Genetic subtypes of invasive bladder cancer

Current Opinion in Urology

Volumn 25, Issue 5, 2015, Pages 449-458

  McConkey, David J ^a   Choi, Woonyoung ^a   Dinney, Colin P N ^a  

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

Author keywords

Basal; Claudin low; Epithelial to mesenchymal transition; Luminal; PDL1; TCGA

Indexed keywords

BIOLOGICAL MARKER; CISPLATIN; DNA; IPILIMUMAB; MESSENGER RNA; MPDL 3280A; ANTINEOPLASTIC AGENT; TUMOR MARKER;

ADJUVANT CHEMOTHERAPY; BREAST CANCER; CANCER GENETICS; CLINICAL TRIAL (TOPIC); COMBINATION CHEMOTHERAPY; CYSTECTOMY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOME; GENOMICS; HUMAN; MUSCLE INVASIVE BLADDER CANCER; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SYSTEMIC THERAPY; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; MOLECULAR DIAGNOSIS; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PERSONALIZED MEDICINE; PHENOTYPE; PREDICTIVE VALUE; PROCEDURES; TUMOR INVASION; URINARY BLADDER NEOPLASMS;

ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; MOLECULAR TARGETED THERAPY; NEOPLASM INVASIVENESS; PHENOTYPE; PRECISION MEDICINE; PREDICTIVE VALUE OF TESTS; RNA, MESSENGER; URINARY BLADDER NEOPLASMS;

EID: 84942591993     PISSN: 09630643     EISSN: 14736586     Source Type: Journal    
DOI: 10.1097/MOU.0000000000000200     Document Type: Review

References (58)

1. Golub TR, Slonim DK, Tamayo P, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 1999; 286:531-537.
2. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000; 403:503-511.
3. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature 2000; 406:747-752.
4. Prat A, Parker JS, Karginova O, Perou CM. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010; 12:R68.
5. Taube JH, Herschkowitz JI, Komurov K, et al. Core epithelial-to-mesenchymal tra nsition interactome gene-expression signature is associated with claudinlow and metaplastic breast cancer subtypes. Proc Natl Acad Sci U S A 2010; 107:15449-15454.
6. Prat A, Ellis MJ, Perou CM. Practical implications of gene-expression-based assays for breast oncologists. Nat Rev Clin Oncol 2012; 9:48-57.
7. Cancer Genome Atlas N. Compre hensive molecular portraits of human breast, tumours. Nature 2012; 490:61-70.
8. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis Genes Dev 2009 23 2563-2577.
9. Prater MD, Petit V, Alasdair Russell I, et al. Mammary stem cells have myoepithelial cell properties. Nat Cell Biol 2014; 16:942-950; 941-947.
10. Sale S, Lafkas D, Artavanis-Tsakonas S. Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages. Nat Cell Biol 2013; 15:451-460.
11. Wang D, Cai C, Dong X, et al. Identification of multipotent mammary stem cells by protein C receptor expression. Nature 2015; 517:81-84.
12. Sorlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas di stinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001; 98:10869-10874.
13. Rehman FL, Lord CJ, Ashworth A. The promise of combining inhibition of PI3K and PARP as cancer therapy. Cancer Discov 2012; 2:982-984.
14. Blaveri E, Simko JP, Korkola JE, et al. Bladder cancer outcome and subtype classification by gene expression. Clin Cancer Res 2005; 11:4044-4055.
15. Dyrskjot L, Thykjaer T, Kruhoffer M, et al. Identifying distinct classes of bladder carcinoma using microarrays. Nat Genet 2003; 33:90-96.
16. Sanchez-Carbayo M, Socci ND, Lozano J, et al. Defining molec ular profiles of poor outcome in patients with invasive bladder cancer using oligonucleotide microarrays. J Clin Oncol 2006; 24:778-789.
17. Lindgren D, Frigyesi A, Gudjonsson S, et al. Combined gene expression and genomic profiling define two intrinsic molecular subtypes of urothelial carcinoma and gene signatures for molecular grading and outcome. Cancer Res 2010; 70:3463-3472.
18. Sjodahl G, Lauss M, Lo vgren K, et al. A molecular taxonomy for urothelial carcinoma. Clin Cancer Res 2012; 18:3377-3386. First identification of the intrinsic subtypes of bladder cancer. The Lund subtypes were largely reproduced in the more recen t efforts, which showed that they shared similarities with the intrinsic subtypes of breast cancer.
19. Volkmer JP, Sahoo D, Chin RK, et al. Three differentiation states risk-stratify bladder cancer into distinct subtypes. Proc Natl Acad Sci U S A 2012; 109:2078-2083.
20. Choi W, Shah JB, Tran M, et al. p63 expression defines a lethal subset of muscle-invasive bladder cancers. PLoS One 2012; 7:e30206.
21. Karni-Schmidt O, Castillo-Martin M, Shen TH, et al. Distinct expression profiles of p63 variants during urothelial development and bladder cancer progression. Am J Pathol 2011; 178: 1350-1360.
22. Cancer Genome Atlas Research N. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 2014; 507:315-322. One of four recent studies that documented the shared propertie s of the intrinsic subtypes of muscle-invasive bladder and breast cancers. This project provided the first high-quality, comprehensive inventory of genetic and epigenetic features of muscle-invasive bladder cancers, which has already become a major resour ce for the research community.
23. Choi W, Porten S, Kim S, et al. Identification of distinct basal and luminal subtypes of muscle-invasive bladder cancer with different sensitivities to frontline chemotherapy. Cancer Cell 2014; 25:152-165. One of four recent studies that documented the shared properties of the intrinsic subtypes of muscle-invasive bladder and breast cancers. This study also showed that tumors in one of the subtypes ('p53-like'), corresponding to the Lund ' infiltrated' tumors and TCGA's cluster II, were resistant to neoadjuvant chemotherapy.
24. Damrauer JS, Hoadley KA, Chism DD, et al. Intrinsic subtypes of high-grade bladder cancer reflect the hallmarks of breast cancer biology. Proc Natl Acad Sci U S A 2014; 111:3110-3115. One of four recent studies that documented the shared properties of the intrinsic subtypes of muscle-invasive bladder and breast cancers. The group from UNC also documented the existence of a m esenchymal, ' claudin-low' subset of basal cancers.
25. Choi W, Czerniak B, Ochoa A, et al. Intrinsic basal and luminal subtypes of muscle-invasive bladder cancer. Nat Rev Urol 2014; 11:400-410.
26. McConkey DJ, ChoiW, Dinney CP. New insights into subtypes of invasive bladder cancer: considerations of the clinician. Eur Urol 2014; 66: 609-610.
27. Rebouissou S,Bernard-Pierrot I,de Reynies A,et al. EGFR as a potential therapeutic target for a subset of muscle-invasive bladder cancers presenting a basal-like phenotype Sci Transl Med 2014 6:244ra291. One of four recent studies that docume n ted the shared properties of the intrinsic subtypes of muscle-invasive bladder and breast cancers. The paper also presented strong preclinical evidence for targeting EGFR in basal cancers.
28. Chan KS, Espinosa I, Chao M, et al. Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci U S A 2009; 106:14016-14021.
29. Hoadley KA, Yau C, Wolf DM, et al. Multiplatform analysis of 12 cancer types reveals molecular classification within and across tissues of origin. Cell 2014; 158:929-944 . The study used TCGA's genomics data from 12 different cancers to document the similarities between basal bladder cancers and basal breast cancers, and revealed that they are even more similar to squamous cancers of the lung and head and neck. The study also confirmed that high level expression of DNp63a is a central feature of these cancers.
30. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009; 9:265-273.
31. Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133:704-715.
32. Ho PL, Lay EJ, Jian W, et al. Stat3 activation in urothelial stem cells leads to direct progression to invasive bladder cancer. Cancer Res 2012; 72:3135-3142.
33. Ho PL, Kurtova A, Chan KS. Normal and neoplastic urothelial stem cells: getting to the root of the problem. Nat Rev Urol 2012; 9:583-594.
34. Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARg. Annu Rev Biochem 2008; 77:289-312.
35. Biton A, Bernard-Pierrot I, Lou Y, et al. Independent component analysis uncovers the landscape of the bladder tumor transcriptome a nd reveals insights into luminal and basal subtypes. Cell Rep 2014; 9:1235-1245. Identified the transcriptional mechanisms underlying basal and luminal gene expression and identified PPARG as a candidate therapeutic target in luminal bladder cancers.
36. Dominick MA, WhiteMR, Sanderson TP, et al. Urothelial carcinogenesis in the urinary bladder of male rats treated with muraglitazar, a PPARa/g agonist: evidence for urolithiasis as the inciting event in the mode of action. Toxicol Pathol 2006; 34:903-920.
37. Egerod FL,Brunner N,Svendsen JE,Oleksiewicz MB. PPARa and PPARg are co-expressed, functional and show positive interactions in the rat ur inary bladder urothelium J Appl Toxicol 2010 30 151-162.
38. Faillie JL, Petit P, Montastruc JL, Hillaire-Buys D. Scientific evidence and controversies about pioglitazone and bladder cancer: which lessons can be drawn? Drug Saf 2013. [Epub ahead of print]
39. McConkey DJ, Choi W, Ochoa A, et al. Therapeutic opportunities in the intrinsic subtypes of muscle-invasive bladder cancer. Hematol Oncol Clin North Am 2015; 29:377-394.
40. Dinney CP, Hansel D, McConkey D, et al. Novel neoadjuvant therapy paradigms for bladder cancer: results from the National Cancer Center Institute Forum. Urol Oncol 2014; 32:1108-1115.
41. Prowell TM, Pa zdur R. Pathological complete response and accelerated drug approval in early breast cancer. N Engl J Med 2012; 366:2438-2441.
42. Kurtova AV, Xiao J, Mo Q, et al. Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance. Nature 2015; 517:209-213. Provided strong preclinical evidence for a role for basal/stem-li ke cancer cells in recurrence and for using COX2 inhibitors with chemotherapy.
43. Harrington EA, Fanidi A, Evan GI. Oncogenes and cell death. Curr Opin Genet Dev 1994; 4:120-129.
44. Jackson JG, Pant V, Li Q, et al. p53-mediated senescence impairs the apoptotic response to chemotherapy and clinical outcome in breast cancer. Cancer Cell 2012; 21:793-806.
45. Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 2015; 27:450-461.
46. Carthon BC, Wolchok JD, Yuan J, et al. Preoperat ive CTLA-4 blockade: tolerability and immune monitoring in the setting of a presurgical clinical trial. Clin Cancer Res 2010; 16:2861-2871.
47. Wolchok JD, Chan TA. Cancer: Antitumour immunity gets a boost. Nature 2014; 515:496-498.
48. Powles T,Eder JP,FineGD et al.MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer Nature 2014 515 558-562. Demons trated that immune checkpoint blockade is clinically active in refractory muscle-invasive bladder cancers. Catalyzed a huge wave of enthusiasm for the further evaluation of checkpoint blockade in both nonmuscle invasive and muscleinvasive bladder cancers.
49. Adam L, Zhong M, Choi W, et al. miR-200 expression regulates epithelial-tomesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res 2 009; 15:5060-5072.
50. Black PC, Brown GA, Inamoto T, et al. Sensitivity to epidermal growth factor receptor inhibitor requires E-cadherin expression in urothelial carcinoma cells. Clin Cancer Res 2008; 14:1478-1486.
51. Witta SE, Gemmill RM, Hirsch FR, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cance r Res 2006; 66:944-950.
52. Zhu K, Chan W, Heymach J, et al. Control of HIF-1a expression by eIF2 alpha phosphorylation-mediated translational repression. Cancer Res 2009; 69: 1836-1843.
53. Semenza GL. HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations. J Clin Invest 2013; 123:3664-3671.
54. Kaelin WGJr. The von Hippel-Lin dau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer 2008; 8:865-873.
55. Wong YN, Litwin S, Vaughn D, et al. Phase II trial of cetuximab with or without paclitaxel in patients wi th advanced urothelial tract carcinoma. J Clin Oncol 2012; 30:3545-3551.
56. Hahn NM, Stadler WM, Zon RT, et al. Phase II trial of cisplatin, gemcitabine, and bevacizumab as first-line therapy for metastatic urothelial carcinoma: Hoosier Oncology Group GU 04-75. J Clin Oncol 2011; 29:1525-1530.
57. Iyer G, Hanrahan AJ, Milowsky MI, et al.Genome sequencing identifies a basis for ever olimus sensitivity. Science 2012; 338:221.
58. Willis DL, F laig TW, Hansel DE, et al. Micropapillary bladder cancer: current treatment patterns and review of the literature. Urol Oncol 2014; 32:826-832.