miRNA-regulated cancer stem cells: understanding the property and the role of miRNA in carcinogenesis

Over the last few years, microRNAs (miRNA)-controlled cancer stem cells have drawn enormous attention. Cancer stem cells are a small population of tumor cells that possess the stem cell property of self-renewal. Recent data shows that miRNA regulates this small population of stem cells. In the present review, we explained different characteristics of cancer stem cells as well as miRNA regulation of self-renewal and differentiation in cancer stem cells. We also described the migration and tumor formation. Finally, we described the different miRNAs that regulate various types of cancer stem cells, such as prostate cancer stem cells, head and neck cancer stem cells, breast cancer stem cells, colorectal cancer stem cells, lung cancer stem cells, gastric cancer stem cells, pancreatic cancer stem cells, etc. Extensive research is needed in order to employ miRNA-based therapeutics to control cancer stem cell population in various cancers in the future.

[1]  Sadegh Babashah,et al.  Targeting of the signal transducer Smo links microRNA‐326 to the oncogenic Hedgehog pathway in CD34+ CML stem/progenitor cells , 2013, International journal of cancer.

[2]  Yvonne Tay,et al.  MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation , 2009, Nature.

[3]  Sanjiban Sekhar Roy,et al.  A hypothetical relationship between the nuclear reprogramming factors for induced pluripotent stem (iPS) cells generation--bioinformatic and algorithmic approach. , 2011, Medical hypotheses.

[4]  P. Nowell The clonal nature of neoplasia. , 1989, Cancer cells.

[5]  E. Hurt,et al.  CD44+CD24− prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis , 2008, British Journal of Cancer.

[6]  F. DiMeco,et al.  Origins and clinical implications of the brain tumor stem cell hypothesis , 2009, Journal of Neuro-Oncology.

[7]  Lengchen Hou,et al.  MicroRNA-17 promotes normal ovarian cancer cells to cancer stem cells development via suppression of the LKB1-p53-p21/WAF1 pathway , 2015, Tumor Biology.

[8]  J. Luketich,et al.  Tumorigenic epithelial stem cells and their normal counterparts. , 2006, Ernst Schering Foundation symposium proceedings.

[9]  Gideon Rechavi,et al.  MIR-451 and Imatinib mesylate inhibit tumor growth of Glioblastoma stem cells. , 2008, Biochemical and biophysical research communications.

[10]  C. Chakraborty,et al.  Network Analysis of Transcription Factors for Nuclear Reprogramming into Induced Pluripotent Stem Cell Using Bioinformatics , 2013, Cell journal.

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

[12]  Mark W. Dewhirst,et al.  Glioma stem cells promote radioresistance by preferential activation of the DNA damage response , 2006, Nature.

[13]  D. Howard,et al.  The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells , 2000, Leukemia.

[14]  S. Bandyopadhyay,et al.  Influence of miRNA in insulin signaling pathway and insulin resistance: micro‐molecules with a major role in type‐2 diabetes , 2014, Wiley interdisciplinary reviews. RNA.

[15]  H. Varmus,et al.  A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. , 1998, Genes & development.

[16]  M. Peter Let-7 and miR-200 microRNAs: Guardians against pluripotency and cancer progression , 2009, Cell cycle.

[17]  Xie-wan Chen,et al.  Essential role of miR-200c in regulating self-renewal of breast cancer stem cells and their counterparts of mammary epithelium , 2015, BMC Cancer.

[18]  Siew Hong Leong,et al.  Cryopreservation of Neurospheres Derived from Human Glioblastoma Multiforme , 2009, Stem cells.

[19]  Yuechao Ding,et al.  MicroRNA-200c overexpression inhibits chemoresistance, invasion and colony formation of human pancreatic cancer stem cells. , 2015, International journal of clinical and experimental pathology.

[20]  Y. Hirohashi,et al.  MicroRNA expression profiles of cancer stem cells in head and neck squamous cell carcinoma , 2015, International journal of oncology.

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

[22]  P. Lansdorp,et al.  Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. , 1997, Blood.

[23]  D. Louis,et al.  PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. , 2001, Genes & development.

[24]  O. Wiestler,et al.  Cancer stem cells : Novel concepts and prospects for tumor therapy , 2007 .

[25]  R. McLendon,et al.  A genetically tractable model of human glioma formation. , 2001, Cancer research.

[26]  R. DePinho,et al.  Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. , 2002, Cancer cell.

[27]  A. Feinberg,et al.  The epigenetic progenitor origin of human cancer , 2006, Nature Reviews Genetics.

[28]  M. Baker Cancer stem cells, becoming common , 2008 .

[29]  Zang Ai-hua,et al.  Stem Cells,Cancer and Cancer Stem Cells , 2005 .

[30]  T. Ichisaka,et al.  Generation of germline-competent induced pluripotent stem cells , 2007, Nature.

[31]  H. Ueno,et al.  A New Prognostic Staging System for Rectal Cancer , 2004, Annals of surgery.

[32]  Takashi Aoi,et al.  Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts , 2008, Nature Biotechnology.

[33]  G. Fuller,et al.  Overexpression of c-MYC promotes an undifferentiated phenotype in cultured astrocytes and allows elevated Ras and Akt signaling to induce gliomas from GFAP-expressing cells in mice. , 2004, Neuron glia biology.

[34]  C. Croce,et al.  MicroRNA-133 controls cardiac hypertrophy , 2007, Nature Medicine.

[35]  Z. Ji,et al.  MicroRNA-7 inhibits the stemness of prostate cancer stem-like cells and tumorigenesis by repressing KLF4/PI3K/Akt/p21 pathway , 2015, Oncotarget.

[36]  E. Bandrés,et al.  MicroRNA‐451 Is Involved in the Self‐renewal, Tumorigenicity, and Chemoresistance of Colorectal Cancer Stem Cells , 2011, Stem cells.

[37]  Michael F. Clarke,et al.  Applying the principles of stem-cell biology to cancer , 2003, Nature Reviews Cancer.

[38]  E. Holland,et al.  Cell type-specific tumor suppression by Ink4a and Arf in Kras-induced mouse gliomagenesis. , 2005, Cancer research.

[39]  William A Weiss,et al.  Genetic determinants of malignancy in a mouse model for oligodendroglioma. , 2003, Cancer research.

[40]  Alfredo Quinones-Hinojosa,et al.  Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection , 2008, Journal of Neuro-Oncology.

[41]  D. Gilliland,et al.  Genetics of myeloid leukemias. , 2003, Annual review of genomics and human genetics.

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

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

[44]  C. Croce,et al.  MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review , 2012, EMBO molecular medicine.

[45]  C. Chakraborty,et al.  Stem cells in the light of evolution , 2012, The Indian journal of medical research.

[46]  P. Pandolfi,et al.  Somatic induction of Pten loss in a preclinical astrocytoma model reveals major roles in disease progression and avenues for target discovery and validation. , 2005, Cancer research.

[47]  Can Liu,et al.  The microRNA miR-34a Inhibits Non-Small Cell Lung Cancer (NSCLC) Growth and the CD44hi Stem-Like NSCLC Cells , 2014, PloS one.

[48]  G. B. Pierce,et al.  Maturation arrest of stem cell differentiation is a common pathway for the cellular origin of teratocarcinomas and epithelial cancers. , 1994, Laboratory investigation; a journal of technical methods and pathology.

[49]  François Vaillant,et al.  Generation of a functional mammary gland from a single stem cell , 2006, Nature.

[50]  A. Kaufmann,et al.  MicroRNA-34a regulates epithelial-mesenchymal transition and cancer stem cell phenotype of head and neck squamous cell carcinoma in vitro. , 2015, International journal of oncology.

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

[52]  P. Dirks,et al.  Cancer stem cells: at the headwaters of tumor development. , 2007, Annual review of pathology.

[53]  B. Thiers Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors , 2008 .

[54]  J. Dick,et al.  Breast cancer stem cells revealed , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Jian Gao,et al.  MiR‐155 targets TP53INP1 to regulate liver cancer stem cell acquisition and self‐renewal , 2015, FEBS letters.

[56]  V. Kim,et al.  Regulation of microRNA biogenesis , 2014, Nature Reviews Molecular Cell Biology.

[57]  G. Piazza,et al.  MicroRNAs are involved in the self-renewal and differentiation of cancer stem cells , 2013, Acta Pharmacologica Sinica.

[58]  R. Jaenisch,et al.  In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state , 2007, Nature.

[59]  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.

[60]  Shridar Ganesan,et al.  Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. , 2005, Genes & development.

[61]  Sanjun Shi,et al.  Cancer stem cells: therapeutic implications and perspectives in cancer therapy , 2013 .

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

[63]  D. Tang,et al.  Understanding cancer stem cell heterogeneity and plasticity , 2012, Cell Research.

[64]  Michael T. McManus,et al.  Dysregulation of Cardiogenesis, Cardiac Conduction, and Cell Cycle in Mice Lacking miRNA-1-2 , 2007, Cell.

[65]  J. Dick,et al.  Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[66]  R. Clarke,et al.  Breast stem cells and cancer. , 2006, Ernst Schering Foundation symposium proceedings.

[67]  J. Tong,et al.  MicroRNA expression profiling identifies miR-328 regulates cancer stem cell-like SP cells in colorectal cancer , 2012, British Journal of Cancer.

[68]  M. Schmid,et al.  5-Azacytidine-induced undercondensations in human chromosomes , 2004, Human Genetics.

[69]  D. Lauffenburger,et al.  Cell Migration: A Physically Integrated Molecular Process , 1996, Cell.

[70]  T. Dittmar,et al.  Recurrence cancer stem cells--made by cell fusion? , 2009, Medical hypotheses.

[71]  Nowell Pc The clonal nature of neoplasia. , 1989 .

[72]  A. Knudson,et al.  [Heredity and cancer in man]. , 1953, Tidsskrift for den Norske laegeforening : tidsskrift for praktisk medicin, ny raekke.

[73]  M. Berger,et al.  Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. , 2001, Cancer research.

[74]  J. Dick,et al.  Retroviral transduction of TLS-ERG initiates a leukemogenic program in normal human hematopoietic cells. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[75]  D. Gutmann,et al.  Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. , 2001, Cancer research.

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

[77]  I. Weissman,et al.  A Genetic Determinant That Specifically Regulates the Frequency of Hematopoietic Stem Cells1 , 2002, The Journal of Immunology.

[78]  T. Visakorpi,et al.  miR-25 Modulates Invasiveness and Dissemination of Human Prostate Cancer Cells via Regulation of αv- and α6-Integrin Expression. , 2015, Cancer research.

[79]  S. Bandyopadhyay,et al.  miRNAs in insulin resistance and diabetes-associated pancreatic cancer: the 'minute and miracle' molecule moving as a monitor in the 'genomic galaxy'. , 2013, Current drug targets.

[80]  Yuichiro Mishima,et al.  miR-1-2 Gets to the Heart of the Matter , 2007, Cell.

[81]  Chaoqian Xu,et al.  The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2 , 2011, Nature Medicine.

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

[83]  W. Yu,et al.  MicroRNA-200c overexpression plays an inhibitory role in human pancreatic cancer stem cells by regulating epithelial-mesenchymal transition. , 2015, Minerva medica.

[84]  Chi-Hung Lin,et al.  MicroRNA-146a directs the symmetric division of Snail-dominant colorectal cancer stem cells , 2014, Nature Cell Biology.

[85]  N. Iwai,et al.  Assessment of the MicroRNA System in Salt-Sensitive Hypertension , 2005, Hypertension Research.

[86]  A. Hamburger,et al.  Primary bioassay of human tumor stem cells. , 1977, Science.

[87]  D. Steindler,et al.  Human cortical glial tumors contain neural stem‐like cells expressing astroglial and neuronal markers in vitro , 2002, Glia.

[88]  Aimee L Jackson,et al.  Myc-regulated microRNAs attenuate embryonic stem cell differentiation , 2009, The EMBO journal.

[89]  H. Ueno,et al.  Tumour `budding' as an index to estimate the potential of aggressiveness in rectal cancer , 2002, Histopathology.

[90]  Lei Wang,et al.  MicroRNA expression profile of gastric cancer stem cells in the MKN-45 cancer cell line. , 2014, Acta biochimica et biophysica Sinica.

[91]  W. De,et al.  Histone Deacetylase 1/Sp1/MicroRNA-200b Signaling Accounts for Maintenance of Cancer Stem-Like Cells in Human Lung Adenocarcinoma , 2014, PloS one.

[92]  Jialing Huang,et al.  Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes , 2007, Nature Medicine.

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

[94]  Yongyi Huang,et al.  EZH2-specific microRNA-98 inhibits human ovarian cancer stem cell proliferation via regulating the pRb-E2F pathway , 2014, Tumor Biology.

[95]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.