Artículo

De Lella Ezcurra, A.L.; Bertolin, A.P.; Kim, K.; Katz, M.J.; Gándara, L.; Misra, T.; Luschnig, S.; Perrimon, N.; Melani, M.; Wappner, P. "miR-190 Enhances HIF-Dependent Responses to Hypoxia in Drosophila by Inhibiting the Prolyl-4-hydroxylase Fatiga" (2016) PLoS Genetics. 12(5)
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Cellular and systemic responses to low oxygen levels are principally mediated by Hypoxia Inducible Factors (HIFs), a family of evolutionary conserved heterodimeric transcription factors, whose alpha- and beta-subunits belong to the bHLH-PAS family. In normoxia, HIFα is hydroxylated by specific prolyl-4-hydroxylases, targeting it for proteasomal degradation, while in hypoxia the activity of these hydroxylases decreases due to low oxygen availability, leading to HIFα accumulation and expression of HIF target genes. To identify microRNAs required for maximal HIF activity, we conducted an overexpression screen in Drosophila melanogaster, evaluating the induction of a HIF transcriptional reporter. miR-190 overexpression enhanced HIF-dependent biological responses, including terminal sprouting of the tracheal system, while in miR-190 loss of function embryos the hypoxic response was impaired. In hypoxic conditions, miR-190 expression was upregulated and required for induction of HIF target genes by directly inhibiting the HIF prolyl-4-hydroxylase Fatiga. Thus, miR-190 is a novel regulator of the hypoxia response that represses the oxygen sensor Fatiga, leading to HIFα stabilization and enhancement of hypoxic responses. © 2016 De Lella Ezcurra et al.

Registro:

Documento: Artículo
Título:miR-190 Enhances HIF-Dependent Responses to Hypoxia in Drosophila by Inhibiting the Prolyl-4-hydroxylase Fatiga
Autor:De Lella Ezcurra, A.L.; Bertolin, A.P.; Kim, K.; Katz, M.J.; Gándara, L.; Misra, T.; Luschnig, S.; Perrimon, N.; Melani, M.; Wappner, P.
Filiación:Instituto Leloir, Buenos Aires, Argentina
Department of Genetics, Harvard Medical School; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, United States
Institute of Molecular Life Sciences, University of Zürich, Zürich, Switzerland
Institute of Neurobiology, University of Münster; Cluster of Excellence EXC 1003, Cells in Motion, CiM, Münster, Germany
Departamento de Fisiología y Biología Molecular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Fatiga; hypoxia inducible factor; hypoxia inducible factor 1alpha; hypoxia inducible factor 1beta; hypoxia inducible factor proline dioxygenase; microRNA; microRNA 190; Sima; transcription factor GAL4; unclassified drug; hypoxia inducible factor 1alpha; microRNA; oxygen; procollagen proline 2 oxoglutarate 4 dioxygenase; 3' untranslated region; Article; controlled study; Drosophila melanogaster; embryo; environmental stress; enzyme inhibition; gene interaction; gene overexpression; hypoxia; lethality; loss of function mutation; nonhuman; oxygen supply; phenotype; protein degradation; protein expression; protein function; protein stability; pupa; RNA interference; trachea; animal; biosynthesis; cell hypoxia; gene expression regulation; genetic transcription; genetics; growth, development and aging; human; metabolism; Animals; Cell Hypoxia; Drosophila melanogaster; Gene Expression Regulation; Humans; Hypoxia-Inducible Factor 1, alpha Subunit; MicroRNAs; Oxygen; Prolyl Hydroxylases; Transcription, Genetic
Año:2016
Volumen:12
Número:5
DOI: http://dx.doi.org/10.1371/journal.pgen.1006073
Título revista:PLoS Genetics
Título revista abreviado:PLoS Genet.
ISSN:15537390
CAS:hypoxia inducible factor 1beta, 138391-32-9; hypoxia inducible factor proline dioxygenase; oxygen, 7782-44-7; procollagen proline 2 oxoglutarate 4 dioxygenase, 9028-06-2; Hypoxia-Inducible Factor 1, alpha Subunit; MicroRNAs; Oxygen; Prolyl Hydroxylases
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_15537390_v12_n5_p_DeLellaEzcurra

Referencias:

  • Weidemann, A., Johnson, R.S., Biology of HIF-1alpha (2008) Cell Death Differ, 15, pp. 621-627. , 10.1038/cdd.2008.12, 18259201, ().:–
  • Firth, J.D., Ebert, B.L., Pugh, C.W., Ratcliffe, P.J., Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3' enhancer (1994) Proc Natl Acad Sci U S A, 91, pp. 6496-6500. , 8022811, ().:–
  • Haase, V.H., Regulation of erythropoiesis by hypoxia-inducible factors (2013) Blood Rev, 27, pp. 41-53. , 10.1016/j.blre.2012.12.003, 23291219, ().:–
  • Semenza, G.L., Wang, G.L., A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation (1992) Mol Cell Biol, 12, pp. 5447-5454. , 1448077, ().:–
  • Rey, S., Semenza, G.L., Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling (2010) Cardiovasc Res, 86, pp. 236-242. , 10.1093/cvr/cvq045, 20164116, ().:–
  • Forsythe, J.A., Jiang, B.H., Iyer, N.V., Agani, F., Leung, S.W., Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1 (1996) Mol Cell Biol, 16, pp. 4604-4613. , 8756616, . ().:–
  • Maxwell, P.H., Pugh, C.W., Ratcliffe, P.J., Inducible operation of the erythropoietin 3' enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism (1993) Proc Natl Acad Sci U S A, 90, pp. 2423-2427. , 8460154, ().:–
  • Wang, G.L., Semenza, G.L., Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia (1993) J Biol Chem, 268, pp. 21513-21518. , 8408001, ().:–
  • Wang, G.L., Semenza, G.L., General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia (1993) Proc Natl Acad Sci U S A, 90, pp. 4304-4308. , 8387214, ().:–
  • Wang, G.L., Semenza, G.L., Purification and characterization of hypoxia-inducible factor 1 (1995) J Biol Chem, 270, pp. 1230-1237. , 7836384, ().:–
  • Semenza, G.L., Hypoxia-inducible factors in physiology and medicine (2012) Cell, 148, pp. 399-408. , 10.1016/j.cell.2012.01.021, 22304911, ().:–
  • Brocato, J., Chervona, Y., Costa, M., Molecular responses to hypoxia-inducible factor 1alpha and beyond (2014) Mol Pharmacol, 85, pp. 651-657. , 10.1124/mol.113.089623, 24569087, ().:–
  • Wang, G.L., Jiang, B.H., Rue, E.A., Semenza, G.L., Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension (1995) Proc Natl Acad Sci U S A, 92, pp. 5510-5514. , 7539918, ().:–
  • Pugh, C.W., O'Rourke, J.F., Nagao, M., Gleadle, J.M., Ratcliffe, P.J., Activation of hypoxia-inducible factor-1; definition of regulatory domains within the alpha subunit (1997) J Biol Chem, 272, pp. 11205-11214. , 9111021, ().:–
  • Greer, S.N., Metcalf, J.L., Wang, Y., Ohh, M., The updated biology of hypoxia-inducible factor (2012) EMBO J, 31, pp. 2448-2460. , 10.1038/emboj.2012.125, 22562152, ().:–
  • Maxwell, P.H., Wiesener, M.S., Chang, G.W., Clifford, S.C., Vaux, E.C., The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis (1999) Nature, 399, pp. 271-275. , 10353251, . ().:–
  • Huang, L.E., Gu, J., Schau, M., Bunn, H.F., Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway (1998) Proc Natl Acad Sci U S A, 95, pp. 7987-7992. , 9653127, ().:–
  • Jaakkola, P., Mole, D.R., Tian, Y.M., Wilson, M.I., Gielbert, J., Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation (2001) Science, 292, pp. 468-472. , 11292861, . ().:–
  • Epstein, A.C., Gleadle, J.M., McNeill, L.A., Hewitson, K.S., O'Rourke, J., C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation (2001) Cell, 107, pp. 43-54. , 11595184, . ().:–
  • Bruick, R.K., McKnight, S.L., A conserved family of prolyl-4-hydroxylases that modify HIF (2001) Science, 294, pp. 1337-1340. , 11598268, ().:–
  • Wenger, R.H., Stiehl, D.P., Camenisch, G., Integration of oxygen signaling at the consensus HRE (2005) Sci STKE, 2005, p. re12. , 16234508, ().:
  • Semenza, G.L., HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus (2001) Cell, 107, pp. 1-3. , 11595178, ().:–
  • Majmundar, A.J., Wong, W.J., Simon, M.C., Hypoxia-inducible factors and the response to hypoxic stress (2010) Mol Cell, 40, pp. 294-309. , 10.1016/j.molcel.2010.09.022, 20965423, ().:–
  • Romero, N.M., Dekanty, A., Wappner, P., Cellular and developmental adaptations to hypoxia: a Drosophila perspective (2007) Methods Enzymol, 435, pp. 123-144. , 17998052, ().:–
  • Nambu, J.R., Chen, W., Hu, S., Crews, S.T., The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1 alpha and Drosophila single-minded (1996) Gene, 172, pp. 249-254. , 8682312, ().:–
  • Sonnenfeld, M., Ward, M., Nystrom, G., Mosher, J., Stahl, S., The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development (1997) Development, 124, pp. 4571-4582. , 9409674, . ().:–
  • Lavista-Llanos, S., Centanin, L., Irisarri, M., Russo, D.M., Gleadle, J.M., Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar (2002) Mol Cell Biol, 22, pp. 6842-6853. , 12215541, . ().:–
  • Gorr, T.A., Tomita, T., Wappner, P., Bunn, H.F., Regulation of Drosophila hypoxia-inducible factor (HIF) activity in SL2 cells: identification of a hypoxia-induced variant isoform of the HIFalpha homolog gene similar (2004) J Biol Chem, 279, pp. 36048-36058. , 15169765, ().:–
  • Centanin, L., Ratcliffe, P.J., Wappner, P., Reversion of lethality and growth defects in Fatiga oxygen-sensor mutant flies by loss of hypoxia-inducible factor-alpha/Sima (2005) EMBO Rep, 6, pp. 1070-1075. , 16179946, ().:–
  • Acevedo, J.M., Centanin, L., Dekanty, A., Wappner, P., Oxygen sensing in Drosophila: multiple isoforms of the prolyl hydroxylase fatiga have different capacity to regulate HIFalpha/Sima (2010) PLoS One, 5. , 10.1371/journal.pone.0012390, 20811646, ().:
  • Dekanty, A., Romero, N.M., Bertolin, A.P., Thomas, M.G., Leishman, C.C., Drosophila genome-wide RNAi screen identifies multiple regulators of HIF-dependent transcription in hypoxia (2010) PLoS Genet, 6. , 10.1371/journal.pgen.1000994, 20585616, . ().:
  • Dietzl, G., Chen, D., Schnorrer, F., Su, K.C., Barinova, Y., A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila (2007) Nature, 448, pp. 151-156. , 17625558, . ().:–
  • Stark, A., Kheradpour, P., Parts, L., Brennecke, J., Hodges, E., Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes (2007) Genome Res, 17, pp. 1865-1879. , 17989255, . ().:–
  • Ruby, J.G., Stark, A., Johnston, W.K., Kellis, M., Bartel, D.P., Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs (2007) Genome Res, 17, pp. 1850-1864. , 17989254, . ().:–
  • Centanin, L., Dekanty, A., Romero, N., Irisarri, M., Gorr, T.A., Cell autonomy of HIF effects in Drosophila: tracheal cells sense hypoxia and induce terminal branch sprouting (2008) Dev Cell, 14, pp. 547-558. , 10.1016/j.devcel.2008.01.020, 18410730, . ().:–
  • Jarecki, J., Johnson, E., Krasnow, M.A., Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF (1999) Cell, 99, pp. 211-220. , 10535739, ().:–
  • Mortimer, N.T., Moberg, K.H., Regulation of Drosophila embryonic tracheogenesis by dVHL and hypoxia (2009) Dev Biol, 329, pp. 294-305. , 10.1016/j.ydbio.2009.03.001, 19285057, ().:–
  • Chen, Y.W., Song, S., Weng, R., Verma, P., Kugler, J.M., Systematic study of Drosophila microRNA functions using a collection of targeted knockout mutations (2014) Dev Cell, 31, pp. 784-800. , 10.1016/j.devcel.2014.11.029, 25535920, . ().:–
  • Baird, N.A., Turnbull, D.W., Johnson, E.A., Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1 (2006) J Biol Chem, 281, pp. 38675-38681. , 17040902, ().:–
  • Brown, N.H., Gregory, S.L., Rickoll, W.L., Fessler, L.I., Prout, M., Talin is essential for integrin function in Drosophila (2002) Dev Cell, 3, pp. 569-579. , 12408808, . ().:–
  • Betel, D., Koppal, A., Agius, P., Sander, C., Leslie, C., Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites (2010) Genome Biol, 11, p. R90. , 10.1186/gb-2010-11-8-r90, 20799968, ().:
  • Betel, D., Wilson, M., Gabow, A., Marks, D.S., Sander, C., The microRNA.org resource: targets and expression (2008) Nucleic Acids Res, 36, pp. D149-153. , 18158296, ().:–
  • Enright, A.J., John, B., Gaul, U., Tuschl, T., Sander, C., MicroRNA targets in Drosophila (2003) Genome Biol, 5, p. R1. , 14709173, . ().:
  • Rehwinkel, J., Behm-Ansmant, I., Gatfield, D., Izaurralde, E., A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing (2005) RNA, 11, pp. 1640-1647. , 16177138, ().:–
  • Lei, Z., Li, B., Yang, Z., Fang, H., Zhang, G.M., Regulation of HIF-1alpha and VEGF by miR-20b tunes tumor cells to adapt to the alteration of oxygen concentration (2009) PLoS One, 4. , 10.1371/journal.pone.0007629, 19893619, . ().:
  • Rane, S., He, M., Sayed, D., Vashistha, H., Malhotra, A., Downregulation of miR-199a derepresses hypoxia-inducible factor-1alpha and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes (2009) Circ Res, 104, pp. 879-886. , 10.1161/CIRCRESAHA.108.193102, 19265035, . ().:–
  • Bruning, U., Cerone, L., Neufeld, Z., Fitzpatrick, S.F., Cheong, A., MicroRNA-155 promotes resolution of hypoxia-inducible factor 1alpha activity during prolonged hypoxia (2011) Mol Cell Biol, 31, pp. 4087-4096. , 10.1128/MCB.01276-10, 21807897, . ().:–
  • Csak, T., Bala, S., Lippai, D., Satishchandran, A., Catalano, D., microRNA-122 regulates hypoxia-inducible factor-1 and vimentin in hepatocytes and correlates with fibrosis in diet-induced steatohepatitis (2014) Liver Int, , . ()
  • Bai, R., Zhao, A.Q., Zhao, Z.Q., Liu, W.L., Jian, D.M., MicroRNA-195 induced apoptosis in hypoxic chondrocytes by targeting hypoxia-inducible factor 1 alpha (2015) Eur Rev Med Pharmacol Sci, 19, pp. 545-551. , 25753868, ().:–
  • Han, F., Wu, Y., Jiang, W., MicroRNA-18a Decreases Choroidal Endothelial Cell Proliferation and Migration by Inhibiting HIF1A Expression (2015) Med Sci Monit, 21, pp. 1642-1647. , 10.12659/MSM.893068, 26044722, ().:–
  • Liu, F.J., Kaur, P., Karolina, D.S., Sepramaniam, S., Armugam, A., MiR-335 Regulates Hif-1alpha to Reduce Cell Death in Both Mouse Cell Line and Rat Ischemic Models (2015) PLoS One, 10. , 10.1371/journal.pone.0128432, 26030758, . ().:
  • Zhou, J., Xu, D., Xie, H., Tang, J., Liu, R., miR-33a functions as a tumor suppressor in melanoma by targeting HIF-1alpha (2015) Cancer Biol Ther, 16, pp. 846-855. , 10.1080/15384047.2015.1030545, 25891797, . ().:–
  • Ghosh, G., Subramanian, I.V., Adhikari, N., Zhang, X., Joshi, H.P., Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis (2010) J Clin Invest, 120, pp. 4141-4154. , 10.1172/JCI42980, 20972335, . ().:–
  • Yuan, Q., Gao, W., Liu, B., Ye, W., Upregulation of miR-184 enhances the malignant biological behavior of human glioma cell line A172 by targeting FIH-1 (2014) Cell Physiol Biochem, 34, pp. 1125-1136. , 10.1159/000366326, 25277131, ().:–
  • Puissegur, M.P., Mazure, N.M., Bertero, T., Pradelli, L., Grosso, S., miR-210 is overexpressed in late stages of lung cancer and mediates mitochondrial alterations associated with modulation of HIF-1 activity (2011) Cell Death Differ, 18, pp. 465-478. , 10.1038/cdd.2010.119, 20885442, . ().:–
  • Kelly, T.J., Souza, A.L., Clish, C.B., Puigserver, P., A hypoxia-induced positive feedback loop promotes hypoxia-inducible factor 1alpha stability through miR-210 suppression of glycerol-3-phosphate dehydrogenase 1-like (2011) Mol Cell Biol, 31, pp. 2696-2706. , 10.1128/MCB.01242-10, 21555452, ().:–
  • Saito, K., Kondo, E., Matsushita, M., MicroRNA 130 family regulates the hypoxia response signal through the P-body protein DDX6 (2011) Nucleic Acids Res, 39, pp. 6086-6099. , 10.1093/nar/gkr194, 21486751, ().:–
  • Sun, G., Zhou, Y., Li, H., Guo, Y., Shan, J., Over-expression of microRNA-494 up-regulates hypoxia-inducible factor-1 alpha expression via PI3K/Akt pathway and protects against hypoxia-induced apoptosis (2013) J Biomed Sci, 20, p. 100. , 10.1186/1423-0127-20-100, 24364919, . ().:
  • Liu, Y., Nie, H., Zhang, K., Ma, D., Yang, G., A feedback regulatory loop between HIF-1alpha and miR-21 in response to hypoxia in cardiomyocytes (2014) FEBS Lett, 588, pp. 3137-3146. , 10.1016/j.febslet.2014.05.067, 24983504, . ().:–
  • Yang, Y., Ma, W., Wu, D., Huang, Y., Li, H., MiR-17 partly promotes hematopoietic cell expansion through augmenting HIF-1alpha in osteoblasts (2013) PLoS One, 8. , 10.1371/journal.pone.0070232, 23936170, . ().:
  • Lando, D., Peet, D.J., Whelan, D.A., Gorman, J.J., Whitelaw, M.L., Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch (2002) Science, 295, pp. 858-861. , 11823643, ().:–
  • Selak, M.A., Armour, S.M., MacKenzie, E.D., Boulahbel, H., Watson, D.G., Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase (2005) Cancer Cell, 7, pp. 77-85. , 15652751, . ().:–
  • Lagos-Quintana, M., Rauhut, R., Meyer, J., Borkhardt, A., Tuschl, T., New microRNAs from mouse and human (2003) RNA, 9, pp. 175-179. , 12554859, ().:–
  • Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., A mammalian microRNA expression atlas based on small RNA library sequencing (2007) Cell, 129, pp. 1401-1414. , 17604727, . ().:–
  • Kozomara, A., Griffiths-Jones, S., miRBase: annotating high confidence microRNAs using deep sequencing data (2014) Nucleic Acids Res, 42, pp. D68-73. , 10.1093/nar/gkt1181, 24275495, ().:–
  • Kozomara, A., Griffiths-Jones, S., miRBase: integrating microRNA annotation and deep-sequencing data (2011) Nucleic Acids Res, 39, pp. D152-157. , 10.1093/nar/gkq1027, 21037258, ().:–
  • Griffiths-Jones, S., Saini, H.K., van Dongen, S., Enright, A.J., miRBase: tools for microRNA genomics (2008) Nucleic Acids Res, 36, pp. D154-158. , 17991681, ().:–
  • Griffiths-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A., Enright, A.J., miRBase: microRNA sequences, targets and gene nomenclature (2006) Nucleic Acids Res, 34, pp. D140-144. , 16381832, ().:–
  • Griffiths-Jones, S., The microRNA Registry (2004) Nucleic Acids Res, 32, pp. D109-111. , 14681370, ().:–
  • Wood, E.J., Lipovich, L., MicroRNAs in opioid addiction: elucidating evolution (2012) Front Genet, 3, p. 241. , 10.3389/fgene.2012.00241, 23233859, ().:
  • Agarwal, V., Bell, G.W., Nam, J.W., Bartel, D.P., Predicting effective microRNA target sites in mammalian mRNAs (2015) Elife, 4. , ()
  • Wong, N., Wang, X., miRDB: an online resource for microRNA target prediction and functional annotations (2015) Nucleic Acids Res, 43, pp. D146-152. , 10.1093/nar/gku1104, 25378301, ().:–
  • Hung, T.M., Ho, C.M., Liu, Y.C., Lee, J.L., Liao, Y.R., Up-regulation of microRNA-190b plays a role for decreased IGF-1 that induces insulin resistance in human hepatocellular carcinoma (2014) PLoS One, 9. , 10.1371/journal.pone.0089446, 24586785, . ().:
  • Kutay, H., Bai, S., Datta, J., Motiwala, T., Pogribny, I., Downregulation of miR-122 in the rodent and human hepatocellular carcinomas (2006) J Cell Biochem, 99, pp. 671-678. , 16924677, . ().:–
  • Guglielmelli, P., Tozzi, L., Pancrazzi, A., Bogani, C., Antonioli, E., MicroRNA expression profile in granulocytes from primary myelofibrosis patients (2007) Exp Hematol, 35, pp. 1708-1718. , 17976522, . ().:–
  • Zhang, Y., Li, M., Wang, H., Fisher, W.E., Lin, P.H., Profiling of 95 microRNAs in pancreatic cancer cell lines and surgical specimens by real-time PCR analysis (2009) World J Surg, 33, pp. 698-709. , 10.1007/s00268-008-9833-0, 19030927, . ().:–
  • Lowery, A.J., Miller, N., Devaney, A., McNeill, R.E., Davoren, P.A., MicroRNA signatures predict oestrogen receptor, progesterone receptor and HER2/neu receptor status in breast cancer (2009) Breast Cancer Res, 11, p. R27. , 10.1186/bcr2257, 19432961, . ().:
  • Volinia, S., Galasso, M., Sana, M.E., Wise, T.F., Palatini, J., Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA (2012) Proc Natl Acad Sci U S A, 109, pp. 3024-3029. , 10.1073/pnas.1200010109, 22315424, . ().:–
  • Cizeron-Clairac, G., Lallemand, F., Vacher, S., Lidereau, R., Bieche, I., MiR-190b, the highest up-regulated miRNA in ERalpha-positive compared to ERalpha-negative breast tumors, a new biomarker in breast cancers? (2015) BMC Cancer, 15, p. 499. , 10.1186/s12885-015-1505-5, 26141719, . ():
  • Gaedcke, J., Grade, M., Camps, J., Sokilde, R., Kaczkowski, B., The rectal cancer microRNAome—microRNA expression in rectal cancer and matched normal mucosa (2012) Clin Cancer Res, 18, pp. 4919-4930. , 22850566, . ().:–
  • Cantara, S., Pilli, T., Sebastiani, G., Cevenini, G., Busonero, G., Circulating miRNA95 and miRNA190 are sensitive markers for the differential diagnosis of thyroid nodules in a Caucasian population (2014) J Clin Endocrinol Metab, 99, pp. 4190-4198. , 10.1210/jc.2014-1923, 25057879, . ().:–
  • Zimna, A., Kurpisz, M., Hypoxia-Inducible Factor-1 in Physiological and Pathophysiological Angiogenesis: Applications and Therapies (2015) Biomed Res Int, 2015, p. 549412. , 10.1155/2015/549412, 26146622, ().:
  • Mabjeesh, N.J., Amir, S., Hypoxia-inducible factor (HIF) in human tumorigenesis (2007) Histol Histopathol, 22, pp. 559-572. , 17330811, ().:–
  • Semenza, G.L., Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics (2010) Oncogene, 29, pp. 625-634. , 10.1038/onc.2009.441, 19946328, ().:–
  • Semenza, G.L., Hypoxia, clonal selection, and the role of HIF-1 in tumor progression (2000) Crit Rev Biochem Mol Biol, 35, pp. 71-103. , 10821478, ().:–
  • Liao, D., Johnson, R.S., Hypoxia: a key regulator of angiogenesis in cancer (2007) Cancer Metastasis Rev, 26, pp. 281-290. , 17603752, ().:–
  • Semenza, G.L., HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations (2013) J Clin Invest, 123, pp. 3664-3671. , 10.1172/JCI67230, 23999440, ().:–
  • Sullivan, R., Graham, C.H., Hypoxia-driven selection of the metastatic phenotype (2007) Cancer Metastasis Rev, 26, pp. 319-331. , 17458507, ().:–
  • Moeller, B.J., Richardson, R.A., Dewhirst, M.W., Hypoxia and radiotherapy: opportunities for improved outcomes in cancer treatment (2007) Cancer Metastasis Rev, 26, pp. 241-248. , 17440683, ().:–
  • Rohwer, N., Cramer, T., Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways (2011) Drug Resist Updat, 14, pp. 191-201. , 10.1016/j.drup.2011.03.001, 21466972, ().:–
  • Semenza, G.L., Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy (2012) Trends Pharmacol Sci, 33, pp. 207-214. , 10.1016/j.tips.2012.01.005, 22398146, ().:–
  • Bhaskaran, M., Mohan, M., MicroRNAs: history, biogenesis, and their evolving role in animal development and disease (2014) Vet Pathol, 51, pp. 759-774. , 10.1177/0300985813502820, 24045890, ().:–
  • Zhang, B., Pan, X., Cobb, G.P., Anderson, T.A., microRNAs as oncogenes and tumor suppressors (2007) Dev Biol, 302, pp. 1-12. , 16989803, ().:–
  • Cho, W.C., OncomiRs: the discovery and progress of microRNAs in cancers (2007) Mol Cancer, 6, p. 60. , 17894887, ().:
  • Beezhold, K., Liu, J., Kan, H., Meighan, T., Castranova, V., miR-190-mediated downregulation of PHLPP contributes to arsenic-induced Akt activation and carcinogenesis (2011) Toxicol Sci, 123, pp. 411-420. , 10.1093/toxsci/kfr188, 21750348, . ().:–
  • Yu, Y., Zhang, D., Huang, H., Li, J., Zhang, M., NF-kappaB1 p50 promotes p53 protein translation through miR-190 downregulation of PHLPP1 (2014) Oncogene, 33, pp. 996-1005. , 10.1038/onc.2013.8, 23396362, . ().:–
  • Du, K., Yu, Y., Zhang, D., Luo, W., Huang, H., NFkappaB1 (p50) suppresses SOD2 expression by inhibiting FoxO3a transactivation in a miR190/PHLPP1/Akt-dependent axis (2013) Mol Biol Cell, 24, pp. 3577-3583. , 10.1091/mbc.E13-06-0343, 24068327, . ().:–
  • Jiang, B.H., Zheng, J.Z., Aoki, M., Vogt, P.K., Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells (2000) Proc Natl Acad Sci U S A, 97, pp. 1749-1753. , 10677529, ().:–
  • Guo, L., Qiu, Z., Wei, L., Yu, X., Gao, X., The microRNA-328 regulates hypoxic pulmonary hypertension by targeting at insulin growth factor 1 receptor and L-type calcium channel-alpha1C (2012) Hypertension, 59, pp. 1006-1013. , 10.1161/HYPERTENSIONAHA.111.185413, 22392900, . ().:–
  • Li, S., Ran, Y., Zhang, D., Chen, J., Zhu, D., MicroRNA-138 plays a role in hypoxic pulmonary vascular remodelling by targeting Mst1 (2013) Biochem J, 452, pp. 281-291. , 10.1042/BJ20120680, 23485012, ().:–
  • Li, S.S., Ran, Y.J., Zhang, D.D., Li, S.Z., Zhu, D., MicroRNA-190 regulates hypoxic pulmonary vasoconstriction by targeting a voltage-gated K(+) channel in arterial smooth muscle cells (2014) J Cell Biochem, 115, pp. 1196-1205. , 10.1002/jcb.24771, 24446351, ().:–
  • Bienertova-Vasku, J., Novak, J., Vasku, A., MicroRNAs in pulmonary arterial hypertension: pathogenesis, diagnosis and treatment (2015) J Am Soc Hypertens, 9, pp. 221-234. , 10.1016/j.jash.2014.12.011, 25660363, ().:–
  • Bejarano, F., Bortolamiol-Becet, D., Dai, Q., Sun, K., Saj, A., A genome-wide transgenic resource for conditional expression of Drosophila microRNAs (2012) Development, 139, pp. 2821-2831. , 10.1242/dev.079939, 22745315, . ().:–
  • Barrio, L., Dekanty, A., Milan, M., MicroRNA-mediated regulation of Dp53 in the Drosophila fat body contributes to metabolic adaptation to nutrient deprivation (2014) Cell Rep, 8, pp. 528-541. , 10.1016/j.celrep.2014.06.020, 25017064, ().:–

Citas:

---------- APA ----------
De Lella Ezcurra, A.L., Bertolin, A.P., Kim, K., Katz, M.J., Gándara, L., Misra, T., Luschnig, S.,..., Wappner, P. (2016) . miR-190 Enhances HIF-Dependent Responses to Hypoxia in Drosophila by Inhibiting the Prolyl-4-hydroxylase Fatiga. PLoS Genetics, 12(5).
http://dx.doi.org/10.1371/journal.pgen.1006073
---------- CHICAGO ----------
De Lella Ezcurra, A.L., Bertolin, A.P., Kim, K., Katz, M.J., Gándara, L., Misra, T., et al. "miR-190 Enhances HIF-Dependent Responses to Hypoxia in Drosophila by Inhibiting the Prolyl-4-hydroxylase Fatiga" . PLoS Genetics 12, no. 5 (2016).
http://dx.doi.org/10.1371/journal.pgen.1006073
---------- MLA ----------
De Lella Ezcurra, A.L., Bertolin, A.P., Kim, K., Katz, M.J., Gándara, L., Misra, T., et al. "miR-190 Enhances HIF-Dependent Responses to Hypoxia in Drosophila by Inhibiting the Prolyl-4-hydroxylase Fatiga" . PLoS Genetics, vol. 12, no. 5, 2016.
http://dx.doi.org/10.1371/journal.pgen.1006073
---------- VANCOUVER ----------
De Lella Ezcurra, A.L., Bertolin, A.P., Kim, K., Katz, M.J., Gándara, L., Misra, T., et al. miR-190 Enhances HIF-Dependent Responses to Hypoxia in Drosophila by Inhibiting the Prolyl-4-hydroxylase Fatiga. PLoS Genet. 2016;12(5).
http://dx.doi.org/10.1371/journal.pgen.1006073