MicroRNA reins in embryonic and cancer stem cells

RNA Biology

Volumn 8, Issue 3, 2011, Pages 415-426

  Mallick, Bibekanand ^a   Chakrabarti, Jayprokas ^b   Ghosh, Zhumur ^c  

^a WADSWORTH CENTER   (United States)

^b DEPARTMENT OF MATERIALS SCIENCE   (India)

^c BOSE INSTITUTE   (India)

Author keywords

Cancer; Cancer stem cells; MicroRNA; miRNA targets; Pluripotency; Reprogramming; SNP

Indexed keywords

MICRORNA;

CANCER STEM CELL; CELL CLONING; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; HUMAN; MICROARRAY ANALYSIS; NONHUMAN; ONCOGENE; PROTEIN EXPRESSION; PROTEIN PROCESSING; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR SUPPRESSOR GENE;

EID: 79956141769     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.8.3.14497     Document Type: Review

References (104)

1. Friel R, van der Sar S, Mee PJ. Embryonic stem cells: understanding their history, cell biology and signalling. Adv Drug Deliv Rev 2005; 57:1894-903. (Pubitemid 41682361)
2. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292:154-6. (Pubitemid 11050741)
3. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-7. (Pubitemid 28516247)
4. Bjerkvig R, Tysnes BB, Aboody KS, Najbauer J, Terzis AJ. Opinion: the origin of the cancer stem cell: current controversies and new insights. Nat Rev Cancer 2005; 5:899-904. (Pubitemid 41746034)
5. Morrison SJ, Qian D, Jerabek L, Thiel BA, Park IK, Ford PS, et al. A genetic determinant that specifically regulates the frequency of hematopoietic stem cells. J Immunol 2002; 168:635-42. (Pubitemid 34049563)
6. Dick JE. Normal and leukemic human stem cells assayed in SCID mice. Semin Immunol 1996; 8:197-206. (Pubitemid 26315854)
7. Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA 1992; 89:2804-8.
8. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science 1988; 241:58-62.
9. Blair A, Sutherland HJ. Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit (CD117). Exp Hematol 2000; 28:660-71. (Pubitemid 30398523)
10. Blair A, Hogge DE, Ailles LE, Lansdorp PM, Sutherland HJ. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood 1997; 89:3104-12. (Pubitemid 27229792)
11. Blair A, Hogge DE, Sutherland HJ. Most acute myeloid leukemia progenitor cells with long-term proliferative ability in vitro and in vivo have the phenotype CD34(+)/ CD71(-)/HLA-DR. Blood 1998; 92:4325-35. (Pubitemid 28544350)
12. Jordan CT, Upchurch D, Szilvassy SJ, Guzman ML, Howard DS, Pettigrew AL, et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 2000; 14:1777-84.
13. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63:5821-8. (Pubitemid 37187480)
14. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100:3983-8. (Pubitemid 36418143)
15. Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 2005; 65:3025-9. (Pubitemid 40524578)
16. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65:10946-51. (Pubitemid 41713363)
17. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445:111-5. (Pubitemid 46067311)
18. Croker AK, Allan AL. Cancer stem cells: implications for the progression and treatment of metastatic disease. J Cell Mol Med 2008; 12:374-90. (Pubitemid 351555122)
19. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F, et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 2008; 26:1276-84.
20. Sun N, Panetta NJ, Gupta DM, Wilson KD, Lee A, Jia F, et al. Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells. Proc Natl Acad Sci USA 2009; 106:15720-5.
21. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-72. (Pubitemid 350138099)
22. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz- Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318:1917-20.
23. Lin SL, Chang DC, Chang-Lin S, Lin CH, Wu DT, Chen DT, Ying SY. Mir-302 reprograms human skin cancer cells into a pluripotent ES-cell-like state. RNA 2008; 14:2115-24.
24. Shin C, Nam JW, Farh KK, Chiang HR, Shkumatava A, Bartel DP. Expanding the microRNA targeting code: functional sites with centered pairing. Mol Cell 2010; 38:789-802.
25. Schembri F, Sridhar S, Perdomo C, Gustafson AM, Zhang X, Ergun A, et al. MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc Natl Acad Sci USA 2009; 106:2319-24.
26. Suh MR, Lee Y, Kim JY, Kim SK, Moon SH, Lee JY, et al. Human embryonic stem cells express a unique set of microRNAs. Dev Biol 2004; 270:488-98. (Pubitemid 38748567)
27. Houbaviy HB, Murray MF, Sharp PA. Embryonic stem cell-specific MicroRNAs. Dev Cell 2003; 5:351-8. (Pubitemid 37006477)
28. Kuwabara T, Hsieh J, Nakashima K, Taira K, Gage FH. A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 2004; 116:779-93. (Pubitemid 38410724)
29. Mallick B, Ghosh Z, Chakrabarti J. MicroRNome analysis unravels the molecular basis of SARS infection in bronchoalveolar stem cells. PLoS One 2009; 4:7837.
30. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ. Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci USA 2005; 102:12135-40. (Pubitemid 41291141)
31. Tang F, Hajkova P, Barton SC, Lao K, Surani MA. MicroRNA expression profiling of single whole embryonic stem cells. Nucleic Acids Res 2006; 34:9.
32. Yang S, Tutton S, Pierce E, Yoon K. Specific doublestranded RNA interference in undifferentiated mouse embryonic stem cells. Mol Cell Biol 2001; 21:7807-16. (Pubitemid 32988789)
33. Judson RL, Babiarz JE, Venere M, Blelloch R. Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 2009; 27:459-61.
34. Ambros V, Chen X. The regulation of genes and genomes by small RNAs. Development 2007; 134:1635-41. (Pubitemid 46796561)
35. Du T, Zamore PD. microPrimer: the biogenesis and function of microRNA. Development 2005; 132:4645-52. (Pubitemid 41685275)
36. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007; 130:89-100. (Pubitemid 47031325)
37. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature 2007; 448:83-6. (Pubitemid 47037009)
38. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Mol Cell 2007; 28:328-36. (Pubitemid 47600007)
39. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can upregulate translation. Science 2007; 318:1931-4.
40. Gangaraju VK, Lin H. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 2009; 10:116-25.
41. Wang Y, Keys DN, Au-Young JK, Chen C. MicroRNAs in embryonic stem cells. J Cell Physiol 2009; 218:251-5.
42. Liu N, Lu M, Tian X, Han Z. Molecular mechanisms involved in self-renewal and pluripotency of embryonic stem cells. J Cell Physiol 2007; 211:279-86. (Pubitemid 46580081)
43. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006; 6:857-66. (Pubitemid 44629897)
44. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med 2009; 60:167-79.
45. Knoepfler PS. Deconstructing stem cell tumorigenicity: a roadmap to safe regenerative medicine. Stem Cells 2009; 27:1050-6.
46. Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, et al. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 2010; 6:468-78.
47. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, Li MZ, et al. Dicer is essential for mouse development. Nat Genet 2003; 35:215-7. (Pubitemid 37363172)
48. Harris KS, Zhang Z, McManus MT, Harfe BD, Sun X. Dicer function is essential for lung epithelium morphogenesis. Proc Natl Acad Sci USA 2006; 103:2208-13. (Pubitemid 43271648)
49. Muljo SA, Ansel KM, Kanellopoulou C, Livingston DM, Rao A, Rajewsky K. Aberrant T cell differentiation in the absence of Dicer. J Exp Med 2005; 202:261-9. (Pubitemid 41043822)
50. Wienholds E, Koudijs MJ, van Eeden FJ, Cuppen E, Plasterk RH. The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat Genet 2003; 35:217-8. (Pubitemid 37363173)
51. Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, Zhao G. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 2005; 280:9330-5. (Pubitemid 40409626)
52. Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 2007; 39:380-5. (Pubitemid 46328490)
53. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008; 455:1124-8.
54. Lu Y, Thomson JM, Wong HY, Hammond SM, Hogan BL. Transgenic overexpression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol 2007; 310:442-53. (Pubitemid 47483685)
55. Calabrese JM, Seila AC, Yeo GW, Sharp PA. RNA sequence analysis defines Dicer's role in mouse embryonic stem cells. Proc Natl Acad Sci USA 2007; 104:18097-102. (Pubitemid 350210826)
56. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS. Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 2006; 24:857-64. (Pubitemid 44464719)
57. Tay YM, Tam WL, Ang YS, Gaughwin PM, Yang H, Wang W, et al. MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1. Stem Cells 2008; 26:17-29.
58. Stadler B, Ivanovska I, Mehta K, Song S, Nelson A, Tan Y, et al. Characterization of microRNAs involved in embryonic stem cell states. Stem Cells Dev 2010; 19:935-50.
59. Delaloy C, Liu L, Lee JA, Su H, Shen F, Yang GY, et al. MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 2010; 6:323-35.
60. Ivey KN, Muth A, Arnold J, King FW, Yeh RF, Fish JE, et al. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2008; 2:219-29. (Pubitemid 351298595)
61. Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H, Majumder S. REST maintains self-renewal and pluripotency of embryonic stem cells. Nature 2008; 453:223-7. (Pubitemid 351667975)
62. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. MicroRNA-145 regulates OCT4, SOX2 and KLF4 and represses pluripotency in human embryonic stem cells. Cell 2009; 137:647-58.
63. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005; 122:947-56. (Pubitemid 41345211)
64. Gunaratne PH. Embryonic stem cell microRNAs: defining factors in induced pluripotent (iPS) and cancer (CSC) stem cells? Curr Stem Cell Res Ther 2009; 4:168-77.
65. Benetti R, Gonzalo S, Jaco I, Munoz P, Gonzalez S, Schoeftner S, et al. A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol 2008; 15:268-79. (Pubitemid 351654050)
66. Sinkkonen L, Hugenschmidt T, Berninger P, Gaidatzis D, Mohn F, Artus-Revel CG, et al. MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat Struct Mol Biol 2008; 15:259-67. (Pubitemid 351654045)
67. Wilson KD, Venkatasubrahmanyam S, Jia F, Sun N, Butte AJ, Wu JC. MicroRNA profiling of human-induced pluripotent stem cells. Stem Cells Dev 2009; 18:749-58.
68. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008; 134:521-33.
69. Kwon C, Han Z, Olson EN, Srivastava D. MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc Natl Acad Sci USA 2005; 102:18986-91. (Pubitemid 43049553)
70. Zhao Y, Ransom JF, Li A, Vedantham V, von Drehle M, Muth AN, et al. Dysregulation of cardiogenesis, cardiac conduction and cell cycle in mice lacking miRNA-1-2. Cell 2007; 129:303-17. (Pubitemid 46574975)
71. Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006; 38:228-33. (Pubitemid 43177239)
72. Tarantino C, Paolella G, Cozzuto L, Minopoli G, Pastore L, Parisi S, Russo T. miRNA 34a, 100 and 137 modulate differentiation of mouse embryonic stem cells. FASEB J 2010; 24:3255-63.
73. Barroso-del Jesus A, Lucena-Aguilar G, Menendez P. The miR-302-367 cluster as a potential stemness regulator in ESCs. Cell Cycle 2009; 8:394-8.
74. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science 2008; 320:97-100. (Pubitemid 351490762)
75. Melton C, Judson RL, Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 2010; 463:621-6.
76. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435:834-8. (Pubitemid 40839735)
77. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007; 131:1109-23. (Pubitemid 350235025)
78. Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 2007; 21:1025-30. (Pubitemid 46686471)
79. Li O, Li J, Droge P. DNA architectural factor and proto-oncogene HMGA2 regulates key developmental genes in pluripotent human embryonic stem cells. FEBS Lett 2007; 581:3533-7. (Pubitemid 47048209)
80. Li O, Vasudevan D, Davey CA, Droge P. High-level expression of DNA architectural factor HMGA2 and its association with nucleosomes in human embryonic stem cells. Genesis 2006; 44:523-9. (Pubitemid 44846647)
81. Godlewski J, Nowicki MO, Bronisz A, Williams S, Otsuki A, Nuovo G, et al. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res 2008; 68:9125-30.
82. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005; 102:13944-9. (Pubitemid 41377683)
83. Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, et al. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 2008; 14:1271-7.
84. Garzia L, Andolfo I, Cusanelli E, Marino N, Petrosino G, De Martino D, et al. MicroRNA-199b-5p impairs cancer stem cells through negative regulation of HES1 in medulloblastoma. PLoS One 2009; 4:4998.
85. Ferretti E, De Smaele E, Miele E, Laneve P, Po A, Pelloni M, et al. Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J 2008; 27:2616-27.
86. He X, He L, Hannon GJ. The guardian's little helper: microRNAs in the p53 tumor suppressor network. Cancer Res 2007; 67:11099-101. (Pubitemid 350248530)
87. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009; 138:592-603.
88. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, et al. A microRNA polycistron as a potential human oncogene. Nature 2005; 435:828-33. (Pubitemid 40839734)
89. Uziel T, Karginov FV, Xie S, Parker JS, Wang YD, Gajjar A, et al. The miR-17~92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastoma. Proc Natl Acad Sci USA 2009; 106:2812-7.
90. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. miR-21-mediated tumor growth. Oncogene 2007; 26:2799-803.
91. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink JA, Bolijn A, et al. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 2008; 68:5795-802.
92. Yu J, Wang F, Yang GH, Wang FL, Ma YN, Du ZW, Zhang JW. Human microRNA clusters: genomic organization and expression profile in leukemia cell lines. Biochem Biophys Res Commun 2006; 349:59-68. (Pubitemid 44331762)
93. Yin G, Chen R, Alvero AB, Fu HH, Holmberg J, Glackin C, et al. TWISTing stemness, inflammation and proliferation of epithelial ovarian cancer cells through MIR199A2/214. Oncogene 2010; 29:3545-53.
94. Stark MS, Tyagi S, Nancarrow DJ, Boyle GM, Cook AL, Whiteman DC, et al. Characterization of the Melanoma miRNAome by Deep Sequencing. PLoS One 2010; 5:9685.
95. Nicoloso MS, Sun H, Spizzo R, Kim H, Wickramasinghe P, Shimizu M, et al. Single-nucleotide polymorphisms inside microRNA target sites influence tumor susceptibility. Cancer Res 2010; 70:2789-98.
96. Ryan BM, Robles AI, Harris CC. Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer 2010; 10:389-402.
97. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, et al. Frequent deletions and downregulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99:15524-9. (Pubitemid 35403967)
98. Wong P, Iwasaki M, Somervaille TC, Ficara F, Carico C, Arnold C, et al. The miR-17-92 microRNA polycistron regulates MLL leukemia stem cell potential by modulating p21 expression. Cancer Res 2010; 70:3833-42.
99. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, et al. RAS is regulated by the let-7 microRNA family. Cell 2005; 120:635-47. (Pubitemid 40343076)
100. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004; 64:3753-6. (Pubitemid 38697282)
101. Chin LJ, Ratner E, Leng S, Zhai R, Nallur S, Babar I, et al. A SNP in a let-7 microRNA complementary site in the KRAS 3′ untranslated region increases non-small cell lung cancer risk. Cancer Res 2008; 68:8535-40.
102. Nelson HH, Christensen BC, Plaza SL, Wiencke JK, Marsit CJ, Kelsey KT. KRAS mutation, KRAS-LCS6 polymorphism and non-small cell lung cancer. Lung Cancer 2009; 69:51-3.
103. Ingman WV, Robertson SA. Mammary gland development in transforming growth factor beta1 null mutant mice: systemic and epithelial effects. Biol Reprod 2008; 79:711-7.
104. Lee NS, Kim JS, Cho WJ, Lee MR, Steiner R, Gompers A, et al. miR-302b maintains "stemness" of human embryonal carcinoma cells by post-transcriptional regulation of Cyclin D2 expression. Biochem Biophys Res Commun 2008; 377:434-40.