Chem 2012;393: 1405-16.
36. Laajala TD, Corander J, Saarinen NM, Makela K, Savolainen S, Suominen MI, et al. Improved statistical modeling of tumor growth and treatment effect in preclinical animal studies with highly heterogeneous responses in vivo. Clin Cancer Res 2012;18:4385-96.
37. Weigelt B, Ghajar CM, Bissell MJ. The need for complex 3D culture models to unravel novel pathways and identify accurate biomarkers in breast cancer. Adv Drug Deliv Rev 2014;69-70:42-51.
38. Debnath J, Brugge JS. Modelling glandular epithelial cancers in threedimensional cultures. Nat Rev Cancer 2005;5:675-88.
39. Rothberg JM, Bailey KM, Wojtkowiak JW, Ben-Nun Y, Bogyo M, Weber E, et al. Acid-mediated tumor proteolysis: contribution of cysteine cathepsins. Neoplasia 2013;15:1125-37.
40. Rixe O, Fojo T. Is cell death a critical end point for anticancer therapies or is cytostasis sufficient? Clin Cancer Res 2007;13:7280-7.
41. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008;14:518-27.
42. Farmer P, BonnefoiH, Anderle P, CameronD, Wirapati P, Becette V, et al. A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. Nat Med 2009;15:68-74.
43. Garber K. MET inhibitors start on road to recovery. Nat Rev Drug Discov 2014;13:563-5.
44. Spigel DR, Ervin TJ, Ramlau R, Daniel DB, Goldschmidt JH, Blumenschein GR, et al. Final efficacy results from OAM4558g, a randomized phase II study evaluating MetMAb or placebo in combination with erlotinib in advanced NSCLC. J Clin Oncol Abstr 2011;29:7505.
45. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003;3:347-61.
46. Chen HH, Su WC, Lin PW, Guo HR, Lee WY. Hypoxia-inducible factor- 1alpha correlates with MET andmetastasis in node-negative breast cancer. Breast Cancer Res Treat 2007;103:167-75.
47. Wilson WR, Hay MP. Targeting hypoxia in cancer therapy. Nat Rev 2011;11:393-410.
48. Sheridan C. Genentech to salvage anti-MET antibody with subgroup analysis. Nat Biotech 2014;32:399-400.