Evolutionary biology of human hepatitis viruses.

Andrea Rasche, Anna-Lena Sander, Victor Max Corman, Jan Felix Drexler
Author Information
  1. Andrea Rasche: Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Virology, 10117 Berlin, Germany; German Center for Infection Research (DZIF), Germany.
  2. Anna-Lena Sander: Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Virology, 10117 Berlin, Germany.
  3. Victor Max Corman: Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Virology, 10117 Berlin, Germany; German Center for Infection Research (DZIF), Germany.
  4. Jan Felix Drexler: Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Virology, 10117 Berlin, Germany; German Center for Infection Research (DZIF), Germany. Electronic address: felix.drexler@charite.de.

Abstract

Hepatitis viruses are major threats to human health. During the last decade, highly diverse viruses related to human hepatitis viruses were found in animals other than primates. Herein, we describe both surprising conservation and striking differences of the unique biological properties and infection patterns of human hepatitis viruses and their animal homologues, including transmission routes, liver tropism, oncogenesis, chronicity, pathogenesis and envelopment. We discuss the potential for translation of newly discovered hepatitis viruses into preclinical animal models for drug testing, studies on pathogenesis and vaccine development. Finally, we re-evaluate the evolutionary origins of human hepatitis viruses and discuss the past and present zoonotic potential of their animal homologues.

Keywords

References

  1. Gastroenterology. 1983 Aug;85(2):260-7 [PMID: 6190699]
  2. World J Gastroenterol. 2014 May 14;20(18):5427-34 [PMID: 24833873]
  3. JAMA Oncol. 2017 Dec 1;3(12):1683-1691 [PMID: 28983565]
  4. Front Cell Infect Microbiol. 2012 Apr 11;2:50 [PMID: 22919641]
  5. PLoS One. 2012;7(8):e42481 [PMID: 22870331]
  6. Emerg Infect Dis. 2018 Dec;24(12):2241-2250 [PMID: 30457530]
  7. N Engl J Med. 1980 Oct 9;303(15):833-41 [PMID: 6997738]
  8. N Engl J Med. 1986 Dec 18;315(25):1575-8 [PMID: 3097544]
  9. Annu Rev Virol. 2016 Sep 29;3(1):53-75 [PMID: 27741408]
  10. J Virol. 2001 Jun;75(11):5084-9 [PMID: 11333889]
  11. Hepatology. 2015 Feb;61(2):447-59 [PMID: 25212983]
  12. Proc Natl Acad Sci U S A. 1998 May 12;95(10):5757-61 [PMID: 9576957]
  13. J Biol Chem. 1996 Mar 1;271(9):4569-72 [PMID: 8617711]
  14. J Virol. 2010 Jan;84(1):303-11 [PMID: 19846521]
  15. Nature. 1979 Oct 25;281(5733):646-50 [PMID: 399327]
  16. Proc Biol Sci. 2013 Feb 01;280(1756):20122753 [PMID: 23378666]
  17. Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):16151-6 [PMID: 24043818]
  18. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8738-43 [PMID: 9238047]
  19. PLoS One. 2014 Jun 17;9(6):e99861 [PMID: 24937350]
  20. J Viral Hepat. 2011 Oct;18(10):e603-8 [PMID: 21914082]
  21. Cold Spring Harb Perspect Med. 2015 Apr 01;5(4): [PMID: 25833941]
  22. Curr Top Microbiol Immunol. 2013;369:1-15 [PMID: 23463195]
  23. Arch Virol. 2018 May;163(5):1187-1193 [PMID: 29387970]
  24. J Virol. 1987 Jul;61(7):2273-9 [PMID: 3586132]
  25. Liver Int. 2011 Jan;31(1):7-21 [PMID: 20880077]
  26. J Infect Dis. 1996 Mar;173(3):592-7 [PMID: 8627022]
  27. Curr Biol. 2013 Mar 4;23(5):392-8 [PMID: 23375891]
  28. Nature. 2016 Mar 17;531(7594):386-9 [PMID: 26983541]
  29. J Microbiol Immunol Infect. 2017 Dec;50(6):771-780 [PMID: 26757847]
  30. Viruses. 2018 Dec 17;10(12): [PMID: 30562970]
  31. Cold Spring Harb Perspect Med. 2015 May 01;5(5):a021410 [PMID: 25934461]
  32. Curr Opin Virol. 2016 Feb;16:1-7 [PMID: 26517843]
  33. Semin Liver Dis. 2013 May;33(2):103-12 [PMID: 23749666]
  34. Nat Rev Dis Primers. 2017 Nov 16;3:17086 [PMID: 29154369]
  35. Annu Rev Virol. 2014 Nov;1(1):539-60 [PMID: 26958733]
  36. Int J Womens Health. 2014 Jun 10;6:605-11 [PMID: 24966696]
  37. PLoS Pathog. 2013;9(6):e1003438 [PMID: 23818848]
  38. Nucleic Acids Res. 2002 Jul 15;30(14):3059-66 [PMID: 12136088]
  39. J Virol. 2015 Oct 21;90(2):659-69 [PMID: 26491167]
  40. Cold Spring Harb Perspect Med. 2015 Jun 01;5(6): [PMID: 26033082]
  41. Hepatology. 1988 Nov-Dec;8(6):1655-61 [PMID: 3192181]
  42. N Engl J Med. 1976 Sep 2;295(10):517-22 [PMID: 950957]
  43. Virus Res. 2011 Jun;158(1-2):116-23 [PMID: 21458509]
  44. Virology. 2018 Jun;519:12-16 [PMID: 29627586]
  45. Emerg Infect Dis. 2010 Sep;16(9):1452-5 [PMID: 20735931]
  46. Viruses. 2018 May 17;10(5): [PMID: 29772771]
  47. J Virol. 2014 Nov;88(22):13352-66 [PMID: 25210167]
  48. JAMA. 1965 Feb 15;191:541-6 [PMID: 14239025]
  49. Philos Trans R Soc Lond B Biol Sci. 2016 Jul 19;371(1699): [PMID: 27325836]
  50. Intervirology. 1983;20(1):23-31 [PMID: 6409836]
  51. J Virol. 1991 Apr;65(4):2056-65 [PMID: 1705995]
  52. Vet Microbiol. 2016 Feb 1;183:30-6 [PMID: 26790932]
  53. J Virol. 1998 Dec;72(12):9714-21 [PMID: 9811705]
  54. Nature. 1986 Oct 9-15;323(6088):508-14 [PMID: 3762705]
  55. Am J Med Sci. 1975 Jul-Aug;270(1):81-5 [PMID: 171954]
  56. Proc Natl Acad Sci U S A. 2013 Jun 4;110(23):9505-10 [PMID: 23690609]
  57. Nature. 2017 Jun 29;546(7660):646-650 [PMID: 28636590]
  58. Emerg Infect Dis. 2012 Dec;18(12):1976-82 [PMID: 23171728]
  59. N Engl J Med. 1975 Apr 10;292(15):767-70 [PMID: 163436]
  60. N Engl J Med. 2014 Mar 20;370(12):1111-20 [PMID: 24645943]
  61. Am J Med. 1980 Jun;68(6):818-24 [PMID: 6770682]
  62. Best Pract Res Clin Gastroenterol. 2017 Jun;31(3):273-279 [PMID: 28774409]
  63. J Mol Evol. 2007 Aug;65(2):197-205 [PMID: 17684696]
  64. Mol Biol Evol. 2010 Nov;27(11):2576-86 [PMID: 20551041]
  65. Proc Natl Acad Sci U S A. 2013 May 14;110(20):8194-9 [PMID: 23610427]
  66. Proc Natl Acad Sci U S A. 2015 Jun 2;112(22):7039-44 [PMID: 26038558]
  67. J Gen Virol. 1991 Jul;72 ( Pt 7):1685-9 [PMID: 1649902]
  68. Virus Res. 2007 Aug;127(2):151-7 [PMID: 17328982]
  69. J Clin Microbiol. 2010 Apr;48(4):1112-25 [PMID: 20107086]
  70. Virol J. 2013 Nov 12;10:333 [PMID: 24220021]
  71. J Gen Virol. 2017 Jan;98(1):2-3 [PMID: 28218572]
  72. Proc Biol Sci. 2014 Sep 22;281(1791):20141122 [PMID: 25080342]
  73. Proc Soc Exp Biol Med. 1979 Feb;160(2):213-21 [PMID: 217023]
  74. mBio. 2019 Apr 2;10(2): [PMID: 30940697]
  75. PLoS Pathog. 2017 Oct 30;13(10):e1006694 [PMID: 29084265]
  76. Nat Commun. 2016 Oct 05;7:12992 [PMID: 27703150]
  77. Nature. 2018 Apr;556(7700):197-202 [PMID: 29618816]
  78. Vet Microbiol. 2013 Apr 12;163(1-2):54-61 [PMID: 23317806]
  79. Emerg Infect Dis. 2013 Aug;19(8):1341-3 [PMID: 23876489]
  80. JAMA. 1967 May 1;200(5):365-73 [PMID: 4164595]
  81. Lancet. 2011 Jul 2;378(9785):73-85 [PMID: 21511329]
  82. Science. 1973 Dec 7;182(4116):1026-8 [PMID: 4356028]
  83. J Virol. 1996 Jul;70(7):4210-9 [PMID: 8676441]
  84. J Virol. 2015 Jul;89(14):7007-15 [PMID: 25926652]
  85. Nature. 2005 Dec 1;438(7068):575-6 [PMID: 16319873]
  86. Vet Res. 2014 Nov 26;45:121 [PMID: 25421429]
  87. PLoS Genet. 2014 Dec 11;10(12):e1004559 [PMID: 25501991]
  88. mBio. 2013 Apr 09;4(2):e00216-13 [PMID: 23572554]
  89. Science. 2005 Sep 2;309(5740):1577-81 [PMID: 16141076]
  90. Nature. 2018 May;557(7705):418-423 [PMID: 29743673]
  91. J Virol. 1980 Dec;36(3):829-36 [PMID: 7463557]
  92. J Virol. 2012 Sep;86(17):9510-3 [PMID: 22718817]
  93. Proc Natl Acad Sci U S A. 2015 Feb 17;112(7):2192-7 [PMID: 25646476]
  94. Nature. 2013 Apr 18;496(7445):367-71 [PMID: 23542590]
  95. J Virol. 2015 Dec;89(23):11801-11 [PMID: 26378165]
  96. Arch Virol. 2015 Jan;160(1):335-7 [PMID: 25193071]
  97. Elife. 2012 Nov 13;1:e00049 [PMID: 23150796]
  98. Clin Microbiol Rev. 2006 Jul;19(3):531-45 [PMID: 16847084]
  99. J Clin Exp Hepatol. 2013 Jun;3(2):134-40 [PMID: 25755487]
  100. Proc R Soc Med. 1946 Aug;39(10):655-7 [PMID: 19993377]
  101. World J Virol. 2015 Nov 12;4(4):313-22 [PMID: 26568914]
  102. J Virol. 1999 Sep;73(9):7860-5 [PMID: 10438880]
  103. Transfusion. 2000 Jun;40(6):718-24 [PMID: 10864995]
  104. N Engl J Med. 2014 Apr 24;370(17):1576-8 [PMID: 24720678]
  105. Dtsch Arztebl Int. 2014 Sep 1;111(35-36):577-83 [PMID: 25249359]
  106. Emerg Infect Dis. 2016 Jul;22(7):1249-52 [PMID: 27315454]
  107. Mol Biol Evol. 2012 Aug;29(8):1969-73 [PMID: 22367748]
  108. Virol Sin. 2018 Feb;33(1):44-58 [PMID: 29500690]
  109. J Infect Dis. 1993 Jun;167(6):1302-6 [PMID: 8501318]
  110. Virology. 1999 Sep 30;262(2):470-8 [PMID: 10502525]
  111. Aging Cell. 2002 Dec;1(2):124-31 [PMID: 12882342]
  112. Curr Opin Virol. 2016 Feb;16:86-94 [PMID: 26897577]
  113. J Gen Virol. 2011 Apr;92(Pt 4):902-8 [PMID: 21228128]
  114. Virology. 2017 May;505:1-11 [PMID: 28213271]
  115. PLoS One. 2015 Apr 23;10(4):e0122102 [PMID: 25906163]
  116. mBio. 2015 Aug 25;6(4): [PMID: 26307166]
  117. Virology. 2015 May;479-480:672-86 [PMID: 25759099]
  118. Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7253-8 [PMID: 17438296]
  119. Cell Host Microbe. 2009 Nov 19;6(5):409-21 [PMID: 19917496]
  120. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9860-5 [PMID: 9275216]
  121. J Virol. 2015 Jun;89(11):5876-82 [PMID: 25787289]
  122. J Hepatol. 2014 Oct;61(4):867-75 [PMID: 24845614]
  123. mBio. 2017 Sep 5;8(5): [PMID: 28874468]
  124. Proc Natl Acad Sci U S A. 1985 May;82(9):2627-31 [PMID: 2986127]
  125. Lancet. 1988 Mar 12;1(8585):550-4 [PMID: 2894491]
  126. Microbiome. 2018 Oct 3;6(1):178 [PMID: 30285857]
  127. Front Microbiol. 2011 Dec 07;2:240 [PMID: 22319510]
  128. Virology. 1996 Apr 1;218(1):214-23 [PMID: 8615024]
  129. Hepatology. 2017 Sep;66(3):703-716 [PMID: 28195359]
  130. J Viral Hepat. 2015 Jan;22(1):55-63 [PMID: 24548489]
  131. Cold Spring Harb Perspect Med. 2018 Dec 3;8(12): [PMID: 29610146]
  132. J Infect Dis. 1998 Oct;178(4):1193-7 [PMID: 9806059]
  133. J Infect Dis. 1980 May;141(5):590-602 [PMID: 6989929]
  134. Nature. 2015 Jan 1;517(7532):85-88 [PMID: 25327248]
  135. Front Microbiol. 2018 May 01;9:854 [PMID: 29765366]
  136. Hepatology. 2013 Mar;57(3):881-9 [PMID: 23175457]
  137. J Hepatol. 2017 Sep 5;: [PMID: 28887164]
  138. N Engl J Med. 2002 May 30;346(22):1682-3 [PMID: 12037146]
  139. J Gen Virol. 2014 Aug;95(Pt 8):1701-1711 [PMID: 24814924]
  140. Bioinformatics. 2012 Jun 15;28(12):1647-9 [PMID: 22543367]
  141. Curr Opin Microbiol. 2013 Aug;16(4):507-13 [PMID: 23850098]
  142. J Hepatol. 2014 Nov;61(1 Suppl):S58-68 [PMID: 25443346]
  143. Hepatology. 2015 May;61(5):1533-46 [PMID: 25580897]
  144. Infect Genet Evol. 2009 Dec;9(6):1287-94 [PMID: 19723592]
  145. J Hepatol. 2012 Oct;57(4):885-96 [PMID: 22634122]
  146. ILAR J. 2001;42(2):103-6 [PMID: 11406712]
  147. Cold Spring Harb Perspect Med. 2016 Jan 04;6(1):a021360 [PMID: 26729756]
  148. Hepatology. 2018 Aug;68(2):435-448 [PMID: 28859226]
  149. PLoS Pathog. 2014 Nov 06;10(11):e1004395 [PMID: 25375777]
  150. Gastroenterol Jpn. 1991 Jul;26 Suppl 3:142-7 [PMID: 1909254]
  151. Nature. 2017 Jan 18;541(7637):302-310 [PMID: 28102248]
  152. J Med Virol. 1988 Nov;26(3):233-42 [PMID: 3204365]
  153. J Virol. 2012 Jun;86(11):6171-8 [PMID: 22491452]
  154. Nat Med. 2013 Jul;19(7):879-88 [PMID: 23836238]
  155. mBio. 2014 Oct 14;5(5):e01933-14 [PMID: 25316698]
  156. Lancet. 2012 Dec 1;380(9857):1956-65 [PMID: 23200504]
  157. Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11608-13 [PMID: 21610165]
  158. J Virol. 2013 Aug;87(16):8971-81 [PMID: 23740998]
  159. Emerg Microbes Infect. 2018 Feb 7;7(1):11 [PMID: 29410449]
  160. Mol Phylogenet Evol. 2015 Dec;93:44-54 [PMID: 26220838]
  161. Science. 1996 Oct 4;274(5284):66-7 [PMID: 8848724]
  162. J Gen Virol. 2001 Apr;82(Pt 4):693-712 [PMID: 11257174]
  163. PLoS Pathog. 2016 May 06;12(5):e1005610 [PMID: 27152966]
  164. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4533-7 [PMID: 212758]
  165. Lancet. 2015 Mar 21;385(9973):1124-35 [PMID: 25687730]
  166. Nat Rev Gastroenterol Hepatol. 2018 Sep;15(9):536-554 [PMID: 29904153]
  167. J Hepatol. 2018 Jun;68(6):1114-1122 [PMID: 29428874]
  168. J Virol. 2010 Jan;84(1):34-43 [PMID: 19828610]
  169. World J Gastroenterol. 2014 Mar 21;20(11):2971-8 [PMID: 24659888]
  170. J Clin Invest. 1999 Jul;104(2):203-12 [PMID: 10411550]
  171. Arch Virol. 2015 Mar;160(3):685-92 [PMID: 25559671]
  172. Nat Genet. 2012 May 27;44(7):765-9 [PMID: 22634754]
  173. Int J Exp Pathol. 2010 Feb;91(1):87-97 [PMID: 20096073]
  174. Proc Natl Acad Sci U S A. 2015 Dec 8;112(49):15190-5 [PMID: 26575627]
  175. Emerg Infect Dis. 2012 Aug;18(8):1369-70 [PMID: 22840220]
  176. Elife. 2018 May 10;7: [PMID: 29745896]
  177. Bioinformatics. 2003 Aug 12;19(12):1572-4 [PMID: 12912839]
  178. Ecohealth. 2019 Mar;16(1):82-94 [PMID: 30564998]
  179. J Viral Hepat. 2001 Jul;8(4):233-42 [PMID: 11454173]
  180. J Gen Virol. 2003 Jan;84(Pt 1):147-155 [PMID: 12533711]
  181. J Virol. 2012 Jul;86(14):7688-91 [PMID: 22553337]
  182. J Virol. 2016 Dec 16;91(1): [PMID: 27795428]
  183. ILAR J. 2017 Dec 1;58(2):172-189 [PMID: 29045731]
  184. Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):6914-6923 [PMID: 28630341]
  185. Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1661-4 [PMID: 10677515]
  186. PLoS Med. 2009 Feb 10;6(2):e31 [PMID: 19209955]
  187. Gastroenterology. 2009 May;136(5):1629-38 [PMID: 19208358]
  188. Genome Biol Evol. 2015 Oct 21;7(11):2996-3008 [PMID: 26494702]
  189. World J Gastroenterol. 2014 Jun 21;20(23):7152-68 [PMID: 24966586]
  190. Cell Host Microbe. 2017 Sep 13;22(3):387-399.e6 [PMID: 28867387]
  191. PLoS One. 2018 Jun 18;13(6):e0199200 [PMID: 29912972]
  192. Nat Med. 2005 Jul;11(7):791-6 [PMID: 15951748]
  193. mBio. 2016 Nov 8;7(6): [PMID: 27834208]
  194. J Virol. 2002 Apr;76(8):4034-43 [PMID: 11907242]
  195. J Clin Invest. 2010 Mar;120(3):924-30 [PMID: 20179355]
  196. J Virol. 1998 Aug;72(8):6621-8 [PMID: 9658108]
  197. J Med Virol. 2012 Sep;84(9):1396-407 [PMID: 22825818]
  198. J Clin Microbiol. 2001 Mar;39(3):918-23 [PMID: 11230404]
  199. Hepatology. 2012 Nov;56(5):1671-80 [PMID: 22610996]
  200. Proc Natl Acad Sci U S A. 2016 Apr 12;113(15):4170-5 [PMID: 27001840]
  201. Lancet. 1970 Apr 4;1(7649):695-8 [PMID: 4190997]
  202. Cell Host Microbe. 2014 Mar 12;15(3):266-82 [PMID: 24629334]
  203. Mol Biol Evol. 2018 Sep 1;35(9):2254-2259 [PMID: 29924338]
  204. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2233-7 [PMID: 3457384]
  205. J Infect Dis. 1988 Jul;158(1):151-9 [PMID: 3392412]
  206. Hepatology. 2007 Dec;46(6):1759-68 [PMID: 18046710]
  207. Vet Microbiol. 1999 Aug 16;68(1-2):119-25 [PMID: 10501168]
  208. Emerg Infect Dis. 2014 Jun;20(6):1044-8 [PMID: 24856611]
  209. N Engl J Med. 2011 Mar 31;364(13):1207-17 [PMID: 21449784]
  210. Hepatology. 2018 Apr;67(4):1560-1599 [PMID: 29405329]
  211. J Virol. 2012 Sep;86(17):9134-47 [PMID: 22696648]
  212. Lancet Infect Dis. 2011 Jan;11(1):45-56 [PMID: 21126914]
  213. Science. 2016 Sep 30;353(6307):1541-1545 [PMID: 27633528]
  214. J Carcinog. 2017 May 29;16:1 [PMID: 28694740]
  215. Nature. 1986 Oct 9-15;323(6088):558-60 [PMID: 2429192]
  216. J Gen Virol. 2010 Mar;91(Pt 3):750-8 [PMID: 19889929]
  217. PLoS One. 2013;8(3):e58340 [PMID: 23505490]
  218. Hepatology. 2015 Jan;61(1):77-87 [PMID: 25069599]
  219. Gut. 1977 Dec;18(12):997-1003 [PMID: 75123]
  220. Nature. 2016 Dec 22;540(7634):539-543 [PMID: 27880757]
  221. Antivir Ther. 2013;18(3 Pt B):489-96 [PMID: 23792884]
  222. J Med Virol. 2001 Aug;64(4):402-9 [PMID: 11468723]
  223. Vet Microbiol. 2015 Oct 22;180(1-2):15-21 [PMID: 26344041]
  224. Sci Rep. 2016 Feb 29;6:22361 [PMID: 26924426]
  225. Mol Biol Evol. 2016 Jul;33(7):1870-4 [PMID: 27004904]
  226. Semin Cancer Biol. 2013 Dec;23(6 Pt B):561-75 [PMID: 24013024]
  227. BMC Evol Biol. 2016 Oct 12;16(1):210 [PMID: 27733122]
  228. J Virol. 2016 Sep 12;90(19):8866-74 [PMID: 27466423]
  229. J Gen Virol. 1988 Jun;69 ( Pt 6):1383-9 [PMID: 2838576]
  230. J Virol. 2016 Aug 12;90(17):7920-33 [PMID: 27334580]
  231. Science. 1998 Oct 30;282(5390):938-41 [PMID: 9794763]
  232. Oecologia. 2018 Sep;188(1):289-302 [PMID: 29936542]
  233. J Virol. 2004 Sep;78(18):9782-9 [PMID: 15331711]
  234. J Med Virol. 2007 Nov;79(11):1741-50 [PMID: 17854046]
  235. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3401-5 [PMID: 7724574]
  236. J Infect Dis. 1989 Apr;159(4):621-4 [PMID: 2538518]
  237. Science. 1989 Apr 21;244(4902):359-62 [PMID: 2523562]
  238. Curr Opin Virol. 2011 Dec;1(6):649-57 [PMID: 22440923]
  239. J Virol. 2016 Nov 14;90(23):10670-10681 [PMID: 27654291]
  240. Science. 2005 Oct 28;310(5748):676-9 [PMID: 16195424]
  241. J Med Virol. 2009 Aug;81(8):1371-9 [PMID: 19551838]
  242. J Clin Microbiol. 2015 Mar;53(3):967-72 [PMID: 25520447]
  243. Infect Genet Evol. 2011 Aug;11(6):1462-8 [PMID: 21645647]
  244. Nat Commun. 2013;4:1791 [PMID: 23653203]
  245. N Engl J Med. 2011 Sep 15;365(11):1014-24 [PMID: 21916639]
  246. Mol Cell Biol. 1993 Jan;13(1):659-67 [PMID: 8380230]
  247. World J Gastroenterol. 2014 Jun 28;20(24):7622-34 [PMID: 24976700]
  248. J Gen Virol. 1999 Mar;80 ( Pt 3):681-690 [PMID: 10092008]
  249. J Infect Dis. 1975 Nov;132(5):532-45 [PMID: 171320]
  250. Nature. 1996 Apr 4;380(6573):454-6 [PMID: 8602246]
  251. Infect Immun. 1983 May;40(2):766-72 [PMID: 6840861]
  252. J Virol. 2018 Jun 13;92(13): [PMID: 29695421]

MeSH Term

Animals
Antiviral Agents
Biological Evolution
Drug Development
Hepatitis Viruses
Hepatitis, Animal
Hepatitis, Viral, Human
Humans
Models, Animal
Viral Hepatitis Vaccines

Chemicals

Antiviral Agents
Viral Hepatitis Vaccines

Word Cloud

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