Coxsackievirus B Exits the Host Cell in Shed Microvesicles Displaying Autophagosomal Markers

1. MuirP, van LoonAM (1997) Enterovirus infections of the central nervous system. Intervirology 40: 153–166.

2. SawyerMH (2002) Enterovirus infections: diagnosis and treatment. Semin Pediatr Infect Dis 13: 40–47.

3. OrnoyA, TenenbaumA (2006) Pregnancy outcome following infections by coxsackie, echo, measles, mumps, hepatitis, polio and encephalitis viruses. Reprod Toxicol 21: 446–457.

4. EuscherE, DavisJ, HolzmanI, NuovoGJ (2001) Coxsackie virus infection of the placenta associated with neurodevelopmental delays in the newborn. Obstet Gynecol 98: 1019–1026.

5. DavidP, BaleriauxD, BankWO, AmromD, DeTD, et al. (1993) MRI of acute disseminated encephalomyelitis after coxsackie B infection. J Neuroradiol 20: 258–265.

6. GraberD, FossoudC, GrouteauE, Gayet-MengelleC, CarriereJP (1994) Acute transverse myelitis and coxsackie A9 virus infection. Pediatr Infect Dis J 13: 77.

7. SuvisaariJ, MautempsN, HaukkaJ, HoviT, LonnqvistJ (2003) Childhood central nervous system viral infections and adult schizophrenia. Am J Psychiatry 160: 1183–1185.

8. RantakallioP, JonesP, MoringJ, VonWL (1997) Association between central nervous system infections during childhood and adult onset schizophrenia and other psychoses: a 28-year follow-up. Int J Epidemiol 26: 837–843.

9. CreeBC, BernardiniGL, HaysAP, LoweG (2003) A fatal case of coxsackievirus B4 meningoencephalitis. Arch Neurol 60: 107–112.

10. WoodallCJ, RidingMH, GrahamDI, ClementsGB (1994) Sequences specific for enterovirus detected in spinal cord from patients with motor neurone disease. BMJ 308: 1541–1543.

11. WoodallCJ, GrahamDI (2004) Evidence for neuronal localisation of enteroviral sequences in motor neurone disease/amyotrophic lateral sclerosis by in situ hybridization. Eur J Histochem 48: 129–134.

12. TsuengG, Tabor-GodwinJM, GopalA, RullerCM, DelineS, et al. (2011) Coxsackievirus preferentially replicates and induces cytopathic effects in undifferentiated neural progenitor cells. J Virol 85: 5718–5732.

13. FeuerR, MenaI, PagariganRR, HarkinsS, HassettDE, et al. (2003) Coxsackievirus B3 and the neonatal CNS: the roles of stem cells, developing neurons, and apoptosis in infection, viral dissemination, and disease. Am J Pathol 163: 1379–1393.

14. FeuerR, PagariganRR, HarkinsS, LiuF, HunzikerIP, et al. (2005) Coxsackievirus targets proliferating neuronal progenitor cells in the neonatal CNS. J Neurosci 25: 2434–2444.

15. FeuerR, WhittonJL (2008) Preferential coxsackievirus replication in proliferating/activated cells: implications for virus tropism, persistence, and pathogenesis. Curr Top Microbiol Immunol 323: 149–173.

16. WhittonJL, CornellCT, FeuerR (2005) Host and virus determinants of picornavirus pathogenesis and tropism. Nat Rev Microbiol 3: 765–776.

17. PucciniJM, RullerCM, RobinsonSM, KnoppKA, BuchmeierMJ, et al. (2014) Distinct neural stem cell tropism, early immune activation, and choroid plexus pathology following coxsackievirus infection in the neonatal central nervous system. Lab Invest 94(2): 161–81.

18. RullerCM, Tabor-GodwinJM, Van DerenDAJ, RobinsonSM, MaciejewskiS, et al. (2012) Neural stem cell depletion and CNS developmental defects after enteroviral infection. Am J Pathol 180: 1107–1120.

19. RhoadesRE, Tabor-GodwinJM, TsuengG, FeuerR (2011) Enterovirus infections of the central nervous system. Virology 411: 288–305.

20. FeuerR, RullerCM, AnN, Tabor-GodwinJM, RhoadesRE, et al. (2009) Viral persistence and chronic immunopathology in the adult central nervous system following Coxsackievirus infection during the neonatal period. J Virol 83: 9356–9369.

21. AlthofN, WhittonJL (2012) Coxsackievirus B3 infects the bone marrow and diminishes the restorative capacity of erythroid and lymphoid progenitors. J Virol 87(5): 2823–34.

22. HorwitzMS, La CavaA, FineC, RodriguezE, IlicA, et al. (2000) Pancreatic expression of interferon-gamma protects mice from lethal coxsackievirus B3 infection and subsequent myocarditis. Nat Med 6: 693–697.

23. TerskikhA, FradkovA, ErmakovaG, ZaraiskyA, TanP, et al. (2000) “Fluorescent timer”: protein that changes color with time. Science 290: 1585–1588.

24. KlionskyDJ, AbdallaFC, AbeliovichH, AbrahamRT, Acevedo-ArozenaA, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8: 445–544.

25. SlifkaMK, PagariganR, MenaI, FeuerR, WhittonJL (2001) Using recombinant coxsackievirus B3 to evaluate the induction and protective efficacy of CD8+ T cells during picornavirus infection. J Virol 75: 2377–2387.

26. FeuerR, MenaI, PagariganR, SlifkaMK, WhittonJL (2002) Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol 76: 4430–4440.

27. Tabor-GodwinJM, RullerCM, BagalsoN, AnN, PagariganRR, et al. (2010) A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS. J Neurosci 30: 8676–8691.

28. Tabor-GodwinJM, TsuengG, SayenMR, GottliebRA, FeuerR (2012) The role of autophagy during coxsackievirus infection of neural progenitor and stem cells. Autophagy 8: 938–953.

29. TsuengG, RhoadesRE, DelineS, FeuerR (2014) Unique 2C and 3A viral protein mutations identified in hypervirulent and attenuated coxsackievirus strains isolated from persistently-infected neural progenitor cell cultures. Manuscript In Preparation

30. AlirezaeiM, FlynnCT, WoodMR, WhittonJL (2012) Pancreatic acinar cell-specific autophagy disruption reduces coxsackievirus replication and pathogenesis in vivo. Cell Host Microbe 11: 298–305.

31. KemballCC, AlirezaeiM, FlynnCT, WoodMR, HarkinsS, et al. (2010) Coxsackievirus infection induces autophagy-like vesicles and megaphagosomes in pancreatic acinar cells in vivo. J Virol 84: 12110–12124.

32. YajimaT (2011) Viral myocarditis: potential defense mechanisms within the cardiomyocyte against virus infection. Future Microbiol 6: 551–566.

33. MukherjeeA, MoroskySA, Delorme-AxfordE, Dybdahl-SissokoN, ObersteMS, et al. (2011) The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog 7: e1001311.

34. HsuNY, IlnytskaO, BelovG, SantianaM, ChenYH, et al. (2010) Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141: 799–811.

35. TaylorMP, BurgonTB, KirkegaardK, JacksonWT (2009) Role of microtubules in extracellular release of poliovirus. J Virol 83: 6599–6609.

36. LuoH, McManusBM (2012) Is autophagy an avenue to modulate coxsackievirus replication and pathogenesis? Future Microbiol 7: 921–4.

37. AlirezaeiM, FlynnCT, WhittonJL (2012) Interactions between enteroviruses and autophagy in vivo. Autophagy 8: 973–975.

38. YoonSY, HaYE, ChoiJE, AhnJ, LeeH, et al. (2008) Coxsackievirus B4 uses autophagy for replication after calpain activation in rat primary neurons. J Virol 82(23): 11976–11978.

39. YoonSY, HaYE, ChoiJE, AhnJ, LeeH, et al. (2009) Autophagy in coxsackievirus-infected neurons. Autophagy 5: 388–389.

40. WongJ, ZhangJ, SiX, GaoG, MaoI, et al. (2008) Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 82(18): 9143–9153.

41. FengZ, HensleyL, McKnightKL, HuF, MaddenV, et al. (2013) A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496(7445): 367–71.

42. MeckesDGJr, Raab-TraubN (2011) Microvesicles and viral infection. J Virol 85: 12844–12854.

43. GottliebRA, MentzerRM (2010) Autophagy during cardiac stress: joys and frustrations of autophagy. Annu Rev Physiol 72: 45–59.

44. XiaoC, Bator-KellyCM, RiederE, ChipmanPR, CraigA, et al. (2005) The crystal structure of coxsackievirus A21 and its interaction with ICAM-1. Structure 13: 1019–1033.

45. GuesciniM, GuidolinD, ValloraniL, CasadeiL, GioacchiniAM, et al. (2010) C2C12 myoblasts release micro-vesicles containing mtDNA and proteins involved in signal transduction. Exp Cell Res 316: 1977–1984.

46. DoceulV, HollinsheadM, van der LindenL, SmithGL (2010) Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327: 873–876.

47. NejmeddineM, BanghamCR (2010) The HTLV-1 Virological Synapse. Viruses 2: 1427–1447.

48. RamsinghAI (2008) CVB-induced pancreatitis and alterations in gene expression. Curr Top Microbiol Immunol 323: 241–58 241–258.

49. LidskyPV, HatoS, BardinaMV, AminevAG, PalmenbergAC, et al. (2006) Nucleocytoplasmic traffic disorder induced by cardioviruses. J Virol 80: 2705–2717.

50. de JongAS, VischHJ, deMF, van DommelenMM, SwartsHG, et al. (2006) The coxsackievirus 2B protein increases efflux of ions from the endoplasmic reticulum and Golgi, thereby inhibiting protein trafficking through the Golgi. J Biol Chem %19;281: 14144–14150.

51. CornellCT, KiossesWB, HarkinsS, WhittonJL (2006) Inhibition of protein trafficking by coxsackievirus b3: multiple viral proteins target a single organelle. J Virol 80: 6637–6647.

52. CornellCT, KiossesWB, HarkinsS, WhittonJL (2007) Coxsackievirus B3 proteins directionally complement each other to downregulate surface major histocompatibility complex class I. J Virol 81: 6785–6797.

53. WesselsE, DuijsingsD, LankeKH, MelchersWJ, JacksonCL, et al. (2007) Molecular determinants of the interaction between coxsackievirus protein 3A and guanine nucleotide exchange factor GBF1. J Virol 81: 5238–5245.

54. LankeKH, van der SchaarHM, BelovGA, FengQ, DuijsingsD, et al. (2009) GBF1, a guanine nucleotide exchange factor for Arf, is crucial for coxsackievirus B3 RNA replication. J Virol 83: 11940–11949.

55. LuoH, McManusBM (2012) Is autophagy an avenue to modulate coxsackievirus replication and pathogenesis? Future Microbiol 7: 4–924 –

56. FengZ, LemonSM (2014) Peek-a-boo: membrane hijacking and the pathogenesis of viral hepatitis. Trends Microbiol 22(2): 59–64.

57. RichardsAL, JacksonWT (2012) Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLoS Pathog 8: e1003046.

58. Izquierdo-UserosN, PuertasMC, BorrasFE, BlancoJ, Martinez-PicadoJ (2011) Exosomes and retroviruses: the chicken or the egg? Cell Microbiol 13: 10–17.

59. DreuxM, GaraigortaU, BoydB, DecembreE, ChungJ, et al. (2012) Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 12: 558–570.

60. WurdingerT, GatsonNN, BalajL, KaurB, BreakefieldXO, et al. (2012) Extracellular vesicles and their convergence with viral pathways. Adv Virol 2012: 767694.

61. JacksonWT, GiddingsTHJr, TaylorMP, MulinyaweS, RabinovitchM, et al. (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3(5): e156.

62. MasciopintoF, GiovaniC, CampagnoliS, Galli-StampinoL, ColombattoP, et al. (2004) Association of hepatitis C virus envelope proteins with exosomes. Eur J Immunol 34: 2834–2842.

63. GalloA, TandonM, AlevizosI, IlleiGG (2012) The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One 7: e30679.

64. GrossJC, ChaudharyV, BartschererK, BoutrosM (2012) Active Wnt proteins are secreted on exosomes. Nat Cell Biol 14: 1036–1045.

65. VidalM (2010) Exosomes in erythropoiesis. Transfus Clin Biol 17: 131–137.

66. FaderCM, ColomboMI (2006) Multivesicular bodies and autophagy in erythrocyte maturation. Autophagy 2: 122–125.

67. ReynoldsS (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 200–211.