Employing an orthotopic model to study the role of epithelialmesenchymal transition in bladder cancer metastasis

Oncotarget

Volumn 8, Issue 21, 2017, Pages 34205-34222

  Roth, Beat ^a,c   Jayaratna, Isuru ^a   Sundi, Debasish ^a   Cheng, Tiewei ^a,b   Melquist, Jonathan ^a   Choi, Woonyoung ^a   Porten, Sima ^a   Nitti, Giovanni ^b   Navai, Neema ^a   Wszolek, Matthew ^a,d   Guo, Charles ^a   Czerniak, Bogdan ^a   McConkey, David ^a   Dinney, Colin ^a  

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

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF BERN   (Switzerland)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Bladder cancer; Circulating tumor cells; Metastasis; Orthotopic xenografts; SNAIL

Indexed keywords

SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BIOLUMINESCENCE; BLADDER CANCER; BLADDER CANCER CELL LINE; CELL COUNT; CIRCULATING TUMOR CELL; CONTROLLED STUDY; DISTANT METASTASIS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METASTASIS POTENTIAL; MOUSE; NONHUMAN; ONCOLOGICAL PROCEDURE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGIONAL METASTASIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BLADDER TUMOR; DISEASE EXACERBATION; DISEASE MODEL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR EMBOLISM; WHOLE GENOME SEQUENCING;

ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; SIGNAL TRANSDUCTION; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; URINARY BLADDER NEOPLASMS; WHOLE GENOME SEQUENCING;

EID: 85019856114     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.11009     Document Type: Article

References (59)

1. Dinney CP, McConkey DJ, Millikan RE, Wu X, Bar-Eli M, Adam L, Kamat AM, Siefker-Radtke AO, Tuziak T, Sabichi AL, Grossman HB, Benedict WF, Czerniak B. Focus on bladder cancer. Cancer cell. 2004; 6:111-116
2. Rosenberg JE, Hoffman-Censits J, Powles T, van der Heijden MS, Balar AV, Necchi A, Dawson N, O'Donnell PH, Balmanoukian A, Loriot Y, Srinivas S, Retz MM, Grivas P, et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial. The Lancet. 2016; 387:1909-20
3. von der Maase H, Hansen SW, Roberts JT, Dogliotti L, Oliver T, Moore MJ, Bodrogi I, Albers P, Knuth A, Lippert CM, Kerbrat P, Sanchez Rovira P, Wersall P, et al. Gemcitabine and cisplatin versus methotrexate, vinblastine, doxorubicin, and cisplatin in advanced or metastatic bladder cancer: results of a large, randomized, multinational, multicenter, phase III study. Journal of clinical oncology. 2000; 18:3068-3077
4. Milowsky MI, Iyer G, Regazzi AM, Al-Ahmadie H, Gerst SR, Ostrovnaya I, Gellert LL, Kaplan R, Garcia-Grossman IR, Pendse D, Balar AV, Flaherty AM, Trout A, et al. Phase II study of everolimus in metastatic urothelial cancer. BJU international. 2013; 112:462-470
5. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011; 147:275-292
6. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674
7. Fidler IJ, Hart IR. Biological diversity in metastatic neoplasms: origins and implications. Science. 1982; 217:998-1003
8. Talmadge JE, Wolman SR, Fidler IJ. Evidence for the clonal origin of spontaneous metastases. Science. 1982; 217:361-363
9. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature reviews Cancer. 2009; 9:265-273
10. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer cell. 2012; 22:725-736
11. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011; 331:1559-1564
12. Chaffer CL, Marjanovic ND, Lee T, Bell G, Kleer CG, Reinhardt F, D'Alessio AC, Young RA, Weinberg RA. Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell. 2013; 154:61-74
13. Tsuji T, Ibaragi S, Hu GF. Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer research. 2009; 69:7135-7139
14. Giese A, Loo MA, Tran N, Haskett D, Coons SW, Berens ME. Dichotomy of astrocytoma migration and proliferation. International journal of cancer. 1996; 67: 275-282
15. Zheng PP, Severijnen LA, van der Weiden M, Willemsen R, Kros JM. Cell proliferation and migration are mutually exclusive cellular phenomena in vivo: implications for cancer therapeutic strategies. Cell cycle. 2009; 8:950-951
16. Giese A, Loo MA, Tran N, Haskett D, Coons SW, Berens ME. Dichotomy of astrocytoma migration and proliferation. International journal of cancer. 1996; 67: 275-282
17. Cheng T, Roth B, Choi W, Black PC, Dinney C, McConkey DJ. Fibroblast growth factor receptors-1 and-3 play distinct roles in the regulation of bladder cancer growth and metastasis: implications for therapeutic targeting. PloS one. 2013; 8:e57284
18. Baumgart E, Cohen MS, Silva Neto B, Jacobs MA, Wotkowicz C, Rieger-Christ KM, Biolo A, Zeheb R, Loda M, Libertino JA, Summerhayes IC. Identification and prognostic significance of an epithelial-mesenchymal transition expression profile in human bladder tumors. Clinical cancer research. 2007; 13:1685-1694
19. Adam L, Zhong M, Choi W, Qi W, Nicoloso M, Arora A, Calin G, Wang H, Siefker-Radtke A, McConkey D, Bar-Eli M, Dinney C. miR-200 expression regulates epithelialto-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clinical cancer research. 2009; 15:5060-5072
20. McConkey DJ, Choi W, Marquis L, Martin F, Williams MB, Shah J, Svatek R, Das A, Adam L, Kamat A, Siefker-Radtke A, Dinney C. Role of epithelial-to-mesenchymal transition (EMT) in drug sensitivity and metastasis in bladder cancer. Cancer metastasis reviews. 2009; 28:335-344
21. Dinney CP, Fishbeck R, Singh RK, Eve B, Pathak S, Brown N, Xie B, Fan D, Bucana CD, Fidler IJ, et al. Isolation and characterization of metastatic variants from human transitional cell carcinoma passaged by orthotopic implantation in athymic nude mice. The Journal of urology. 1995; 154:1532-1538
22. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, Concannon KF, Donaldson MC, Sequist LV, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013; 339:580-584
23. Hwu D, Boutrus S, Greiner C, DiMeo T, Kuperwasser C, Georgakoudi I. Assessment of the role of circulating breast cancer cells in tumor formation and metastatic potential using in vivo flow cytometry. Journal of biomedical optics. 2011; 16:040501
24. Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, Velculescu VE, Kinzler KW, Vogelstein B, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature. 2010; 467:1114-1117
25. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, Arteaga CL, Moses HL. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Molecular biology of the cell. 2001; 12:27-36
26. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelialmesenchymal cell transition. Molecular biology of the cell. 2005; 16:1987-2002
27. Hurley PJ, Marchionni L, Simons BW, Ross AE, Peskoe SB, Miller RM, Erho N, Vergara IA, Ghadessi M, Huang Z, Gurel B, Park BH, Davicioni E, et al. Secreted protein, acidic and rich in cysteine-like 1 (SPARCL1) is down regulated in aggressive prostate cancers and is prognostic for poor clinical outcome. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109:14977-14982
28. Gohji K, Nakajima M, Dinney C, Fan D, Pathak S, Killion J, Voneschenbach A, Fidler I. The importance of orthotopic implantation to the isolation and biological characterization of a metastatic human clear cell renal-carcinoma in nudemice. International journal of oncology. 1993; 2:23-32
29. Stephenson RA, Dinney CP, Gohji K, Ordonez NG, Killion JJ, Fidler IJ. Metastatic model for human prostate cancer using orthotopic implantation in nude mice. Journal of the National Cancer Institute. 1992; 84:951-957
30. Harding MA, Arden KC, Gildea JW, Gildea JJ, Perlman EJ, Viars C, Theodorescu D. Functional genomic comparison of lineage-related human bladder cancer cell lines with differing tumorigenic and metastatic potentials by spectral karyotyping, comparative genomic hybridization, and a novel method of positional expression profiling. Cancer research. 2002; 62:6981-6989
31. Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, Williams ED. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer research. 2006; 66:11271-11278
32. Krasnapolski MA, Todaro LB, de Kier Joffe EB. Is the epithelial-to-mesenchymal transition clinically relevant for the cancer patient? Current pharmaceutical biotechnology. 2011; 12:1891-1899
33. Brabletz T. EMT and MET in metastasis: where are the cancer stem cells? Cancer cell. 2012; 22:699-701
34. Fidler IJ, Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science. 1977; 197:893-895
35. Fidler IJ, Ellis LM. The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell. 1994; 79:185-188
36. Jaggupilli A, Elkord E. Significance of CD44 and CD24 as cancer stem cell markers: an enduring ambiguity. Clinical & developmental immunology. 2012; 2012:708036
37. Pecot CV, Bischoff FZ, Mayer JA, Wong KL, Pham T, Bottsford-Miller J, Stone RL, Lin YG, Jaladurgam P, Roh JW, Goodman BW, Merritt WM, Pircher TJ, et al. A novel platform for detection of CK+ and CK-CTCs. Cancer discovery. 2011; 1:580-586
38. Armstrong AJ, Marengo MS, Oltean S, Kemeny G, Bitting RL, Turnbull JD, Herold CI, Marcom PK, George DJ, Garcia-Blanco MA. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Molecular cancer research. 2011; 9:997-1007
39. Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelialmesenchymal-like transition and promotes metastasis. Cancer cell. 2011; 20:576-590
40. Zheng X, Carstens JL, Kim J, Scheible M, Kaye J, Sugimoto H, Wu CC, LeBleu VS, Kalluri R. Epithelial-tomesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015; 527:525-530
41. Fischer KR, Durrans A, Lee S, Sheng J, Li F, Wong ST, Choi H, El Rayes T, Ryu S, Troeger J, Schwabe RF, Vahdat LT, Altorki NK, et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature. 2015; 527:472-476
42. Wang H, Zhang C, Xu L, Zang K, Ning Z, Jiang F, Chi H, Zhu X, Meng Z. Bufalin suppresses hepatocellular carcinoma invasion and metastasis by targeting HIF-1a via the PI3K/AKT/mTOR pathway. Oncotarget. 2016; 7:20193-208. doi: 10.18632/oncotarget.7935
43. Li Q, Liu Z, Xu M, Xue Y, Yao B, Dou C, Jia Y, Wang Y, Tu K, Zheng X, Yao Y. PCAF inhibits hepatocellular carcinoma metastasis by inhibition of epithelial-mesenchymal transition by targeting Gli-1. Cancer letters. 2016; 375:190-8
44. Chang C, Yu J, Hsieh Y, Yao C, Chao J, Chen P, Hsieh H, Hsiung C, Chu H, Shen C, Cheng C. MicroRNA-30a increases tight junction protein expression to suppress the epithelial-mesenchymal transition and metastasis by targeting Slug in breast cancer. Oncotarget. 2016; 7:16462-78. doi: 10.18632/oncotarget.7656
45. Lv YF, Dai H, Yan GN, Meng G, Zhang X, Guo QN. Downregulation of tumor suppressing STF cDNA 3 promotes epithelial-mesenchymal transition and tumor metastasis of osteosarcoma by the Wnt/GSK-3beta/betacatenin/Snail signaling pathway. Cancer letters. 2016; 373:164-173
46. Subramani R, Gonzalez E, Arumugam A, Nandy S, Gonzalez V, Medel J, Camacho F, Ortega A, Bonkoungou S, Narayan M, Dwivedi AK, Lakshmanaswamy R. Nimbolide inhibits pancreatic cancer growth and metastasis through ROS-mediated apoptosis and inhibition of epithelial-tomesenchymal transition. Scientific reports. 2016; 6:19819
47. Madersbacher S, Hochreiter W, Burkhard F, Thalmann GN, Danuser H, Markwalder R, Studer UE. Radical cystectomy for bladder cancer today-a homogeneous series without neoadjuvant therapy. Journal of clinical oncology. 2003; 21:690-696
48. Goss PE, Chambers AF. Does tumour dormancy offer a therapeutic target? Nature reviews Cancer. 2010; 10:871-877
49. Garber K. Epithelial-to-mesenchymal transition is important to metastasis, but questions remain. Journal of the National Cancer Institute. 2008; 100:232-233, 239
50. Guzzo TJ, McNeil BK, Bivalacqua TJ, Elliott DJ, Sokoll LJ, Schoenberg MP. The presence of circulating tumor cells does not predict extravesical disease in bladder cancer patients prior to radical cystectomy. Urologic oncology. 2012; 30:44-48
51. Naoe M, Ogawa Y, Morita J, Omori K, Takeshita K, Shichijyo T, Okumura T, Igarashi A, Yanaihara A, Iwamoto S, Fukagai T, Miyazaki A, Yoshida H. Detection of circulating urothelial cancer cells in the blood using the CellSearch System. Cancer. 2007; 109:1439-1445
52. Rink M, Chun FK, Dahlem R, Soave A, Minner S, Hansen J, Stoupiec M, Coith C, Kluth LA, Ahyai SA, Friedrich MG, Shariat SF, Fisch M, et al. Prognostic role and HER2 expression of circulating tumor cells in peripheral blood of patients prior to radical cystectomy: a prospective study. European urology. 2012; 61:810-817
53. Gupta V, Jafferji I, Garza M, Melnikova VO, Hasegawa DK, Pethig R, Davis DW. ApoStream(), a new dielectrophoretic device for antibody independent isolation and recovery of viable cancer cells from blood. Biomicrofluidics. 2012; 6:24133
54. Desitter I, Guerrouahen BS, Benali-Furet N, Wechsler J, Janne PA, Kuang Y, Yanagita M, Wang L, Berkowitz JA, Distel RJ, Cayre YE. A new device for rapid isolation by size and characterization of rare circulating tumor cells. Anticancer research. 2011; 31:427-441
55. Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, Bartlett BR, Wang H, Luber B, Alani RM, Antonarakis ES, Azad NS, Bardelli A, et al. Detection of circulating tumor DNA in early-and late-stage human malignancies. Science translational medicine. 2014; 6:224ra224
56. Kobayashi T, Owczarek TB, McKiernan JM, Abate-Shen C. Modelling bladder cancer in mice: opportunities and challenges. Nature reviews Cancer. 2014; 15:42-54
57. Marquis L, Tran M, Choi W, Lee IL, Huszar D, Siefker-Radtke A, Dinney C, McConkey DJ. p63 expression correlates with sensitivity to the Eg5 inhibitor ZD4877 in bladder cancer cells. Cancer biology & therapy. 2012; 13:477-486
58. Wang J, Duncan D, Shi Z, Zhang B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic acids research. 2013; 41:W77-83
59. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America. 1998; 95:14863-14868