MicroRNAs induced in melanoma treated with combination targeted therapy of Temsirolimus and Bevacizumab

Journal of Translational Medicine

Volumn 11, Issue 1, 2013, Pages

  Wagenseller, Aubrey G ^a   Shada, Amber ^a   D'Auria, Kevin M ^a   Murphy, Cheryl ^a   Sun, Dandan ^a   Molhoek, Kerrington R ^a   Papin, Jason A ^a   Dutta, Anindya ^a   Slingluff, Craig L ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; BEVACIZUMAB; MICRORNA; MICRORNA 100; MICRORNA 10B; MICRORNA 125B; MICRORNA 140 3P; MICRORNA 145; MICRORNA 29C; MICRORNA 320A; MICRORNA 320B; MICRORNA 320C; MICRORNA 320D; MICRORNA 320E; MICRORNA 4328; MICRORNA 7B; MICRORNA 7C; MICRORNA 99A; RAPAMYCIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CLINICAL ARTICLE; CONCENTRATION (PARAMETERS); DISEASE ACTIVITY; DRUG EFFECT; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE INDUCTION; GENE MUTATION; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MELANOMA; MICROARRAY ANALYSIS; MOLECULARLY TARGETED THERAPY; ONCOGENE; PHASE 2 CLINICAL TRIAL (TOPIC); TREATMENT RESPONSE; UPREGULATION;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MICRORNAS; MOLECULAR TARGETED THERAPY; PILOT PROJECTS; PROTO-ONCOGENE PROTEINS B-RAF; REPRODUCIBILITY OF RESULTS; SIROLIMUS;

EID: 84884200479     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-11-218     Document Type: Article

References (60)

1. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011, 364:2507-2516.
2. Ko JM, Fisher DE. A new era: melanoma genetics and therapeutics. J Pathol 2011, 223:241-250.
3. Huang S, Houghton PJ. Targeting mTOR signaling for cancer therapy. Curr Opin Pharmacol 2003, 3:371-377.
4. Stahl JM, Sharma A, Cheung M, Zimmerman M, Cheng JQ, Bosenberg MW, Kester M, Sandirasegarane L, Robertson GP. Deregulated Akt3 activity promotes development of malignant melanoma. Cancer Res 2004, 64:7002-7010.
5. Guba M, von BP, Steinbauer M, Koehl G, Flegel S, Hornung M, Bruns CJ, Zuelke C, Farkas S, Anthuber M, et al. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat Med 2002, 8:128-135.
6. Molhoek KR, Griesemann H, Shu J, Gershenwald JE, Brautigan DL, Slingluff CL. Human melanoma cytolysis by combined inhibition of mTOR and VEGF/VEGFR-2. Cancer Res 2008, 68:4392-4397.
7. Margolin K, Longmate J, Baratta T, Synold T, Christensen S, Weber J, Gajewski T, Quirt I, Doroshow JH. CCI-779 in metastatic melanoma: a phase II trial of the California Cancer Consortium. Cancer 2005, 104:1045-1048.
8. Molhoek KR, Shada AL, Smolkin M, Chowbina S, Papin J, Brautigan DL, Slingluff CL. Comprehensive analysis of receptor tyrosine kinase activation in human melanomas reveals autocrine signaling through IGF-1R. Melanoma Res 2011, 21:274-284.
9. Molhoek KR, Erdag G, Rasamny J, Murphy C, Deacon D, Patterson JW, Slingluff CL, Brautigan DL. VEGFR-2 expression in human melanoma: revised assessment. Int J Cancer 2011, 129:2807-2815.
10. Varker KA, Biber JE, Kefauver C, Jensen R, Lehman A, Young D, Wu H, Lesinski GB, Kendra K, Chen HX, et al. A randomized phase 2 trial of Bevacizumab with or without daily low-dose interferon alfa-2b in metastatic malignant melanoma. Ann Surg Oncol 2007, 14:2367-2376.
11. Schuster C, Eikesdal HP, Puntervoll H, Geisler J, Geisler S, Heinrich D, Molven A, Lonning PE, Akslen LA, Straume O. Clinical efficacy and safety of Bevacizumab Monotherapy in patients with metastatic melanoma: predictive importance of induced early hypertension. PLoS One 2012, 7:e38364.
12. Slingluff CL, Petroni GR, Molhoek KR, Brautigan DL, Chianese-Bullock KA, Shada AL, Smolkin ME, Olson WC, Gaucher A, Chase CM, et al. Clinical activity and safety of combination therapy with temsirolimus and Bevacizumab for advanced melanoma: a phase II trial (CTEP 7190/ Mel47). Clin Cancer Res 2013, published online ahead of print.
13. Lee YS, Dutta A. MicroRNAs in cancer. Annu Rev Pathol 2009, 4:199-227. doi:10.1146/annurev.pathol.4.110807.092222.
14. Cheng AM, Byrom MW, Shelton J, Ford LP. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 2005, 33:1290-1297.
15. Ceppi P, Mudduluru G, Kumarswamy R, Rapa I, Scagliotti GV, Papotti M, Allgayer H. Loss of miR-200c expression induces an aggressive, invasive, and chemo resistant phenotype in non-small cell lung cancer. Mol Cancer Res 2010, 8:1207-1216.
16. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647.
17. Chen Z, Zeng H, Guo Y, Liu P, Pan H, Deng A, Hu J. miRNA-145 inhibits non-small cell lung cancer cell proliferation by targeting c-Myc. J Exp Clin Cancer Res 2010, 29:151. doi:10.1186/1756-9966-29-151.
18. Jiang S, Zhang HW, Lu MH, He XH, Li Y, Gu H, Liu MF, Wang ED. MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res 2010, 70:3119-3127.
19. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006, 6:857-866.
20. Segura MF, Greenwald HS, Hanniford D, Osman I, Hernando E. MicroRNA and cutaneous melanoma: from discovery to prognosis and therapy. Carcinogenesis 2012, 33:1823-1832.
21. Molhoek KR, Brautigan DL, Slingluff CL. Synergistic inhibition of human melanoma proliferation by combination treatment with B-Raf inhibitor BAY43-9006 and mTOR inhibitor Rapamycin. J Transl Med 2005, 3:39. 39.
22. Yamshchikov GV, Mullins DW, Chang CC, Ogino T, Thompson L, Pressley J, Galavotti H, Aquila W, Deacon D, Ross WG, et al. Sequential immune escape and shifting of T cell responses in a long-term survivor of melanoma. JI 2005, 174:6863-6871.
23. Darrow TL, Slingluff CLJ, Seigler HF. The role of HLA class I antigens in recognition of melanoma cells by tumor-specific cytotoxic T lymphocytes. Evidence for shared tumor antigens. JI 1989, 142:3329-3335.
24. Slingluff CL, Colella TA, Thompson L, Graham DD, Skipper JC, Caldwell J, Brinckerhoff L, Kittlesen DJ, Deacon DH, Oei C, et al. Melanomas with concordant loss of multiple melanocytic differentiation proteins: immune escape that may be overcome by targeting unique or undefined antigens. Cancer Immunol Immunother 2000, 48:661-672.
25. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98:5116-5121.
26. Wang FZ, Weber F, Croce C, Liu CG, Liao X, Pellett PE. Human cytomegalovirus infection alters the expression of cellular microRNA species that affect its replication. J Virol 2008, 82:9065-9074.
27. Glud M, Rossing M, Hother C, Holst L, Hastrup N, Nielsen FC, Gniadecki R, Drzewiecki KT. Downregulation of miR-125b in metastatic cutaneous malignant melanoma. Melanoma Res 2010, 20:479-484.
28. Glud M, Manfe V, Biskup E, Holst L, Dirksen AM, Hastrup N, Nielsen FC, Drzewiecki KT, Gniadecki R. MicroRNA miR-125b induces senescence in human melanoma cells. Melanoma Res 2011, 21:253-256.
29. Liang L, Wong CM, Ying Q, Fan DN, Huang S, Ding J, Yao J, Yan M, Li J, Yao M, et al. MicroRNA-125b suppressesed human liver cancer cell proliferation and metastasis by directly targeting oncogene LIN28B2. Hepatology 2010, 52:1731-1740.
30. Ling HY, Ou HS, Feng SD, Zhang XY, Tuo QH, Chen LX, Zhu BY, Gao ZP, Tang CK, Yin WD, et al. Changes in microRNA (miR) profile and effects of miR-320 in insulin-resistant 3T3-L1 adipocytes. Clin Exp Pharmacol Physiol 2009, 36:e32-e39.
31. Wang XH, Qian RZ, Zhang W, Chen SF, Jin HM, Hu RM. MicroRNA-320 expression in myocardial microvascular endothelial cells and its relationship with insulin-like growth factor-1 in type 2 diabetic rats. Clin Exp Pharmacol Physiol 2009, 36:181-188.
32. Duan H, Jiang Y, Zhang H, Wu Y. MiR-320 and miR-494 affect cell cycles of primary murine bronchial epithelial cells exposed to benzo[a]pyrene. Toxicol In Vitro 2010, 24:928-935.
33. Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 2007, 21:1025-1030.
34. Guo Y, Chen Y, Ito H, Watanabe A, Ge X, Kodama T, Aburatani H. Identification and characterization of lin-28 homolog B (LIN28B) in human hepatocellular carcinoma. Gene 2006, 384:51-61. Epub %2006 Jul 28.:51-61.
35. Schultz J, Lorenz P, Gross G, Ibrahim S, Kunz M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res 2008, 18:549-557.
36. Nguyen T, Kuo C, Nicholl MB, Sim MS, Turner RR, Morton DL, Hoon DS. Downregulation of microRNA-29c is associated with hypermethylation of tumor-related genes and disease outcome in cutaneous melanoma. Epigenetics 2011, 6:388-394.
37. Xiong Y, Fang JH, Yun JP, Yang J, Zhang Y, Jia WH, Zhuang SM. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 2010, 51:836-845.
38. Park SY, Lee JH, Ha M, Nam JW, Kim VN. miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol 2009, 16:23-29.
39. Martinez I, Cazalla D, Almstead LL, Steitz JA, DiMaio D. miR-29 and miR-30 regulate B-Myb expression during cellular senescence. Proc Natl Acad Sci USA 2011, 108:522-527.
40. Xu H, Cheung IY, Guo HF, Cheung NK. MicroRNA miR-29 modulates expression of immunoinhibitory molecule B7-H3: potential implications for immune based therapy of human solid tumors. Cancer Res 2009, 69:6275-6281.
41. Nagaraja AK, Creighton CJ, Yu Z, Zhu H, Gunaratne PH, Reid JG, Olokpa E, Itamochi H, Ueno NT, Hawkins SM, et al. A link between mir-100 and FRAP1/mTOR in clear cell ovarian cancer. Mol Endocrinol 2010, 24:447-463.
42. Sun D, Lee YS, Malhotra A, Kim HK, Matecic M, Evans C, Jensen RV, Moskaluk CA, Dutta A. miR-99 family of MicroRNAs suppresses the expression of prostate-specific antigen and prostate cancer cell proliferation. Cancer Res 2011, 71:1313-1324.
43. La RG, Badin M, Shi B, Xu SQ, Deangelis T, Sepp-Lorenzinoi L, Baserga R. Mechanism of growth inhibition by MicroRNA 145: the role of the IGF-I receptor signaling pathway. J Cell Physiol 2009, 220:485-491.
44. Kim SJ, Oh JS, Shin JY, Lee KD, Sung KW, Nam SJ, Chun KH. Development of microRNA-145 for therapeutic application in breast cancer. J Control Release 2011, 155:427-434.
45. Sun Y, Ge Y, Drnevich J, Zhao Y, Band M, Chen J. Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis. J Cell Biol 2010, 189:1157-1169.
46. Di LG, Croce CM. Roles of small RNAs in tumor formation. Trends Mol Med 2010, 16:257-267.
47. Hummel R, Wang T, Watson DI, Michael MZ, Van der Hoek M, Haier J, Hussey DJ. Chemotherapy-induced modification of microRNA expression in esophageal cancer. Oncol Rep 2011, 26:1011-1017.
48. Wang WL, Chatterjee N, Chittur SV, Welsh J, Tenniswood MP. Effects of 1alpha, 25 dihydroxyvitamin D3 and testosterone on miRNA and mRNA expression in LNCaP cells. Mol Cancer 2011, 10:58. doi: 10.1186/1476-4598-10-58.
49. Sampson VB, Rong NH, Han J, Yang Q, Aris V, Soteropoulos P, Petrelli NJ, Dunn SP, Krueger LJ. MicroRNA let-7a downregulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res 2007, 67:9762-9770.
50. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science 2008, 320:97-100.
51. Kantrow SM, Boyd AS, Ellis DL, Nanney LB, Richmond A, Shyr Y, Robbins JB. Expression of activated Akt in benign nevi, Spitz nevi and melanomas. J Cutan Pathol 2007, 34:593-596.
52. Iliopoulos D, Rotem A, Struhl K. Inhibition of miR-193a expression by Max and RXRalpha activates K-Ras and PLAU to mediate distinct aspects of cellular transformation. Cancer Res 2011, 71:5144-5153.
53. Caramuta S, Egyhazi S, Rodolfo M, Witten D, Hansson J, Larsson C, Lui WO. MicroRNA expression profiles associated with mutational status and survival in malignant melanoma. J Invest Dermatol 2010, 130:2062-2070.
54. Sakurai K, Furukawa C, Haraguchi T, Inada K, Shiogama K, Tagawa T, Fujita S, Ueno Y, Ogata A, Ito M, et al. MicroRNAs miR-199a-5p and -3p target the Brm subunit of SWI/SNF to generate a double-negative feedback loop in a variety of human cancers. Cancer Res 2011, 71:1680-1689.
55. Fornari F, Milazzo M, Chieco P, Negrini M, Calin GA, Grazi GL, Pollutri D, Croce CM, Bolondi L, Gramantieri L. MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 2010, 70:5184-5193.
56. Lehmusvaara S, Erkkila T, Urbanucci A, Jalava S, Seppala J, Kaipia A, Kujala P, Lahdesmaki H, Tammela TL, Visakorpi T. Goserelin and Bicalutamide treatments alter the expression of microRNAs in the prostate. Prostate 2013, 73:101-112.
57. Zhao Y, Zacur H, Cheadle C, Ning N, Fan J, Vlahos NF. Effect of luteal-phase support on endometrial microRNA expression following controlled ovarian stimulation. Reprod Biol Endocrinol 2012, 10:72. doi:10.1186/1477-7827-10-72.
58. Liu A, Tetzlaff MT, Vanbelle P, Elder D, Feldman M, Tobias JW, Sepulveda AR, Xu X. MicroRNA expression profiling outperforms mRNA expression profiling in formalin-fixed paraffin-embedded tissues. Int J Clin Exp Pathol 2009, 2:519-527. %20.
59. Glud M, Klausen M, Gniadecki R, Rossing M, Hastrup N, Nielsen FC, Drzewiecki KT. MicroRNA expression in melanocytic nevi: the usefulness of formalin-fixed, paraffin-embedded material for miRNA microarray profiling. J Invest Dermatol 2009, 129:1219-1224.
60. Fedorowicz G, Guerrero S, Wu TD, Modrusan Z. Microarray analysis of RNA extracted from formalin-fixed, paraffin-embedded and matched fresh-frozen ovarian adenocarcinomas. BMC Med Genomics 2009, 2:23. doi:10.1186/1755-8794-2-23.