MiR-34a is an intracellular and exosomal predictive biomarker for response to docetaxel with clinical relevance to prostate cancer progression

Prostate

Volumn 74, Issue 13, 2014, Pages 1320-1334

  Corcoran, Claire ^a   Rani, Sweta ^a   O'Driscoll, Lorraine ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

BCL 2; biomarkers; docetaxel resistance; exosomes; microRNA; miR 34a; prostate cancer

Indexed keywords

BCL-2; BIOMARKERS; DOCETAXEL-RESISTANCE; EXOSOMES; MICRORNA; MIR-34A; PROSTATE CANCER;

ANTINEOPLASTIC AGENTS; BIOLOGICAL MARKERS; CELL LINE, TUMOR; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; EXOSOMES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICRORNAS; PROGNOSIS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; SURVIVAL RATE; TAXOIDS; TREATMENT OUTCOME;

EID: 84905902711     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.22848     Document Type: Article

References (64)

1. Catalona WJ, Smith DS, Ratliff TL, Dodds KM, Coplen DE, Yuan JJ, Petros JA, Andriole GL,. Measurement of prostate-specific antigen in serum as a screening test for prostate cancer. N Engl J Med 1991; 324 (17): 1156-1161.
2. Gjertson CK, Albertsen PC,. Use and assessment of PSA in prostate cancer. Med Clin North Am 2011; 95 (1): 191-200.
3. Galsky MD, Vogelzang NJ,. Docetaxel-based combination therapy for castration-resistant prostate cancer. Ann Oncol 2010; 21 (11): 2135-2144.
4. Berthold DR, Sternberg CN, Tannock IF,. Management of advanced prostate cancer after first-line chemotherapy. J Clin Oncol 2005; 23 (32): 8247-8252.
5. Munoz M, Henderson M, Haber M, Norris M,. Role of the MRP1/ABCC1 multidrug transporter protein in cancer. IUBMB Life 2007; 59 (12): 752-757.
6. Corcoran C, Rani S, O'Brien K, O'Neill A, Prencipe M, Sheikh R, Webb G, McDermott R, Watson W, Crown J, O'Driscoll L,. Docetaxel-resistance in prostate cancer: Evaluating associated phenotypic changes and potential for resistance transfer via exosomes. PLoS ONE 2012; 7 (12): e50999.
7. O'Neill AJ, Prencipe M, Dowling C, Fan Y, Mulrane L, Gallagher WM, O'Connor D, O'Connor R, Devery A, Corcoran C, Rani S, O'Driscoll L, Fitzpatrick JM, Watson RW,. Characterisation and manipulation of docetaxel resistant prostate cancer cell lines. Mol Cancer 2011; 10: 126.
8. Corcoran C, Friel AM, Duffy MJ, Crown J, O'Driscoll L,. Intracellular and extracellular microRNAs in breast cancer. Clin Chem 2011; 57 (1): 18-32.
9. Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, Benjamin H, Kushnir M, Cholakh H, Melamed N, Bentwich Z, Hod M, Goren Y, Chajut A,. Serum microRNAs are promising novel biomarkers. PLoS ONE 2008; 3 (9): e3148.
10. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO,. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9 (6): 654-659.
11. Rabinowits G, Gerçel-Taylor C, Day J, Taylor D, Kloecker G,. Exosomal microRNA: A diagnostic marker for lung cancer. Clin Lung Cancer 2009; 10 (1): 42-46.
12. Xiao D, Ohlendorf J, Chen Y, Taylor DD, Rai SN, Waigel S, Zacharias W, Hao H, McMasters KM,. Identifying mRNA, microRNA and protein profiles of melanoma exosomes. PLoS ONE 2012; 7 (10): e46874.
13. O'Brien K, Rani S, Corcoran C, Wallace R, Hughes L, Friel AM, McDonnell S, Crown J, Radomski MW, O'Driscoll L,. Exosomes from triple-negative breast cancer cells can transfer phenotypic traits representing their cells of origin to secondary cells. Eur J Cancer 2013; 49 (8): 1845-1859.
14. McCready J, Sims JD, Chan D, Jay DG,. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: A role for plasminogen activation. BMC Cancer 2010; 10: 294.
15. Lässer C, Eldh M, Lötvall J,. Isolation and characterization of RNA-containing exosomes. J Vis Exp 2012; (59): e3037.
16. Shtanko O, Watanabe S, Jasenosky LD, Watanabe T, Kawaoka Y,. ALIX/AIP1 is required for NP incorporation into Mopeia virus Z-induced virus-like particles. J Virol 2011; 85 (7): 3631-3641.
17. Fernández-Llama P, Khositseth S, Gonzales PA, Star RA, Pisitkun T, Knepper MA,. Tamm-Horsfall protein and urinary exosome isolation. Kidney Int 2010; 77 (8): 736-742.
18. Guescini M, Genedani S, Stocchi V, Agnati LF,. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J Neural Transm 2010; 117 (1): 1-4.
19. Hennessy E, O'Driscoll L,. MicroRNA expression analysis: Techniques suitable for studies of intercellular and extracellular microRNAs. Methods Mol Biol 2011; 784: 99-107.
20. Antonov AV, Knight RA, Melino G, Barlev NA, Tsvetkov PO,. MIRUMIR: An online tool to test microRNAs as biomarkers to predict survival in cancer using multiple clinical data sets. Cell Death Differ 2013; 20 (2): 367.
21. Dweep H, Sticht C, Pandey P, Gretz N,. miRWalk-database: Prediction of possible miRNA binding sites by "walking" the genes of three genomes. J Biomed Inform 2011; 44 (5): 839-847.
22. Théry C, Ostrowski M, Segura E,. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9 (8): 581-593.
23. Rani S, O'Brien K, Kelleher FC, Corcoran C, Germano S, Radomski MW, Crown J, O'Driscoll L,. Isolation of exosomes for subsequent mRNA, MicroRNA, and protein profiling. Methods Mol Biol 2011; 784: 181-195.
24. Bruce JY, Lang JM, McNeel DG, Liu G,. Current controversies in the management of biochemical failure in prostate cancer. Clin Adv Hematol Oncol 2012; 10 (11): 716-722.
25. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR,. MicroRNA expression profiles classify human cancers. Nature 2005; 435 (7043): 834-838.
26. Calin GA, Croce CM,. MicroRNA signatures in human cancers. Nat Rev Cancer 2006; 6 (11): 857-866.
27. Ma J, Dong C, Ji C,. MicroRNA and drug resistance. Cancer Gene Ther 2010; 17 (8): 523-531.
28. Taylor D, Gercel-Taylor C,. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110 (1): 13-21.
29. Skog J, Würdinger T, van Rijn S, Meijer D, Gainche L, Sena-Esteves M, Curry WJ, Carter B, Krichevsky A, Breakefield X,. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10 (12): 1470-1476.
30. Hunter M, Ismail N, Zhang X, Aguda B, Lee E, Yu L, Xiao T, Schafer J, Lee M, Schmittgen T, Nana-Sinkam S, Jarjoura D, Marsh C,. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 2008; 3 (11): e3694.
31. Pigati L, Yaddanapudi SC, Iyengar R, Kim DJ, Hearn SA, Danforth D, Hastings ML, Duelli DM,. Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS ONE 2010; 5 (10): e13515.
32. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González M, Bernad A, Sánchez-Madrid F,. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011; 2: 282.
33. Lin SL, Chiang A, Chang D, Ying SY,. Loss of mir-146a function in hormone-refractory prostate cancer. RNA 2008; 14 (3): 417-424.
34. Xu B, Feng NH, Li PC, Tao J, Wu D, Zhang ZD, Tong N, Wang JF, Song NH, Zhang W, Hua LX, Wu HF,. A functional polymorphism in pre-miR-146a gene is associated with prostate cancer risk and mature miR-146a expression in vivo. Prostate 2010; 70 (5): 467-472.
35. Xu B, Wang N, Wang X, Tong N, Shao N, Tao J, Li P, Niu X, Feng N, Zhang L, Hua L, Wang Z, Chen M,. MiR-146a suppresses tumor growth and progression by targeting EGFR pathway and in a p-ERK-dependent manner in castration-resistant prostate cancer. Prostate 2012; 72 (11): 1171-1178.
36. Fujita Y, Kojima K, Ohhashi R, Hamada N, Nozawa Y, Kitamoto A, Sato A, Kondo S, Kojima T, Deguchi T, Ito M,. MiR-148a attenuates paclitaxel resistance of hormone-refractory, drug-resistant prostate cancer PC3 cells by regulating MSK1 expression. J Biol Chem 2010; 285 (25): 19076-19084.
37. Murata T, Takayama K, Katayama S, Urano T, Horie-Inoue K, Ikeda K, Takahashi S, Kawazu C, Hasegawa A, Ouchi Y, Homma Y, Hayashizaki Y, Inoue S,. miR-148a is an androgen-responsive microRNA that promotes LNCaP prostate cell growth by repressing its target CAND1 expression. Prostate Cancer Prostatic Dis 2010; 13 (4): 356-361.
38. Pogribny IP, Filkowski JN, Tryndyak VP, Golubov A, Shpyleva SI, Kovalchuk O,. Alterations of microRNAs and their targets are associated with acquired resistance of MCF-7 breast cancer cells to cisplatin. Int J Cancer 2010; 127 (8): 1785-1794.
39. Tomokuni A, Eguchi H, Tomimaru Y, Wada H, Kawamoto K, Kobayashi S, Marubashi S, Tanemura M, Nagano H, Mori M, Doki Y,. miR-146a suppresses the sensitivity to interferon-α in hepatocellular carcinoma cells. Biochem Biophys Res Commun 2011; 414 (4): 675-680.
40. Hummel R, Watson DI, Smith C, Kist J, Michael MZ, Haier J, Hussey DJ,. Mir-148a improves response to chemotherapy in sensitive and resistant oesophageal adenocarcinoma and squamous cell carcinoma cells. J Gastrointest Surg 2011; 15 (3): 429-438.
41. Yamamura S, Saini S, Majid S, Hirata H, Ueno K, Deng G, Dahiya R,. MicroRNA-34a modulates c-Myc transcriptional complexes to suppress malignancy in human prostate cancer cells. PLoS ONE 2012; 7 (1): e29722.
42. Kong D, Heath E, Chen W, Cher M, Powell I, Heilbrun L, Li Y, Ali S, Sethi S, Hassan O, Hwang C, Gupta N, Chitale D, Sakr WA, Menon M, Sarkar FH,. Epigenetic silencing of miR-34a in human prostate cancer cells and tumor tissue specimens can be reversed by BR-DIM treatment. Am J Transl Res 2012; 4 (1): 14-23.
43. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG,. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 2011; 17 (2): 211-215.
44. Fujita Y, Kojima K, Hamada N, Ohhashi R, Akao Y, Nozawa Y, Deguchi T, Ito M,. Effects of miR-34a on cell growth and chemoresistance in prostate cancer PC3 cells. Biochem Biophys Res Commun 2008; 377 (1): 114-119.
45. Kastl L, Brown I, Schofield AC,. miRNA-34a is associated with docetaxel resistance in human breast cancer cells. Breast Cancer Res Treat 2012; 131 (2): 445-454.
46. Vinall RL, Ripoll AZ, Wang S, Pan CX, deVere White RW,. MiR-34a chemosensitizes bladder cancer cells to cisplatin treatment regardless of p53-Rb pathway status. Int J Cancer 2012; 130 (11): 2526-2538.
47. Kojima K, Fujita Y, Nozawa Y, Deguchi T, Ito M,. MiR-34a attenuates paclitaxel-resistance of hormone-refractory prostate cancer PC3 cells through direct and indirect mechanisms. Prostate 2010; 70 (14): 1501-1512.
48. Yang F, Li QJ, Gong ZB, Zhou L, You N, Wang S, Li XL, Li JJ, An JZ, Wang DS, He Y, Dou KF,. MicroRNA-34a targets Bcl-2 and sensitizes human hepatocellular carcinoma cells to sorafenib treatment. Technol Cancer Res Treat 2014; 13 (1): 77-86.
49. Haarman EG, Kaspers GJ, Pieters R, van Zantwijk CH, Broekema GJ, Hählen K, Veerman AJ,. BCL-2 expression in childhood leukemia versus spontaneous apoptosis, drug induced apoptosis, and in vitro drug resistance. Adv Exp Med Biol 1999; 457: 325-333.
50. Borgovan T, Bellistri JP, Slack KN, Kopelovich L, Desai M, Joe AK,. Inhibition of BCL2 expression and activity increases H460 sensitivity to the growth inhibitory effects of polyphenon E. J Exp Ther Oncol 2009; 8 (2): 129-144.
51. Volm M, Mattern J,. Increased expression of bcl-2 in drug-resistant squamous-cell lung carcinomas. Int J Oncol 1995; 7 (6): 1333-1338.
52. Di Martino MT, Leone E, Amodio N, Foresta U, Lionetti M, Pitari MR, Cantafio ME, Gullà A, Conforti F, Morelli E, Tomaino V, Rossi M, Negrini M, Ferrarini M, Caraglia M, Shammas MA, Munshi NC, Anderson KC, Neri A, Tagliaferri P, Tassone P,. Synthetic miR-34a mimics as a novel therapeutic agent for multiple myeloma: In vitro and in vivo evidence. Clin Cancer Res 2012; 18 (22): 6260-6270.
53. Nakatani F, Ferracin M, Manara MC, Ventura S, Del Monaco V, Ferrari S, Alberghini M, Grilli A, Knuutila S, Schaefer KL, Mattia G, Negrini M, Picci P, Serra M, Scotlandi K,. miR-34a predicts survival of Ewing's sarcoma patients and directly influences cell chemo-sensitivity and malignancy. J Pathol 2012; 226 (5): 796-805.
54. Weeraratne SD, Amani V, Neiss A, Teider N, Scott DK, Pomeroy SL, Cho YJ,. miR-34a confers chemosensitivity through modulation of MAGE-A and p53 in medulloblastoma. Neuro Oncol 2011; 13 (2): 165-175.
55. Ye Q, Wang TF, Peng YF, Xie J, Feng B, Qiu MY, Li LH, Lu AG, Liu BY, Zheng MH,. Expression of alpha-, beta- and gamma-synuclein in colorectal cancer, and potential clinical significance in progression of the disease. Oncol Rep 2010; 23 (2): 429-436.
56. Matsuo Y, Kamitani T,. Parkinson's disease-related protein, alpha-synuclein, in malignant melanoma. PLoS ONE 2010; 5 (5): e10481.
57. Bruening W, Giasson BI, Klein-Szanto AJ, Lee VM, Trojanowski JQ, Godwin AK,. Synucleins are expressed in the majority of breast and ovarian carcinomas and in preneoplastic lesions of the ovary. Cancer 2000; 88 (9): 2154-2163.
58. Fung KM, Rorke LB, Giasson B, Lee VM, Trojanowski JQ,. Expression of alpha-, beta-, and gamma-synuclein in glial tumors and medulloblastomas. Acta Neuropathol 2003; 106 (2): 167-175.
59. Wang Q, Bailey CG, Ng C, Tiffen J, Thoeng A, Minhas V, Lehman ML, Hendy SC, Buchanan G, Nelson CC, Rasko JE, Holst J,. Androgen receptor and nutrient signaling pathways coordinate the demand for increased amino acid transport during prostate cancer progression. Cancer Res 2011; 71 (24): 7525-7536.
60. Sakata T, Ferdous G, Tsuruta T, Satoh T, Baba S, Muto T, Ueno A, Kanai Y, Endou H, Okayasu I,. L-type amino-Acid transporter 1 as a novel biomarker for high-grade malignancy in prostate cancer. Pathol Int 2009; 59 (1): 7-18.
61. Kaira K, Toyoda M, Shino M, Sakakura K, Takahashi K, Tominaga H, Oriuchi N, Kanai Y, Oyama T, Chikamatsu K,. Clinicopathological significance of L-type amino acid transporter 1 (LAT1) expression in patients with adenoid cystic carcinoma. Pathol Oncol Res 2013; 19 (4): 649-656.
62. Mihály Z, Kormos M, Lánczky A, Dank M, Budczies J, Szász MA, Gyarffy B,. A meta-Analysis of gene expression-based biomarkers predicting outcome after tamoxifen treatment in breast cancer. Breast Cancer Res Treat 2013; 140 (2): 219-232.
63. 18F-FAMT PET and L-type amino acid transporter 1 (LAT1) expression in oral squamous cell carcinoma. Eur J Nucl Med Mol Imaging 2013; 40 (11): 1692-1700.
64. Yanagisawa N, Ichinoe M, Mikami T, Nakada N, Hana K, Koizumi W, Endou H, Okayasu I,. High expression of L-type amino acid transporter 1 (LAT1) predicts poor prognosis in pancreatic ductal adenocarcinomas. J Clin Pathol 2012; 65 (11): 1019-1023.