Skip to main content
Erschienen in: Pediatric Cardiology 3/2011

01.03.2011 | Riley Symposium

Cardioprotective MicroRNAs

verfasst von: Maha Abdellatif

Erschienen in: Pediatric Cardiology | Ausgabe 3/2011

Einloggen, um Zugang zu erhalten

Abstract

MicroRNAs (miRNAs) are involved in almost every aspect of a mammalian cell’s functionality, from stem cell differentiation to aging and pathogenesis; however, their role in immediate cell signaling is less defined. This has been recently demonstrated by the rapid increase or decrease of miR-21’s abundance within minutes of activation or inhibition of the v-akt murine thymoma viral oncogene homolog 1 (AKT) pathway, respectively, which mediates its regulation of Fas ligand and phosphatase and tensin homologue deleted on chromosome 10 expression, among other targets. Conversely, AKT induces rapid downregulation of miR-199a-5p to effect upregulation of hypoxia-inducible factor 1α and sirtuin 1. This suggests that posttranscriptional mechanisms regulate miRNAs’ processing and/or stability to induce the rapid fluctuation in their levels. In support, a growing number of studies are showing specific posttranscriptional regulation of miRNAs. The data potentially explain how AKT, and plausibly other signaling pathways, can specifically and promptly modulate a gene’s translation while circumventing the need for transcription during transient signaling events.
Literatur
1.
Zurück zum Zitat Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S et al (2007) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128–2136PubMedCrossRef Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S et al (2007) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128–2136PubMedCrossRef
2.
Zurück zum Zitat Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF et al (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68:7846–7854PubMedCrossRef Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF et al (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68:7846–7854PubMedCrossRef
3.
Zurück zum Zitat Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294:1337–1340PubMedCrossRef Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294:1337–1340PubMedCrossRef
4.
Zurück zum Zitat Cheng Y, Zhu P, Yang J, Liu X, Dong S, Wang X et al (2010) Ischaemic preconditioning-regulated miR-21 protects heart against ischaemia/reperfusion injury via anti-apoptosis through its target PDCD4. Cardiovasc Res 87:431–439PubMedCrossRef Cheng Y, Zhu P, Yang J, Liu X, Dong S, Wang X et al (2010) Ischaemic preconditioning-regulated miR-21 protects heart against ischaemia/reperfusion injury via anti-apoptosis through its target PDCD4. Cardiovasc Res 87:431–439PubMedCrossRef
5.
Zurück zum Zitat Ciechomska I, Pyrzynska B, Kazmierczak P, Kaminska B (2003) Inhibition of Akt kinase signalling and activation of Forkhead are indispensable for upregulation of FasL expression in apoptosis of glioma cells. Oncogene 22:7617–7627PubMedCrossRef Ciechomska I, Pyrzynska B, Kazmierczak P, Kaminska B (2003) Inhibition of Akt kinase signalling and activation of Forkhead are indispensable for upregulation of FasL expression in apoptosis of glioma cells. Oncogene 22:7617–7627PubMedCrossRef
6.
Zurück zum Zitat Davis BN, Hilyard AC, Lagna G, Hata A (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454:56–61PubMedCrossRef Davis BN, Hilyard AC, Lagna G, Hata A (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454:56–61PubMedCrossRef
7.
Zurück zum Zitat Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X et al (2009) MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem 284:29514–29525PubMedCrossRef Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X et al (2009) MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem 284:29514–29525PubMedCrossRef
8.
Zurück zum Zitat Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH (2008) Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 283:1026–1033PubMedCrossRef Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH (2008) Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 283:1026–1033PubMedCrossRef
9.
Zurück zum Zitat Garofalo M, Di Leva G, Romano G, Nuovo G, Suh SS, Ngankeu A et al (2009) miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 16:498–509PubMedCrossRef Garofalo M, Di Leva G, Romano G, Nuovo G, Suh SS, Ngankeu A et al (2009) miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 16:498–509PubMedCrossRef
10.
Zurück zum Zitat Guo C, Sah JF, Beard L, Willson JK, Markowitz SD, Guda K (2008) The noncoding RNA, miR-126, suppresses the growth of neoplastic cells by targeting phosphatidylinositol 3-kinase signaling and is frequently lost in colon cancers. Genes Chromosom Cancer 47:939–946PubMedCrossRef Guo C, Sah JF, Beard L, Willson JK, Markowitz SD, Guda K (2008) The noncoding RNA, miR-126, suppresses the growth of neoplastic cells by targeting phosphatidylinositol 3-kinase signaling and is frequently lost in colon cancers. Genes Chromosom Cancer 47:939–946PubMedCrossRef
11.
Zurück zum Zitat Hlobilkova A, Knillova J, Bartek J, Lukas J, Kolar Z (2003) The mechanism of action of the tumour suppressor gene PTEN. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 147:19–25PubMed Hlobilkova A, Knillova J, Bartek J, Lukas J, Kolar Z (2003) The mechanism of action of the tumour suppressor gene PTEN. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 147:19–25PubMed
12.
Zurück zum Zitat Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H et al (2007) MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 100:1579–1588PubMedCrossRef Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H et al (2007) MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 100:1579–1588PubMedCrossRef
13.
Zurück zum Zitat Kato M, Putta S, Wang M, Yuan H, Lanting L, Nair I et al (2009) GF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 11:881–889PubMedCrossRef Kato M, Putta S, Wang M, Yuan H, Lanting L, Nair I et al (2009) GF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 11:881–889PubMedCrossRef
14.
Zurück zum Zitat Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S, Baba T (2009) Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev 23:433–438PubMedCrossRef Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S, Baba T (2009) Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev 23:433–438PubMedCrossRef
15.
Zurück zum Zitat Li Y, Song YH, Mohler J, Delafontaine P (2006) ANG II induces apoptosis of human vascular smooth muscle via extrinsic pathway involving inhibition of Akt phosphorylation and increased FasL expression. Am J Physiol Heart Circ Physiol 290:H2116–H2123PubMedCrossRef Li Y, Song YH, Mohler J, Delafontaine P (2006) ANG II induces apoptosis of human vascular smooth muscle via extrinsic pathway involving inhibition of Akt phosphorylation and increased FasL expression. Am J Physiol Heart Circ Physiol 290:H2116–H2123PubMedCrossRef
16.
Zurück zum Zitat Li Y, Li W, Yang Y, Lu Y, He C, Hu G et al (2009) MicroRNA-21 targets LRRFIP1 and contributes to VM-26 resistance in glioblastoma multiforme. Brain Res 25:13–18CrossRef Li Y, Li W, Yang Y, Lu Y, He C, Hu G et al (2009) MicroRNA-21 targets LRRFIP1 and contributes to VM-26 resistance in glioblastoma multiforme. Brain Res 25:13–18CrossRef
17.
Zurück zum Zitat Ling HY, Ou HS, Feng SD, Zhang XY, Tuo QH, Chen LX et al (2009) Changes in microRNA profile and effects of miR-320 in insulin-resistant 3T3-L1 adipocytes. Clin Exp Pharmacol Physiol 36:e32–e39CrossRef Ling HY, Ou HS, Feng SD, Zhang XY, Tuo QH, Chen LX et al (2009) Changes in microRNA profile and effects of miR-320 in insulin-resistant 3T3-L1 adipocytes. Clin Exp Pharmacol Physiol 36:e32–e39CrossRef
18.
Zurück zum Zitat Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME et al (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271–275PubMedCrossRef Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME et al (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271–275PubMedCrossRef
19.
Zurück zum Zitat Meng F, Henson R, Lang M, Wehbe H, Maheshwari S, Mendell JT et al (2006) Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology 130:2113–2129PubMedCrossRef Meng F, Henson R, Lang M, Wehbe H, Maheshwari S, Mendell JT et al (2006) Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology 130:2113–2129PubMedCrossRef
20.
Zurück zum Zitat Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133:647–658PubMedCrossRef Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133:647–658PubMedCrossRef
21.
Zurück zum Zitat Michlewski G, Guil S, Semple CA, Caceres JF (2008) Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell 32:383–393PubMedCrossRef Michlewski G, Guil S, Semple CA, Caceres JF (2008) Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell 32:383–393PubMedCrossRef
22.
Zurück zum Zitat Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136PubMed Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136PubMed
23.
Zurück zum Zitat O’Connell RM, Chaudhuri AA, Rao DS, Baltimore D (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 106:7113–7118PubMedCrossRef O’Connell RM, Chaudhuri AA, Rao DS, Baltimore D (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 106:7113–7118PubMedCrossRef
24.
Zurück zum Zitat Papa V, Tazzari PL, Chiarini F, Cappellini A, Ricci F, Billi AM et al (2008) Proapoptotic activity and chemosensitizing effect of the novel Akt inhibitor perifosine in acute myelogenous leukemia cells. Leukemia 22:147–160PubMedCrossRef Papa V, Tazzari PL, Chiarini F, Cappellini A, Ricci F, Billi AM et al (2008) Proapoptotic activity and chemosensitizing effect of the novel Akt inhibitor perifosine in acute myelogenous leukemia cells. Leukemia 22:147–160PubMedCrossRef
25.
Zurück zum Zitat Rane S, He M, Sayed D, Vashistha H, Malhotra A, Sadoshima J et al (2009) Downregulation of MiR-199a derepresses hypoxia-inducible factor-1{alpha} and sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res 104:879–886PubMedCrossRef Rane S, He M, Sayed D, Vashistha H, Malhotra A, Sadoshima J et al (2009) Downregulation of MiR-199a derepresses hypoxia-inducible factor-1{alpha} and sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res 104:879–886PubMedCrossRef
26.
Zurück zum Zitat Rane S, He M, Sayed D, Yan L, Vatner D, Abdellatif M (2010) An antagonism between the AKT and beta-adrenergic signaling pathways mediated through their reciprocal effects on miR-199a-5p. Cell Signal 22:1054–1062PubMedCrossRef Rane S, He M, Sayed D, Yan L, Vatner D, Abdellatif M (2010) An antagonism between the AKT and beta-adrenergic signaling pathways mediated through their reciprocal effects on miR-199a-5p. Cell Signal 22:1054–1062PubMedCrossRef
27.
Zurück zum Zitat Rowland RT, Meng X, Cleveland JC, Meldrum DR, Harken AH, Brown JM (1997) Cardioadaptation induced by cyclic ischemic preconditioning is mediated by translational regulation of de novo protein synthesis. J Surg Res 71:155–160PubMedCrossRef Rowland RT, Meng X, Cleveland JC, Meldrum DR, Harken AH, Brown JM (1997) Cardioadaptation induced by cyclic ischemic preconditioning is mediated by translational regulation of de novo protein synthesis. J Surg Res 71:155–160PubMedCrossRef
28.
Zurück zum Zitat Ruggiero T, Trabucchi M, De Santa F, Zupo S, Harfe BD, McManus MT et al (2009) LPS induces KH-type splicing regulatory protein-dependent processing of microRNA-155 precursors in macrophages. FASEB J 23:2898–2908PubMedCrossRef Ruggiero T, Trabucchi M, De Santa F, Zupo S, Harfe BD, McManus MT et al (2009) LPS induces KH-type splicing regulatory protein-dependent processing of microRNA-155 precursors in macrophages. FASEB J 23:2898–2908PubMedCrossRef
29.
Zurück zum Zitat Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R et al (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10:987–993PubMedCrossRef Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R et al (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10:987–993PubMedCrossRef
30.
Zurück zum Zitat Sayed D, He M, Hong C, Gao S, Rane S, Yang Z et al (2010) MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J Biol Chem 285:20281–20290PubMedCrossRef Sayed D, He M, Hong C, Gao S, Rane S, Yang Z et al (2010) MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J Biol Chem 285:20281–20290PubMedCrossRef
31.
Zurück zum Zitat Small EM, O’Rourke JR, Moresi V, Sutherland LB, McAnally J, Gerard RD et al (2010) Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc Natl Acad Sci USA 107:4218–4423PubMedCrossRef Small EM, O’Rourke JR, Moresi V, Sutherland LB, McAnally J, Gerard RD et al (2010) Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc Natl Acad Sci USA 107:4218–4423PubMedCrossRef
32.
Zurück zum Zitat Suhara T, Kim HS, Kirshenbaum LA, Walsh K (2002) Suppression of Akt signaling induces Fas ligand expression: involvement of caspase and Jun kinase activation in Akt-mediated Fas ligand regulation. Mol Cell Biol 22:680–691PubMedCrossRef Suhara T, Kim HS, Kirshenbaum LA, Walsh K (2002) Suppression of Akt signaling induces Fas ligand expression: involvement of caspase and Jun kinase activation in Akt-mediated Fas ligand regulation. Mol Cell Biol 22:680–691PubMedCrossRef
33.
Zurück zum Zitat Tong H, Chen W, Steenbergen C, Murphy E (2000) Ischemic preconditioning activates phosphatidylinositol-3-kinase upstream of protein kinase C. Circ Res 87:309–315PubMed Tong H, Chen W, Steenbergen C, Murphy E (2000) Ischemic preconditioning activates phosphatidylinositol-3-kinase upstream of protein kinase C. Circ Res 87:309–315PubMed
34.
Zurück zum Zitat Trabucchi M, Briata P, Garcia-Mayoral M, Haase AD, Filipowicz W, Ramos A et al (2009) The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 459:1010–1014PubMedCrossRef Trabucchi M, Briata P, Garcia-Mayoral M, Haase AD, Filipowicz W, Ramos A et al (2009) The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 459:1010–1014PubMedCrossRef
35.
Zurück zum Zitat Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T et al (2010) MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 70:2339–2349PubMedCrossRef Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T et al (2010) MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 70:2339–2349PubMedCrossRef
36.
Zurück zum Zitat Uriarte SM, Joshi-Barve S, Song Z, Sahoo R, Gobejishvili L, Jala VR et al (2005) Akt inhibition upregulates FasL, downregulates c-FLIPs and induces caspase-8-dependent cell death in Jurkat T lymphocytes. Cell Death Differ 12:233–242PubMedCrossRef Uriarte SM, Joshi-Barve S, Song Z, Sahoo R, Gobejishvili L, Jala VR et al (2005) Akt inhibition upregulates FasL, downregulates c-FLIPs and induces caspase-8-dependent cell death in Jurkat T lymphocytes. Cell Death Differ 12:233–242PubMedCrossRef
37.
Zurück zum Zitat Wang K, Li PF (2010) Foxo3a regulates apoptosis by negatively targeting miR-21. J Biol Chem 285:16958–16966PubMedCrossRef Wang K, Li PF (2010) Foxo3a regulates apoptosis by negatively targeting miR-21. J Biol Chem 285:16958–16966PubMedCrossRef
38.
Zurück zum Zitat Wang GL, Semenza GL (1993) General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90:4304–4308PubMedCrossRef Wang GL, Semenza GL (1993) General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90:4304–4308PubMedCrossRef
39.
Zurück zum Zitat Yamanaka Y, Tagawa H, Takahashi N, Watanabe A, Guo YM, Iwamoto K et al (2009) Aberrant overexpression of microRNAs activate AKT signaling via downregulation of tumor suppressors in NK-cell lymphoma/leukemia. Blood 114:3265–3275PubMedCrossRef Yamanaka Y, Tagawa H, Takahashi N, Watanabe A, Guo YM, Iwamoto K et al (2009) Aberrant overexpression of microRNAs activate AKT signaling via downregulation of tumor suppressors in NK-cell lymphoma/leukemia. Blood 114:3265–3275PubMedCrossRef
40.
Zurück zum Zitat Yin C, Salloum FN, Kukreja RC (2009) A novel role of microRNA in late preconditioning. Upregulation of endothelial nitric oxide synthase and heat shock protein 70. Circ Res 104:572–575PubMedCrossRef Yin C, Salloum FN, Kukreja RC (2009) A novel role of microRNA in late preconditioning. Upregulation of endothelial nitric oxide synthase and heat shock protein 70. Circ Res 104:572–575PubMedCrossRef
41.
Zurück zum Zitat Yu J, Ryan DG, Getsios S, Oliveira-Fernandes M, Fatima A, Lavker RM (2008) MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proc Natl Acad Sci USA 105:19300–19305PubMedCrossRef Yu J, Ryan DG, Getsios S, Oliveira-Fernandes M, Fatima A, Lavker RM (2008) MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proc Natl Acad Sci USA 105:19300–19305PubMedCrossRef
42.
Zurück zum Zitat Zhu S, Si ML, Wu H, Mo YY (2007) MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem 282:14328–14336PubMedCrossRef Zhu S, Si ML, Wu H, Mo YY (2007) MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem 282:14328–14336PubMedCrossRef
Metadaten
Titel
Cardioprotective MicroRNAs
verfasst von
Maha Abdellatif
Publikationsdatum
01.03.2011
Verlag
Springer-Verlag
Erschienen in
Pediatric Cardiology / Ausgabe 3/2011
Print ISSN: 0172-0643
Elektronische ISSN: 1432-1971
DOI
https://doi.org/10.1007/s00246-010-9882-7

Weitere Artikel der Ausgabe 3/2011

Pediatric Cardiology 3/2011 Zur Ausgabe

Update Kardiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.