Coxsackievirus-Induced miR-21 Disrupts Cardiomyocyte Interactions via the Downregulation of Intercalated Disk Components

PLoS Pathogens

Volumn 10, Issue 4, 2014, Pages

  Ye, Xin ^a   Zhang, Huifang Mary ^a   Qiu, Ye ^a   Hanson, Paul J ^a   Hemida, Maged Gomaa ^a   Wei, Wei ^b   Hoodless, Pamela A ^b   Chu, Fanny ^a   Yang, Decheng ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; ENHANCED GREEN FLUORESCENT PROTEIN; FLOTILLIN 1; FLUORESCENT TIMER PROTEIN; MOLECULAR MARKER; PROTEIN VP1; RIBAVIRIN; UNCLASSIFIED DRUG; DESMIN; MICRORNA; MIRN21 MICRORNA, MOUSE;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; COXSACKIE VIRUS B; CROSS LINKING; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; LIGHT CHAIN; NONHUMAN; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; VIRUS RELEASE; VIRUS REPLICATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL COMMUNICATION; ENTEROVIRUS; ENTEROVIRUS INFECTION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HEART MUSCLE CELL; MALE; METABOLISM; MOUSE; PATHOLOGY; PROTEIN DEGRADATION; UBIQUITINATION; VIROLOGY;

ANIMALS; CELL COMMUNICATION; DESMIN; ENTEROVIRUS B, HUMAN; ENTEROVIRUS INFECTIONS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; MALE; MICE; MICRORNAS; MYOCYTES, CARDIAC; PROTEOLYSIS; UBIQUITINATION;

EID: 84901359419     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004070     Document Type: Article

References (62)

1. He L, Hannon GJ, (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531.
2. Pasquinelli AE, (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13: 271-282.
3. Small EM, Frost RJ, Olson EN, (2010) MicroRNAs add a new dimension to cardiovascular disease. Circulation 121: 1022-1032.
4. Skalsky RL, Cullen BR, (2010) Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64: 123-141.
5. Kumarswamy R, Volkmann I, Thum T, (2011) Regulation and function of miRNA-21 in health and disease. RNA Biol 8: 706-713.
6. Cheng Y, Zhang C, (2010) MicroRNA-21 in cardiovascular disease. J Cardiovasc Transl Res 3: 251-255.
7. Sayed D, Rane S, Lypowy J, He M, Chen IY, et al. (2008) MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol Biol Cell 19: 3272-3282.
8. Bauersachs J, (2012) miR-21: a central regulator of fibrosis not only in the broken heart. Cardiovasc Res 96: 227-229 discussion 230-223.
9. Dong S, Cheng Y, Yang J, Li J, Liu 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: 29514-29525.
10. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, et al. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456: 980-984.
11. Tatsuguchi M, Seok HY, Callis TE, Thomson JM, Chen JF, et al. (2007) Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy. J Mol Cell Cardiol 42: 1137-1141.
12. Cheng Y, Liu X, Zhang S, Lin Y, Yang J, et al. (2009) MicroRNA-21 protects against the H(2)O(2)-induced injury on cardiac myocytes via its target gene PDCD4. J Mol Cell Cardiol 47: 5-14.
13. Patrick DM, Montgomery RL, Qi X, Obad S, Kauppinen S, et al. (2010) Stress-dependent cardiac remodeling occurs in the absence of microRNA-21 in mice. J Clin Invest 120: 3912-3916.
14. Rosato P, Anastasiadou E, Garg N, Lenze D, Boccellato F, et al. (2012) Differential regulation of miR-21 and miR-146a by Epstein-Barr virus-encoded EBNA2. Leukemia 26: 2343-2352.
15. Chen Y, Chen J, Wang H, Shi J, Wu K, et al. (2013) HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog 9: e1003248.
16. Huber SA, Gauntt CJ, Sakkinen P, (1998) Enteroviruses and myocarditis: viral pathogenesis through replication, cytokine induction, and immunopathogenicity. Adv Virus Res 51: 35-80.
17. Eckart RE, Scoville SL, Campbell CL, Shry EA, Stajduhar KC, et al. (2004) Sudden death in young adults: a 25-year review of autopsies in military recruits. Ann Intern Med 141: 829-834.
18. Ho BC, Yu SL, Chen JJ, Chang SY, Yan BS, et al. (2011) Enterovirus-induced miR-141 contributes to shutoff of host protein translation by targeting the translation initiation factor eIF4E. Cell Host Microbe 9: 58-69.
19. Corsten MF, Papageorgiou A, Verhesen W, Carai P, Lindow M, et al. (2012) MicroRNA profiling identifies microRNA-155 as an adverse mediator of cardiac injury and dysfunction during acute viral myocarditis. Circ Res 111: 415-425.
20. Hemida MG, Ye X, Zhang HM, Hanson PJ, Liu Z, et al. (2013) MicroRNA-203 enhances coxsackievirus B3 replication through targeting zinc finger protein-148. Cell Mol Life Sci 70: 277-291.
21. Xu HF, Ding YJ, Shen YW, Xue AM, Xu HM, et al. (2012) MicroRNA- 1 represses Cx43 expression in viral myocarditis. Mol Cell Biochem 362: 141-148.
22. Liu YL, Wu W, Xue Y, Gao M, Yan Y, et al. (2013) MicroRNA-21 and-146b are involved in the pathogenesis of murine viral myocarditis by regulating TH-17 differentiation. Arch Virol 7: 593-608.
23. Sheikh F, Ross RS, Chen J, (2009) Cell-cell connection to cardiac disease. Trends Cardiovasc Med 19: 182-190.
24. Garrod DR, Berika MY, Bardsley WF, Holmes D, Tabernero L, (2005) Hyper-adhesion in desmosomes: its regulation in wound healing and possible relationship to cadherin crystal structure. J Cell Sci 118: 5743-5754.
25. Jamora C, Fuchs E, (2002) Intercellular adhesion, signalling and the cytoskeleton. Nat Cell Biol 4: E101-108.
26. Noorman M, van der Heyden MA, van Veen TA, Cox MG, Hauer RN, et al. (2009) Cardiac cell-cell junctions in health and disease: Electrical versus mechanical coupling. J Mol Cell Cardiol 47: 23-31.
27. Dennert R, Crijns HJ, Heymans S, (2008) Acute viral myocarditis. Eur Heart J 29: 2073-2082.
28. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
29. Dweep H, Sticht C, Pandey P, Gretz N, (2011) miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. J Biomed Inform 44: 839-847.
30. Baron CP, Jacobsen S, Purslow PP, (2004) Cleavage of desmin by cysteine proteases: Calpains and cathepsin B. Meat Sci 68: 447-456.
31. Chen F, Chang R, Trivedi M, Capetanaki Y, Cryns VL, (2003) Caspase proteolysis of desmin produces a dominant-negative inhibitor of intermediate filaments and promotes apoptosis. J Biol Chem 278: 6848-6853.
32. Cohen S, Zhai B, Gygi SP, Goldberg AL, (2012) Ubiquitylation by Trim32 causes coupled loss of desmin, Z-bands, and thin filaments in muscle atrophy. J Cell Biol 198: 575-589.
33. Ernst R, Mueller B, Ploegh HL, Schlieker C, (2009) The otubain YOD1 is a deubiquitinating enzyme that associates with p97 to facilitate protein dislocation from the ER. Mol Cell 36: 28-38.
34. Newton K, Matsumoto ML, Wertz IE, Kirkpatrick DS, Lill JR, et al. (2008) Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134: 668-678.
35. Wagner SA, Beli P, Weinert BT, Scholz C, Kelstrup CD, et al. (2012) Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol Cell Proteomics 11: 1578-1585.
36. Xu G, Paige JS, Jaffrey SR, (2010) Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat Biotechnol 28: 868-873.
37. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, et al. (2011) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 44: 325-340.
38. Fujita S, Ito T, Mizutani T, Minoguchi S, Yamamichi N, et al. (2008) miR-21 Gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J Mol Biol 378: 492-504.
39. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K, (2010) STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 39: 493-506.
40. Perdiguero E, Sousa-Victor P, Ruiz-Bonilla V, Jardi M, Caelles C, et al. (2011) p38/MKP-1-regulated AKT coordinates macrophage transitions and resolution of inflammation during tissue repair. J Cell Biol 195: 307-322.
41. Yasukawa H, Yajima T, Duplain H, Iwatate M, Kido M, et al. (2003) The suppressor of cytokine signaling-1 (SOCS1) is a novel therapeutic target for enterovirus-induced cardiac injury. J Clin Invest 111: 469-478.
42. Jensen KJ, Garmaroudi FS, Zhang J, Lin J, Boroomand S, et al. (2013) An ERK-p38 subnetwork coordinates host cell apoptosis and necrosis during coxsackievirus B3 infection. Cell Host Microbe 13: 67-76.
43. Banerjee I, Fuseler JW, Price RL, Borg TK, Baudino TA, (2007) Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 293: H1883-1891.
44. Shi Y, Chen C, Lisewski U, Wrackmeyer U, Radke M, et al. (2009) Cardiac deletion of the Coxsackievirus-adenovirus receptor abolishes Coxsackievirus B3 infection and prevents myocarditis in vivo. J Am Coll Cardiol 53: 1219-1226.
45. Roy S, Khanna S, Hussain SR, Biswas S, Azad A, et al. (2009) MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res 82: 21-29.
46. Abston ED, Coronado MJ, Bucek A, Onyimba JA, Brandt JE, et al. (2013) TLR3 deficiency induces chronic inflammatory cardiomyopathy in resistant mice following coxsackievirus B3 infection: role for IL-4. Am J Physiol Regul Integr Comp Physiol 304: R267-277.
47. Gui J, Yue Y, Chen R, Xu W, Xiong S, (2012) A20 (TNFAIP3) alleviates CVB3-induced myocarditis via inhibiting NF-kappaB signaling. PLoS One 7: e46515.
48. Smigielska-Czepiel K, van den Berg A, Jellema P, Slezak-Prochazka I, Maat H, et al. (2013) Dual role of miR-21 in CD4+ T-cells: activation-induced miR-21 supports survival of memory T-cells and regulates CCR7 expression in naive T-cells. PLoS One 8: e76217.
49. Ju Y, Wang T, Li Y, Xin W, Wang S, et al. (2007) Coxsackievirus B3 affects endothelial tight junctions: possible relationship to ZO-1 and F-actin, as well as p38 MAPK activity. Cell Biol Int 31: 1207-1213.
50. Kartenbeck J, Franke WW, Moser JG, Stoffels U, (1983) Specific attachment of desmin filaments to desmosomal plaques in cardiac myocytes. EMBO J 2: 735-742.
51. McLendon PM, Robbins J, (2011) Desmin-related cardiomyopathy: an unfolding story. Am J Physiol Heart Circ Physiol 301: H1220-1228.
52. Balogh J, Merisckay M, Li Z, Paulin D, Arner A, (2002) Hearts from mice lacking desmin have a myopathy with impaired active force generation and unaltered wall compliance. Cardiovasc Res 53: 439-450.
53. Li Z, Colucci-Guyon E, Pincon-Raymond M, Mericskay M, Pournin S, et al. (1996) Cardiovascular lesions and skeletal myopathy in mice lacking desmin. Dev Biol 175: 362-366.
54. Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y, (1996) Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 134: 1255-1270.
55. Goncharov T, Niessen K, de Almagro MC, Izrael-Tomasevic A, Fedorova AV, et al. (2013) OTUB1 modulates c-IAP1 stability to regulate signalling pathways. EMBO J 32: 1103-1114.
56. Sun XX, Challagundla KB, Dai MS, (2012) Positive regulation of p53 stability and activity by the deubiquitinating enzyme Otubain 1. EMBO J 31: 576-592.
57. Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, et al. (2009) Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137: 133-145.
58. Pickart CM, Fushman D, (2004) Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 8: 610-616.
59. Marchant D, Si X, Luo H, McManus B, Yang D, (2008) The impact of CVB3 infection on host cell biology. Curr Top Microbiol Immunol 323: 177-198.
60. Zemljic-Harpf AE, Miller JC, Henderson SA, Wright AT, Manso AM, et al. (2007) Cardiac-myocyte-specific excision of the vinculin gene disrupts cellular junctions, causing sudden death or dilated cardiomyopathy. Mol Cell Biol 27: 7522-7537.
61. Ralfkiaer U, Hagedorn PH, Bangsgaard N, Lovendorf MB, Ahler CB, et al. (2011) Diagnostic microRNA profiling in cutaneous T-cell lymphoma (CTCL). Blood 118: 5891-5900.
62. Marchant D, Dou Y, Luo H, Garmaroudi FS, McDonough JE, et al. (2009) Bosentan enhances viral load via endothelin-1 receptor type-A-mediated p38 mitogen-activated protein kinase activation while improving cardiac function during coxsackievirus-induced myocarditis. Circ Res 104: 813-821.