MicroRNA-150 Expression Induces Myeloid Differentiation of Human Acute Leukemia Cells and Normal Hematopoietic Progenitors

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Morris, Valerie A ^a,b   Zhang, Ailin ^a   Yang, Taimei ^a   Stirewalt, Derek L ^a   Ramamurthy, Ranjani ^b   Meshinchi, Soheil ^a   Oehler, Vivian G ^a,b  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN EPSILON; CD11B ANTIGEN; CD34 ANTIGEN; MICRORNA; MICRORNA 150; PROTEIN MYB; RETINOIC ACID RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; ARTICLE; CELL DIFFERENTIATION; CEPBA GENE; CEPBE GENE; CHILD; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TARGETING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LEUKEMIA CELL LINE; LEUKEMOGENESIS; NUCLEOTIDE SEQUENCE; ONCOGENE MYB; PHENOTYPE;

ANTIGENS, CD34; CELL DIFFERENTIATION; CELL LINE, TUMOR; GENE EXPRESSION PROFILING; HEMATOPOIETIC STEM CELLS; HL-60 CELLS; HUMANS; K562 CELLS; LEUKEMIA, MYELOID, ACUTE; MICRORNAS; MYELOID CELLS; RECEPTORS, RETINOIC ACID; SIGNAL TRANSDUCTION;

EID: 84884560027     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075815     Document Type: Article

References (73)

1. Marcucci G, Haferlach T, Döhner H, (2011) Molecular genetics of adult acute myeloid leukemia: Prognostic and therapeutic implications. J Clin Oncol 29: 475-486. doi:10.1200/JCO.2010.30.2554. PubMed: 21220609.
2. Melo JV, Barnes DJ, (2007) Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer 7: 441-453. doi:10.1038/nrc2147. PubMed: 17522713.
3. Inui M, Martello G, Piccolo S, (2010) MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 11: 252-263. doi:10.1038/nrm2868. PubMed: 20216554.
4. Farazi TA, Spitzer JI, Morozov P, Tuschl T, (2011) miRNAs in human cancer. J Pathol 223: 102-115. doi:10.1002/path.2806. PubMed: 21125669. doi:10.1002/path.2806.
5. Graf T, Enver T, (2009) Forcing cells to change lineages. Nature 462: 587-594. doi:10.1038/nature08533. PubMed: 19956253.
6. Laslo P, Pongubala JM, Lancki DW, Singh H, (2008) Gene regulatory networks directing myeloid and lymphoid cell fates within the immune system. Semin Immunol 20: 228-235. doi:10.1016/j.smim.2008.08.003. PubMed: 18771937.
7. Rosenbauer F, Tenen DG, (2007) Transcription factors in myeloid development: Balancing differentiation with transformation. Nat Rev Immunol 7: 105-117. doi:10.1038/nri2024. PubMed: 17259967.
8. Georgantas RW 3rd, Hildreth R, Morisot S, Alder J, Liu CG, et al. (2007) CD34+ hematopoietic stem-progenitor cell microRNA expression and function: A circuit diagram of differentiation control. Proc Natl Acad Sci U S A 104: 2750-2755. doi:10.1073/pnas.0610983104. PubMed: 17293455.
9. Lu J, Guo S, Ebert BL, Zhang H, Peng X, et al. (2008) MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell 14: 843-853. doi:10.1016/j.devcel.2008.03.012. PubMed: 18539114.
10. Petriv OI, Kuchenbauer F, Delaney AD, Lecault V, White A, et al. (2010) Comprehensive microRNA expression profiling of the hematopoietic hierarchy. Proc Natl Acad Sci U S A 107: 15443-15448. doi:10.1073/pnas.1009320107. PubMed: 20702766.
11. O'Connell RM, Zhao JL, Rao DS, (2011) MicroRNA function in myeloid biology. Blood 118: 2960-2969. doi:10.1182/blood-2011-03-291971. PubMed: 21725054.
12. El Gazzar M, McCall CE, (2011) MicroRNAs regulatory networks in myeloid lineage development and differentiation: Regulators of the regulators. Immunol Cell Biol 90: 587-593. doi:10.1038/icb.2011.74. PubMed: 21912420. doi:10.1038/icb.2011.74.
13. Bissels U, Bosio A, Wagner W, (2011) MicroRNAs are shaping the hematopoietic landscape. Haematologica 97: 160-167. doi:10.3324/haematol.2011.051730. PubMed: 22058204.
14. Ghani S, Riemke P, Schönheit J, Lenze D, Stumm J, et al. (2011) Macrophage development from HSCs requires PU.1-coordinated microRNA expression. Blood 118: 2275-2284. doi:10.1182/blood-2011-02-335141. PubMed: 21730352.
15. Rosa A, Ballarino M, Sorrentino A, Sthandier O, De Angelis FG, et al. (2007) The interplay between the master transcription factor PU.1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci U S A 104: 19849-19854. doi:10.1073/pnas.0706963104. PubMed: 18056638.
16. Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML, et al. (2005) A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 123: 819-831. doi:10.1016/j.cell.2005.09.023. PubMed: 16325577.
17. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, et al. (2008) Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 451: 1125-1129. doi:10.1038/nature06607. PubMed: 18278031.
18. Li Z, Lu J, Sun M, Mi S, Zhang H, et al. (2008) Distinct microRNA expression profiles in acute myeloid leukemia with common translocations. Proc Natl Acad Sci U S A 105: 15535-15540. doi:10.1073/pnas.0808266105. PubMed: 18832181.
19. Marcucci G, Mrózek K, Radmacher MD, Garzon R, Bloomfield CD, (2011) The prognostic and functional role of microRNAs in acute myeloid leukemia. Blood 117: 1121-1129. doi:10.1182/blood-2010-09-191312. PubMed: 21045193.
20. Eiring AM, Harb JG, Neviani P, Garton C, Oaks JJ, et al. (2010) miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 140: 652-665. doi:10.1016/j.cell.2010.01.007. PubMed: 20211135.
21. Wang XS, Gong JN, Yu J, Wang F, Zhang XH, et al. (2012) MicroRNA-29a and microRNA-142-3p are regulators of myeloid differentiation and acute myeloid leukemia. Blood 119: 4992-5004. doi:10.1182/blood-2011-10-385716. PubMed: 22493297.
22. Senyuk V, Zhang Y, Liu Y, Ming M, Premanand K, et al. (2013) Critical role of miR-9 in myelopoiesis and EVI1-induced leukemogenesis. Proc Natl Acad Sci U S A 110: 5594-5599. doi:10.1073/pnas.1302645110. PubMed: 23509296. doi:10.1073/pnas.1302645110.
23. Li Y, Gao L, Luo X, Wang L, Gao X, et al. (2013) Epigenetic silencing of microRNA-193a contributes to leukemogenesis in t(8;21) acute myeloid leukemia by activating the PTEN/PI3K signal pathway. Blood 121: 499-509. doi:10.1182/blood-2012-07-444729. PubMed: 23223432. doi:10.1182/blood-2012-07-444729.
24. Agirre X, Jiménez-Velasco A, Jose-Eneriz, San E, Garate L, Bandres E,et al (2008) Down-regulation of hsa-miR-10a in chronic myeloid leukemia CD34+ cells increases USF2-mediated cell growth. Mol Cancer Res 6: 1830-1840. doi:10.1158/1541-7786.MCR-08-0167. PubMed: 19074828.
25. Machová Poláková K, Lopotová T, Klamová H, Burda P, Trněný M, et al. (2011) Expression patterns of microRNAs associated with CML phases and their disease related targets. Mol Cancer 1041:: 41-. doi:10.1186/1476-4598-10-41. PubMed: 21501493.
26. Li Z, Huang H, Li Y, Jiang X, Chen P, et al. (2012) Up-regulation of a HOXA-PBX3 homeobox-gene signature following down-regulation of miR-181 is associated with adverse prognosis in patients with cytogenetically abnormal AML. Blood 119: 2314-2324. doi:10.1182/blood-2011-10-386235. PubMed: 22251480. doi:10.1182/blood-2011-10-386235.
27. Jiang X, Huang H, Li Z, Li Y, Wang X, et al. (2012) Blockade of miR-150 maturation by MLL-fusion/MYC/LIN-28 is required for MLL-associated leukemia. Cancer Cell 22: 524-535. doi:10.1016/j.ccr.2012.08.028. PubMed: 23079661. doi:10.1016/j.ccr.2012.08.028.
28. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, et al. (2007) MiR-150 controls B cell differentiation by targeting the transcription factor c-myb. Cell 131: 146-159. doi:10.1016/j.cell.2007.07.021. PubMed: 17923094.
29. Zhou B, Wang S, Mayr C, Bartel DP, Lodish HF, (2007) miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely. Proc Natl Acad Sci U S A 104: 7080-7085. doi:10.1073/pnas.0702409104. PubMed: 17438277.
30. Bezman NA, Chakraborty T, Bender T, Lanier LL, (2011) miR-150 regulates the development of NK and iNKT cells. J Exp Med 208: 2717-2731. doi:10.1084/jem.20111386. PubMed: 22124110.
31. Watanabe A, Tagawa H, Yamashita J, Teshima K, Nara M, et al. (2011) The role of microRNA-150 as a tumor suppressor in malignant lymphoma. Leukemia 25: 1324-1334. doi:10.1038/leu.2011.81. PubMed: 21502955.
32. Bianchi E, Zini R, Salati S, Tenedini E, Norfo R, et al. (2010) C-myb supports erythropoiesis through the transactivation of KLF1 and LMO2 expression. Blood 116: e99-110. doi:10.1182/blood-2009-08-238311. PubMed: 20686118.
33. Liebermann DA, Hoffman B, (1994) Differentiation primary response genes and proto-oncogenes as positive and negative regulators of terminal hematopoietic cell differentiation. Stem Cells 12: 352-369. doi:10.1002/stem.5530120402. PubMed: 7951003.
34. Patel JP, Gönen M, Figueroa ME, Fernandez H, Sun Z, et al. (2012) Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N Engl J Med 366: 1079-1089. doi:10.1056/NEJMoa1112304. PubMed: 22417203. doi:10.1056/NEJMoa1112304.
35. Oehler VG, Guthrie KA, Cummings CL, Sabo K, Wood BL, et al. (2009) The preferentially expressed antigen in melanoma (PRAME) inhibits myeloid differentiation in normal hematopoietic and leukemic progenitor cells. Blood 114: 3299-3308. doi:10.1182/blood-2008-07-170282. PubMed: 19625708.
36. Stegmaier K, Ross KN, Colavito SA, O'Malley S, Stockwell BR, et al. (2004) Gene expression-based high-throughput screening(GE-HTS) and application to leukemia differentiation. Nat Genet 36: 257-263. doi:10.1038/ng1305. PubMed: 14770183.
37. Hahn CK, Berchuck JE, Ross KN, Kakoza RM, Clauser K, et al. (2009) Proteomic and genetic approaches identify syk as an AML target. Cancer Cell 16: 281-294. doi:10.1016/j.ccr.2009.08.018. PubMed: 19800574.
38. Roth J, Vogl T, Sorg C, Sunderkötter C, (2003) Phagocyte-specific S100 proteins: A novel group of proinflammatory molecules. Trends Immunol 24: 155-158. doi:10.1016/S1471-4906(03)00062-0. PubMed: 12697438.
39. Kuchenbauer F, Mah SM, Heuser M, McPherson A, Rüschmann J, et al. (2011) Comprehensive analysis of mammalian miRNA* species and their role in myeloid cells. Blood 118: 3350-3358. doi:10.1182/blood-2010-10-312454. PubMed: 21628414.
40. Huang X, Gschweng E, Van Handel B, Cheng D, Mikkola HK, et al. (2011) Regulated expression of microRNAs-126/126* inhibits erythropoiesis from human embryonic stem cells. Blood 117: 2157-2165. doi:10.1182/blood-2010-08-302711. PubMed: 21163928.
41. Varnum-Finney B, Xu L, Brashem-Stein C, Nourigat C, Flowers D, et al. (2000) Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat Med 61278-1281:: 1278-81. doi:10.1038/81390. PubMed: 11062542.
42. Apfel C, Bauer F, Crettaz M, Forni L, Kamber M, et al. (1992) A retinoic acid receptor alpha antagonist selectively counteracts retinoic acid effects. Proc Natl Acad Sci U S A 89: 7129-7133. doi:10.1073/pnas.89.15.7129. PubMed: 1323127.
43. Zuber J, Rappaport AR, Luo W, Wang E, Chen C, et al. (2011) An integrated approach to dissecting oncogene addiction implicates a myb-coordinated self-renewal program as essential for leukemia maintenance. Genes Dev 25: 1628-1640. doi:10.1101/gad.17269211. PubMed: 21828272.
44. Zhao H, Kalota A, Jin S, Gewirtz AM, (2009) The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood 113: 505-516. doi:10.1182/blood-2008-01-136218. PubMed: 18818396.
45. Gao SM, Yang J, Chen C, Zhang S, Xing CY, et al. (2011) miR-15a/16-1 enhances retinoic acid-mediated differentiation of leukemic cells and is up-regulated by retinoic acid. Leuk Lymphoma 52: 2365-2371. doi:10.3109/10428194.2011.601476. PubMed: 21838537.
46. Ferrari S, Donelli A, Manfredini R, Sarti M, Roncaglia R, et al. (1990) Differential effects of c-myb and c-fes antisense oligodeoxynucleotides on granulocytic differentiation of human myeloid leukemia HL60 cells. Cell Growth Differ 1: 543-548. PubMed: 2088479.
47. Alemdehy MF, van Boxtel NG, de Looper HW, van den Berge IJ, Sanders MA, et al. (2012) Dicer1 deletion in myeloid-committed progenitors causes neutrophil dysplasia and blocks macrophage/dendritic cell development in mice. Blood 119: 4723-4730. doi:10.1182/blood-2011-10-386359. PubMed: 22353998.
48. Garzon R, Pichiorri F, Palumbo T, Visentini M, Aqeilan R, et al. (2007) MicroRNA gene expression during retinoic acid-induced differentiation of human acute promyelocytic leukemia. Oncogene 26: 4148-4157. doi:10.1038/sj.onc.1210186. PubMed: 17260024.
49. De Marchis ML, Ballarino M, Salvatori B, Puzzolo MC, Bozzoni I, et al. (2009) A new molecular network comprising PU.1, interferon regulatory factor proteins and miR-342 stimulates ATRA-mediated granulocytic differentiation of acute promyelocytic leukemia cells. Leukemia 23: 856-862. doi:10.1038/leu.2008.372. PubMed: 19151778.
50. Koschmieder S, Halmos B, Levantini E, Tenen DG, (2009) Dysregulation of the C/EBPalpha differentiation pathway in human cancer. J Clin Oncol 27: 619-628. doi:10.1200/JCO.2008.17.9812. PubMed: 19075268.
51. Radomska HS, Huettner CS, Zhang P, Cheng T, Scadden DT, et al. (1998) CCAAT/enhancer binding protein alpha is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Mol Cell Biol 18: 4301-4314. PubMed: 9632814.
52. Bedi R, Du J, Sharma AK, Gomes I, Ackerman SJ, (2009) Human C/EBP-epsilon activator and repressor isoforms differentially reprogram myeloid lineage commitment and differentiation. Blood 113: 317-327. doi:10.1182/blood-2008-02-139741. PubMed: 18832658. doi:10.1182/blood-2008-02-139741.
53. Halene S, Gaines P, Sun H, Zibello T, Lin S, et al. (2010) C/EBPepsilon directs granulocytic-vs-monocytic lineage determination and confers chemotactic function via hlx. Exp Hematol 38: 90-103. doi:10.1016/j.exphem.2009.11.004. PubMed: 19925846. doi:10.1016/j.exphem.2009.11.004.
54. Kaplan IM, Morisot S, Heiser D, Cheng WC, Kim MJ, et al. (2011) Deletion of tristetraprolin caused spontaneous reactive granulopoiesis by a non-cell-autonomous mechanism without disturbing long-term hematopoietic stem cell quiescence. J Immunol 186: 2826-2834. doi:10.4049/jimmunol.1002806. PubMed: 21270394.
55. Tabe Y, Konopleva M, Andreeff M, Ohsaka A, (2012) Effects of PPARgamma ligands on leukemia. PPAR Res. doi:10.1155/2012/483656.
56. Tano N, Kim HW, Ashraf M, (2011) microRNA-150 regulates mobilization and migration of bone marrow-derived mononuclear cells by targeting Cxcr4. PLOS ONE 6: e23114. doi:10.1371/journal.pone.0023114. PubMed: 22039399.
57. Delgado MD, Albajar M, Gomez-Casares MT, Batlle A, León J, (2013) MYC oncogene in myeloid neoplasias. Clin Transl Oncol 15: 87-94. doi:10.1007/s12094-012-0926-8. PubMed: 22911553. doi:10.1007/s12094-012-0926-8.
58. Lidonnici MR, Corradini F, Waldron T, Bender TP, Calabretta B, (2008) Requirement of c-myb for p210(BCR/ABL)-dependent transformation of hematopoietic progenitors and leukemogenesis. Blood 111: 4771-4779. doi:10.1182/blood-2007-08-105072. PubMed: 18227349.
59. Walz C, Ahmed W, Lazarides K, Betancur M, Patel N, et al. (2012) Essential role for Stat5a/b in myeloproliferative neoplasms induced by BCR-ABL1 and JAK2V617F in mice. Blood 119: 3550-3560. doi:10.1182/blood-2011-12-397554. PubMed: 22234689.
60. Yamada Y, Warren AJ, Dobson C, Forster A, Pannell R, et al. (1998) The T cell leukemia LIM protein Lmo2 is necessary for adult mouse hematopoiesis. Proc Natl Acad Sci U S A 95: 3890-3895. doi:10.1073/pnas.95.7.3890. PubMed: 9520463.
61. Malumbres R, Sarosiek KA, Cubedo E, Ruiz JW, Jiang X, et al. (2009) Differentiation stage-specific expression of microRNAs in B lymphocytes and diffuse large B-cell lymphomas. Blood 113: 3754-3764. doi:10.1182/blood-2008-10-184077. PubMed: 19047678.
62. Sanz MA, Lo-Coco F, (2011) Modern approaches to treating acute promyelocytic leukemia. J Clin Oncol 29: 495-503. doi:10.1200/JCO.2010.32.1067. PubMed: 21220600.
63. Breccia M, Lo-Coco F, (2012) Arsenic trioxide for management of acute promyelocytic leukemia: Current evidence on its role in front-line therapy and recurrent disease. Expert Opin Pharmacother 13: 1031-1043. doi:10.1517/14656566.2012.677436. PubMed: 22468778. doi:10.1517/14656566.2012.677436.
64. Kubonishi I, Machida K, Niiya K, Sonobe H, Ohtsuki Y, et al. (1984) Establishment of a new peroxidase-positive human myeloid cell line, PL-21. Blood 63: 254-259. PubMed: 6362749.
65. Koeffler HP, Golde DW, (1978) Acute myelogenous leukemia: A human cell line responsive to colony-stimulating activity. Science 200: 1153-1154. doi:10.1126/science.306682. PubMed: 306682.
66. Lange B, Valtieri M, Santoli D, Caracciolo D, Mavilio F, et al. (1987) Growth factor requirements of childhood acute leukemia: Establishment of GM-CSF-dependent cell lines. Blood 70: 192-199. PubMed: 3496132.
67. Lozzio CB, Lozzio BB, (1975) Human chronic myelogenous leukemia cell-line with positive philadelphia chromosome. Blood 45: 321-334. PubMed: 163658.
68. Seigneurin D, Champelovier P, Mouchiroud G, Berthier R, Leroux D, et al. (1987) Human chronic myeloid leukemic cell line with positive philadelphia chromosome exhibits megakaryocytic and erythroid characteristics. Exp Hematol 15: 822-832. PubMed: 3476310.
69. Kubonishi I, Miyoshi I, (1983) Establishment of a Ph1 chromosome-positive cell line from chronic myelogenous leukemia in blast crisis. Int J Cell Cloning 1: 105-117. doi:10.1002/stem.5530010205. PubMed: 6321612.
70. Collins SJ, Gallo RC, Gallagher RE, (1977) Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature 270: 347-349. doi:10.1038/270347a0. PubMed: 271272.
71. Lanotte M, Martin-Thouvenin V, Najman S, Balerini P, Valensi F, et al. (1991) NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood 77: 1080-1086. PubMed: 1995093.
72. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, et al. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26: 171-176. doi:10.1002/ijc.2910260208. PubMed: 6970727.
73. Nguyen HQ, Hoffman-Liebermann B, Liebermann DA, (1993) The zinc finger transcription factor egr-1 is essential for and restricts differentiation along the macrophage lineage. Cell 72: 197-209. doi:10.1016/0092-8674(93)90660-I. PubMed: 7678779.