miR-29s: A family of epi-miRNAs with therapeutic implications in hematologic malignancies

Oncotarget

Volumn 6, Issue 15, 2015, Pages 12837-12861

  Amodio, Nicola ^a   Rossi, Marco ^a   Raimondi, Lavinia ^b   Pitari, Maria Rita ^a   Botta, Cirino ^a   Tagliaferri, Pierosandro ^a   Tassone, Pierfrancesco ^a,c  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^b RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^c Temple University   (United States)

Author keywords

Hematologic malignancies; miR 29a; miR 29b; miR 29c; Multiple myeloma

Indexed keywords

4 PHENYLBUTYRIC ACID; AZACITIDINE; BORTEZOMIB; DECITABINE; ENTINOSTAT; EPI MICRORNA; HISTONE DEACETYLASE INHIBITOR; MICRORNA; MICRORNA 29S; PANOBINOSTAT; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VORINOSTAT; MIRN29 MICRORNA, HUMAN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; ARTICLE; CARCINOGENESIS; DNA METHYLATION; EPIGENETICS; GENETIC DISORDER; HEMATOLOGIC MALIGNANCY; HISTONE MODIFICATION; HUMAN; MULTIPLE CYCLE TREATMENT; MULTIPLE MYELOMA; MYELODYSPLASTIC SYNDROME; NEUROPATHY; NONHUMAN; SIGNAL TRANSDUCTION; SKIN LYMPHOMA; T CELL LYMPHOMA; TUMOR GROWTH; ANIMAL; GENETIC EPIGENESIS; GENETICS; HEMATOLOGIC NEOPLASMS; MOLECULARLY TARGETED THERAPY;

ANIMALS; DNA METHYLATION; EPIGENESIS, GENETIC; HEMATOLOGIC NEOPLASMS; HUMANS; MICRORNAS; MOLECULAR TARGETED THERAPY;

EID: 84931088607     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3805     Document Type: Article

References (224)

1. Hanahan D and Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
2. Cagnetta A, Adamia S, Acharya C, Patrone F, Miglino M, Nencioni A, Gobbi M and Cea M. Role of genotype-based approach in the clinical management of adult acute myeloid leukemia with normal cytogenetics. Leukemia research. 2014; 38:649-659.
3. Morgan GJ, Walker BA and Davies FE. The genetic architecture of multiple myeloma. Nature reviews Cancer. 2012; 12:335-348.
4. Virani S, Colacino JA, Kim JH and Rozek LS. Cancer epigenetics: a brief review. ILAR journal / National Research Council, Institute of Laboratory Animal Resources. 2012; 53:359-369.
5. Han Y and Garcia BA. Combining genomic and proteomic approaches for epigenetics research. Epigenomics. 2013; 5:439-452.
6. Baylin SB and Jones PA. A decade of exploring the cancer epigenome - biological and translational implications. Nature reviews Cancer. 2011; 11:726-734.
7. Berger SL, Kouzarides T, Shiekhattar R and Shilatifard A. An operational definition of epigenetics. Genes & development. 2009; 23:781-783.
8. Falkenberg KJ and Johnstone RW. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nature reviews Drug discovery. 2014; 13:673-691.
9. Singal R and Ginder GD. DNA methylation. Blood. 1999; 93:4059-4070.
10. Robertson KD and Wolffe AP. DNA methylation in health and disease. Nature reviews Genetics. 2000; 1:11-19.
11. Esteller M. Non-coding RNAs in human disease. Nature reviews Genetics. 2011; 12:861-874.
12. Popovic R, Shah MY and Licht JD. Epigenetic therapy of hematological malignancies: where are we now? Therapeutic advances in hematology. 2013; 4:81-91.
13. Mair B, Kubicek S and Nijman SM. Exploiting epigenetic vulnerabilities for cancer therapeutics. Trends in pharmacological sciences. 2014; 35:136-145.
14. Kasinski AL and Slack FJ. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nature reviews Cancer. 2011; 11:849-864.
15. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136:215-233.
16. Ebert MS and Sharp PA. Roles for microRNAs in conferring robustness to biological processes. Cell. 2012; 149:515-524.
17. Sun K and Lai EC. Adult-specific functions of animal microRNAs. Nature reviews Genetics. 2013; 14:535-548.
18. Calin GA and Croce CM. MicroRNA signatures in human cancers. Nature reviews Cancer. 2006; 6:857-866.
19. Esquela-Kerscher A and Slack FJ. Oncomirs - microRNAs with a role in cancer. Nature reviews Cancer. 2006; 6:259-269.
20. Leone E, Morelli E, Di Martino MT, Amodio N, Foresta U, Gulla A, Rossi M, Neri A, Giordano A, Munshi NC, Anderson KC, Tagliaferri P and Tassone P. Targeting miR-21 inhibits in vitro and in vivo multiple myeloma cell growth. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19:2096-2106.
21. Di Martino MT, Gulla A, Gallo Cantafio ME, Altomare E, Amodio N, Leone E, Morelli E, Lio SG, Caracciolo D, Rossi M, Frandsen NM, Tagliaferri P and Tassone P. In vitro and in vivo activity of a novel locked nucleic acid (LNA)-inhibitor-miR-221 against multiple myeloma cells. PloS one. 2014; 9:e89659.
22. Di Martino MT, Gulla A, Cantafio ME, Lionetti M, Leone E, Amodio N, Guzzi PH, Foresta U, Conforti F, Cannataro M, Neri A, Giordano A, Tagliaferri P and Tassone P. In vitro and in vivo anti-tumor activity of miR-221/222 inhibitors in multiple myeloma. Oncotarget. 2013; 4:242-255.
23. Leotta M, Biamonte L, Raimondi L, Ronchetti D, Di Martino MT, Botta C, Leone E, Pitari MR, Neri A, Giordano A, Tagliaferri P, Tassone P and Amodio N. A p53-dependent tumor suppressor network is induced by selective miR-125a-5p inhibition in multiple myeloma cells. Journal of cellular physiology. 2014; 229:2106-2116.
24. Di Martino MT, Leone E, Amodio N, Foresta U, Lionetti M, Pitari MR, Cantafio ME, Gulla A, Conforti F, Morelli E, Tomaino V, Rossi M, Negrini M, Ferrarini M, Caraglia M, Shammas MA, et al. Synthetic miR-34a mimics as a novel therapeutic agent for multiple myeloma: in vitro and in vivo evidence. Clinical cancer research: an official journal of the American Association for Cancer Research. 2012; 18:6260-6270.
25. Raimondi L, Amodio N, Di Martino MT, Altomare E, Leotta M, Caracciolo D, Gulla A, Neri A, Taverna S, D'Aquila P, Alessandro R, Giordano A, Tagliaferri P and Tassone P. Targeting of multiple myeloma-related angiogenesis by miR-199a-5p mimics: in vitro and in vivo anti-tumor activity. Oncotarget. 2014; 5:3039-3054.
26. Amodio N, Bellizzi D, Leotta M, Raimondi L, Biamonte L, D'Aquila P, Di Martino MT, Calimeri T, Rossi M, Lionetti M, Leone E, Passarino G, Neri A, Giordano A, Tagliaferri P and Tassone P. miR-29b induces SOCS-1 expression by promoter demethylation and negatively regulates migration of multiple myeloma and endothelial cells. Cell Cycle. 2013; 12:3650-3662.
27. Amodio N, Di Martino MT, Foresta U, Leone E, Lionetti M, Leotta M, Gulla AM, Pitari MR, Conforti F, Rossi M, Agosti V, Fulciniti M, Misso G, Morabito F, Ferrarini M, Neri A, et al. miR-29b sensitizes multiple myeloma cells to bortezomib-induced apoptosis through the activation of a feedback loop with the transcription factor Sp1. Cell death & disease. 2012; 3:e436.
28. Amodio N, Leotta M, Bellizzi D, Di Martino MT, D'Aquila P, Lionetti M, Fabiani F, Leone E, Gulla AM, Passarino G, Caraglia M, Negrini M, Neri A, Giordano A, Tagliaferri P and Tassone P. DNA-demethylating and anti-tumor activity of synthetic miR-29b mimics in multiple myeloma. Oncotarget. 2012; 3:1246-1258.
29. Di Martino MT, Campani V, Misso G, Gallo Cantafio ME, Gulla A, Foresta U, Guzzi PH, Castellano M, Grimaldi A, Gigantino V, Franco R, Lusa S, Cannataro M, Tagliaferri P, De Rosa G, Tassone P, et al. In vivo activity of miR-34a mimics delivered by stable nucleic acid lipid particles (SNALPs) against multiple myeloma. PloS one. 2014; 9:e90005.
30. Rossi M, Pitari MR, Amodio N, Di Martino MT, Conforti F, Leone E, Botta C, Paolino FM, Del Giudice T, Iuliano E, Caraglia M, Ferrarini M, Giordano A, Tagliaferri P and Tassone P. miR-29b negatively regulates human osteoclastic cell differentiation and function: implications for the treatment of multiple myeloma-related bone disease. Journal of cellular physiology. 2013; 228:1506-1515.
31. Tagliaferri P, Rossi M, Di Martino MT, Amodio N, Leone E, Gulla A, Neri A and Tassone P. Promises and challenges of MicroRNA-based treatment of multiple myeloma. Current cancer drug targets. 2012; 12:838-846.
32. Amodio N, Di Martino MT, Neri A, Tagliaferri P and Tassone P. Non-coding RNA: a novel opportunity for the personalized treatment of multiple myeloma. Expert opinion on biological therapy. 2013; 13 Suppl 1:S125-137.
33. Misso G, Zappavigna S, Castellano M, De Rosa G, Di Martino MT, Tagliaferri P, Tassone P and Caraglia M. Emerging pathways as individualized therapeutic target of multiple myeloma. Expert opinion on biological therapy. 2013; 13 Suppl 1:S95-109.
34. Rossi M, Amodio N, Di Martino MT, Caracciolo D, Tagliaferri P and Tassone P. From target therapy to miRNA therapeutics of human multiple myeloma: theoretical and technological issues in the evolving scenario. Current drug targets. 2013; 14:1144-1149.
35. Rossi M, Amodio N, Di Martino MT, Tagliaferri P, Tassone P and Cho WC. MicroRNA and multiple myeloma: from laboratory findings to translational therapeutic approaches. Current pharmaceutical biotechnology. 2014; 15:459-467.
36. Misso G, Di Martino MT, De Rosa G, Farooqi AA, Lombardi A, Campani V, Zarone MR, Gulla A, Tagliaferri P, Tassone P and Caraglia M. Mir-34: a new weapon against cancer? Molecular therapy Nucleic acids. 2014; 3:e194.
37. Challagundla KB, Fanini F, Vannini I, Wise P, Murtadha M, Malinconico L, Cimmino A and Fabbri M. microRNAs in the tumor microenvironment: solving the riddle for a better diagnostics. Expert review of molecular diagnostics. 2014; 14:565-574.
38. Zhang X, Tang J, Zhi X, Xie K, Wang W, Li Z, Zhu Y, Yang L, Xu H and Xu Z. miR-874 functions as a tumor suppressor by inhibiting angiogenesis through STAT3/VEGF-A pathway in gastric cancer. Oncotarget. 2015; 6:1605-1617.
39. Zhang K, Chen J, Chen D, Huang J, Feng B, Han S, Chen Y, Song H, De W, Zhu Z, Wang R and Chen L. Aurora-A promotes chemoresistance in hepatocelluar carcinoma by targeting NF-kappaB/microRNA-21/PTEN signaling pathway. Oncotarget. 2014; 5:12916-12935.
40. Zhao JJ and Carrasco RD. Crosstalk between microRNA30a/b/c/d/e-5p and the canonical Wnt pathway:implications for multiple myeloma therapy. Cancer research. 2014; 74:5351-5358.
41. Malumbres M. miRNAs and cancer: an epigenetics view. Molecular aspects of medicine. 2013; 34:863-874.
42. Garzon R, Liu S, Fabbri M, Liu Z, Heaphy CE, Callegari E, Schwind S, Pang J, Yu J, Muthusamy N, Havelange V, Volinia S, Blum W, Rush LJ, Perrotti D, Andreeff M, et al. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood. 2009; 113:6411-6418.
43. Liu S, Wu LC, Pang J, Santhanam R, Schwind S, Wu YZ, Hickey CJ, Yu J, Becker H, Maharry K, Radmacher MD, Li C, Whitman SP, Mishra A, Stauffer N, Eiring AM, et al. Sp1/NFkappaB/HDAC/miR-29b regulatory network in KIT-driven myeloid leukemia. Cancer cell. 2010; 17:333-347.
44. Sandoval J and Esteller M. Cancer epigenomics: beyond genomics. Current opinion in genetics & development. 2012; 22:50-55.
45. Struhl K and Segal E. Determinants of nucleosome positioning. Nature structural & molecular biology. 2013; 20:267-273.
46. Azizi M, Teimoori-Toolabi L, Arzanani MK, Azadmanesh K, Fard-Esfahani P and Zeinali S. MicroRNA-148b and microRNA-152 reactivate tumor suppressor genes through suppression of DNA methyltransferase-1 gene in pancreatic cancer cell lines. Cancer biology & therapy. 2014; 15:419-427.
47. Lee JY, Jeong W, Lim W, Lim CH, Bae SM, Kim J, Bazer FW and Song G. Hypermethylation and post-transcriptional regulation of DNA methyltransferases in the ovarian carcinomas of the laying hen. PloS one. 2013; 8:e61658.
48. Braconi C, Huang N and Patel T. MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology. 2010; 51:881-890.
49. Li HP, Huang HY, Lai YR, Huang JX, Chang KP, Hsueh C and Chang YS. Silencing of miRNA-148a by hypermethylation activates the integrin-mediated signaling pathway in nasopharyngeal carcinoma. Oncotarget. 2014; 5:7610-7624.
50. Chen BF, Suen YK, Gu S, Li L and Chan WY. A miR-199a/miR-214 self-regulatory network via PSMD10, TP53 and DNMT1 in testicular germ cell tumor. Scientific reports. 2014; 4:6413.
51. Xu L, Beckebaum S, Iacob S, Wu G, Kaiser GM, Radtke A, Liu C, Kabar I, Schmidt HH, Zhang X, Lu M and Cicinnati VR. MicroRNA-101 inhibits human hepatocellular carcinoma progression through EZH2 downregulation and increased cytostatic drug sensitivity. Journal of hepatology. 2014; 60:590-598.
52. Konno Y, Dong P, Xiong Y, Suzuki F, Lu J, Cai M, Watari H, Mitamura T, Hosaka M, Hanley SJ, Kudo M and Sakuragi N. MicroRNA-101 targets EZH2, MCL-1 and FOS to suppress proliferation, invasion and stem celllike phenotype of aggressive endometrial cancer cells. Oncotarget. 2014; 5:6049-6062.
53. Zhang K, Zhang Y, Ren K, Zhao G, Yan K and Ma B. MicroRNA-101 inhibits the metastasis of osteosarcoma cells by downregulation of EZH2 expression. Oncology reports. 2014; 32:2143-2149.
54. Francis NJ, Kingston RE and Woodcock CL. Chromatin compaction by a polycomb group protein complex. Science. 2004; 306:1574-1577.
55. Zhang D, Ni Z, Xu X and Xiao J. MiR-32 functions as a tumor suppressor and directly targets EZH2 in human oral squamous cell carcinoma. Medical science monitor :international medical journal of experimental and clinical research. 2014; 20:2527-2535.
56. Yang WS, Chadalapaka G, Cho SG, Lee SO, Jin UH, Jutooru I, Choi K, Leung YK, Ho SM, Safe S and Kim K. The Transcriptional Repressor ZBTB4 Regulates EZH2 Through a MicroRNA-ZBTB4-Specificity Protein Signaling Axis. Neoplasia. 2014; 16:1059-1069.
57. Zhao X, Lwin T, Zhang X, Huang A, Wang J, Marquez VE, Chen-Kiang S, Dalton WS, Sotomayor E and Tao J. Disruption of the MYC-miRNA-EZH2 loop to suppress aggressive B-cell lymphoma survival and clonogenicity. Leukemia. 2013; 27:2341-2350.
58. Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, Rossi S, Calin GA and Mukherjee P. MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer research. 2009; 69:9090-9095.
59. Yu X, Jiang X, Li H, Guo L, Jiang W and Lu SH. miR-203 inhibits the proliferation and self-renewal of esophageal cancer stem-like cells by suppressing stem renewal factor Bmi-1. Stem cells and development. 2014; 23:576-585.
60. Venkataraman S, Alimova I, Fan R, Harris P, Foreman N and Vibhakar R. MicroRNA 128a increases intracellular ROS level by targeting Bmi-1 and inhibits medulloblastoma cancer cell growth by promoting senescence. PloS one. 2010; 5:e10748.
61. Zhu Y, Yu F, Jiao Y, Feng J, Tang W, Yao H, Gong C, Chen J, Su F, Zhang Y and Song E. Reduced miR-128 in breast tumor-initiating cells induces chemotherapeutic resistance via Bmi-1 and ABCC5. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17:7105-7115.
62. Dong P, Kaneuchi M, Watari H, Hamada J, Sudo S, Ju J and Sakuragi N. MicroRNA-194 inhibits epithelial to mesenchymal transition of endometrial cancer cells by targeting oncogene BMI-1. Molecular cancer. 2011; 10:99.
63. Liu S, Tetzlaff MT, Cui R and Xu X. miR-200c inhibits melanoma progression and drug resistance through downregulation of BMI-1. The American journal of pathology. 2012; 181:1823-1835.
64. Chesi M, Nardini E, Lim RS, Smith KD, Kuehl WM and Bergsagel PL. The t(4;14) translocation in myeloma dysregulates both FGFR3 and a novel gene, MMSET, resulting in IgH/MMSET hybrid transcripts. Blood. 1998; 92(9):3025-3034.
65. Kuo AJ, Cheung P, Chen K, Zee BM, Kioi M, Lauring J, Xi Y, Park BH, Shi X, Garcia BA, Li W and Gozani O. NSD2 links dimethylation of histone H3 at lysine 36 to oncogenic programming. Molecular cell. 2011; 44:609-620.
66. Brito JL, Walker B, Jenner M, Dickens NJ, Brown NJ, Ross FM, Avramidou A, Irving JA, Gonzalez D, Davies FE and Morgan GJ. MMSET deregulation affects cell cycle progression and adhesion regulons in t(4;14) myeloma plasma cells. Haematologica. 2009; 94(1):78-86.
67. Cao W, Younis RH, Li J, Chen H, Xia R, Mao L, Chen W and Ren H. EZH2 promotes malignant phenotypes and is a predictor of oral cancer development in patients with oral leukoplakia. Cancer Prev Res (Phila). 2011; 4:1816-1824.
68. Asangani IA, Ateeq B, Cao Q, Dodson L, Pandhi M, Kunju LP, Mehra R, Lonigro RJ, Siddiqui J, Palanisamy N, Wu YM, Cao X, Kim JH, Zhao M, Qin ZS, Iyer MK, et al. Characterization of the EZH2-MMSET histone methyltransferase regulatory axis in cancer. Molecular cell. 2013; 49:80-93.
69. Min DJ, Ezponda T, Kim MK, Will CM, Martinez-Garcia E, Popovic R, Basrur V, Elenitoba-Johnson KS and Licht JD. MMSET stimulates myeloma cell growth through microRNA-mediated modulation of c-MYC. Leukemia. 2013; 27:686-694.
70. Chu L, Su MY, Maggi LB, Jr., Lu L, Mullins C, Crosby S, Huang G, Chng WJ, Vij R and Tomasson MH. Multiple myeloma-associated chromosomal translocation activates orphan snoRNA ACA11 to suppress oxidative stress. The Journal of clinical investigation. 2012; 122:2793-2806.
71. Bedford MT and Richard S. Arginine methylation an emerging regulator of protein function. Molecular cell. 2005; 18:263-272.
72. Pal S, Baiocchi RA, Byrd JC, Grever MR, Jacob ST and Sif S. Low levels of miR-92b/96 induce PRMT5 translation and H3R8/H4R3 methylation in mantle cell lymphoma. The EMBO journal. 2007; 26(15):3558-3569.
73. Wang L, Pal S and Sif S. Protein arginine methyltransferase 5 suppresses the transcription of the RB family of tumor suppressors in leukemia and lymphoma cells. Molecular and cellular biology. 2008; 28:6262-6277.
74. Roccaro AM, Sacco A, Jia X, Azab AK, Maiso P, Ngo HT, Azab F, Runnels J, Quang P and Ghobrial IM. microRNA-dependent modulation of histone acetylation in Waldenstrom macroglobulinemia. Blood. 2010; 116:1506-1514.
75. Agostini M and Knight RA. miR-34: from bench to bedside. Oncotarget. 2014; 5:872-881.
76. Wang AM, Huang TT, Hsu KW, Huang KH, Fang WL, Yang MH, Lo SS, Chi CW, Lin JJ and Yeh TS. Yin Yang 1 is a target of microRNA-34 family and contributes to gastric carcinogenesis. Oncotarget. 2014; 5:5002-5016.
77. Scognamiglio I, Di Martino MT, Campani V, Virgilio A, Galeone A, Gulla A, Gallo Cantafio ME, Misso G, Tagliaferri P, Tassone P, Caraglia M and De Rosa G. Transferrin-conjugated SNALPs encapsulating 2'-O-methylated miR-34a for the treatment of multiple myeloma. BioMed research international. 2014; 2014:217365.
78. Siemens H, Jackstadt R, Kaller M and Hermeking H. Repression of c-Kit by p53 is mediated by miR-34 and is associated with reduced chemoresistance, migration and stemness. Oncotarget. 2013; 4:1399-1415.
79. Wu MY, Fu J, Xiao X, Wu J and Wu RC. MiR-34a regulates therapy resistance by targeting HDAC1 and HDAC7 in breast cancer. Cancer letters. 2014; 354:311-319.
80. Chen DQ, Pan BZ, Huang JY, Zhang K, Cui SY, De W, Wang R and Chen LB. HDAC 1/4-mediated silencing of microRNA-200b promotes chemoresistance in human lung adenocarcinoma cells. Oncotarget. 2014; 5:3333-3349.
81. Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, Volinia S, Guler G, Morrison CD, Chan KK, Marcucci G, Calin GA, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104:15805-15810.
82. Mott JL, Kobayashi S, Bronk SF and Gores GJ. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene. 2007; 26:6133-6140.
83. Di Fiore R, Drago-Ferrante R, Pentimalli F, Di Marzo D, Forte IM, D'Anneo A, Carlisi D, De Blasio A, Giuliano M, Tesoriere G, Giordano A and Vento R. MicroRNA-29b-1 impairs in vitro cell proliferation, selfrenewal and chemoresistance of human osteosarcoma 3AB-OS cancer stem cells. International journal of oncology. 2014; 45:2013-2023.
84. Fang JH, Zhou HC, Zeng C, Yang J, Liu Y, Huang X, Zhang JP, Guan XY and Zhuang SM. MicroRNA-29b suppresses tumor angiogenesis, invasion, and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology. 2011; 54:1729-1740.
85. Wang B, Li W, Liu H, Yang L, Liao Q, Cui S, Wang H and Zhao L. miR-29b suppresses tumor growth and metastasis in colorectal cancer via downregulating Tiam1 expression and inhibiting epithelial-mesenchymal transition. Cell death & disease. 2014; 5:e1335.
86. Qiang W, Liu Z, Serna VA, Druschitz SA, Liu Y, Espona-Fiedler M, Wei JJ and Kurita T. Down-regulation of miR-29b is essential for pathogenesis of uterine leiomyoma. Endocrinology. 2014; 155:663-669.
87. Dai F, Zhang Y, Zhu X, Shan N and Chen Y. Anticancer role of MUC1 aptamer-miR-29b chimera in epithelial ovarian carcinoma cells through regulation of PTEN methylation. Targeted oncology. 2012; 7:217-225.
88. Jacobsen A, Silber J, Harinath G, Huse JT, Schultz N and Sander C. Analysis of microRNA-target interactions across diverse cancer types. Nature structural & molecular biology. 2013; 20:1325-1332.
89. Lagos-Quintana M, Rauhut R, Lendeckel W and Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001; 294:853-858.
90. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W and Tuschl T. Identification of tissue-specific microRNAs from mouse. Current biology: CB. 2002; 12:735-739.
91. Dostie J, Mourelatos Z, Yang M, Sharma A and Dreyfuss G. Numerous microRNPs in neuronal cells containing novel microRNAs. RNA. 2003; 9:180-186.
92. Hwang HW, Wentzel EA and Mendell JT. A hexanucleotide element directs microRNA nuclear import. Science. 2007; 315:97-100.
93. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E and Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brainexpressed microRNAs with possible roles in murine and human neuronal differentiation. Genome biology. 2004; 5:R13.
94. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM, Dang CV, Thomas-Tikhonenko A and Mendell JT. Widespread microRNA repression by Myc contributes to tumorigenesis. Nature genetics. 2008; 40:43-50.
95. Mott JL, Kurita S, Cazanave SC, Bronk SF, Werneburg NW and Fernandez-Zapico ME. Transcriptional suppression of mir-29b-1/mir-29a promoter by c-Myc, hedgehog, and NFkappaB. Journal of cellular biochemistry. 2010; 110:1155-1164.
96. Wang H, Garzon R, Sun H, Ladner KJ, Singh R, Dahlman J, Cheng A, Hall BM, Qualman SJ, Chandler DS, Croce CM and Guttridge DC. NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer cell. 2008; 14:369-381.
97. Eyholzer M, Schmid S, Wilkens L, Mueller BU and Pabst T. The tumour-suppressive miR-29a/b1 cluster is regulated by CEBPA and blocked in human AML. British journal of cancer. 2010; 103:275-284.
98. Kapinas K, Kessler C, Ricks T, Gronowicz G and Delany AM. miR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. The Journal of biological chemistry. 2010; 285:25221-25231.
99. Schmitt MJ, Philippidou D, Reinsbach SE, Margue C, Wienecke-Baldacchino A, Nashan D, Behrmann I and Kreis S. Interferon-gamma-induced activation of Signal Transducer and Activator of Transcription 1 (STAT1) upregulates the tumor suppressing microRNA-29 family in melanoma cells. Cell communication and signaling: CCS. 2012; 10:41.
100. Maurer B, Stanczyk J, Jungel A, Akhmetshina A, Trenkmann M, Brock M, Kowal-Bielecka O, Gay RE, Michel BA, Distler JH, Gay S and Distler O. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis and rheumatism. 2010; 62:1733-1743.
101. Zhou L, Wang L, Lu L, Jiang P, Sun H and Wang H. Inhibition of miR-29 by TGF-beta-Smad3 signaling through dual mechanisms promotes transdifferentiation of mouse myoblasts into myofibroblasts. PloS one. 2012; 7:e33766.
102. Zhang Z, Zou J, Wang GK, Zhang JT, Huang S, Qin YW and Jing Q. Uracils at nucleotide position 9-11 are required for the rapid turnover of miR-29 family. Nucleic acids research. 2011; 39:4387-4395.
103. Montagner S, Deho L and Monticelli S. MicroRNAs in hematopoietic development. BMC immunology. 2014; 15:14.
104. Pagano F, De Marinis E, Grignani F and Nervi C. Epigenetic role of miRNAs in normal and leukemic hematopoiesis. Epigenomics. 2013; 5:539-552.
105. Xiao C and Rajewsky K. MicroRNA control in the immune system: basic principles. Cell. 2009; 136:26-36.
106. Bissels U, Bosio A and Wagner W. MicroRNAs are shaping the hematopoietic landscape. Haematologica. 2012; 97:160-167.
107. Papadopoulou AS, Dooley J, Linterman MA, Pierson W, Ucar O, Kyewski B, Zuklys S, Hollander GA, Matthys P, Gray DH, De Strooper B and Liston A. The thymic epithelial microRNA network elevates the threshold for infection-associated thymic involution via miR-29a mediated suppression of the IFN-alpha receptor. Nature immunology. 2012; 13:181-187.
108. Ma F, Xu S, Liu X, Zhang Q, Xu X, Liu M, Hua M, Li N, Yao H and Cao X. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nature immunology. 2011; 12:861-869.
109. Steiner DF, Thomas MF, Hu JK, Yang Z, Babiarz JE, Allen CD, Matloubian M, Blelloch R and Ansel KM. MicroRNA-29 regulates T-box transcription factors and interferon-gamma production in helper T cells. Immunity. 2011; 35:169-181.
110. Smith KM, Guerau-de-Arellano M, Costinean S, Williams JL, Bottoni A, Mavrikis Cox G, Satoskar AR, Croce CM, Racke MK, Lovett-Racke AE and Whitacre CC. miR-29ab1 deficiency identifies a negative feedback loop controlling Th1 bias that is dysregulated in multiple sclerosis. J Immunol. 2012; 189:1567-1576.
111. Brain O, Owens BM, Pichulik T, Allan P, Khatamzas E, Leslie A, Steevels T, Sharma S, Mayer A, Catuneanu AM, Morton V, Sun MY, Jewell D, Coccia M, Harrison O, Maloy K, et al. The intracellular sensor NOD2 induces microRNA-29 expression in human dendritic cells to limit IL-23 release. Immunity. 2013; 39:521-536.
112. Salama A, Fichou N, Allard M, Dubreil L, De Beaurepaire L, Viel A, Jegou D, Bosch S and Bach JM. MicroRNA-29b modulates innate and antigen-specific immune responses in mouse models of autoimmunity. PloS one. 2014; 9:e106153.
113. Tassone P, Neri P, Carrasco DR, Burger R, Goldmacher VS, Fram R, Munshi V, Shammas MA, Catley L, Jacob GS, Venuta S, Anderson KC and Munshi NC. A clinically relevant SCID-hu in vivo model of human multiple myeloma. Blood. 2005; 106:713-716.
114. Calimeri T, Battista E, Conforti F, Neri P, Di Martino MT, Rossi M, Foresta U, Piro E, Ferrara F, Amorosi A, Bahlis N, Anderson KC, Munshi N, Tagliaferri P, Causa F and Tassone P. A unique three-dimensional SCID-polymeric scaffold (SCID-synth-hu) model for in vivo expansion of human primary multiple myeloma cells. Leukemia. 2011; 25:707-711.
115. Tassone P, Tagliaferri P, Rossi M, Calimeri T, Bulotta A, Abbruzzese A, Caraglia M and Neri P. Challenging the current approaches to multiple myeloma-related bone disease: from bisphosphonates to target therapy. Current cancer drug targets. 2009; 9:854-870.
116. Tassone P, Neri P, Burger R, Di Martino MT, Leone E, Amodio N, Caraglia M and Tagliaferri P. Mouse models as a translational platform for the development of new therapeutic agents in multiple myeloma. Current cancer drug targets. 2012; 12:814-822.
117. Ditzel Santos D, Ho AW, Tournilhac O, Hatjiharissi E, Leleu X, Xu L, Tassone P, Neri P, Hunter ZR, Chemaly MA, Branagan AR, Manning RJ, Patterson CJ, Moreau AS, Ciccarelli B, Adamia S, et al. Establishment of BCWM.1 cell line for Waldenstrom's macroglobulinemia with productive in vivo engraftment in SCID-hu mice. Experimental hematology. 2007; 35:1366-1375.
118. Tassone P, Neri P, Kutok JL, Tournilhac O, Santos DD, Hatjiharissi E, Munshi V, Venuta S, Anderson KC, Treon SP and Munshi NC. A SCID-hu in vivo model of human Waldenstrom macroglobulinemia. Blood. 2005; 106:1341-1345.
119. Rossi M, Di Martino MT, Morelli E, Leotta M, Rizzo A, Grimaldi A, Misso G, Tassone P and Caraglia M. Molecular targets for the treatment of multiple myeloma. Current cancer drug targets. 2012; 12:757-767.
120. Neri P, Tagliaferri P, Di Martino MT, Calimeri T, Amodio N, Bulotta A, Ventura M, Eramo PO, Viscomi C, Arbitrio M, Rossi M, Caraglia M, Munshi NC, Anderson KC and Tassone P. In vivo anti-myeloma activity and modulation of gene expression profile induced by valproic acid, a histone deacetylase inhibitor. British journal of haematology. 2008; 143:520-531.
121. Neri P, Ren L, Gratton K, Stebner E, Johnson J, Klimowicz A, Duggan P, Tassone P, Mansoor A, Stewart DA, Lonial S, Boise LH and Bahlis NJ. Bortezomib-induced "BRCAness" sensitizes multiple myeloma cells to PARP inhibitors. Blood. 2011; 118:6368-6379.
122. Yasui H, Hideshima T, Hamasaki M, Roccaro AM, Shiraishi N, Kumar S, Tassone P, Ishitsuka K, Raje N, Tai YT, Podar K, Chauhan D, Leoni LM, Kanekal S, Elliott G, Munshi NC, et al. SDX-101, the R-enantiomer of etodolac, induces cytotoxicity, overcomes drug resistance, and enhances the activity of dexamethasone in multiple myeloma. Blood. 2005; 106:706-712.
123. Tassone P, Galea E, Forciniti S, Tagliaferri P and Venuta S. The IL-6 receptor super-antagonist Sant7 enhances antiproliferative and apoptotic effects induced by dexamethasone and zoledronic acid on multiple myeloma cells. International journal of oncology. 2002; 21:867-873.
124. Fulciniti M, Hideshima T, Vermot-Desroches C, Pozzi S, Nanjappa P, Shen Z, Patel N, Smith ES, Wang W, Prabhala R, Tai YT, Tassone P, Anderson KC and Munshi NC. A high-affinity fully human anti-IL-6 mAb, 1339, for the treatment of multiple myeloma. Clinical cancer research :an official journal of the American Association for Cancer Research. 2009; 15:7144-7152.
125. Ishitsuka K, Hideshima T, Neri P, Vallet S, Shiraishi N, Okawa Y, Shen Z, Raje N, Kiziltepe T, Ocio EM, Chauhan D, Tassone P, Munshi N, Campbell RM, Dios AD, Shih C, et al. p38 mitogen-activated protein kinase inhibitor LY2228820 enhances bortezomib-induced cytotoxicity and inhibits osteoclastogenesis in multiple myeloma; therapeutic implications. British journal of haematology. 2008; 141:598-606.
126. Tassone P, Forciniti S, Galea E, Savino R, Turco MC, Iacopino P, Tagliaferri P, Morrone G, Ciliberto G and Venuta S. Synergistic induction of growth arrest and apoptosis of human myeloma cells by the IL-6 superantagonist Sant7 and Dexamethasone. Cell death and differentiation. 2000; 7:327-328.
127. Burger R, Le Gouill S, Tai YT, Shringarpure R, Tassone P, Neri P, Podar K, Catley L, Hideshima T, Chauhan D, Caulder E, Neilan CL, Vaddi K, Li J, Gramatzki M, Fridman JS, et al. Janus kinase inhibitor INCB20 has antiproliferative and apoptotic effects on human myeloma cells in vitro and in vivo. Molecular cancer therapeutics. 2009; 8:26-35.
128. Marra M, Salzano G, Leonetti C, Tassone P, Scarsella M, Zappavigna S, Calimeri T, Franco R, Liguori G, Cigliana G, Ascani R, La Rotonda MI, Abbruzzese A, Tagliaferri P, Caraglia M and De Rosa G. Nanotechnologies to use bisphosphonates as potent anticancer agents: the effects of zoledronic acid encapsulated into liposomes. Nanomedicine: nanotechnology, biology, and medicine. 2011; 7:955-964.
129. Fulciniti M, Amin S, Nanjappa P, Rodig S, Prabhala R, Li C, Minvielle S, Tai YT, Tassone P, Avet-Loiseau H, Hideshima T, Anderson KC and Munshi NC. Significant biological role of sp1 transactivation in multiple myeloma. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17:6500-6509.
130. Fulciniti M, Amodio N, Bandi RL, Munshi M, Yang G, Xu L, Hunter Z, Tassone P, Anderson KC, Treon SP and Munshi NC. MYD88-independent growth and survival effects of Sp1 transactivation in Waldenstrom macroglobulinemia. Blood. 2014; 123:2673-2681.
131. Jagannathan S, Vad N, Vallabhapurapu S, Vallabhapurapu S, Anderson KC and Driscoll JJ. MiR-29b replacement inhibits proteasomes and disrupts aggresome+autophagosome formation to enhance the antimyeloma benefit of bortezomib. Leukemia. 2015; 29:727-738.
132. Sevcikova S, Kubiczkova L, Sedlarikova L, Slaby O and Hajek R. Serum miR-29a as a marker of multiple myeloma. Leukemia & lymphoma. 2013; 54:189-191.
133. Galm O, Wilop S, Reichelt J, Jost E, Gehbauer G, Herman JG and Osieka R. DNA methylation changes in multiple myeloma. Leukemia. 2004; 18:1687-1692.
134. Kaiser MF, Johnson DC, Wu P, Walker BA, Brioli A, Mirabella F, Wardell CP, Melchor L, Davies FE and Morgan GJ. Global methylation analysis identifies prognostically important epigenetically inactivated tumor suppressor genes in multiple myeloma. Blood. 2013; 122:219-226.
135. Brakensiek K, Langer F, Schlegelberger B, Kreipe H and Lehmann U. Hypermethylation of the suppressor of cytokine signalling-1 (SOCS-1) in myelodysplastic syndrome. British journal of haematology. 2005; 130:209-217.
136. Anderson KC, Alsina M, Bensinger W, Biermann JS, Chanan-Khan A, Cohen AD, Devine S, Djulbegovic B, Faber EA, Jr., Gasparetto C, Huff CA, Kassim A, Medeiros BC, Meredith R, Raje N, Schriber J, et al. Multiple myeloma. Journal of the National Comprehensive Cancer Network: JNCCN. 2011; 9:1146-1183.
137. Rogers MJ, Frith JC, Luckman SP, Coxon FP, Benford HL, Monkkonen J, Auriola S, Chilton KM and Russell RG. Molecular mechanisms of action of bisphosphonates. Bone. 1999; 24:73S-79S.
138. Russell RG, Rogers MJ, Frith JC, Luckman SP, Coxon FP, Benford HL, Croucher PI, Shipman C and Fleisch HA. The pharmacology of bisphosphonates and new insights into their mechanisms of action. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 1999; 14 Suppl 2:53-65.
139. Marra M, Abbruzzese A, Addeo R, Del Prete S, Tassone P, Tonini G, Tagliaferri P, Santini D and Caraglia M. Cutting the limits of aminobisphosphonates: new strategies for the potentiation of their anti-tumour effects. Current cancer drug targets. 2009; 9:791-800.
140. Caraglia M, D'Alessandro AM, Marra M, Giuberti G, Vitale G, Viscomi C, Colao A, Prete SD, Tagliaferri P, Tassone P, Budillon A, Venuta S and Abbruzzese A. The farnesyl transferase inhibitor R115777 (Zarnestra) synergistically enhances growth inhibition and apoptosis induced on epidermoid cancer cells by Zoledronic acid (Zometa) and Pamidronate. Oncogene. 2004; 23:6900-6913.
141. Tassone P, Tagliaferri P, Viscomi C, Palmieri C, Caraglia M, D'Alessandro A, Galea E, Goel A, Abbruzzese A, Boland CR and Venuta S. Zoledronic acid induces antiproliferative and apoptotic effects in human pancreatic cancer cells in vitro. British journal of cancer. 2003; 88:1971-1978.
142. Tassone P, Forciniti S, Galea E, Morrone G, Turco MC, Martinelli V, Tagliaferri P and Venuta S. Growth inhibition and synergistic induction of apoptosis by zoledronate and dexamethasone in human myeloma cell lines. Leukemia. 2000; 14:841-844.
143. Mellis DJ, Itzstein C, Helfrich MH and Crockett JC. The skeleton: a multi-functional complex organ: the role of key signalling pathways in osteoclast differentiation and in bone resorption. The Journal of endocrinology. 2011; 211:131-143.
144. Blair HC and Athanasou NA. Recent advances in osteoclast biology and pathological bone resorption. Histology and histopathology. 2004; 19:189-199.
145. Yuan L, Chan GC, Fung KL and Chim CS. RANKL expression in myeloma cells is regulated by a network involving RANKL promoter methylation, DNMT1, microRNA and TNFalpha in the microenvironment. Biochimica et biophysica acta. 2014; 1843:1834-1838.
146. Kapinas K and Delany AM. MicroRNA biogenesis and regulation of bone remodeling. Arthritis research & therapy. 2011; 13:220.
147. Li Z, Hassan MQ, Jafferji M, Aqeilan RI, Garzon R, Croce CM, van Wijnen AJ, Stein JL, Stein GS and Lian JB. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. The Journal of biological chemistry. 2009; 284:15676-15684.
148. Calin GA, Liu CG, Sevignani C, Ferracin M, Felli N, Dumitru CD, Shimizu M, Cimmino A, Zupo S, Dono M, Dell'Aquila ML, Alder H, Rassenti L, Kipps TJ, Bullrich F, Negrini M, et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proceedings of the National Academy of Sciences of the United States of America. 2004; 101:11755-11760.
149. Pekarsky Y, Santanam U, Cimmino A, Palamarchuk A, Efanov A, Maximov V, Volinia S, Alder H, Liu CG, Rassenti L, Calin GA, Hagan JP, Kipps T and Croce CM. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer research. 2006; 66:11590-11593.
150. Bichi R, Shinton SA, Martin ES, Koval A, Calin GA, Cesari R, Russo G, Hardy RR and Croce CM. Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99:6955-6960.
151. Santanam U, Zanesi N, Efanov A, Costinean S, Palamarchuk A, Hagan JP, Volinia S, Alder H, Rassenti L, Kipps T, Croce CM and Pekarsky Y. Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107:12210-12215.
152. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, Iuliano R, Palumbo T, Pichiorri F, Roldo C, Garzon R, Sevignani C, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. The New England journal of medicine. 2005; 353:1793-1801.
153. Pekarsky Y and Croce CM. Is miR-29 an oncogene or tumor suppressor in CLL? Oncotarget. 2010; 1:224-227.
154. Calin GA, Cimmino A, Fabbri M, Ferracin M, Wojcik SE, Shimizu M, Taccioli C, Zanesi N, Garzon R, Aqeilan RI, Alder H, Volinia S, Rassenti L, Liu X, Liu CG, Kipps TJ, et al. MiR-15a and miR-16-1 cluster functions in human leukemia. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105:5166-5171.
155. Garzon R, Heaphy CE, Havelange V, Fabbri M, Volinia S, Tsao T, Zanesi N, Kornblau SM, Marcucci G, Calin GA, Andreeff M and Croce CM. MicroRNA 29b functions in acute myeloid leukemia. Blood. 2009; 114:5331-5341.
156. Li S, Moffett HF, Lu J, Werner L, Zhang H, Ritz J, Neuberg D, Wucherpfennig KW, Brown JR and Novina CD. MicroRNA expression profiling identifies activated B cell status in chronic lymphocytic leukemia cells. PloS one. 2011; 6:e16956.
157. Sampath D, Liu C, Vasan K, Sulda M, Puduvalli VK, Wierda WG and Keating MJ. Histone deacetylases mediate the silencing of miR-15a, miR-16, and miR-29b in chronic lymphocytic leukemia. Blood. 2012; 119:1162-1172.
158. Lowenberg B, Downing JR and Burnett A. Acute myeloid leukemia. The New England journal of medicine. 1999; 341:1051-1062.
159. Hu W, Dooley J, Chung SS, Chandramohan D, Cimmino L, Mukherjee S, Mason CE, Strooper B, Liston A and Park CY. MiR-29a maintains mouse hematopoietic stem cell self-renewal by regulating Dnmt3a. Blood. 2015; 125:2206-2216.
160. Han YC, Park CY, Bhagat G, Zhang J, Wang Y, Fan JB, Liu M, Zou Y, Weissman IL and Gu H. microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. The Journal of experimental medicine. 2010; 207:475-489.
161. Wang XS, Gong JN, Yu J, Wang F, Zhang XH, Yin XL, Tan ZQ, Luo ZM, Yang GH, Shen C and Zhang JW. MicroRNA-29a and microRNA-142-3p are regulators of myeloid differentiation and acute myeloid leukemia. Blood. 2012; 119:4992-5004.
162. Garzon R, Volinia S, Liu CG, Fernandez-Cymering C, Palumbo T, Pichiorri F, Fabbri M, Coombes K, Alder H, Nakamura T, Flomenberg N, Marcucci G, Calin GA, Kornblau SM, Kantarjian H, Bloomfield CD, et al. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood. 2008; 111:3183-3189.
163. Garzon R, Garofalo M, Martelli MP, Briesewitz R, Wang L, Fernandez-Cymering C, Volinia S, Liu CG, Schnittger S, Haferlach T, Liso A, Diverio D, Mancini M, Meloni G, Foa R, Martelli MF, et al. Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105:3945-3950.
164. Xu L, Xu Y, Jing Z, Wang X, Zha X, Zeng C, Chen S, Yang L, Luo G, Li B and Li Y. Altered expression pattern of miR-29a, miR-29b and the target genes in myeloid leukemia. Experimental hematology & oncology. 2014; 3:17.
165. Gong JN, Yu J, Lin HS, Zhang XH, Yin XL, Xiao Z, Wang F, Wang XS, Su R, Shen C, Zhao HL, Ma YN and Zhang JW. The role, mechanism and potentially therapeutic application of microRNA-29 family in acute myeloid leukemia. Cell death and differentiation. 2014; 21:100-112.
166. Huang X, Schwind S, Yu B, Santhanam R, Wang H, Hoellerbauer P, Mims A, Klisovic R, Walker AR, Chan KK, Blum W, Perrotti D, Byrd JC, Bloomfield CD, Caligiuri MA, Lee RJ, et al. Targeted delivery of microRNA-29b by transferrin-conjugated anionic lipopolyplex nanoparticles:a novel therapeutic strategy in acute myeloid leukemia. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19:2355-2367.
167. Mizuno S, Chijiwa T, Okamura T, Akashi K, Fukumaki Y, Niho Y and Sasaki H. Expression of DNA methyltransferases DNMT1, 3A, and 3B in normal hematopoiesis and in acute and chronic myelogenous leukemia. Blood. 2001; 97:1172-1179.
168. Mishra A, Liu S, Sams GH, Curphey DP, Santhanam R, Rush LJ, Schaefer D, Falkenberg LG, Sullivan L, Jaroncyk L, Yang X, Fisk H, Wu LC, Hickey C, Chandler JC, Wu YZ, et al. Aberrant overexpression of IL-15 initiates large granular lymphocyte leukemia through chromosomal instability and DNA hypermethylation. Cancer cell. 2012; 22:645-655.
169. Blum W, Garzon R, Klisovic RB, Schwind S, Walker A, Geyer S, Liu S, Havelange V, Becker H, Schaaf L, Mickle J, Devine H, Kefauver C, Devine SM, Chan KK, Heerema NA, et al. Clinical response and miR-29b predictive significance in older AML patients treated with a 10-day schedule of decitabine. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107:7473-7478.
170. Mims A, Walker AR, Huang X, Sun J, Wang H, Santhanam R, Dorrance AM, Walker C, Hoellerbauer P, Tarighat SS, Chan KK, Klisovic RB, Perrotti D, Caligiuri MA, Byrd JC, Chen CS, et al. Increased anti-leukemic activity of decitabine via AR-42-induced upregulation of miR-29b:a novel epigenetic-targeting approach in acute myeloid leukemia. Leukemia. 2013; 27:871-878.
171. Blum W, Schwind S, Tarighat SS, Geyer S, Eisfeld AK, Whitman S, Walker A, Klisovic R, Byrd JC, Santhanam R, Wang H, Curfman JP, Devine SM, Jacob S, Garr C, Kefauver C, et al. Clinical and pharmacodynamic activity of bortezomib and decitabine in acute myeloid leukemia. Blood. 2012; 119:6025-6031.
172. Xu Z, Zhang L, Fei X, Yi X, Li W and Wang Q. The miR-29b-Sirt1 axis regulates self-renewal of mouse embryonic stem cells in response to reactive oxygen species. Cellular signalling. 2014; 26:1500-1505.
173. Li Y, Wang H, Tao K, Xiao Q, Huang Z, Zhong L, Cao W, Wen J and Feng W. miR-29b suppresses CML cell proliferation and induces apoptosis via regulation of BCR/ABL1 protein. Experimental cell research. 2013; 319:1094-1101.
174. Lee TY, Ezelle HJ, Venkataraman T, Lapidus RG, Scheibner KA and Hassel BA. Regulation of human RNase-L by the miR-29 family reveals a novel oncogenic role in chronic myelogenous leukemia. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research. 2013; 33:34-42.
175. Di Lisio L, Sanchez-Beato M, Gomez-Lopez G, Rodriguez ME, Montes-Moreno S, Mollejo M, Menarguez J, Martinez MA, Alves FJ, Pisano DG, Piris MA and Martinez N. MicroRNA signatures in B-cell lymphomas. Blood cancer journal. 2012; 2:e57.
176. Ruiz-Ballesteros E, Mollejo M, Mateo M, Algara P, Martinez P and Piris MA. MicroRNA losses in the frequently deleted region of 7q in SMZL. Leukemia. 2007; 21:2547-2549.
177. Zhao JJ, Lin J, Lwin T, Yang H, Guo J, Kong W, Dessureault S, Moscinski LC, Rezania D, Dalton WS, Sotomayor E, Tao J and Cheng JQ. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood. 2010; 115:2630-2639.
178. Zhang X, Zhao X, Fiskus W, Lin J, Lwin T, Rao R, Zhang Y, Chan JC, Fu K, Marquez VE, Chen-Kiang S, Moscinski LC, Seto E, Dalton WS, Wright KL, Sotomayor E, et al. Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer cell. 2012; 22:506-523.
179. de Carvalho F, Colleoni GW, Almeida MS, Carvalho AL and Vettore AL. TGFbetaR2 aberrant methylation is a potential prognostic marker and therapeutic target in multiple myeloma. International journal of cancer Journal international du cancer. 2009; 125:1985-1991.
180. Zhang P, Huang B, Xu X and Sessa WC. Ten-eleven translocation (Tet) and thymine DNA glycosylase (TDG), components of the demethylation pathway, are direct targets of miRNA-29a. Biochemical and biophysical research communications. 2013; 437:368-373.
181. Wang C, Bian Z, Wei D and Zhang JG. miR-29b regulates migration of human breast cancer cells. Molecular and cellular biochemistry. 2011; 352:197-207.
182. Wang C, Gao C, Zhuang JL, Ding C and Wang Y. A combined approach identifies three mRNAs that are downregulated by microRNA-29b and promote invasion ability in the breast cancer cell line MCF-7. Journal of cancer research and clinical oncology. 2012; 138:2127-2136.
183. Zhao X, Pan F, Holt CM, Lewis AL and Lu JR. Controlled delivery of antisense oligonucleotides: a brief review of current strategies. Expert opinion on drug delivery. 2009; 6:673-686.
184. Yan J, Guo X, Xia J, Shan T, Gu C, Liang Z, Zhao W and Jin S. MiR-148a regulates MEG3 in gastric cancer by targeting DNA methyltransferase 1. Med Oncol. 2014; 31:879.
185. Gailhouste L, Gomez-Santos L, Hagiwara K, Hatada I, Kitagawa N, Kawaharada K, Thirion M, Kosaka N, Takahashi RU, Shibata T, Miyajima A and Ochiya T. miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology. 2013; 58:1153-1165.
186. Xiang Y, Ma N, Wang D, Zhang Y, Zhou J, Wu G, Zhao R, Huang H, Wang X, Qiao Y, Li F, Han D, Wang L, Zhang G and Gao X. MiR-152 and miR-185 co-contribute to ovarian cancer cells cisplatin sensitivity by targeting DNMT1 directly: a novel epigenetic therapy independent of decitabine. Oncogene. 2014; 33:378-386.
187. Das S, Foley N, Bryan K, Watters KM, Bray I, Murphy DM, Buckley PG and Stallings RL. MicroRNA mediates DNA demethylation events triggered by retinoic acid during neuroblastoma cell differentiation. Cancer research. 2010; 70:7874-7881.
188. Nishioka C, Ikezoe T, Yang J, Nobumoto A, Tsuda M and Yokoyama A. Downregulation of miR-217 correlates with resistance of Ph(+) leukemia cells to ABL tyrosine kinase inhibitors. Cancer science. 2014; 105:297-307.
189. Tang H, Liu P, Yang L, Xie X, Ye F, Wu M, Liu X, Chen B, Zhang L and Xie X. miR-185 suppresses tumor proliferation by directly targeting E2F6 and DNMT1 and indirectly upregulating BRCA1 in triple-negative breast cancer. Molecular cancer therapeutics. 2014; 13:3185-3197.
190. Takata A, Otsuka M, Yoshikawa T, Kishikawa T, Hikiba Y, Obi S, Goto T, Kang YJ, Maeda S, Yoshida H, Omata M, Asahara H and Koike K. MicroRNA-140 acts as a liver tumor suppressor by controlling NF-kappaB activity by directly targeting DNA methyltransferase 1 (Dnmt1) expression. Hepatology. 2013; 57:162-170.
191. Wang H, Wu J, Meng X, Ying X, Zuo Y, Liu R, Pan Z, Kang T and Huang W. MicroRNA-342 inhibits colorectal cancer cell proliferation and invasion by directly targeting DNA methyltransferase 1. Carcinogenesis. 2011; 32:1033-1042.
192. Shen JZ, Zhang YY, Fu HY, Wu DS and Zhou HR. Overexpression of microRNA-143 inhibits growth and induces apoptosis in human leukemia cells. Oncology reports. 2014; 31:2035-2042.
193. Chen BF, Gu S, Suen YK, Li L and Chan WY. microRNA-199a-3p, DNMT3A, and aberrant DNA methylation in testicular cancer. Epigenetics: official journal of the DNA Methylation Society. 2014; 9:119-128.
194. Nohata N, Hanazawa T, Kinoshita T, Inamine A, Kikkawa N, Itesako T, Yoshino H, Enokida H, Nakagawa M, Okamoto Y and Seki N. Tumour-suppressive microRNA-874 contributes to cell proliferation through targeting of histone deacetylase 1 in head and neck squamous cell carcinoma. British journal of cancer. 2013; 108:1648-1658.
195. Shen Q, Yao Q, Sun J, Feng L, Lu H, Ma Y, Liu L, Wang F, Li J, Yue Y, Jin H and Wang X. Downregulation of histone deacetylase 1 by microRNA-520h contributes to the chemotherapeutic effect of doxorubicin. FEBS letters. 2014; 588:184-191.
196. Noonan EJ, Place RF, Basak S, Pookot D and Li LC. miR-449a causes Rb-dependent cell cycle arrest and senescence in prostate cancer cells. Oncotarget. 2010; 1:349-358.
197. Noh JH, Chang YG, Kim MG, Jung KH, Kim JK, Bae HJ, Eun JW, Shen Q, Kim SJ, Kwon SH, Park WS, Lee JY and Nam SW. MiR-145 functions as a tumor suppressor by directly targeting histone deacetylase 2 in liver cancer. Cancer letters. 2013; 335:455-462.
198. Ren J, Huang HJ, Gong Y, Yue S, Tang LM and Cheng SY. MicroRNA-206 suppresses gastric cancer cell growth and metastasis. Cell & bioscience. 2014; 4:26.
199. Yuan JH, Yang F, Chen BF, Lu Z, Huo XS, Zhou WP, Wang F and Sun SH. The histone deacetylase 4/SP1/microrna-200a regulatory network contributes to aberrant histone acetylation in hepatocellular carcinoma. Hepatology. 2011; 54:2025-2035.
200. Iliopoulos D, Lindahl-Allen M, Polytarchou C, Hirsch HA, Tsichlis PN and Struhl K. Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Molecular cell. 2010; 39:761-772.
201. Carvalho J, van Grieken NC, Pereira PM, Sousa S, Tijssen M, Buffart TE, Diosdado B, Grabsch H, Santos MA, Meijer G, Seruca R, Carvalho B and Oliveira C. Lack of microRNA-101 causes E-cadherin functional deregulation through EZH2 up-regulation in intestinal gastric cancer. The Journal of pathology. 2012; 228:31-44.
202. Penna E, Orso F and Taverna D. miR-214 as a Key Hub that Controls Cancer Networks: Small Player, Multiple Functions. The Journal of investigative dermatology. 2015; 135:960-969.
203. Bao B, Wang Z, Ali S, Ahmad A, Azmi AS, Sarkar SH, Banerjee S, Kong D, Li Y, Thakur S and Sarkar FH. Metformin inhibits cell proliferation, migration and invasion by attenuating CSC function mediated by deregulating miRNAs in pancreatic cancer cells. Cancer Prev Res (Phila). 2012; 5:355-364.
204. Bestor TH. The DNA methyltransferases of mammals. Human molecular genetics. 2000; 9:2395-2402.
205. Deaton AM and Bird A. CpG islands and the regulation of transcription. Genes & development. 2011; 25:1010-1022.
206. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nature reviews Genetics. 2012; 13:484-492.
207. Toyota M, Kopecky KJ, Toyota MO, Jair KW, Willman CL and Issa JP. Methylation profiling in acute myeloid leukemia. Blood. 2001; 97:2823-2829.
208. Song YF, Xu R, Zhang XH, Chen BB, Chen Q, Chen YM and Xie Y. High-frequency promoter hypermethylation of the deleted in liver cancer-1 gene in multiple myeloma. Journal of clinical pathology. 2006; 59:947-951.
209. Stanganelli C, Arbelbide J, Fantl DB, Corrado C and Slavutsky I. DNA methylation analysis of tumor suppressor genes in monoclonal gammopathy of undetermined significance. Annals of hematology. 2010; 89:191-199.
210. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, An J, Lamperti ED, Koh KP, Ganetzky R, Liu XS, Aravind L, Agarwal S, Maciejewski JP and Rao A. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature. 2010; 468:839-843.
211. Guo JU, Su Y, Zhong C, Ming GL and Song H. Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond. Cell Cycle. 2011; 10:2662-2668.
212. Shih AH, Abdel-Wahab O, Patel JP and Levine RL. The role of mutations in epigenetic regulators in myeloid malignancies. Nature reviews Cancer. 2012; 12:599-612.
213. Kihslinger JE and Godley LA. The use of hypomethylating agents in the treatment of hematologic malignancies. Leukemia & lymphoma. 2007; 48:1676-1695.
214. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S and van Kuilenburg AB. Histone deacetylases (HDACs):characterization of the classical HDAC family. The Biochemical journal. 2003; 370:737-749.
215. Selvi RB and Kundu TK. Reversible acetylation of chromatin: implication in regulation of gene expression, disease and therapeutics. Biotechnology journal. 2009; 4:375-390.
216. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV and Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009; 325:834-840.
217. Mann BS, Johnson JR, Cohen MH, Justice R and Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. The oncologist. 2007; 12:1247-1252.
218. Dimicoli S, Jabbour E, Borthakur G, Kadia T, Estrov Z, Yang H, Kelly M, Pierce S, Kantarjian H and Garcia-Manero G. Phase II study of the histone deacetylase inhibitor panobinostat (LBH589) in patients with low or intermediate-1 risk myelodysplastic syndrome. American journal of hematology. 2012; 87:127-129.
219. Kaufman JL, Fabre C, Lonial S and Richardson PG. Histone deacetylase inhibitors in multiple myeloma: rationale and evidence for their use in combination therapy. Clinical lymphoma, myeloma & leukemia. 2013; 13:370-376.
220. Greer EL and Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nature reviews Genetics. 2012; 13:343-357.
221. Albert M and Helin K. Histone methyltransferases in cancer. Seminars in cell & developmental biology. 2010; 21:209-220.
222. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, Liu Y, Graves AP, Della Pietra A, 3rd, Diaz E, LaFrance LV, Mellinger M, Duquenne C, Tian X, Kruger RG, McHugh CF, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. 2012; 492:108-112.
223. Kroeze LI, Nikoloski G, da Silva-Coelho P, van Hoogen P, Stevens-Linders E, Kuiper RP, Schnittger S, Haferlach T, Pahl HL, van der Reijden BA and Jansen JH. Genetic defects in PRC2 components other than EZH2 are not common in myeloid malignancies. Blood. 2012; 119:1318-1319.
224. Martinez-Garcia E, Popovic R, Min DJ, Sweet SM, Thomas PM, Zamdborg L, Heffner A, Will C, Lamy L, Staudt LM, Levens DL, Kelleher NL and Licht JD. The MMSET histone methyl transferase switches global histone methylation and alters gene expression in t(4;14) multiple myeloma cells. Blood. 2011; 117:211-220.