Pig model mimicking chronic hepatitis e virus infection in immunocompromised patients to assess immune correlates during chronicity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 27, 2017, Pages 6914-6923

  Cao, Dianjun ^a   Cao, Qian M ^a   Subramaniam, Sakthivel ^a   Yugo, Danielle M ^a   Lynn Heffron, C ^a   Rogers, Adam J ^a   Kenney, Scott P ^a   Tian, Debin ^a   Matzinger, Shannon R ^a   Overend, Christopher ^a   Catanzaro, Nicholas ^a   LeRoith, Tanya ^a   Wang, Heng ^a   Piñeyro, Pablo ^a   Lindstrom, Nicole ^a   Clark Deener, Sherrie ^a   Yuan, Lijuan ^a   Meng, Xiang Jin ^a  

^a VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

Author keywords

Cell mediated immune responses; Chronic HEV infection; Hepatitis E virus; Immunosuppression; Pig

Indexed keywords

AZATHIOPRINE; CYCLOSPORIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; METHYLPREDNISOLONE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; TUMOR NECROSIS FACTOR; VIRUS RNA; CYTOKINE; GAMMA GLUTAMYLTRANSFERASE; IMMUNOSUPPRESSIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHRONIC HEPATITIS; CHRONICITY; COMBINATION DRUG THERAPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FECES; FLOW CYTOMETRY; GRAFT RECIPIENT; HEPATITIS E; HEPATITIS E VIRUS; IMMUNOCOMPROMISED PATIENT; IMMUNOSUPPRESSIVE TREATMENT; LIVER GRAFT REJECTION; LIVER TRANSPLANTATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PORCINE MODEL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL; VIRUS IMMUNITY; VIRUS SHEDDING; ANIMAL; BLOOD; CELLULAR IMMUNITY; CHEMICALLY INDUCED; CHRONIC DISEASE; DISEASE MODEL; HUMAN; IMMUNOLOGY; METABOLISM; PATHOLOGY; PIG;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; CYTOKINES; DISEASE MODELS, ANIMAL; GAMMA-GLUTAMYLTRANSFERASE; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; IMMUNITY, CELLULAR; IMMUNOCOMPROMISED HOST; IMMUNOSUPPRESSIVE AGENTS; SWINE; TH1 CELLS; TH2 CELLS;

EID: 85021715288     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1705446114     Document Type: Article

References (54)

1. Rein DB, Stevens GA, Theaker J, Wittenborn JS, Wiersma ST (2012) The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology 55:988-997.
2. Lozano R, et al. (2012) Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: A systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2095-2128.
3. Cao D, Meng XJ (2012) Molecular biology and replication of hepatitis E virus. Emerg Microbes Infect 1:e17.
4. Smith DB, et al.; International Committee on Taxonomy of Viruses Hepeviridae Study Group (2014) Consensus proposals for classification of the family Hepeviridae. J Gen Virol 95:2223-2232.
5. Emerson SU, Purcell RH (2007) Hepatitis E virus. Fields Virology, eds Knipe DM, Howley PM (Lippincott-Raven Publishers, Philadelphia), 5th Ed, pp 3048-3059.
6. Pérez-Gracia MT, García M, Suay B, Mateos-Lindemann ML (2015) Current knowledge on hepatitis E. J Clin Transl Hepatol 3:117-126.
7. Dalton HR, Webb GW, Norton BC, Woolson KL (2016) Hepatitis E virus: Time to change the textbooks. Dig Dis 34:308-316.
8. Kamar N, Dalton HR, Abravanel F, Izopet J (2014) Hepatitis E virus infection. Clin Microbiol Rev 27:116-138.
9. Haagsma EB, et al. (2008) Chronic hepatitis E virus infection in liver transplant recipients. Liver Transpl 14:547-553.
10. Sue PK, et al. (2016) Hepatitis E virus infection among solid organ transplant recipients at a North American Transplant Center. Open Forum Infect Dis 3:ofw006.
11. Lee GY, et al. (2015) Hepatitis E virus infection: Epidemiology and treatment implications. World J Virol 4:343-355.
12. Ding Q, et al. (2017) Hepatitis E virus ORF3 is a functional ion channel required for release of infectious particles. Proc Natl Acad Sci USA 114:1147-1152.
13. Meng XJ (2016) Expanding host range and cross-species infection of hepatitis E virus. PLoS Pathog 12:e1005695.
14. Meng XJ (2011) From barnyard to food table: The omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Res 161:23-30.
15. Feagins AR, Opriessnig T, Huang YW, Halbur PG, Meng XJ (2008) Cross-species infection of specific-pathogen-free pigs by a genotype 4 strain of human hepatitis E virus. J Med Virol 80:1379-1386.
16. Halbur PG, et al. (2001) Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J Clin Microbiol 39:918-923.
17. Meng XJ (2010) Hepatitis E virus: Animal reservoirs and zoonotic risk. Vet Microbiol 140:256-265.
18. Murali AR, Kotwal V, Chawla S (2015) Chronic hepatitis E: A brief review. World J Hepatol 7:2194-2201.
19. Singh A, et al. (2016) Chronic hepatitis E-An emerging disease in an immunocompromised host. Gastroenterol Rep (Oxf), 10.1093/gastro/gow024.
20. Yugo DM, Cossaboom CM, Meng XJ (2014) Naturally occurring animal models of human hepatitis E virus infection. ILAR J 55:187-199.
21. van de Garde MD, et al. (2016) Hepatitis E virus (HEV) genotype 3 infection of human liver chimeric mice as a model for chronic HEV infection. J Virol 90:4394-4401.
22. Allweiss L, et al. (2016) Human liver chimeric mice as a new model of chronic hepatitis E virus infection and preclinical drug evaluation. J Hepatol 64:1033-1040.
23. Sayed IM, et al. (2017) Study of hepatitis E virus infection of genotype 1 and 3 in mice with humanised liver. Gut 66:920-929.
24. Meng XJ, et al. (1998) Experimental infection of pigs with the newly identified swine hepatitis E virus (swine HEV), but not with human strains of HEV. Arch Virol 143: 1405-1415.
25. Feagins AR, et al. (2011) Intergenotypic chimeric hepatitis E viruses (HEVs) with the genotype 4 human HEV capsid gene in the backbone of genotype 3 swine HEV are infectious in pigs. Virus Res 156:141-146.
26. Sanford BJ, et al. (2011) Prior infection of pigs with a genotype 3 swine hepatitis E virus (HEV) protects against subsequent challenges with homologous and heterologous genotypes 3 and 4 human HEV. Virus Res 159:17-22.
27. Chauhan A, et al. (1993) Hepatitis E virus transmission to a volunteer. Lancet 341: 149-150.
28. Kamar N, Rostaing L, Legrand-Abravanel F, Izopet J (2013) How should hepatitis E virus infection be defined in organ-transplant recipients?. Am J Transplant 13: 1935-1936.
29. Marion O, Abravanel F, Lhomme S, Izopet J, Kamar N (2016) Hepatitis E in transplantation. Curr Infect Dis Rep 18:8.
30. Gérolami R, Moal V, Picard C, Colson P (2009) Hepatitis E virus as an emerging cause of chronic liver disease in organ transplant recipients. J Hepatol 50:622-624.
31. Gardinali NR, et al. (2017) Cynomolgus monkeys are successfully and persistently infected with hepatitis E virus genotype 3 (HEV-3) after long-term immunosuppressive therapy. PLoS One 12:e0174070.
32. Lhomme S, et al. (2012) Hepatitis E virus quasispecies and the outcome of acute hepatitis E in solid-organ transplant patients. J Virol 86:10006-10014.
33. Kamar N, et al. (2008) Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med 358:811-817.
34. Wack A, Openshaw P, O'Garra A (2011) Contribution of cytokines to pathology and protection in virus infection. Curr Opin Virol 1:184-195.
35. Ober BT, et al. (1998) Vaccine-induced, pseudorabies virus-specific, extrathymic CD4+CD8+ memory T-helper cells in swine. J Virol 72:4866-4873.
36. Zuckermann FA, Husmann RJ (1996) Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 87:500-512.
37. Tripathy AS, Das R, Rathod SB, Arankalle VA (2012) Cytokine profiles, CTL response and T cell frequencies in the peripheral blood of acute patients and individuals recovered from hepatitis E infection. PLoS One 7:e31822.
38. Brown A, et al. (2016) Characterization of the specificity, functionality, and durability of host T-cell responses against the full-length hepatitis E virus. Hepatology 64: 1934-1950.
39. Dean SK, Horley DC, Tuch BE (2003) The immunosuppression of pigs: A review. Transplant Rev 17:45-59.
40. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR (2007) Multiplecytokine- producing antiviral CD4 T cells are functionally superior to single-cytokineproducing cells. J Virol 81:8468-8476.
41. Gerner W, Käser T, Saalmüller A (2009) Porcine T lymphocytes and NK cells-An update. Dev Comp Immunol 33:310-320.
42. Saravanabalaji S, et al. (2009) Viral load, antibody titers and recombinant open reading frame 2 protein-induced TH1/TH2 cytokines and cellular immune responses in self-limiting and fulminant hepatitis e. Intervirology 52:78-85.
43. Yin X, Ambardekar C, Lu Y, Feng Z (2016) Distinct entry mechanisms for nonenveloped and Quasi-enveloped hepatitis E viruses. J Virol 90:4232-4242.
44. Ndure J, Flanagan KL (2014) Targeting regulatory T cells to improve vaccine immunogenicity in early life. Front Microbiol 5:477.
45. Boer MC, Joosten SA, Ottenhoff TH (2015) Regulatory T-cells at the interface between human host and pathogens in infectious diseases and vaccination. Front Immunol 6: 217.
46. Hoeppli RE, Wu D, Cook L, Levings MK (2015) The environment of regulatory T cell biology: Cytokines, metabolites, and the microbiome. Front Immunol 6:61.
47. Meng XJ, et al. (1998) Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol 72:9714-9721.
48. Adam SJ, Counter CM (2008) A method to generate genetically defined tumors in pigs. Methods Enzymol 439:39-51.
49. Stokes CR (2017) The development and role of microbial-host interactions in gut mucosal immune development. J Anim Sci Biotechnol 8:12.
50. Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR (2006) A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods 131:65-71.
51. Mokhtari C, et al. (2013) Comparison of real-time RT-PCR assays for hepatitis E virus RNA detection. J Clin Virol 58:36-40.
52. Liu S, et al. (1997) Removal of endotoxin from recombinant protein preparations. Clin Biochem 30:455-463.
53. Yuan L, et al. (2008) Virus-specific intestinal IFN-gamma producing T cell responses induced by human rotavirus infection and vaccines are correlated with protection against rotavirus diarrhea in gnotobiotic pigs. Vaccine 26:3322-3331.
54. Wen K, et al. (2012) CD4+ CD25- FoxP3+ regulatory cells are the predominant responding regulatory T cells after human rotavirus infection or vaccination in gnotobiotic pigs. Immunology 137:160-171.