miRNA function and modulation in stem cells and cancer stem cells

• Authors: Andrew J. DeCastro , James DiRenzo
• Languages of publication: EN

Abstracts

EN

Stem cells belong to a unique class of cells
that is collectively responsible for the development
and subsequent maintenance of all tissues comprising
multicellular organisms. These cells possess unique
characteristics that allow them to remain in a pluripotent
state, while also continuing to generate differentiated
cells. microRNAs, a specialized class of non-coding RNAs,
are integral components of the network of pathways that
modulates this combination of abilities. This review
highlights recent discoveries about the roles miRNAs
play in governing stem cell phenotype, and discusses the
potential therapeutic utility that miRNAs may have in the
treatment of multiple diseases. Additionally, it addresses a
novel mode of regulation of stem cell phenotype through
lincRNA-mediated modulation of select miRNAs, and the
role of secreted, stem cell-derived miRNAs in exerting a
paracrine influence on surrounding non-stem cells.

Keywords

EN

microRNAs; long non-codingRNAs; cancer stem cells; stemness; TP53; exosome ; microvesicles

• Publisher: De Gruyter Open
• Journal: microRNA Diagnostics and Therapeutics
• Year: 2014
• Volume: 1
• Issue: 1

Dates

received

15 - 1 - 2014

online

17 - 12 - 2014

accepted

24 - 6 - 2014

Contributors

author

Andrew J. DeCastro

• Program in Experimental and Molecular
  Medicine, Geisel School of Medicine at Dartmouth, Hanover, NH,
  USA

author

James DiRenzo

• Department of Pharmacology
  and Toxicology, Geisel School of Medicine at Dartmouth, Hanover, NH,
  USA

References

• [1] Vaish M., Mismatch repair deficiencies transforming stem cellsinto cancer stem cells and therapeutic implications, Molecularcancer, 2007, 6, 26.
• [2] White J., Dalton S., Cell cycle control of embryonic stem cells,Stem cell reviews, 2005, 1, 131-138.
• [3] Melton C., Blelloch R., MicroRNA Regulation of EmbryonicStem Cell Self-Renewal and Differentiation, Advances inexperimental medicine and biology, 2010, 695, 105-117.
• [4] Hatfield S., Ruohola-Baker H., microRNA and stem cell function,Cell and tissue research, 2008, 331, 57-66.
• [5] Bentwich I., Avniel A., Karov Y., Aharonov R., Gilad S., Barad O.,Barzilai A., Einat P., Einav U., Meiri E., et al., Identification ofhundreds of conserved and nonconserved human microRNAs,Nature genetics, 2005, 37, 766-770.[Crossref]
• [6] Lewis B.P., Burge C.B., Bartel D.P., Conserved seed pairing,often flanked by adenosines, indicates that thousands ofhuman genes are microRNA targets, Cell, 2005, 120, 15-20.[Crossref]
• [7] Friedman R.C., Farh K.K., Burge C.B., Bartel D.P., Mostmammalian mRNAs are conserved targets of microRNAs,Genome research, 2009, 19, 92-105.
• [8] Kim V.N., MicroRNA biogenesis: coordinated cropping anddicing, Nature reviews. Molecular cell biology, 2005, 6,376-385.
• [9] Krol J., Loedige I., Filipowicz W., The widespread regulationof microRNA biogenesis, function and decay, Nature reviews.Genetics, 2010, 11, 597-610.
• [10] Tay Y., Zhang J., Thomson A.M., Lim B., Rigoutsos I., MicroRNAsto Nanog, Oct4 and Sox2 coding regions modulate embryonicstem cell differentiation, Nature, 2008, 455, 1124-1128.
• [11] Hollstein M., Sidransky D., Vogelstein B., Harris C.C., p53mutations in human cancers, Science, 1991, 253, 49-53.
• [12] Vogelstein B., Lane D., Levine A.J., Surfing the p53 network,Nature, 2000, 408, 307-310.
• [13] Levine A.J., Hu W., Feng Z., The P53 pathway: what questionsremain to be explored?, Cell death and differentiation, 2006,13, 1027-1036.[PubMed]
• [14] Vigneron A., Vousden K.H., p53, ROS and senescence in thecontrol of aging, Aging, 2010, 2, 471-474.
• [15] Vousden K.H., Lu X., Live or let die: the cell’s response to p53,Nature reviews. Cancer, 2002, 2, 594-604.[Crossref]
• [16] Ko L.J., Prives C., p53: puzzle and paradigm, Genes &development, 1996, 10, 1054-1072.
• [17] Prives C., Hall P.A., The p53 pathway, The Journal of pathology,1999, 187, 112-126.
• [18] Riley T., Sontag E., Chen P., Levine A., Transcriptional controlof human p53-regulated genes, Nature reviews. Molecular cellbiology, 2008, 9, 402-412.
• [19] Vousden K.H., Prives C., Blinded by the Light: The GrowingComplexity of p53, Cell, 2009, 137, 413-431.
• [20] Suzuki H.I., Yamagata K., Sugimoto K., Iwamoto T., Kato S.,Miyazono K., Modulation of microRNA processing by p53,Nature, 2009, 460, 529-533.
• [21] Qin H., Yu T., Qing T., Liu Y., Zhao Y., Cai J., Li J., Song Z., Qu X.,Zhou P., et al., Regulation of apoptosis and differentiation byp53 in human embryonic stem cells, The Journal of biologicalchemistry, 2007, 282, 5842-5852.
• [22] Lin T., Chao C., Saito S., Mazur S.J., Murphy M.E., Appella E., XuY., p53 induces differentiation of mouse embryonic stem cellsby suppressing Nanog expression, Nature cell biology, 2005, 7,165-171.
• [23] Sabapathy K., Klemm M., Jaenisch R., Wagner E.F., Regulationof ES cell differentiation by functional and conformationalmodulation of p53, The EMBO journal, 1997, 16, 6217-6229.[Crossref]
• [24] He L., He X., Lim L.P., de Stanchina E., Xuan Z., Liang Y., Xue W.,Zender L., Magnus J., Ridzon D., et al., A microRNA componentof the p53 tumour suppressor network, Nature, 2007, 447,1130-1134.
• [25] Chang T.C., Wentzel E.A., Kent O.A., Ramachandran K.,Mullendore M., Lee K.H., Feldmann G., Yamakuchi M., FerlitoM., Lowenstein C.J., et al., Transactivation of miR-34a by p53broadly influences gene expression and promotes apoptosis,Molecular cell, 2007, 26, 745-752.[Crossref]
• [26] Raver-Shapira N., Marciano E., Meiri E., Spector Y., RosenfeldN., Moskovits N., Bentwich Z., Oren M., Transcriptionalactivation of miR-34a contributes to p53-mediated apoptosis,Molecular cell, 2007, 26, 731-743.[Crossref]
• [27] Tarasov V., Jung P., Verdoodt B., Lodygin D., EpanchintsevA., Menssen A., Meister G., Hermeking H., Differentialregulation of microRNAs by p53 revealed by massively parallelsequencing: miR-34a is a p53 target that induces apoptosisand G1-arrest, Cell Cycle, 2007, 6, 1586-1593.[Crossref]
• [28] Tarantino C., Paolella G., Cozzuto L., Minopoli G., PastoreL., Parisi S., Russo T., miRNA 34a, 100, and 137 modulatedifferentiation of mouse embryonic stem cells, FASEB journal :official publication of the Federation of American Societies forExperimental Biology, 2010, 24, 3255-3263.[Crossref]
• [29] Aranha M.M., Santos D.M., Sola S., Steer C.J., Rodrigues C.M.,miR-34a regulates mouse neural stem cell differentiation, PloSone, 2011, 6, e21396.
• [30] Hermeking H., The miR-34 family in cancer and apoptosis, Celldeath and differentiation, 2010, 17, 193-199.
• [31] Jain A.K., Allton K., Iacovino M., Mahen E., Milczarek R.J.,Zwaka T.P., Kyba M., Barton M.C., p53 regulates cell cycle andmicroRNAs to promote differentiation of human embryonicstem cells, PLoS biology, 2012, 10, e1001268.[Crossref]
• [32] Yamakuchi M., Ferlito M., Lowenstein C.J., miR-34a repressionof SIRT1 regulates apoptosis, Proceedings of the NationalAcademy of Sciences of the United States of America, 2008,105, 13421-13426.
• [33] Saunders L.R., Sharma A.D., Tawney J., Nakagawa M., Okita K.,Yamanaka S., Willenbring H., Verdin E., miRNAs regulate SIRT1expression during mouse embryonic stem cell differentiationand in adult mouse tissues, Aging, 2010, 2, 415-431.
• [34] Liu T., Liu P.Y., Marshall G.M., The critical role of the class IIIhistone deacetylase SIRT1 in cancer, Cancer research, 2009,69, 1702-1705.
• [35] Calvanese V., Lara E., Suarez-Alvarez B., Abu Dawud R.,Vazquez-Chantada M., Martinez-Chantar M.L., Embade N.,Lopez-Nieva P., Horrillo A., Hmadcha A., et al., Sirtuin 1regulation of developmental genes during differentiation ofstem cells, Proceedings of the National Academy of Sciences ofthe United States of America, 2010, 107, 13736-13741.
• [36] Xu N., Papagiannakopoulos T., Pan G., Thomson J.A., KosikK.S., MicroRNA-145 regulates OCT4, SOX2, and KLF4 andrepresses pluripotency in human embryonic stem cells, Cell,2009, 137, 647-658.
• [37] Choi Y.J., Lin C.P., Ho J.J., He X., Okada N., Bu P., Zhong Y., KimS.Y., Bennett M.J., Chen C., et al., miR-34 miRNAs provide abarrier for somatic cell reprogramming, Nature cell biology,2011, 13, 1353-1360.
• [38] Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O.,Nakagawa M., Okita K., Yamanaka S., Suppression of inducedpluripotent stem cell generation by the p53-p21 pathway,Nature, 2009, 460, 1132-1135.
• [39] Richards M., Tan S.P., Tan J.H., Chan W.K., Bongso A., Thetranscriptome profile of human embryonic stem cells asdefined by SAGE, Stem Cells, 2004, 22, 51-64.[Crossref]
• [40] Viswanathan S.R., Daley G.Q., Gregory R.I., Selective blockadeof microRNA processing by Lin28, Science, 2008, 320, 97-100.
• [41] Yu F., Yao H., Zhu P., Zhang X., Pan Q., Gong C., Huang Y., HuX., Su F., Lieberman J., et al., let-7 regulates self renewal andtumorigenicity of breast cancer cells, Cell, 2007, 131, 1109-1123.
• [42] King C.E., Cuatrecasas M., Castells A., Sepulveda A.R., Lee J.S.,Rustgi A.K., LIN28B promotes colon cancer progression andmetastasis, Cancer research, 2011, 71, 4260-4268.[Crossref]
• [43] Li L., Wang L., Li L., Wang Z., Ho Y., McDonald T., HolyoakeT.L., Chen W., Bhatia R., Activation of p53 by SIRT1 inhibitionenhances elimination of CML leukemia stem cells incombination with imatinib, Cancer cell, 2012, 21, 266-281.[Crossref]
• [44] Lodygin D., Tarasov V., Epanchintsev A., Berking C., KnyazevaT., Korner H., Knyazev P., Diebold J., Hermeking H., Inactivationof miR-34a by aberrant CpG methylation in multiple types ofcancer, Cell Cycle, 2008, 7, 2591-2600.[Crossref]
• [45] Zenz T., Mohr J., Eldering E., Kater A.P., Buhler A., Kienle D.,Winkler D., Durig J., van Oers M.H., Mertens D., et al., miR-34aas part of the resistance network in chronic lymphocyticleukemia, Blood, 2009, 113, 3801-3808.[Crossref]
• [46] Sun F., Fu H., Liu Q., Tie Y., Zhu J., Xing R., Sun Z., Zheng X.,Downregulation of CCND1 and CDK6 by miR-34a induces cellcycle arrest, FEBS letters, 2008, 582, 1564-1568.
• [47] Lefort K., Brooks Y., Ostano P., Cario-Andre M., Calpini V.,Guinea-Viniegra J., Albinger-Hegyi A., Hoetzenecker W.,Kolfschoten I., Wagner E.F., et al., A miR-34a-SIRT6 axis in thesquamous cell differentiation network, The EMBO journal,2013, 32, 2248-2263.[Crossref]
• [48] Kumar B., Yadav A., Lang J., Teknos T.N., Kumar P.,Dysregulation of microRNA-34a expression in head and necksquamous cell carcinoma promotes tumor growth and tumorangiogenesis, PloS one, 2012, 7, e37601.
• [49] Campayo M., Navarro A., Vinolas N., Diaz T., Tejero R., GimferrerJ.M., Molins L., Cabanas M.L., Ramirez J., Monzo M., et al., LowmiR-145 and high miR-367 are associated with unfavourableprognosis in resected nonsmall cell lung cancer, The Europeanrespiratory journal, 2013, 41, 1172-1178.
• [50] Avgeris M., Stravodimos K., Fragoulis E.G., Scorilas A., Theloss of the tumour-suppressor miR-145 results in the shorterdisease-free survival of prostate cancer patients, British journalof cancer, 2013, 108, 2573-2581.
• [51] Sachdeva M., Zhu S., Wu F., Wu H., Walia V., Kumar S., ElbleR., Watabe K., Mo Y.Y., p53 represses c-Myc through inductionof the tumor suppressor miR-145, Proceedings of the NationalAcademy of Sciences of the United States of America, 2009,106, 3207-3212.
• [52] Speranza M.C., Frattini V., Pisati F., Kapetis D., Porrati P.,Eoli M., Pellegatta S., Finocchiaro G., NEDD9, a novel targetof miR-145, increases the invasiveness of glioblastoma,Oncotarget, 2012, 3, 723-734.
• [53] Siemens H., Jackstadt R., Kaller M., Hermeking H., Repressionof c-Kit by p53 is mediated by miR-34 and is associatedwith reduced chemoresistance, migration and stemness,Oncotarget, 2013, 4, 1399-1415.
• [54] Zhang J., Sun Q., Zhang Z., Ge S., Han Z.G., Chen W.T., Loss ofmicroRNA-143/145 disturbs cellular growth and apoptosis ofhuman epithelial cancers by impairing the MDM2-p53 feedbackloop, Oncogene, 2013, 32, 61-69.
• [55] Yang Y.P., Chien Y., Chiou G.Y., Cherng J.Y., Wang M.L., Lo W.L.,Chang Y.L., Huang P.I., Chen Y.W., Shih Y.H., et al., Inhibitionof cancer stem cell-like properties and reduced chemoradioresistanceof glioblastoma using microRNA145 with cationicpolyurethane-short branch PEI, Biomaterials, 2012, 33,1462-1476.[Crossref]
• [56] Lee H.K., Finniss S., Cazacu S., Bucris E., Ziv-Av A., Xiang C.,Bobbitt K., Rempel S.A., Hasselbach L., Mikkelsen T., et al.,Mesenchymal stem cells deliver synthetic microRNA mimicsto glioma cells and glioma stem cells and inhibit their cellmigration and self-renewal, Oncotarget, 2013, 4, 346-361.
• [57] Yang J., Weinberg R.A., Epithelial-mesenchymal transition:at the crossroads of development and tumor metastasis,Developmental cell, 2008, 14, 818-829.[Crossref]
• [58] Thiery J.P., Epithelial-mesenchymal transitions in tumourprogression, Nature reviews. Cancer, 2002, 2, 442-454.[Crossref]
• [59] Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., ZhouA.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., et al.,The epithelial-mesenchymal transition generates cells withproperties of stem cells, Cell, 2008, 133, 704-715.
• [60] Polyak K., Weinberg R.A., Transitions between epithelial andmesenchymal states: acquisition of malignant and stem celltraits, Nature reviews. Cancer, 2009, 9, 265-273.[Crossref]
• [61] Kalluri R., Weinberg R.A., The basics of epithelial-mesenchymaltransition, The Journal of clinical investigation, 2009, 119,1420-1428.
• [62] Clarke M.F., Fuller M., Stem cells and cancer: two faces of eve,Cell, 2006, 124, 1111-1115.[Crossref]
• [63] Chang C.J., Chao C.H., Xia W., Yang J.Y., Xiong Y., Li C.W., YuW.H., Rehman S.K., Hsu J.L., Lee H.H., et al., p53 regulatesepithelial-mesenchymal transition and stem cell propertiesthrough modulating miRNAs, Nature cell biology, 2011, 13,317-323.
• [64] Park S.M., Gaur A.B., Lengyel E., Peter M.E., The miR-200family determines the epithelial phenotype of cancer cells bytargeting the E-cadherin repressors ZEB1 and ZEB2, Genes &development, 2008, 22, 894-907.
• [65] Shimono Y., Zabala M., Cho R.W., Lobo N., Dalerba P., Qian D.,Diehn M., Liu H., Panula S.P., Chiao E., et al., Downregulationof miRNA-200c links breast cancer stem cells with normal stemcells, Cell, 2009, 138, 592-603.
• [66] Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F.,Sonntag A., Waldvogel B., Vannier C., Darling D., zur HausenA., et al., The EMT-activator ZEB1 promotes tumorigenicity byrepressing stemness-inhibiting microRNAs, Nature cell biology,2009, 11, 1487-1495.
• [67] Lim Y.Y., Wright J.A., Attema J.L., Gregory P.A., Bert A.G., SmithE., Thomas D., Lopez A.F., Drew P.A., Khew-Goodall Y., et al.,Epigenetic modulation of the miR-200 family is associated withtransition to a breast cancer stem-cell-like state, Journal of cellscience, 2013, 126, 2256-2266.
• [68] Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J.,Clarke M.F., Prospective identification of tumorigenic breastcancer cells, Proceedings of the National Academy of Sciencesof the United States of America, 2003, 100, 3983-3988.
• [69] Reya T., Morrison S.J., Clarke M.F., Weissman I.L., Stem cells,cancer, and cancer stem cells, Nature, 2001, 414, 105-111.
• [70] Jordan C.T., Guzman M.L., Noble M., Cancer stem cells, TheNew England journal of medicine, 2006, 355, 1253-1261.
• [71] Raza U., Zhang J.D., Sahin O., MicroRNAs: master regulatorsof drug resistance, stemness, and metastasis, Journal ofmolecular medicine, 2014, 92, 321-336.
• [72] Rolfo C., Fanale D., Hong D.S., Tsimberidou A.M., Piha-PaulS.A., Pauwels P., Van Meerbeeck J.P., Caruso S., BazanV., Cicero G., et al., Impact of MicroRNAs in Resistance toChemotherapy and Novel Targeted Agents in Non-Small CellLung Cancer, Current pharmaceutical biotechnology, 2014,
• [73] Ventura A., Kirsch D.G., McLaughlin M.E., Tuveson D.A., GrimmJ., Lintault L., Newman J., Reczek E.E., Weissleder R., Jacks T.,Restoration of p53 function leads to tumour regression in vivo,Nature, 2007, 445, 661-665.
• [74] Xue W., Zender L., Miething C., Dickins R.A., Hernando E.,Krizhanovsky V., Cordon-Cardo C., Lowe S.W., Senescence andtumour clearance is triggered by p53 restoration in murine livercarcinomas, Nature, 2007, 445, 656-660.
• [75] Brabletz S., Brabletz T., The ZEB/miR-200 feedback loop--amotor of cellular plasticity in development and cancer?, EMBOreports, 2010, 11, 670-677.[Crossref]
• [76] Magenta A., Cencioni C., Fasanaro P., Zaccagnini G., Greco S.,Sarra-Ferraris G., Antonini A., Martelli F., Capogrossi M.C.,miR-200c is upregulated by oxidative stress and inducesendothelial cell apoptosis and senescence via ZEB1 inhibition,Cell death and differentiation, 2011, 18, 1628-1639.
• [77] Cufi S., Vazquez-Martin A., Oliveras-Ferraros C., QuirantesR., Segura-Carretero A., Micol V., Joven J., Bosch-BarreraJ., Del Barco S., Martin-Castillo B., et al., Metformin lowersthe threshold for stress-induced senescence: a role for themicroRNA-200 family and miR-205, Cell Cycle, 2012, 11,1235-1246.
• [78] Marson A., Levine S.S., Cole M.F., Frampton G.M., BrambrinkT., Johnstone S., Guenther M.G., Johnston W.K., Wernig M.,Newman J., et al., Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells,Cell, 2008, 134, 521-533.
• [79] Lichner Z., Pall E., Kerekes A., Pallinger E., MaraghechiP., Bosze Z., Gocza E., The miR-290-295 cluster promotespluripotency maintenance by regulating cell cycle phasedistribution in mouse embryonic stem cells, Differentiation;research in biological diversity, 2011, 81, 11-24.
• [80] Wang Y., Baskerville S., Shenoy A., Babiarz J.E., Baehner L.,Blelloch R., Embryonic stem cell-specific microRNAs regulatethe G1-S transition and promote rapid proliferation, Naturegenetics, 2008, 40, 1478-1483.[Crossref]
• [81] Abbas T., Dutta A., p21 in cancer: intricate networks andmultiple activities, Nature reviews. Cancer, 2009, 9, 400-414.[Crossref]
• [82] Aladjem M.I., Spike B.T., Rodewald L.W., Hope T.J., Klemm M.,Jaenisch R., Wahl G.M., ES cells do not activate p53-dependentstress responses and undergo p53-independent apoptosisin response to DNA damage, Current biology : CB, 1998, 8,145-155.
• [83] Solozobova V., Rolletschek A., Blattner C., Nuclearaccumulation and activation of p53 in embryonic stem cellsafter DNA damage, BMC cell biology, 2009, 10, 46.
• [84] Dolezalova D., Mraz M., Barta T., Plevova K., Vinarsky V.,Holubcova Z., Jaros J., Dvorak P., Pospisilova S., Hampl A.,MicroRNAs regulate p21(Waf1/Cip1) protein expression and theDNA damage response in human embryonic stem cells, StemCells, 2012, 30, 1362-1372.[Crossref]
• [85] Wang Y., Blelloch R., Cell cycle regulation by MicroRNAs inembryonic stem cells, Cancer research, 2009, 69, 4093-4096.[Crossref]
• [86] Li Y., Pei J., Xia H., Ke H., Wang H., Tao W., Lats2, a putativetumor suppressor, inhibits G1/S transition, Oncogene, 2003,22, 4398-4405.[Crossref]
• [87] Hong Y., Stambrook P.J., Restoration of an absent G1 arrestand protection from apoptosis in embryonic stem cells afterionizing radiation, Proceedings of the National Academyof Sciences of the United States of America, 2004, 101,14443-14448.
• [88] Solozobova V., Blattner C., Regulation of p53 in embryonic stemcells, Experimental cell research, 2010, 316, 2434-2446.
• [89] Zheng G.X., Ravi A., Calabrese J.M., Medeiros L.A., Kirak O.,Dennis L.M., Jaenisch R., Burge C.B., Sharp P.A., A latentpro-survival function for the mir-290-295 cluster in mouseembryonic stem cells, PLoS genetics, 2011, 7, e1002054.
• [90] Neveu P., Kye M.J., Qi S., Buchholz D.E., Clegg D.O., Sahin M.,Park I.H., Kim K.S., Daley G.Q., Kornblum H.I., et al., MicroRNAprofiling reveals two distinct p53-related human pluripotentstem cell states, Cell stem cell, 2010, 7, 671-681.
• [91] Sengupta S., Nie J., Wagner R.J., Yang C., Stewart R., ThomsonJ.A., MicroRNA 92b controls the G1/S checkpoint gene p57 inhuman embryonic stem cells, Stem Cells, 2009, 27, 1524-1528.[Crossref]
• [92] Bar M., Wyman S.K., Fritz B.R., Qi J., Garg K.S., Parkin R.K.,Kroh E.M., Bendoraite A., Mitchell P.S., Nelson A.M., et al.,MicroRNA discovery and profiling in human embryonic stemcells by deep sequencing of small RNA libraries, Stem Cells,2008, 26, 2496-2505.[Crossref]
• [93] Koledova Z., Kramer A., Kafkova L.R., Divoky V., Cell-cycleregulation in embryonic stem cells: centrosomal decisionson self-renewal, Stem cells and development, 2010, 19,1663-1678.
• [94] Garg N., Po A., Miele E., Campese A.F., Begalli F., SilvanoM., Infante P., Capalbo C., De Smaele E., Canettieri G., et al.,microRNA-17-92 cluster is a direct Nanog target and controlsneural stem cell through Trp53inp1, The EMBO journal, 2013,[Crossref]
• [95] Bian S., Hong J., Li Q., Schebelle L., Pollock A., Knauss J.L.,Garg V., Sun T., MicroRNA cluster miR-17-92 regulates neuralstem cell expansion and transition to intermediate progenitorsin the developing mouse neocortex, Cell reports, 2013, 3,1398-1406.
• [96] Liu X.S., Chopp M., Wang X.L., Zhang L., Hozeska-SolgotA., Tang T., Kassis H., Zhang R.L., Chen C., Xu J., et al.,MicroRNA-17-92 cluster mediates the proliferation and survivalof neural progenitor cells after stroke, The Journal of biologicalchemistry, 2013, 288, 12478-12488.
• [97] Melino G., De Laurenzi V., Vousden K.H., p73: Friend or foe intumorigenesis, Nature reviews. Cancer, 2002, 2, 605-615.[Crossref]
• [98] Yang A., Kaghad M., Caput D., McKeon F., On the shoulders ofgiants: p63, p73 and the rise of p53, Trends in genetics : TIG,2002, 18, 90-95.
• [99] Knouf E.C., Garg K., Arroyo J.D., Correa Y., Sarkar D., ParkinR.K., Wurz K., O’Briant K.C., Godwin A.K., Urban N.D., et al.,An integrative genomic approach identifies p73 and p63 asactivators of miR-200 microRNA family transcription, Nucleicacids research, 2012, 40, 499-510.
• [100] DeCastro A.J., Dunphy K.A., Hutchinson J., BalboniA.L., Cherukuri P., Jerry D.J., DiRenzo J., MiR203 mediatessubversion of stem cell properties during mammary epithelialdifferentiation via repression of DeltaNP63alpha and promotesmesenchymal-to-epithelial transition, Cell death & disease,2013, 4, e514.
• [101] Nekulova M., Holcakova J., Coates P., Vojtesek B., The role ofp63 in cancer, stem cells and cancer stem cells, Cellular &molecular biology letters, 2011, 16, 296-327.
• [102] Boominathan L., The guardians of the genome (p53, TA-p73,and TA-p63) are regulators of tumor suppressor miRNAsnetwork, Cancer metastasis reviews, 2010, 29, 613-639.
• [103] Boominathan L., The tumor suppressors p53, p63, and p73 areregulators of microRNA processing complex, PloS one, 2010,5, e10615.
• [104] Selbach M., Schwanhausser B., Thierfelder N., Fang Z., KhaninR., Rajewsky N., Widespread changes in protein synthesisinduced by microRNAs, Nature, 2008, 455, 58-63.
• [105] Baek D., Villen J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P.,The impact of microRNAs on protein output, Nature, 2008,455, 64-71.
• [106] Guttman M., Amit I., Garber M., French C., Lin M.F., Feldser D.,Huarte M., Zuk O., Carey B.W., Cassady J.P., et al., Chromatinsignature reveals over a thousand highly conserved largenon-coding RNAs in mammals, Nature, 2009, 458, 223-227.
• [107] Khalil A.M., Guttman M., Huarte M., Garber M., Raj A.,Rivea Morales D., Thomas K., Presser A., Bernstein B.E.,van Oudenaarden A., et al., Many human large intergenicnoncoding RNAs associate with chromatin-modifyingcomplexes and affect gene expression, Proceedings of theNational Academy of Sciences of the United States of America,2009, 106, 11667-11672.
• [108] Guttman M., Donaghey J., Carey B.W., Garber M., GrenierJ.K., Munson G., Young G., Lucas A.B., Ach R., Bruhn L., etal., lincRNAs act in the circuitry controlling pluripotency anddifferentiation, Nature, 2011, 477, 295-300.
• [109] Alves C.P., Fonseca A.S., Muys B.R., de Barros E.L.B.R., BurgerM.C., de Souza J.E., Valente V., Zago M.A., Silva W.A., Jr., The lincRNA Hotair is required for epithelial-to-mesenchymaltransition and stemness maintenance of cancer cells lines,Stem Cells, 2013,
• [110] Gupta R.A., Shah N., Wang K.C., Kim J., Horlings H.M., WongD.J., Tsai M.C., Hung T., Argani P., Rinn J.L., et al., Longnon-coding RNA HOTAIR reprograms chromatin state topromote cancer metastasis, Nature, 2010, 464, 1071-1076.
• [111] Wang Y., Xu Z., Jiang J., Xu C., Kang J., Xiao L., Wu M., XiongJ., Guo X., Liu H., Endogenous miRNA sponge lincRNA-RoRregulates Oct4, Nanog, and Sox2 in human embryonic stemcell self-renewal, Developmental cell, 2013, 25, 69-80.
• [112] Zhou X., Gao Q., Wang J., Zhang X., Liu K., Duan Z.,Linc-RNA-RoR acts as a “sponge” against mediation ofthe differentiation of endometrial cancer stem cells bymicroRNA-145, Gynecologic oncology, 2014, 133, 333-339.
• [113] Cesana M., Cacchiarelli D., Legnini I., Santini T., Sthandier O.,Chinappi M., Tramontano A., Bozzoni I., A long noncoding RNAcontrols muscle differentiation by functioning as a competingendogenous RNA, Cell, 2011, 147, 358-369.
• [114] Deregibus M.C., Tetta C., Camussi G., The dynamic stem cellmicroenvironment is orchestrated by microvesicle-mediatedtransfer of genetic information, Histology and histopathology,2010, 25, 397-404.
• [115] Yuan A., Farber E.L., Rapoport A.L., Tejada D., DeniskinR., Akhmedov N.B., Farber D.B., Transfer of microRNAs byembryonic stem cell microvesicles, PloS one, 2009, 4, e4722.
• [116] Chen T.S., Lai R.C., Lee M.M., Choo A.B., Lee C.N., Lim S.K.,Mesenchymal stem cell secretes microparticles enriched inpre-microRNAs, Nucleic acids research, 2010, 38, 215-224.
• [117] Ratajczak J., Wysoczynski M., Hayek F., Janowska-WieczorekA., Ratajczak M.Z., Membrane-derived microvesicles:important and underappreciated mediators of cell-to-cellcommunication, Leukemia, 2006, 20, 1487-1495.[Crossref]
• [118] Mathivanan S., Ji H., Simpson R.J., Exosomes: extracellularorganelles important in intercellular communication, Journalof proteomics, 2010, 73, 1907-1920.
• [119] Zoller M., Tetraspanins: push and pull in suppressing andpromoting metastasis, Nature reviews. Cancer, 2009, 9, 40-55.[Crossref]
• [120] Raposo G., Stoorvogel W., Extracellular vesicles: exosomes,microvesicles, and friends, The Journal of cell biology, 2013,200, 373-383.
• [121] Ratajczak J., Miekus K., Kucia M., Zhang J., Reca R., DvorakP., Ratajczak M.Z., Embryonic stem cell-derived microvesiclesreprogram hematopoietic progenitors: evidence for horizontaltransfer of mRNA and protein delivery, Leukemia, 2006, 20,847-856.[Crossref]
• [122] Katsman D., Stackpole E.J., Domin D.R., Farber D.B., Embryonicstem cell-derived microvesicles induce gene expressionchanges in Muller cells of the retina, PloS one, 2012, 7,e50417.
• [123] Judson R.L., Babiarz J.E., Venere M., Blelloch R., Embryonicstem cell-specific microRNAs promote induced pluripotency,Nature biotechnology, 2009, 27, 459-461.
• [124] Cantaluppi V., Gatti S., Medica D., Figliolini F., Bruno S.,Deregibus M.C., Sordi A., Biancone L., Tetta C., Camussi G.,Microvesicles derived from endothelial progenitor cells protectthe kidney from ischemia-reperfusion injury by microRNAdependentreprogramming of resident renal cells, Kidneyinternational, 2012, 82, 412-427.[Crossref]
• [125] Collino F., Deregibus M.C., Bruno S., Sterpone L., Aghemo G.,Viltono L., Tetta C., Camussi G., Microvesicles derived fromadult human bone marrow and tissue specific mesenchymalstem cells shuttle selected pattern of miRNAs, PloS one, 2010,5, e11803.

Identifiers

DOI

10.2478/micrnat-2014-0004