microRNA in the control of stem-like phenotype of cancer cells

Cancer therapies nowadays still cannot overcome the problems of tumor recurrence after chemo-, immuno-, or radiotherapy. This is mainly caused by ineffective eradication of cancer stem cells (also known as tumor initiating cells), that are responsible for tumor recurrence. These cells possess the capabilities of self-renewal, differentiation, and augmented resistance against conventional anticancer drugs. The stem-like properties of cancer cells are controlled by microRNAs (miRNAs), whose expression is usually disturbed during tumorigenesis. In cancer and cancer stem cells, several important miRNAs acting as tumor suppressors are downregulated, triggering proliferation and resistance to apoptosis, while several other oncogenic miRNAs are overexpressed, promoting self-renewal or dedifferentiation of cancer cells. MicroRNAs are small non-coding RNA molecules with regulatory activity. They act as negative regulators of gene expression by binding to complementary sequences on the target mRNA. mRNA with bound miRNA cannot be translated and often, such an RNA duplex is degraded. Novel anti-cancer therapies currently being elucidated, benefit from the importance of miRNA for cancer maintenance, and intend to target aberrantly-expressed miRNA molecules in cancer cells. This review summarizes recent achievements regarding miRNA-mediated control of cancer stemlike properties, and first attempts to provide miRNA – targeted therapies.

[1]  M. Czyz,et al.  Sphere formation and self-renewal capacity of melanoma cells is affected by the microenvironment , 2012, Melanoma research.

[2]  Yi Luo,et al.  microRNA-150 inhibits human CD133-positive liver cancer stem cells through negative regulation of the transcription factor c-Myb. , 2011, International journal of oncology.

[3]  Yong You,et al.  Stability and Mismatch Discrimination of Locked Nucleic Acid–DNA Duplexes , 2011, Biochemistry.

[4]  K. Kelnar,et al.  The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. , 2011, Nature medicine.

[5]  Rajvir Dahiya,et al.  Regulatory Role of mir-203 in Prostate Cancer Progression and Metastasis , 2010, Clinical Cancer Research.

[6]  S. Morrison,et al.  Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. , 2010, Cancer cell.

[7]  S. Anand,et al.  MicroRNA-132–mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis , 2010, Nature Medicine.

[8]  P. Lu,et al.  Octamer 4 (Oct4) mediates chemotherapeutic drug resistance in liver cancer cells through a potential Oct4–AKT–ATP‐binding cassette G2 pathway , 2010, Hepatology.

[9]  R. Dahiya,et al.  The functional significance of microRNA-145 in prostate cancer , 2010, British Journal of Cancer.

[10]  H. Lehrach,et al.  Cancer stem cells in solid tumors: elusive or illusive? , 2010, Cell Communication and Signaling.

[11]  Shinji Tanaka,et al.  miR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. , 2010, Carcinogenesis.

[12]  V. Ambros,et al.  Inhibiting miRNA in Caenorhabditis elegans using a potent and selective antisense reagent , 2010, Silence.

[13]  H. Hermeking The miR-34 family in cancer and apoptosis , 2010, Cell Death and Differentiation.

[14]  F. Slack,et al.  Regression of murine lung tumors by the let-7 microRNA , 2009, Oncogene.

[15]  Julia Schüler,et al.  The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs , 2009, Nature Cell Biology.

[16]  E. Sahai,et al.  Intravital imaging reveals transient changes in pigment production and Brn2 expression during metastatic melanoma dissemination. , 2009, Cancer research.

[17]  Robert E. Kingston,et al.  Mechanisms of Polycomb gene silencing: knowns and unknowns , 2009, Nature Reviews Molecular Cell Biology.

[18]  O. Er,et al.  Cancer Stem Cells in Solid Tumors , 2009, Oncology Research and Treatment.

[19]  R. Weinberg,et al.  Cancer stem cells: mirage or reality? , 2009, Nature Medicine.

[20]  Min Zhang,et al.  MicroRNA miR-34 Inhibits Human Pancreatic Cancer Tumor-Initiating Cells , 2009, PloS one.

[21]  T. Park,et al.  siRNA delivery systems for cancer treatment. , 2009, Advanced drug delivery reviews.

[22]  Michael F. Clarke,et al.  Downregulation of miRNA-200c Links Breast Cancer Stem Cells with Normal Stem Cells , 2009, Cell.

[23]  X. Wang,et al.  Identification of microRNA‐181 by genome‐wide screening as a critical player in EpCAM–positive hepatic cancer stem cells , 2009, Hepatology.

[24]  Eric S. Lander,et al.  Identification of Selective Inhibitors of Cancer Stem Cells by High-Throughput Screening , 2009, Cell.

[25]  F. Slack,et al.  The mir-34 microRNA is required for the DNA damage response in vivo in C. elegans and in vitro in human breast cancer cells , 2009, Oncogene.

[26]  Kathryn A. O’Donnell,et al.  Therapeutic microRNA Delivery Suppresses Tumorigenesis in a Murine Liver Cancer Model , 2009, Cell.

[27]  W. Filipowicz,et al.  Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. , 2009, Current opinion in cell biology.

[28]  G. Pan,et al.  MicroRNA-145 Regulates OCT4, SOX2, and KLF4 and Represses Pluripotency in Human Embryonic Stem Cells , 2009, Cell.

[29]  Fang Liu,et al.  Tobacco smoke induces polycomb-mediated repression of Dickkopf-1 in lung cancer cells. , 2009, Cancer research.

[30]  P. Northcott,et al.  MicroRNA-199b-5p Impairs Cancer Stem Cells through Negative Regulation of HES1 in Medulloblastoma , 2009, PloS one.

[31]  P. Menéndez,et al.  The miR-302-367 cluster as a potential stemness regulator in ESCs , 2009, Cell cycle.

[32]  D. Bartel MicroRNAs: Target Recognition and Regulatory Functions , 2009, Cell.

[33]  Michael Niepmann,et al.  microRNA-122 stimulates translation of hepatitis C virus RNA , 2008, The EMBO journal.

[34]  Agnieszka Bronisz,et al.  Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. , 2008, Cancer research.

[35]  Donald C. Chang,et al.  Mir-302 reprograms human skin cancer cells into a pluripotent ES-cell-like state. , 2008, RNA.

[36]  Min Zhang,et al.  Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres , 2008, BMC Cancer.

[37]  R. Jaenisch,et al.  A drug-inducible system for direct reprogramming of human somatic cells to pluripotency. , 2008, Cell stem cell.

[38]  Leping Li,et al.  Oct4/Sox2-Regulated miR-302 Targets Cyclin D1 in Human Embryonic Stem Cells , 2008, Molecular and Cellular Biology.

[39]  Terry Hyslop,et al.  A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation , 2008, The Journal of cell biology.

[40]  M. Lohuizen,et al.  Bmi1 Regulates Stem Cells and Proliferation and Differentiation of Committed Cells in Mammary Epithelium , 2008, Current Biology.

[41]  T. Wurdinger,et al.  MicroRNA 21 Promotes Glioma Invasion by Targeting Matrix Metalloproteinase Regulators , 2008, Molecular and Cellular Biology.

[42]  K. Helin,et al.  Polycomb Complex 2 Is Required for E-cadherin Repression by the Snail1 Transcription Factor , 2008, Molecular and Cellular Biology.

[43]  U. A. Ørom,et al.  MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. , 2008, Molecular cell.

[44]  T. Brabletz,et al.  A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells , 2008, EMBO reports.

[45]  G. Goodall,et al.  The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1 , 2008, Nature Cell Biology.

[46]  Michael T. McManus,et al.  Conditional Loss of Dicer Disrupts Cellular and Tissue Morphogenesis in the Cortex and Hippocampus , 2008, The Journal of Neuroscience.

[47]  J. Inazawa,et al.  Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. , 2008, Cancer research.

[48]  S. Natsugoe,et al.  CD133 expression is correlated with lymph node metastasis and vascular endothelial growth factor-C expression in pancreatic cancer , 2008, British Journal of Cancer.

[49]  F. Slack,et al.  The let-7 microRNA reduces tumor growth in mouse models of lung cancer , 2008, Cell cycle.

[50]  Phillip A Sharp,et al.  Suppression of non-small cell lung tumor development by the let-7 microRNA family , 2008, Proceedings of the National Academy of Sciences.

[51]  N. Rajewsky,et al.  Dicer Ablation Affects Antibody Diversity and Cell Survival in the B Lymphocyte Lineage , 2008, Cell.

[52]  F. Slack,et al.  Small non-coding RNAs in animal development , 2008, Nature Reviews Molecular Cell Biology.

[53]  Michael D. Schneider,et al.  Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure , 2008, Proceedings of the National Academy of Sciences.

[54]  E. Izaurralde,et al.  Getting to the Root of miRNA-Mediated Gene Silencing , 2008, Cell.

[55]  J. Lieberman,et al.  let-7 Regulates Self Renewal and Tumorigenicity of Breast Cancer Cells , 2007, Cell.

[56]  F. Slack,et al.  The let-7 microRNA represses cell proliferation pathways in human cells. , 2007, Cancer research.

[57]  Ying Feng,et al.  Supplemental Data P53-mediated Activation of Mirna34 Candidate Tumor-suppressor Genes , 2022 .

[58]  Asli Silahtaroglu,et al.  miR-200b mediates post-transcriptional repression of ZFHX1B. , 2007, RNA.

[59]  C. Sander,et al.  A Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing , 2007, Cell.

[60]  M. Stoffel,et al.  Specificity, duplex degradation and subcellular localization of antagomirs , 2007, Nucleic acids research.

[61]  Caterina A M La Porta,et al.  Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. , 2007, European journal of cancer.

[62]  Lena Smirnova,et al.  The FASEB Journal • Research Communication Post-transcriptional regulation of the let-7 microRNA during neural cell specification , 2022 .

[63]  Rudolf Jaenisch,et al.  DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal , 2007, Nature Genetics.

[64]  J. Dick,et al.  A human colon cancer cell capable of initiating tumour growth in immunodeficient mice , 2007, Nature.

[65]  Takahiro Kunisada,et al.  Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. , 2006, Biochemical and biophysical research communications.

[66]  Jane Goodall,et al.  Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. , 2006, Genes & development.

[67]  Irving L Weissman,et al.  Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. , 2006, Cancer research.

[68]  J. Dick,et al.  Targeting of CD44 eradicates human acute myeloid leukemic stem cells , 2006, Nature Medicine.

[69]  J. Zeitlinger,et al.  Polycomb complexes repress developmental regulators in murine embryonic stem cells , 2006, Nature.

[70]  T. Okanoue,et al.  Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues , 2006, Oncogene.

[71]  N. Rajewsky,et al.  Silencing of microRNAs in vivo with ‘antagomirs’ , 2005, Nature.

[72]  N. Maitland,et al.  Prospective identification of tumorigenic prostate cancer stem cells. , 2005, Cancer research.

[73]  Y. Yatabe,et al.  A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. , 2005, Cancer research.

[74]  P. Dalerba,et al.  Identification of pancreatic cancer stem cells. , 2006, Cancer research.

[75]  D. Elder,et al.  A tumorigenic subpopulation with stem cell properties in melanomas. , 2005, Cancer research.

[76]  Thomas Kirchner,et al.  Migrating cancer stem cells — an integrated concept of malignant tumour progression , 2005, Nature Reviews Cancer.

[77]  Danila Coradini,et al.  Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. , 2005, Cancer research.

[78]  G. Glinsky,et al.  Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. , 2005, The Journal of clinical investigation.

[79]  W. Sadee,et al.  ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. , 2005, Cancer research.

[80]  G. Dontu,et al.  Mammary stem cells, self-renewal pathways, and carcinogenesis , 2005, Breast Cancer Research.

[81]  T. Golub,et al.  Critical role of CDK2 for melanoma growth linked to its melanocyte-specific transcriptional regulation by MITF. , 2004, Cancer cell.

[82]  R. Henkelman,et al.  Identification of human brain tumour initiating cells , 2004, Nature.

[83]  G. Dontu,et al.  Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells , 2004, Breast Cancer Research.

[84]  G. Rubanyi,et al.  Hedgehog-interacting protein is highly expressed in endothelial cells but down-regulated during angiogenesis and in several human tumors , 2004, BMC Cancer.

[85]  Y. Yatabe,et al.  Reduced Expression of the let-7 MicroRNAs in Human Lung Cancers in Association with Shortened Postoperative Survival , 2004, Cancer Research.

[86]  D. Bartel,et al.  MicroRNAs Modulate Hematopoietic Lineage Differentiation , 2004, Science.

[87]  Jean Paul Thiery,et al.  Epithelial-mesenchymal transitions in development and pathologies. , 2003, Current opinion in cell biology.

[88]  B. Osborne,et al.  Notch signaling as a therapeutic target in cancer: a new approach to the development of cell fate modifying agents , 2003, Oncogene.

[89]  Irving L. Weissman,et al.  Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells , 2003, Nature.

[90]  G. Dontu,et al.  In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. , 2003, Genes & development.

[91]  J. Aster,et al.  Notch signaling as a therapeutic target. , 2002, Current opinion in chemical biology.

[92]  B. Reinhart,et al.  The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans , 2000, Nature.

[93]  J. Dick,et al.  Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell , 1997, Nature Medicine.

[94]  M. Caligiuri,et al.  A cell initiating human acute myeloid leukaemia after transplantation into SCID mice , 1994, Nature.

[95]  P. Nowell The clonal evolution of tumor cell populations. , 1976, Science.

[96]  Junjie Xiao,et al.  MicroRNA Therapeutics. , 2015, Mini reviews in medicinal chemistry.

[97]  Y. Akao,et al.  Comparative study of anti-oncogenic microRNA-145 in canine and human malignant melanoma. , 2012, The Journal of veterinary medical science.

[98]  P. Bahadoran,et al.  Mitf is the key molecular switch between mouse or human melanoma initiating cells and their differentiated progeny , 2011, Oncogene.

[99]  P. Lu,et al.  Octamer 4 ( Oct 4 ) Mediates Chemotherapeutic Drug Resistance in Liver Cancer Cells Through a Potential Oct 4 – AKT – ATP-Binding Cassette G 2 Pathway , 2010 .

[100]  K. Kelnar,et al.  The microRNA miR-34 a inhibits prostate cancer stem cells and metastasis by directly repressing CD 44 , 2010 .

[101]  C. Croce,et al.  MicroRNA signatures in human ovarian cancer. , 2007, Cancer research.

[102]  H. Clevers Wnt/beta-catenin signaling in development and disease. , 2006, Cell.

[103]  Rolf Bjerkvig,et al.  Opinion: the origin of the cancer stem cell: current controversies and new insights. , 2005, Nature reviews. Cancer.

[104]  A. Maitra,et al.  Urological Survey UROLOGICAL ONCOLOGY: PROSTATE CANCER Hedgehog Signalling in Prostate Regeneration, Neoplasia and Metastasis , 2005 .

[105]  R. Ferrante,et al.  Prospective identification of tumorigenic breast cancer cells , 2003 .

[106]  Ministerial Meeting,et al.  Summary of the , 1994 .