Identification of nuclear-enriched miRNAs during mouse granulopoiesis

Journal of Hematology and Oncology

Volumn 7, Issue 1, 2014, Pages

  Wong, Justin J L ^a,b   Ritchie, William ^a,b   Gao, Dadi ^a,b   Lau, Katherine A ^a,b   Gonzalez, Maria ^a,b   Choudhary, Anupma ^c   Taft, Ryan J ^c   Rasko, John E J ^a,b,d   Holst, Jeff ^a,b  

^a CENTENARY INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d ROYAL PRINCE ALFRED HOSPITAL   (Australia)

Author keywords

Gene expression; Granulopoiesis; miRNAs; mRNA targets; Nuclear; Stem cell

Indexed keywords

LET 7 PROTEIN; MESSENGER RNA; MICRORNA; MICRORNA 1792; MICRORNA 467A; MICRORNA 690; MICRORNA 706; MICRORNA 709; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BONE MARROW CELL; CELL DENSITY; CELL FRACTIONATION; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GENE TARGETING; GRANULOCYTE; GRANULOPOIESIS; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMYELOCYTE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHOLE CELL;

ANIMALS; CELL LINE; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GRANULOCYTE PRECURSOR CELLS; GRANULOCYTES; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84902291652     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/1756-8722-7-42     Document Type: Article

References (74)

1. Identification of novel genes coding for small expressed RNAs. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T, Science 2001 294 853 858 10.1126/science.1064921 11679670
2. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Lau NC, Lim LP, Weinstein EG, Bartel DP, Science 2001 294 858 862 10.1126/science.1065062 11679671
3. An extensive class of small RNAs in Caenorhabditis elegans. Lee RC, Ambros V, Science 2001 294 862 864 10.1126/science.1065329 11679672
4. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R, Nat Genet 2008 40 1478 1483 10.1038/ng.250 18978791
5. GAM/ZFp/ZNF512B is central to a gene sensor circuitry involving cell-cycle regulators, TGFβ effectors, Drosha and microRNAs with opposite oncogenic potentials. Tili E, Michaille J-J, Liu C-G, Alder H, Taccioli C, Volinia S, Calin GA, Croce CM, Nucleic Acids Res 2010 38 7673 7688 10.1093/nar/gkq637 20639536
6. MicroRNAs and immunity: Tiny players in a big field. Taganov KD, Boldin MP, Baltimore D, Immunity 2007 26 133 137 10.1016/j.immuni.2007.02.005 17307699
7. MicroRNA control in the immune system: Basic principles. Xiao C, Rajewsky K, Cell 2009 136 26 36 10.1016/j.cell.2008.12.027 19135886
8. Differential microRNA regulation of HLA-C expression and its association with HIV control. Kulkarni S, Savan R, Qi Y, Gao X, Yuki Y, Bass SE, Martin MP, Hunt P, Deeks SG, Telenti A, Pereyra F, Goldstein D, Wolinsky S, Walker B, Young HA, Carrington M, Nature 2011 472 495 498 10.1038/nature09914 21499264
9. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Chen J-F, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang D-Z, Nat Genet 2006 38 228 233 10.1038/ng1725 16380711
10. A skin microRNA promotes differentiation by repressing 'stemness'. Yi R, Poy MN, Stoffel M, Fuchs E, Nature 2008 452 225 229 10.1038/nature06642 18311128
11. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. McKenna LB, Schug J, Vourekas A, McKenna JB, Bramswig NC, Friedman JR, Kaestner KH, Gastroenterol 2010 139 1654 1664 e1651 10.1053/j.gastro.2010.07.040
12. Transcription factors in myeloid development: Balancing differentiation with transformation. Rosenbauer F, Tenen DG, Nat Rev Immunol 2007 7 105 117 10.1038/nri2024 17259967
13. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Novershtern N, Subramanian A, Lawton LN, Mak RH, Haining WN, McConkey ME, Habib N, Yosef N, Chang CY, Shay T, Frampton GM, Drake ACB, Leskov I, Nilsson B, Preffer F, Dombkowski D, Evans JW, Liefeld T, Smutko JS, Chen J, Friedman N, Young RA, Golub TR, Regev A, Ebert BL, Cell 2011 144 296 309 10.1016/j.cell.2011.01.004 21241896
14. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O, Brummelkamp TR, Fleming MD, Camargo FD, Nature 2008 451 1125 1129 10.1038/nature06607 18278031
15. Cell-cycle regulator E2F1 and microRNA-223 comprise an autoregulatory negative feedback loop in acute myeloid leukemia. Pulikkan JA, Dengler V, Peramangalam PS, Peer Zada AA, Müller-Tidow C, Bohlander SK, Tenen DG, Behre G, Blood 2010 115 1768 1778 10.1182/blood-2009-08-240101 20029046
16. MicroRNA-146a disrupts hematopoietic differentiation and survival. Starczynowski DT, Kuchenbauer F, Wegrzyn J, Rouhi A, Petriv O, Hansen CL, Humphries RK, Karsan A, Exp Hematol 2011 39 167 178 e164 10.1016/j.exphem.2010. 09.011 20933052
17. Altered expression profiles of microRNAs during TPA-induced differentiation of HL-60 cells. Kasashima K, Nakamura Y, Kozu T, Biochem Biophys Res Commun 2004 322 403 410 10.1016/j.bbrc.2004.07.130 15325244
18. MicroRNA expression changes during human leukemic HL-60 cell differentiation induced by 4-hydroxynonenal, a product of lipid peroxidation. Pizzimenti S, Ferracin M, Sabbioni S, Toaldo C, Pettazzoni P, Dianzani MU, Negrini M, Barrera G, Free Radic Biol Med 2009 46 282 288 10.1016/j. freeradbiomed.2008.10.035 19022373
19. Transition of highly specific microRNA expression patterns in association with discrete maturation stages of human granulopoiesis. Sun SM, Dijkstra MK, Bijkerk AC, Brooimans RA, Valk PJM, Erkeland SJ, Löwenberg B, Jongen-Lavrencic M, Br J Haematol 2011 155 395 398 10.1111/j.1365-2141.2011. 08682.x 21554257
20. MicroRNA profiling in human neutrophils during bone marrow granulopoiesis and in vivo exudation. Larsen MT, Hother C, Häger M, Pedersen CC, Theilgaard-Mönch K, Borregaard N, Cowland JB, PLoS ONE 2013 8 58454 10.1371/journal.pone.0058454 23554893
21. MicroRNAs: Target recognition and regulatory functions. Bartel DP, Cell 2009 136 215 233 10.1016/j.cell.2009.01.002 19167326
22. Expression profiling of human immune cell subsets identifies miRNA-mRNA regulatory relationships correlated with cell type specific expression. Allantaz F, Cheng DT, Bergauer T, Ravindran P, Rossier MF, Ebeling M, Badi L, Reis B, Bitter H, D'Asaro M, Chiappe A, Sridhar S, Pacheco GD, Burczynski ME, Hochstrasser D, Vonderscher J, Matthes T, PLoS ONE 2012 7 29979 10.1371/journal.pone.0029979 22276136
23. MicroRNA-206 colocalizes with ribosome-rich regions in both the nucleolus and cytoplasm of rat myogenic cells. Ritland Politz JC, Zhang F, Pederson T, Proc Natl Acad Sci U S A 2006 103 18957 18962 10.1073/pnas.0609466103 17135348
24. A hexanucleotide element directs microRNA nuclear import. Hwang H-W, Wentzel EA, Mendell JT, Science 2007 315 97 100 10.1126/science.1136235 17204650
25. DNA damage-induced upregulation of miR-709 in the germline downregulates BORIS to counteract aberrant DNA hypomethylation. Tamminga J, Kathiria P, Koturbash I, Kovalchuk O, Cell Cycle 2008 7 3731 3736 10.4161/cc.7.23.7186 19029807
26. MicroRNAs with a nucleolar location. Ritland Politz JC, Hogan EM, Pederson T, RNA 2009 15 1705 1715 10.1261/rna.1470409 19628621
27. Deep sequencing of human nuclear and cytoplasmic small RNAs reveals an unexpectedly complex subcellular distribution of miRNAs and tRNA 3' trailers. Liao J-Y, Ma L-M, Guo Y-H, Zhang Y-C, Zhou H, Shao P, Chen Y-Q, Qu L-H, PLoS ONE 2010 5 10563 10.1371/journal.pone.0010563 20498841
28. Mature microRNAs identified in highly purified nuclei from HCT116 colon cancer cells. Park C-W, Zeng Y, Zhang X, Subramanian S, Steer CJ, RNA Biol 2010 7 606 614 10.4161/rna.7.5.13215 20864815
29. Nuclear-localized tiny RNAs are associated with transcription initiation and splice sites in metazoans. Taft RJ, Simons C, Nahkuri S, Oey H, Korbie DJ, Mercer TR, Holst J, Ritchie W, Wong JJL, Rasko JEJ, Rokhsar DS, Degnan BM, Mattick JS, Nat Struct Mol Biol 2010 17 1030 1034 10.1038/nsmb.1841 20622877
30. Nuclear and cytoplasmic localization of neural stem cell microRNAs. Jeffries CD, Fried HM, Perkins DO, RNA 2011 17 675 686 10.1261/rna.2006511 21363885
31. Mouse miRNA-709 directly regulates miRNA-15a/16-1 biogenesis at the posttranscriptional level in the nucleus: evidence for a microRNA hierarchy system. Tang R, Li L, Zhu D, Hou D, Cao T, Gu H, Zhang J, Chen J, Zhang C-Y, Zen K, Cell Res 2011 22 504 515 21862971
32. MicroRNA-373 induces expression of genes with complementary promoter sequences. Place RF, Li L-C, Pookot D, Noonan EJ, Dahiya R, Proc Natl Acad Sci U S A 2008 105 1608 1613 10.1073/pnas.0707594105 18227514
33. MicroRNA-directed transcriptional gene silencing in mammalian cells. Kim DH, Sætrom P, Snøve O, Rossi JJ, Proc Natl Acad Sci U S A 2008 105 16230 16235 10.1073/pnas.0808830105 18852463
34. An analysis of quantitative PCR reliability through replicates using the C method. Stowers CC, Haselton FR, Boczko EM, J Biomed Sci Eng 2010 3 459 469 10.4236/jbise.2010.35064 20634997
35. microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. Han Y-C, Park CY, Bhagat G, Zhang J, Wang Y, Fan J-B, Liu M, Zou Y, Weissman IL, Gu H, J Exp Med 2010 207 475 489 10.1084/jem.20090831 20212066
36. Gfi1 regulates miR-21 and miR-196b to control myelopoiesis. Velu CS, Baktula AM, Grimes HL, Blood 2009 113 4720 4728 10.1182/blood-2008-11-190215 19278956
37. mimiRNA: A microRNA expression profiler and classification resource designed to identify functional correlations between microRNAs and their targets. Ritchie W, Flamant S, Rasko JEJ, Bioinformatics 2010 26 223 227 10.1093/bioinformatics/btp649 19933167
38. miR-15 and miR-16 induce apoptosis by targeting BCL2. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu CG, Kipps TJ, Negrini M, Croce CM, Proc Natl Acad Sci U S A 2005 102 13944 13949 10.1073/pnas.0506654102 16166262
39. miR-29 and miR-30 regulate B-Myb expression during cellular senescence. Martinez I, Cazalla D, Almstead LL, Steitz JA, DiMaio D, Proc Natl Acad Sci U S A 2011 108 522 527 10.1073/pnas.1017346108 21187425
40. MicroRNA-26a Targets the Histone Methyltransferase Enhancer of Zeste homolog 2 during Myogenesis. Wong CF, Tellam RL, J Biol Chem 2008 283 9836 9843 10.1074/jbc.M709614200 18281287
41. Fast and effective prediction of microRNA/target duplexes. Rehmsmeier M, Stefen P, Höchmann M, Giegerich R, RNA 2004 10 1507 1517 10.1261/rna.5248604 15383676
42. Double-stranded regions are essential design components of potent inhibitors of RISC function. Vermeulen A, Robertson B, Dalby AB, Marshall WS, Karpilow J, Leake D, Khvorova A, Baskerville S, RNA 2007 13 723 730 10.1261/rna.448107 17400817
43. c-Myc Is a Critical Target for C/EBP in Granulopoiesis. Johansen LM, Iwama A, Lodie TA, Sasaki K, Felsher DW, Golub TR, Tenen DG, Mol Cell Biol 2001 21 3789 3806 10.1128/MCB.21.11.3789-3806.2001 11340171
44. MicroRNAs and their role in the generation of myeloid derived suppressor cells (MDSC) by cannabidiol in vivo. Hegde VL, Nagarkatti P, Nagarkatti M, J Immunol 2012 188 48.16
45. C/EBP regulated microRNA-34a targets E2F3 during granulopoiesis and is down-regulated in AML with CEBPA mutations. Pulikkan JA, Peramangalam PS, Dengler V, Ho PA, Preudhomme C, Meshinchi S, Christopeit M, Nibourel O, Müller-Tidow C, Bohlander SK, Tenen DG, Behre G, Blood 2010 116 5638 5649 10.1182/blood-2010-04-281600 20889924
46. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. 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, Andreeff M, Croce CM, Blood 2008 111 3183 3189 10.1182/blood-2007-07-098749 18187662
47. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Garzon R, Liu S, Fabbri M, Liu Z, Heaphy CEA, Callegari E, Schwind S, Pang J, Yu J, Muthusamy N, Havelange V, Volinia S, Blum W, Rush LJ, Perrotti D, Andreeff M, Bloomfield CD, Byrd JC, Chan K, Wu L-C, Croce CM, Marcucci G, Blood 2009 113 6411 6418 10.1182/blood-2008-07-170589 19211935
48. The miR-17-92 microRNA polycistron regulates MLL leukemia stem cell potential by modulating p21 expression. Wong P, Iwasaki M, Somervaille TCP, Ficara F, Carico C, Arnold C, Chen C-Z, Cleary ML, Cancer Res 2010 70 3833 3842 10.1158/0008-5472.CAN-09-3268 20406979
49. miR-223 suppresses differentiation of tumor-induced CD11b + Gr1 + myeloid-derived suppressor cells from bone marrow cells. Liu Q, Zhang M, Jiang X, Zhang Z, Dai L, Min S, Wu X, He Q, Liu J, Zhang Y, Zhang Z, Yang R, Int J Cancer 2011 129 2662 2673 10.1002/ijc.25921 21213211
50. c-Myb and p300 regulate hematopoietic stem cell proliferation and differentiation. Sandberg ML, Sutton SE, Pletcher MT, Wiltshire T, Tarantino LM, Hogenesch JB, Cooke MP, Dev Cell 2005 8 153 166 10.1016/j.devcel.2004.12.015 15691758
51. A microRNA polycistron as a potential human oncogene. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM, Nature 2005 435 828 833 10.1038/nature03552 15944707
52. mir-17-92, a cluster of miRNAs in the midst of the cancer network. Olive V, Jiang I, He L, Int J Biochem Cell Biol 2010 42 1348 1354 10.1016/j.biocel. 2010.03.004 20227518
53. Leukaemogenesis: more than mutant genes. Chen J, Odenike O, Rowley JD, Nat Rev Cancer 2010 10 23 36 10.1038/nrc2765 20029422
54. Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Muckenthaler MU, Ganser A, Eder M, Scherr M, Blood 2007 109 4399 4405 10.1182/blood-2006-09-045104 17284533
55. Micro-RNA response to imatinib mesylate in patients with chronic myeloid leukemia. Flamant S, Ritchie W, Guilhot J, Holst J, Bonnet M-L, Chomel J-C, Guilhot F, Turhan AG, Rasko JEJ, Haematologica 2010 95 1325 1333 10.3324/haematol.2009.020636 20460641
56. Response to imatinib mesylate in patients with chronic myeloproliferative diseases with rearrangements of the platelet-derived growth factor receptor beta. Apperley JF, Gardembas M, Melo JV, Russell-Jones R, Bain BJ, Baxter EJ, Chase A, Chessells JM, Colombat M, Dearden CE, Dimitrijevic S, Mahon F-X, Marin D, Nikolova Z, Olavarria E, Silberman S, Schultheis B, Cross NCP, Goldman JM, N Engl J Med 2002 347 481 487 10.1056/NEJMoa020150 12181402
57. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, Henderson JM, Kutok JL, Rajewsky K, Nat Immunol 2008 9 405 414 10.1038/ni1575 18327259
58. Targeted deletion reveals essential and overlapping functions of the miR-17-92 family of miRNA clusters. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T, Cell 2008 132 875 886 10.1016/j.cell.2008.02.019 18329372
59. Genetic screen identifies microRNA cluster 99b/let-7e/125a as a regulator of primitive hematopoietic cells. Gerrits A, Walasek MA, Olthof S, Weersing E, Ritsema M, Zwart E, van Os R, Bystrykh LV, de Haan G, Blood 2011 119 377 387 22123844
60. Dynamic microRNA gene transcription and processing during T cell development. Kirigin FF, Lindstedt K, Sellars M, Ciofani M, Low SL, Jones L, Bell F, Pauli F, Bonneau R, Myers RM, Littman DR, Chong MMW, J Immunol 2012 188 3257 3267 10.4049/jimmunol.1103175 22379031
61. Comprehensive microRNA expression profiling of the hematopoietic hierarchy. Petriv OI, Kuchenbauer F, Delaney AD, Lecault V, White A, Kent D, Marmolejo L, Heuser M, Berg T, Copley M, Ruschmann J, Sekulovic S, Benz C, Kuroda E, Ho V, Antignano F, Halim T, Giambra V, Krystal G, Takei CJF, Weng AP, Piret J, Eaves C, Marra MA, Humphries RK, Hansen CL, Proc Natl Acad Sci U S A 2010 107 15443 15448 10.1073/pnas.1009320107 20702766
62. Hierarchical and ontogenic positions serve to define the molecular basis of human hematopoietic stem cell behavior. Shojaei F, Trowbridge J, Gallacher L, Yuefei L, Goodale D, Karanu F, Levac K, Bhatia M, Dev Cell 2005 8 651 663 10.1016/j.devcel.2005.03.004 15866157
63. The MYCN oncogene and differentiation in neuroblastoma. Westermark UK, Wilhelm M, Frenzel A, Henriksson MA, Semin Cancer Biol 2011 21 256 266 10.1016/j.semcancer.2011.08.001 21849159
64. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Takahashi K, Yamanaka S, Cell 2006 126 663 676 10.1016/j.cell.2006.07.024 16904174
65. Klf5 is involved in self-renewal of mouse embryonic stem cells. Parisi S, Passaro F, Aloia L, Manabe I, Nagai R, Pastore L, Russo T, J Cell Sci 2008 121 2629 2634 10.1242/jcs.027599 18653541
66. Conserved expression patterns predict microRNA targets. Ritchie W, Rajasekhar M, Flamant S, Rasko JEJ, PLoS Comput Biol 2009 5 1000513 10.1371/journal.pcbi.1000513 19779543
67. Distinct microRNA expression profile and targeted biological pathways in functional myeloid-derived suppressor cells induced by Δ9- Tetrahydrocannabinol in vivo: Regulation of CCAAT/enhancer binding protein alpha by microRNA-690. Hegde VL, Tomar S, Jackson A, Rao R, Yang X, Singh U, Singh NP, Nagarkatti PS, Nagarkatti M, J Biol Chem 2013 288 36810 36826 10.1074/jbc.M113.503037 24202177
68. Dicer1 deletion in myeloid-committed progenitors causes neutrophil dysplasia and blocks macrophage/dendritic cell development in mice. Alemdehy MF, van Boxtel NGJA, de Looper HWJ, van den Berge IJ, Sanders MA, Cupedo T, Touw IP, Erkeland SJ, Blood 2012 119 4723 4730 10.1182/blood-2011-10-386359 22353998
69. Generation of T-cell receptor retrogenic mice. Holst J, Szymczak-Workman AL, Vignali KM, Burton AR, Workman CJ, Vignali DAA, Nat Protoc 2006 1 406 417 10.1038/nprot.2006.61 17406263
70. Rapid analysis of T-cell selection in vivo using T cell-receptor retrogenic mice. Holst J, Vignali KM, Burton AR, Vignali DAA, Nat Meth 2006 3 191 197 10.1038/nmeth858
71. Orchestrated intron retention regulates normal granulocyte differentiation. Wong JJL, Ritchie W, Ebner O, Selbach M, Wong JWH, Huang Y, Gao D, Pinello N, Gonzalez M, Baidya K, Thoeng A, Khoo T-L, Bailey CG, Holst J, Rasko JE, Cell 2013 154 583 595 10.1016/j.cell.2013.06.052 23911323
72. Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells. Holst J, Watson S, Lord MS, Eamegdool SS, Bax DV, Nivison-Smith LB, Kondyurin A, Ma L, Oberhauser AF, Weiss AS, Rasko JEJ, Nat Biotech 2010 28 1123 1128 10.1038/nbt.1687
73. Identification of a myeloid committed progenitor as the cancer-initiating cell in acute promyelocytic leukemia. Guibal FC, Alberich-Jorda M, Hirai H, Ebralidze A, Levantini E, Di Ruscio A, Zhang P, Santana-Lemos BA, Neuberg D, Wagers AJ, Rego EM, Tenen DG, Blood 2009 114 5415 5425 10.1182/blood-2008-10- 182071 19797526
74. Evaluation of low density array technology for quantitative parallel measurement of multiple genes in human tissue. Goulter A, Harmer D, Clark K, BMC Genomics 2006 7 34 10.1186/1471-2164-7-34 16504128