Dicer mediating the expression of miR-143 and miR-155 regulates hexokinase II associated cellular response to hypoxia

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 307, Issue 11, 2014, Pages L829-L837

  Yao, Mengying ^a   Wang, Xinhua ^a   Tang, Ying ^b   Zhang, Weihong ^c   Cui, Bing ^a   Liu, Qiuhong ^a   Xing, Lihua ^a  

^a THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

^b Shanghai Institute of Medical Genetics   (China)

^c ZHENGZHOU UNIVERSITY   (China)

Author keywords

Apoptosis; Glycolysis; Hypoxic damage; Lung alveolar epithelial cell; Micro ribonucleic acid

Indexed keywords

DICER; HEXOKINASE; HEXOKINASE 2; HYPOXIA INDUCIBLE FACTOR 1; LACTIC ACID; MICRORNA 143; MICRORNA 155; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; GLUCOSE; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MICRORNA; MIRN143 MICRORNA, HUMAN; MIRN155 MICRORNA, HUMAN; RIBONUCLEASE III;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL HYPOXIA; GENE EXPRESSION; GENE SILENCING; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LUNG ALVEOLUS EPITHELIUM; MOUSE; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; DISEASE MODEL; GENETICS; LUNG; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; CELL HYPOXIA; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; GLUCOSE; GLYCOLYSIS; HEXOKINASE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LACTIC ACID; LUNG; MICE; MICE, INBRED BALB C; MICRORNAS; RIBONUCLEASE III; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84913594663     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00081.2014     Document Type: Article

References (42)

1. Babar IA, Czochor J, Steinmetz A, Weidhaas JB, Glazer PM, Slack FJ. Inhibition of hypoxia-induced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol Ther 12: 908–914, 2011.
2. Bristow RG, Hill RP. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability Nature reviews. Cancer 8: 180–192, 2008.
3. Carpenter TC, Stenmark KR. Hypoxia decreases lung neprilysin expression and increases pulmonary vascular leak. Am J Physiol Lung Cell Mol Physiol 281: L941–L948, 2001.
4. Caruso P, MacLean MR, Khanin R, McClure J, Soon E, Southgate M, MacDonald RA, Greig JA, Robertson KE, Masson R, Denby L, Dempsie Y, Long L, Morrell NW, Baker AH. Dynamic changes in lung microRNA profiles during the development of pulmonary hypertension due to chronic hypoxia and monocrotaline. Arteriosclerosis Thromb Vasc Biol 30: 716–723, 2010.
5. Donnem T, Eklo K, Berg T, Sorbye SW, Lonvik K, Al-Saad S, Al-Shibli K, Andersen S, Stenvold H, Bremnes RM, Busund LT. Prognostic impact of MiR-155 in non-small cell lung cancer evaluated by in situ hybridization (Abstract). J Trans Med 9: 6, 2011.
6. Fang R, Xiao T, Fang Z, Sun Y, Li F, Gao Y, Feng Y, Li L, Wang Y, Liu X, Chen H, Liu XY, Ji H. MicroRNA-143 (miR-143) regulates cancer glycolysis via targeting hexokinase 2 gene. J Biol Chem 287: 23227–23235, 2012.
7. Farkas L, Gauldie J, Voelkel NF, Kolb M. Pulmonary hypertension and idiopathic pulmonary fibrosis: a tale of angiogenesis, apoptosis, and growth factors. Am J Respir Cell Mol Biol 45: 1–15, 2011.
8. Fish JE, Matouk CC, Yeboah E, Bevan SC, Khan M, Patil K, Ohh M, Marsden PA. Hypoxia-inducible expression of a natural cis-antisense transcript inhibits endothelial nitric-oxide synthase. J Biol Chem 282: 15652–15666, 2007.
9. Frohlich S, Boylan J, McLoughlin P. Hypoxia-induced inflammation in the lung: a potential therapeutic target in acute lung injury? Am J Respir Cell Mol Biol 48: 271–279, 2013.
10. Gonzalez NC, Wood JG. Alveolar hypoxia-induced systemic inflammation: what low PO(2) does and does not do. Adv Exp Med Biol 662: 27–32, 2010.
11. Heikkinen S, Suppola S, Malkki M, Deeb SS, Janne J, Laakso M. Mouse hexokinase II gene: structure, cDNA, promoter analysis, and expression pattern. Mamm Genome 11: 91–96, 2000.
12. Ho JJ, Man HS, Marsden PA. Nitric oxide signaling in hypoxia. J Mol Med 90: 217–231, 2012.
13. Ho JJ, Metcalf JL, Yan MS, Turgeon PJ, Wang JJ, Chalsev M, Petruzziello-Pellegrini TN, Tsui AK, He JZ, Dhamko H, Man HS, Robb GB, Teh BT, Ohh M, Marsden PA. Functional importance of Dicer protein in the adaptive cellular response to hypoxia. J Biol Chem 287: 29003–29020, 2012.
14. Jiang S, Zhang LF, Zhang HW, Hu S, Lu MH, Liang S, Li B, Li Y, Li D, Wang ED, Liu MF. A novel miR-155/miR-143 cascade controls glycolysis by regulating hexokinase 2 in breast cancer cells. EMBO J 31: 1985–1998, 2012.
15. Krol J, Loedige I, Filipowicz W. The widespread regulation of mi-croRNA biogenesis, function and decay. Nat Rev Genet 11: 597–610, 2010.
16. Madjdpour C, Jewell UR, Kneller S, Ziegler U, Schwendener R, Booy C, Klausli L, Pasch T, Schimmer RC, Beck-Schimmer B. Decreased alveolar oxygen induces lung inflammation. Am J Physiol Lung Cell Mol Physiol 284: L360–L367, 2003.
17. Mathupala SP, Heese C, Pedersen PL. Glucose catabolism in cancer cells. The type II hexokinase promoter contains functionally active response elements for the tumor suppressor p53. J Biol Chem 272: 22776–22780, 1997.
18. Mathupala SP, Ko YH, Pedersen PL. Hexokinase-2 bound to mitochondria: cancer’s stygian link to the “Warburg Effect” and a pivotal target for effective therapy. Semin Cancer Biol 19: 17–24, 2009.
19. Matsuda S, Ichigotani Y, Okuda T, Irimura T, Nakatsugawa S, Hamaguchi M. Molecular cloning and characterization of a novel human gene (HERNA) which encodes a putative RNA-helicase. Biochim Biophys Acta 1490: 163–169, 2000.
20. McQuillan LP, Leung GK, Marsden PA, Kostyk SK, Kourembanas S. Hypoxia inhibits expression of eNOS via transcriptional and posttranscrip-tional mechanisms. Am J Physiol Heart Circ Physiol 267: H1921–H1927, 1994.
21. Minamino T, Christou H, Hsieh CM, Liu Y, Dhawan V, Abraham NG, Perrella MA, Mitsialis SA, Kourembanas S. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc Natl Acad Sci USA 98: 8798–8803, 2001.
22. Nederlof R, Eerbeek O, Hollmann MW, Southworth R, Zuurbier CJ. Targeting hexokinase II to mitochondria to modulate energy metabolism and reduce ischaemia-reperfusion injury in heart. Br J Pharmacol 171: 2067–2079, 2014.
23. Parsaee H, Asili J, Mousavi SH, Soofi H, Emami SA, Tayarani-Najaran Z. Apoptosis induction of salvia chorassanica root extract on human cervical cancer cell line. Iranian J Pharm Re 12: 75–83, 2013.
24. Pedersen PL. Warburg, me and Hexokinase 2: multiple discoveries of key molecular events underlying one of cancers’ most common phenotypes, the “Warburg Effect”, i.e., elevated glycolysis in the presence of oxygen. J Bioenerget Biomembr 39: 211–222, 2007.
25. Pedersen PL, Mathupala S, Rempel A, Geschwind JF, Ko YH. Mito-chondrial bound type II hexokinase: a key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim Biophys Acta 1555: 14–20, 2002.
26. Perevoshchikova IV, Zorov SD, Kotova EA, Zorov DB, Antonenko YN. Hexokinase inhibits flux of fluorescently labeled ATP through mito-chondrial outer membrane porin. FEBS Lett 584: 2397–2402, 2010.
27. Peschiaroli A, Giacobbe A, Formosa A, Markert EK, Bongiorno-Borbone L, Levine AJ, Candi E, D’Alessandro A, Zolla L, Finazzi Agro A, Melino G. miR-143 regulates hexokinase 2 expression in cancer cells. Oncogene 32: 797–802, 2013.
28. Riddle SR, Ahmad A, Ahmad S, Deeb SS, Malkki M, Schneider BK, Allen CB, White CW. Hypoxia induces hexokinase II gene expression in human lung cell line A549. Am J Physiol Lung Cell Mol Physiol 278: L407–L416, 2000.
29. Rio Frio T, Bahubeshi A, Kanellopoulou C, Hamel N, Niedziela M, Sabbaghian N, Pouchet C, Gilbert L, O’Brien PK, Serfas K, Broder-ick P, Houlston RS, Lesueur F, Bonora E, Muljo S, Schimke RN, Bouron-Dal Soglio D, Arseneau J, Schultz KA, Priest JR, Nguyen VH, Harach HR, Livingston DM, Foulkes WD, Tischkowitz M. DICER1 mutations in familial multinodular goiter with and without ovarian Sertoli-Leydig cell tumors. J Am Med Assoc 305: 68–77, 2011.
30. Schaible B, Schaffer K, Taylor CT. Hypoxia, innate immunity and infection in the lung. Respir Physiol Neurobiol 174: 235–243, 2010.
31. Schoof CR, Botelho EL, Izzotti A, Vasques Ldos R. MicroRNAs in cancer treatment and prognosis. Am J Cancer Res 2: 414–433, 2012.
32. Schumacker PT. Lung cell hypoxia: role of mitochondrial reactive oxygen species signaling in triggering responses. Proc Am Thoracic Soc 8: 477–484, 2011.
33. Semenza GL. Life with oxygen. Science 318: 62–64, 2007.
34. Shen J, Xia W, Khotskaya YB, Huo L, Nakanishi K, Lim SO, Du Y, Wang Y, Chang WC, Chen CH, Hsu JL, Wu Y, Lam YC, James BP, Liu X, Liu CG, Patel DJ, Hung MC. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 497: 383–387, 2013.
35. Vergadi E, Chang MS, Lee C, Liang OD, Liu X, Fernandez-Gonzalez A, Mitsialis SA, Kourembanas S. Early macrophage recruitment and alternative activation are critical for the later development of hypoxia-induced pulmonary hypertension. Circulation 123: 1986–1995, 2011.
36. Voelkel NF, Mizuno S, Bogaard HJ. The role of hypoxia in pulmonary vascular diseases: a perspective. Am J Physiol Lung Cell Mol Physiol 304: L457–L465, 2013.
37. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103: 2257–2261, 2006.
38. Wolf A, Agnihotri S, Micallef J, Mukherjee J, Sabha N, Cairns R, Hawkins C, Guha A. Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme. J Exp Med 208: 313–326, 2011.
39. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, Calin GA, Liu CG, Croce CM, Harris CC. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9: 189–198, 2006.
40. Yoshino H, Enokida H, Itesako T, Kojima S, Kinoshita T, Tatarano S, Chiyomaru T, Nakagawa M, Seki N. Tumor-suppressive microRNA-143/145 cluster targets hexokinase-2 in renal cell carcinoma. Cancer Sci 104: 1567–1574, 2013.
41. Yu SL, Chen HY, Yang PC, Chen JJ. Unique MicroRNA signature and clinical outcome of cancers. DNA Cell Biol 26: 283–292, 2007.
42. Zampetaki A, Mitsialis SA, Pfeilschifter J, Kourembanas S. Hypoxia induces macrophage inflammatory protein-2 (MIP-2) gene expression in murine macrophages via NF-kappaB: the prominent role of p42/p44 and PI3 kinase pathways. FASEB J 18: 1090–1092, 2004.