The role of autophagy during coxsackievirus infection of neural progenitor and stem cells

Autophagy

Volumn 8, Issue 6, 2012, Pages 938-953

  Tabor Godwin, Jenna M ^a   Tsueng, Ginger ^a   Sayen, M Richard ^b   Gottlieb, Roberta A ^b   Feuer, Ralph ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Autophagy; Central nervous system; Coxsackievirus; Encephalitis; Enterovirus; Meningitis; Neural stem cells; Neurotropic virus

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; CELL LINE; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; HEART MUSCLE CELL; INFECTION SENSITIVITY; MOUSE; NEURAL PROGENITOR AND STEM CELL; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EID: 84864871729     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.19781     Document Type: Article

References (68)

1. Gustafsson AB, Gottlieb RA. Recycle or die: the role of autophagy in cardioprotection. J Mol Cell Cardiol 2008; 44:654-61; PMID:18353358; http://dx.doi.org/10.1016/j.yjmcc.2008.01.010
2. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003
3. Kudchodkar SB, Levine B. Viruses and autophagy. Rev Med Virol 2009; 19:359-78; PMID:19750559; http://dx.doi.org/10.1002/rmv.630
4. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; http://dx.doi.org/10.1038/nature09782
5. Deretic V. Multiple regulatory and effector roles of autophagy in immunity. Curr Opin Immunol 2009; 21:53-62; PMID:19269148; http://dx.doi.org/10. 1016/j.coi.2009.02.002
6. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66; PMID:15607973; http://dx.doi.org/10.1016/j.cell.2004.11.038
7. Lee YR, Lei HY, Liu MT, Wang JR, Chen SH, Jiang-Shieh YF, et al. Autophagic machinery activated by dengue virus enhances virus replication. Virology 2008; 374:240-8; PMID:18353420; http://dx.doi.org/10.1016/j.virol.2008. 02.016
8. Alexander DE, Leib DA. Xenophagy in herpes simplex virus replication and pathogenesis. Autophagy 2008; 4:101-3; PMID:18000391
9. Orvedahl A, Levine B. Autophagy and viral neurovirulence. Cell Microbiol 2008; 10:1747-56; PMID:18503639; http://dx.doi.org/10.1111/j.1462-5822. 2008.01175.x
10. Dreux M, Gastaminza P, Wieland SF, Chisari FV. The autophagy machinery is required to initiate hepatitis C virus replication. Proc Natl Acad Sci U S A 2009; 106:14046-51; PMID:19666601; http://dx.doi.org/10.1073/pnas.0907344106
11. Dreux M, Chisari FV. Autophagy proteins promote hepatitis C virus replication. Autophagy 2009; 5:1224-5; PMID:19844160; http://dx.doi.org/10.4161/ auto.5.8.10219
12. Lin LT, Dawson PW, Richardson CD. Viral interactions with macroautophagy: a double-edged sword. Virology 2010; 402:1-10; PMID:20413139; http://dx.doi.org/10.1016/j.virol.2010.03.026
13. Berger JR, Chumley W, Pittman T, Given C, Nuovo G. Persistent Coxsackie B encephalitis: Report of a case and review of the literature. J Neurovirol 2006; 12:511-6; PMID:17162666; http://dx.doi.org/10.1080/13550280601090546
14. Whitton JL, Cornell CT, Feuer R. Host and virus determinants of picornavirus pathogenesis and tropism. Nat Rev Microbiol 2005; 3:765-76; PMID:16205710; http://dx.doi.org/10.1038/nrmicro1284
15. Romero JR. Pediatric group B coxsackievirus infections. Curr Top Microbiol Immunol 2008; 323:223-39; PMID:18357772; http://dx.doi.org/10.1007/ 978-3-540-75546-3-10
16. Wikswo ME, Khetsuriani N, Fowlkes AL, Zheng X, Peñaranda S, Verma N, et al. Increased activity of Coxsackievirus B1 strains associated with severe disease among young infants in the United States, 2007-2008. Clin Infect Dis 2009; 49:e44-51; PMID:19622041; http://dx.doi.org/10.1086/605090
17. Chamberlain RN, Christie PN, Holt KS, Huntley RM, Pollard R, Roche MC. A study of school children who had identified virus infections of the central nervous system during infancy. Child Care Health Dev 1983; 9:29-47; PMID:6303619; http://dx.doi.org/10.1111/j.1365-2214.1983.tb00301.x
18. Kühl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, et al. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with "idiopathic" left ventricular dysfunction. Circulation 2005; 111:887-93; PMID:15699250; http://dx.doi.org/10.1161/01.CIR. 0000155616.07901.35
19. Romero JR. Pediatric group B coxsackievirus infections. Curr Top Microbiol Immunol 2008; 323:223-39; PMID:18357772; http://dx.doi.org/10.1007/ 978-3-540-75546-3-10
20. Wikswo ME, Khetsuriani N, Fowlkes AL, Zheng X, Peñaranda S, Verma N, et al. Increased activity of Coxsackievirus B1 strains associated with severe disease among young infants in the United States, 2007-2008. Clin Infect Dis 2009; 49:e44-51; PMID:19622041; http://dx.doi.org/10.1086/605090
21. Chamberlain RN, Christie PN, Holt KS, Huntley RM, Pollard R, Roche MC. A study of school children who had identified virus infections of the central nervous system during infancy. Child Care Health Dev 1983; 9:29-47; PMID:6303619; http://dx.doi.org/10.1111/j.1365-2214.1983.tb00301.x
22. Kühl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, et al. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with "idiopathic" left ventricular dysfunction. Circulation 2005; 111:887-93; PMID:15699250; http://dx.doi.org/10.1161/01.CIR. 0000155616.07901.35
23. Feuer R, Mena I, Pagarigan RR, Harkins S, Hassett DE, Whitton JL. Coxsackievirus B3 and the neonatal CNS: the roles of stem cells, developing neurons, and apoptosis in infection, viral dissemination, and disease. Am J Pathol 2003; 163:1379-93; PMID:14507646; http://dx.doi.org/10.1016/S0002- 9440(10)63496-7
24. Feuer R, Pagarigan RR, Harkins S, Liu F, Hunziker IP, Whitton JL. Coxsackievirus targets proliferating neuronal progenitor cells in the neonatal CNS. J Neurosci 2005; 25:2434-44; PMID:15745971; http://dx.doi.org/10.1523/ JNEUROSCI.4517-04.2005
25. Tabor-Godwin JM, Ruller CM, Bagalso N, An N, Pagarigan RR, Harkins S, et al. A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS. J Neurosci 2010; 30:8676-91; PMID:20573913; http://dx.doi.org/10.1523/JNEUROSCI.1860-10.2010
26. Rhoades RE, Tabor-Godwin JM, Tsueng G, Feuer R. Enterovirus infections of the central nervous system. Virology 2011; 411:288-305; PMID:21251690; http://dx.doi.org/10.1016/j.virol.2010.12.014
27. Suhy DA, Giddings TH, Jr., Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 2000; 74:8953-65; PMID:10982339; http://dx.doi.org/10.1128/JVI.74. 19.8953-8965.2000
28. Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, et al. Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 2008; 82:9143-53; PMID:18596087; http://dx.doi.org/10.1128/JVI.00641-08
29. Huang SC, Chang CL, Wang PS, Tsai Y, Liu HS. Enterovirus 71-induced autophagy detected in vitro and in vivo promotes viral replication. J Med Virol 2009; 81:1241-52; PMID:19475621; http://dx.doi.org/10.1002/jmv.21502
30. JacksonWT, Giddings TH, Jr., Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 2005; 3:e156; PMID:15884975; http://dx.doi.org/10.1371/ journal.pbio.0030156
31. Taylor MP, Kirkegaard K. Modification of cellular autophagy protein LC3 by poliovirus. J Virol 2007; 81:12543-53; PMID:17804493; http://dx.doi.org/10. 1128/JVI.00755-07
32. Taylor MP, Kirkegaard K. Potential subversion of autophagosomal pathway by picornaviruses. Autophagy 2008; 4:286-9; PMID:18094610
33. Kemball CC, Alirezaei M, Flynn CT, Wood MR, Harkins S, Kiosses WB, et al. Coxsackievirus infection induces autophagy-like vesicles and megaphagosomes in pancreatic acinar cells in vivo. J Virol 2010; 84:12110-24; PMID:20861268; http://dx.doi.org/10.1128/JVI.01417-10
34. Dreux M, Gastaminza P, Wieland SF, Chisari FV. The autophagy machinery is required to initiate hepatitis C virus replication. Proc Natl Acad Sci U S A 2009; 106:14046-51; PMID:19666601; http://dx.doi.org/10.1073/pnas.0907344106
35. Yoon SY, Ha YE, Choi JE, Ahn J, Lee H, Kim DH. Autophagy in coxsackievirus-infected neurons. Autophagy 2009; 5:388-9; PMID:19158511; http://dx.doi.org/10.4161/auto.5.3.7723
36. Yoon SY, Ha YE, Choi JE, Ahn J, Lee H, Kweon HS, et al. Coxsackievirus B4 uses autophagy for replication after calpain activation in rat primary neurons. J Virol 2008; 82:11976-8; PMID:18799585; http://dx.doi.org/10.1128/JVI.01028-08
37. Tsueng G, Tabor-Godwin JM, Gopal A, Ruller CM, Deline S, An N, et al. Coxsackievirus preferentially replicates and induces cytopathic effects in undifferentiated neural progenitor cells. J Virol 2011; 85:5718-32; PMID:21471247; http://dx.doi.org/10.1128/JVI.02261-10
38. Eriksson C, Björklund A, Wictorin K. Neuronal differentiation following transplantation of expanded mouse neurosphere cultures derived from different embryonic forebrain regions. Exp Neurol 2003; 184:615-35; PMID:14769354; http://dx.doi.org/10.1016/S0014-4886(03)00271-1
39. Feuer R, Mena I, Pagarigan R, Slifka MK, Whitton JL. Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol 2002; 76:4430-40; PMID:11932410; http://dx.doi.org/10.1128/JVI.76.9.4430- 4440.2002
40. Claycomb WC, Lanson NA, Jr., Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, et al. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci U S A 1998; 95:2979-84; PMID:9501201; http://dx.doi.org/10.1073/pnas.95.6. 2979
41. Yuan J, Cheung PK, Zhang H, Chau D, Yanagawa B, Cheung C, et al. A phosphorothioate antisense oligodeoxynucleotide specifically inhibits coxsackievirus B3 replication in cardiomyocytes and mouse hearts. Lab Invest 2004; 84:703-14; PMID:15094712; http://dx.doi.org/10.1038/labinvest.3700083
42. Yitzhaki S, Huang C, Liu W, Lee Y, Gustafsson AB, Mentzer RM, Jr., et al. Autophagy is required for preconditioning by the adenosine A1 receptor-selective agonist CCPA. Basic Res Cardiol 2009; 104:157-67; PMID:19242639; http://dx.doi.org/10.1007/s00395-009-0006-6
43. Seglen PO, Gordon PB. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 1982; 79:1889-92; PMID:6952238; http://dx.doi.org/10.1073/pnas. 79.6.1889
44. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36:585-95; PMID:15146184; http://dx.doi.org/10.1038/ng1362
45. Carreira RS, Lee Y, Ghochani M, Gustafsson AB, Gottlieb RA. Cyclophilin D is required for mitochondrial removal by autophagy in cardiac cells. Autophagy 2010; 6:6; PMID:20364102; http://dx.doi.org/10.4161/auto.6.4.11553
46. Esfandiarei M, Luo H, Yanagawa B, Suarez A, Dabiri D, Zhang J, et al. Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J Virol 2004; 78:4289-98; PMID:15047842; http://dx.doi.org/10.1128/JVI.78.8.4289-4298.2004
47. Stafford MR, Bartlett PF, Adams DJ. Purinergic receptor activation inhibits mitogen-stimulated proliferation in primary neurospheres from the adult mouse subventricular zone. Mol Cell Neurosci 2007; 35:535-48; PMID:17553694; http://dx.doi.org/10.1016/j.mcn.2007.04.013
48. Yu SW, Baek SH, Brennan RT, Bradley CJ, Park SK, Lee YS, et al. Autophagic death of adult hippocampal neural stem cells following insulin withdrawal. Stem Cells 2008; 26:2602-10; PMID:18653772; http://dx.doi.org/10. 1634/stemcells.2008-0153
49. Cárdenas-Aguayo MdelC, Santa-Olalla J, Baizabal JM, Salgado LM, Covarrubias L. Growth factor deprivation induces an alternative non-apoptotic death mechanism that is inhibited by Bcl2 in cells derived from neural precursor cells. J Hematother Stem Cell Res 2003; 12:735-48; PMID:14977482; http://dx.doi.org/10.1089/15258160360732759
50. Nichols LA, Adang LA, Kedes DH. Rapamycin blocks production of KSHV/HHV8: insights into the antitumor activity of an immunosuppressant drug. PLoS One 2011; 6:e14535; PMID:21264294; http://dx.doi.org/10.1371/journal.pone.0014535
51. Sanz JM, Vendite D, Fernández M, Andrés A, Ros M. Adenosine A1 receptors in cultured cerebellar granule cells: role of endogenous adenosine. J Neurochem 1996; 67:1469-77; PMID:8858929; http://dx.doi.org/10. 1046/j.1471-4159.1996.67041469.x
52. D'Alimonte I, Ballerini P, Nargi E, Buccella S, Giuliani P, Di Iorio P, et al. Staurosporine-induced apoptosis in astrocytes is prevented by A1 adenosine receptor activation. Neurosci Lett 2007; 418:66-71; PMID:17400382; http://dx.doi.org/10.1016/j.neulet.2007.02.061
53. Othman T, Yan H, Rivkees SA. Oligodendrocytes express functional A1 adenosine receptors that stimulate cellular migration. Glia 2003; 44:166-72; PMID:14515332; http://dx.doi.org/10.1002/glia.10281
54. Désiré L, Courtois Y, Jeanny JC. Endogenous and exogenous fibroblast growth factor 2 support survival of chick retinal neurons by control of neuronal neuronal bcl-x(L) and bcl-2 expression through a fibroblast berowth factor receptor 1- and ERK-dependent pathway. J Neurochem 2000; 75:151-63; PMID:10854258; http://dx.doi.org/10.1046/j.1471-4159. 2000.0750151.x
55. Euscher E, Davis J, Holzman I, Nuovo GJ. Coxsackie virus infection of the placenta associated with neurodevelopmental delays in the newborn. Obstet Gynecol 2001; 98:1019-26; PMID:11755547; http://dx.doi.org/10.1016/S0029- 7844(01)01625-8
56. Sawyer MH. Enterovirus infections: diagnosis and treatment. Semin Pediatr Infect Dis 2002; 13:40-7; PMID:12118843; http://dx.doi.org/10.1053/spid.2002. 29756
57. Rantakallio P, Jones P, Moring J, Von Wendt L. Association between central nervous system infections during childhood and adult onset schizophrenia and other psychoses: a 28-year follow-up. Int J Epidemiol 1997; 26:837-43; PMID:9279617; http://dx.doi.org/10.1093/ije/26.4.837
58. Verboon-Maciolek MA, Utrecht FG, Cowan F, Govaert P, van Loon AM, de Vries LS. White matter damage in neonatal enterovirus meningoencephalitis. Neurology 2008; 71:536; PMID:18695167; http://dx.doi.org/10.1212/01.wnl. 0000324706.94229.88
59. Daley AJ, Isaacs D, Dwyer DE, Gilbert GL. A cluster of cases of neonatal coxsackievirus B meningitis and myocarditis. J Paediatr Child Health 1998; 34:196-8; PMID:9588649; http://dx.doi.org/10.1046/j.1440-1754.1998.00176.x
60. Knowlton KU. CVB infection and mechanisms of viral cardiomyopathy. Curr Top Microbiol Immunol 2008; 323:315-35; PMID:18357777; http://dx.doi.org/10. 1007/978-3-540-75546-3-15
61. Adachi T, Takanaga H, Sakurai Y, Ishido M, Kunimoto M, Asou H. Influence of cell density and thyroid hormone on glial cell development in primary cultures of embryonic rat cerebral hemisphere. J Neurosci Res 2002; 69:61-71; PMID:12111816; http://dx.doi.org/10.1002/jnr.10279
62. Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nat Cell Biol 2010; 12:823-30; PMID:20811354; http://dx.doi.org/10.1038/ncb0910-823
63. Brady NR, Hamacher-Brady A, Yuan H, Gottlieb RA. The autophagic response to nutrient deprivation in the hl-1 cardiac myocyte is modulated by Bcl-2 and sarco/endoplasmic reticulum calcium stores. FEBS J 2007; 274:3184-97; PMID:17540004; http://dx.doi.org/10.1111/j.1742-4658.2007.05849.x
64. Colston JT, Chandrasekar B, Freeman GL. Expression of apoptosis-related proteins in experimental coxsackievirus myocarditis. Cardiovasc Res 1998; 38:158-68; PMID:9683918; http://dx.doi.org/10.1016/S0008-6363(97)00323-4
65. Kim KS, Tracy S, Tapprich W, Bailey J, Lee CK, Kim K, et al. 5'-Terminal deletions occur in coxsackie-virus B3 during replication in murine hearts and cardiac myocyte cultures and correlate with encapsidation of negative-strand viral RNA. J Virol 2005; 79:7024-41; PMID:15890942; http://dx.doi.org/10.1128/ JVI.79.11.7024-7041.2005
66. Feuer R, Ruller CM, An N, Tabor-Godwin JM, Rhoades RE, Maciejewski S, et al. Viral persistence and chronic immunopathology in the adult central nervous system following Coxsackievirus infection during the neonatal period. J Virol 2009; 83:9356-69; PMID:19570873; http://dx.doi.org/10.1128/JVI.02382-07
67. Feuer R, Whitton JL. Preferential coxsackievirus replication in proliferating/activated cells: implications for virus tropism, persistence, and pathogenesis. Curr Top Microbiol Immunol 2008; 323:149-73; PMID:18357769; http://dx.doi.org/10.1007/978-3-540-75546-3-7
68. Slifka MK, Pagarigan R, Mena I, Feuer R, Whitton JL. Using recombinant coxsackievirus B3 to evaluate the induction and protective efficacy of CD8+ T cells during picornavirus infection. J Virol 2001; 75:2377-87; PMID:11160741; http://dx.doi.org/10.1128/JVI.75.5.2377-2387.2001