The Impact of Juvenile Coxsackievirus Infection on Cardiac Progenitor Cells and Postnatal Heart Development
Coxsackievirus B (CVB) is a significant human pathogen, causing myocarditis, aseptic meningitis and encephalitis. The lasting consequences of juvenile CVB infection on the developing host have yet to be adequately inspected. Here, we show that CVB efficiently infected juvenile cardiac progenitor cells both in culture and the young heart. Furthermore, we describe a mouse model of juvenile infection with a subclinical dose of CVB which showed no symptoms of disease into adulthood. However following physiological or pharmacologically-induced cardiac stress, juvenile-infected mice underwent cardiac hypertrophy and dilation indicative of progression to heart failure. These results suggest that mild CVB infection in the young host may impair the ability of the heart to adapt to increased load leading to pathological remodeling later in adult life.
Vyšlo v časopise:
The Impact of Juvenile Coxsackievirus Infection on Cardiac Progenitor Cells and Postnatal Heart Development. PLoS Pathog 10(7): e32767. doi:10.1371/journal.ppat.1004249
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004249
Souhrn
Coxsackievirus B (CVB) is a significant human pathogen, causing myocarditis, aseptic meningitis and encephalitis. The lasting consequences of juvenile CVB infection on the developing host have yet to be adequately inspected. Here, we show that CVB efficiently infected juvenile cardiac progenitor cells both in culture and the young heart. Furthermore, we describe a mouse model of juvenile infection with a subclinical dose of CVB which showed no symptoms of disease into adulthood. However following physiological or pharmacologically-induced cardiac stress, juvenile-infected mice underwent cardiac hypertrophy and dilation indicative of progression to heart failure. These results suggest that mild CVB infection in the young host may impair the ability of the heart to adapt to increased load leading to pathological remodeling later in adult life.
Zdroje
1. CarthyCM, YangD, AndersonDR, WilsonJE, McManusBM (1997) Myocarditis as systemic disease: new perspectives on pathogenesis. Clin Exp Pharmacol Physiol 24: 997–1003.
2. SoleMJ, LiuP (1993) Viral myocarditis: a paradigm for understanding the pathogenesis and treatment of dilated cardiomyopathy. J Am Coll Cardiol 22: 99A–105A.
3. TamPE (2006) Coxsackievirus myocarditis: interplay between virus and host in the pathogenesis of heart disease. Viral Immunol 19: 133–146.
4. GristNR, BellEJ (1969) Coxsackie viruses and the heart. Am Heart J 77: 295–300.
5. WhittonJL, CornellCT, FeuerR (2005) Host and virus determinants of picornavirus pathogenesis and tropism. Nat Rev Microbiol 3: 765–776.
6. WardC (1978) Severe arrhythmias in Coxsackievirus B3 myopericarditis. Arch Dis Child 53: 174–176.
7. FujiokaS, KitauraY, DeguchiH, ShimizuA, IsomuraT, et al. (2004) Evidence of viral infection in the myocardium of American and Japanese patients with idiopathic dilated cardiomyopathy. Am J Cardiol 94: 602–605.
8. PetitjeanJ, KopeckaH, FreymuthF, LanglardJM, ScanuP, et al. (1992) Detection of enteroviruses in endomyocardial biopsy by molecular approach. J Med Virol 37: 76–82.
9. ChiangFT, LinLI, TsengYZ, TsengCD, HsuKL, et al. (1992) Detection of enterovirus RNA in patients with idiopathic dilated cardiomyopathy by polymerase chain reaction. J Formos Med Assoc 91: 569–574.
10. 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.
11. FeuerR, PagariganRR, HarkinsS, LiuF, HunzikerIP, et al. (2005) Coxsackievirus targets proliferating neuronal progenitor cells in the neonatal CNS. J Neurosci 25: 2434–2444.
12. Tabor-GodwinJM, TsuengG, SayenMR, GottliebRA, FeuerR (2012) The role of autophagy during coxsackievirus infection of neural progenitor and stem cells. Autophagy 8: 938–953.
13. FeuerR, WhittonJL (2008) Preferential coxsackievirus replication in proliferating/activated cells: implications for virus tropism, persistence, and pathogenesis. Curr Top Microbiol Immunol 323: 149–173.
14. RhoadesRE, Tabor-GodwinJM, TsuengG, FeuerR (2011) Enterovirus infections of the central nervous system. Virology 411: 288–305.
15. 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.
16. 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.
17. AlthofN, WhittonJL (2012) Coxsackievirus B3 infects the bone marrow and diminishes the restorative capacity of erythroid and lymphoid progenitors. J Virol 87: 2823–2834.
18. RobinsonSM, TsuengG, SinJ, MangaleV, RahawiS, et al. (2014) Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLoS Pathog 10: e1004045.
19. JacksonWT, GiddingsTHJr, TaylorMP, MulinyaweS, RabinovitchM, et al. (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3(5): e156.
20. AnversaP, KajsturaJ, RotaM, LeriA (2013) Regenerating new heart with stem cells. J Clin Invest 123: 62–70.
21. LiuJ, WangY, DuW, YuB (2013) Sca-1-Positive Cardiac Stem Cell migration in a Cardiac Infarction Model. Inflammation 36: 738–749.
22. OhH, BradfuteSB, GallardoTD, NakamuraT, GaussinV, et al. (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100: 12313–12318.
23. BeltramiAP, BarlucchiL, TorellaD, BakerM, LimanaF, et al. (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell %19 114: 763–776.
24. FischerKM, CottageCT, WuW, DinS, GudeNA, et al. (2009) Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation 120: 2077–2087.
25. HuangC, ZhangX, RamilJM, RikkaS, KimL, et al. (2010) Juvenile exposure to anthracyclines impairs cardiac progenitor cell function and vascularization resulting in greater susceptibility to stress-induced myocardial injury in adult mice. Circulation 121: 675–683.
26. PucciniJM, RullerCM, RobinsonSM, KnoppKA, BuchmeierMJ, et al. (2013) Distinct neural stem cell tropism, early immune activation, and choroid plexus pathology following coxsackievirus infection in the neonatal central nervous system. Lab Invest (In Press)..
27. ZhangY, SimpsonAA, LedfordRM, BatorCM, ChakravartyS, et al. (2004) Structural and virological studies of the stages of virus replication that are affected by antirhinovirus compounds. J Virol 78: 11061–11069.
28. AnversaP, FitzpatrickD, ArganiS, CapassoJM (1991) Myocyte mitotic division in the aging mammalian rat heart. Circ Res 69: 1159–1164.
29. PearceBD, SteffensenSC, PaolettiAD, HenriksenSJ, BuchmeierMJ (1996) Persistent dentate granule cell hyperexcitability after neonatal infection with lymphocytic choriomeningitis virus. J Neurosci 16: 220–228.
30. WesselyR, KlingelK, KnowltonKU, KandolfR (2001) Cardioselective infection with coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication. Circulation 103: 756–761.
31. KimKS, HufnagelG, ChapmanNM, TracyS (2001) The group B coxsackieviruses and myocarditis. Rev Med Virol 11: 355–368.
32. FeuerR, MenaI, PagariganRR, HassettDE, WhittonJL (2004) Coxsackievirus replication and the cell cycle: a potential regulatory mechanism for viral persistence/latency. Med Microbiol Immunol (Berl) 193: 83–90.
33. 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.
34. DeyD, HanL, BauerM, SanadaF, OikonomopoulosA, et al. (2013) Dissecting the molecular relationship among various cardiogenic progenitor cells. Circ Res 112: 1253–1262.
35. MagentaA, AvitabileD, PompilioG, CapogrossiMC (2013) c-kit-Positive cardiac progenitor cells: the heart of stemness. Circ Res 112: 1202–1204.
36. EptingCL, LopezJE, ShenX, LiuL, BristowJ, et al. (2004) Stem cell antigen-1 is necessary for cell-cycle withdrawal and myoblast differentiation in C2C12 cells. J Cell Sci 117: 6185–6195.
37. HolmesC, StanfordWL (2007) Concise review: stem cell antigen-1: expression, function, and enigma. Stem Cells 25: 1339–1347.
38. GalindoCL, SkinnerMA, ErramiM, OlsonLD, WatsonDA, et al. (2009) Transcriptional profile of isoproterenol-induced cardiomyopathy and comparison to exercise-induced cardiac hypertrophy and human cardiac failure. BMC Physiol 9: 23 doi:–10.1186/1472-6793-9-23.: 23–29
39. HorwitzMS, BradleyLM, HarbertsonJ, KrahlT, LeeJ, et al. (1998) Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 4: 781–785.
40. 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.
41. KemballCC, FlynnCT, HoskingMP, BottenJ, WhittonJL (2012) Wild-type coxsackievirus infection dramatically alters the abundance, heterogeneity, and immunostimulatory capacity of conventional dendritic cells in vivo. Virology 429: 74–90.
42. AlthofN, HarkinsS, KemballCC, FlynnCT, AlirezaeiM, et al. (2014) In vivo ablation of type I interferon receptor from cardiomyocytes delays coxsackieviral clearance and accelerates myocardial disease. J Virol 88: 5087–99.
43. GuanJL, SimonAK, PrescottM, MenendezJA, LiuF, et al. (2013) Autophagy in stem cells. Autophagy 9: 830–49.
44. van BerloJH, KanisicakO, MailletM, VagnozziRJ, KarchJ, et al. (2014) c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 509: 337–341.
45. 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.
46. FeuerR, MenaI, PagariganR, SlifkaMK, WhittonJL (2002) Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol 76: 4430–4440.
47. KnowltonKU, JeonES, BerkleyN, WesselyR, HuberS (1996) A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3. J Virol 70: 7811–7818.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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