Cross talk between nucleotide synthesis pathways with cellular immunity in constraining hepatitis e virus replication

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 5, 2016, Pages 2834-2848

  Wang, Yijin ^a   Wang, Wenshi ^a   Xu, Lei ^a   Zhou, Xinying ^a   Shokrollahi, Ehsan ^a   Felczak, Krzysztof ^b   Van Der Laan, Luc J W ^a   Pankiewicz, Krzysztof W ^b   Sprengers, Dave ^a   Raat, Nicolaas J H ^a   Metselaar, Herold J ^a   Peppelenbosch, Maikel P ^a   Pan, Qiuwei ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE; MYCOPHENOLIC ACID; PURINE NUCLEOTIDE; PYRIMIDINE; RIBAVIRIN; STAT PROTEIN; ALPHA INTERFERON; ANTIVIRUS AGENT; GUANOSINE; INOSINATE DEHYDROGENASE; NUCLEOTIDE; URIDINE;

ANTIVIRAL ACTIVITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; HEK293 CELL LINE; HEPATITIS E; HEPATITIS E VIRUS; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PURINE SYNTHESIS; PYRIMIDINE SYNTHESIS; VIRUS REPLICATION; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANTIVIRAL AGENTS; CELL LINE, TUMOR; GUANOSINE; HEPATITIS E VIRUS; HUMANS; IMMUNITY, CELLULAR; IMP DEHYDROGENASE; INTERFERON-ALPHA; MYCOPHENOLIC ACID; NUCLEOTIDES; RIBAVIRIN; URIDINE; VIRUS REPLICATION;

EID: 84964978281     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02700-15     Document Type: Article

References (61)

1. Kamar N, Bendall R, Legrand-Abravanel F, Xia NS, Ijaz S, Izopet J, Dalton HR. 2012. Hepatitis E. Lancet 379:2477-2488. http://dx.doi.org /10.1016/S0140-6736(11)61849-7.
2. Kamar N, Selves J, Mansuy JM, Ouezzani L, Peron JM, Guitard J, Cointault O, Esposito L, Abravanel F, Danjoux M, Durand D, Vinel JP, Izopet J, Rostaing L. 2008. Hepatitis E virus and chronic hepatitis in organ-transplant recipients.NEngl J Med 358:811-817. http://dx.doi.org /10.1056/NEJMoa0706992.
3. Zhou X, de Man RA, de Knegt RJ, Metselaar HJ, Peppelenbosch MP, Pan Q. 2013. Epidemiology and management of chronic hepatitis E infection in solid organ transplantation: a comprehensive literature review. Rev Med Virol 23:295-304. http://dx.doi.org/10.1002/rmv.1751.
4. Kamar N, Garrouste C, Haagsma EB, Garrigue V, Pischke S, Chauvet C, Dumortier J, Cannesson A, Cassuto-Viguier E, Thervet E, Conti F, Lebray P, Dalton HR, Santella R, Kanaan N, Essig M, Mousson C, Radenne S, Roque-Afonso AM, Izopet J, Rostaing L. 2011. Factors associated with chronic hepatitis in patients with hepatitis E virus infection who have received solid organ transplants. Gastroenterology 140: 1481-1489. http://dx.doi.org/10.1053/j.gastro.2011.02.050.
5. van der Eijk AA, Pas SD, Cornelissen JJ, de Man RA. 2014. Hepatitis E virus infection in hematopoietic stem cell transplant recipients. Curr Opin Infect Dis 27:309-315. http://dx.doi.org/10.1097/QCO.0000000000000076.
6. Lane AN, Fan TW. 2015. Regulation of mammalian nucleotide metabolism and biosynthesis. Nucleic Acids Res 43:2466-2485. http://dx.doi.org /10.1093/nar/gkv047.
7. Moffatt BA, Ashihara H. 2002. Purine and pyrimidine nucleotide synthesis and metabolism. Arabidopsis Book 1:e0018. http://dx.doi.org/10 .1199/tab.0018.
8. Blakley RL, Vitols E. 1968. The control of nucleotide biosynthesis. Annu Rev Biochem 37:201-224. http://dx.doi.org/10.1146/annurev.bi.37.0701 68.001221.
9. Christopherson RI, Lyons SD, Wilson PK. 2002. Inhibitors of de novo nucleotide biosynthesis as drugs. Acc Chem Res 35:961-971. http://dx.doi .org/10.1021/ar0000509.
10. Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Goncales FL, Jr, Haussinger D, Diago M, Carosi G, Dhumeaux D, Craxi A, Lin A, Hoffman J, Yu J. 2002. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 347:975-982. http://dx.doi.org /10.1056/NEJMoa020047.
11. Avery RK, Bolwell BJ, Yen-Lieberman B, Lurain N, Waldman WJ, Longworth DL, Taege AJ, Mossad SB, Kohn D, Long JR, Curtis J, Kalaycio M, Pohlman B, Williams JW. 2004. Use of leflunomide in an allogeneic bone marrow transplant recipient with refractory cytomegalovirus infection. Bone Marrow Transplant 34:1071-1075. http://dx.doi.org /10.1038/sj.bmt.1704694.
12. Farasati NA, Shapiro R, Vats A, Randhawa P. 2005. Effect of leflunomide and cidofovir on replication of BK virus in an in vitro culture system. Transplantation 79:116-118. http://dx.doi.org/10.1097/01.TP.0000149 338.97084.5F.
13. Chong AS, Zeng H, Knight DA, Shen J, Meister GT, Williams JW, Waldman WJ. 2006. Concurrent antiviral and immunosuppressive activities of leflunomide in vivo. Am J Transplant 6:69-75. http://dx.doi.org /10.1111/j.1600-6143.2005.01152.x.
14. Takhampunya R, Ubol S, Houng HS, Cameron CE, Padmanabhan R. 2006. Inhibition of dengue virus replication by mycophenolic acid and ribavirin. J Gen Virol 87:1947-1952. http://dx.doi.org/10.1099/vir.0.81655-0.
15. Ying C, Colonno R, De Clercq E, Neyts J. 2007. Ribavirin and mycophenolic acid markedly potentiate the anti-hepatitis B virus activity of entecavir. Antiviral Res 73:192-196. http://dx.doi.org/10.1016/j.antiviral .2006.10.003.
16. Wang QY, Bushell S, Qing M, Xu HY, Bonavia A, Nunes S, Zhou J, Poh MK, Florez de Sessions P, Niyomrattanakit P, Dong H, Hoffmaster K, Goh A, Nilar S, Schul W, Jones S, Kramer L, Compton T, Shi PY. 2011. Inhibition of dengue virus through suppression of host pyrimidine biosynthesis. J Virol 85:6548-6556. http://dx.doi.org/10 .1128/JVI.02510-10.
17. Hoppe-Seyler K, Sauer P, Lohrey C, Hoppe-Seyler F. 2012. The inhibitors of nucleotide biosynthesis leflunomide, FK778, and mycophenolic acid activate hepatitis B virus replication in vitro. Hepatology 56:9-16. http://dx.doi.org/10.1002/hep.25602.
18. Wang Y, Zhou X, Debing Y, Chen K, Van Der Laan LJ, Neyts J, Janssen HL, Metselaar HJ, Peppelenbosch MP, Pan Q. 2014. Calcineurin inhibitors stimulate and mycophenolic acid inhibits replication of hepatitis E virus. Gastroenterology 146:1775-1783. http://dx.doi.org/10.1053/j .gastro.2014.02.036.
19. Pan Q, de Ruiter PE, Metselaar HJ, Kwekkeboom J, de Jonge J, Tilanus HW, Janssen HL, van der Laan LJ. 2012. Mycophenolic acid augments interferon-stimulated gene expression and inhibits hepatitis C virus infection in vitro and in vivo. Hepatology 55:1673-1683. http://dx.doi.org/10 .1002/hep.25562.
20. Debing Y, Emerson SU, Wang Y, Pan Q, Balzarini J, Dallmeier K, Neyts J. 2014. Ribavirin inhibits in vitro hepatitis E virus replication through depletion of cellular GTP pools and is moderately synergistic with alpha interferon. Antimicrob Agents Chemother 58:267-273. http://dx.doi.org /10.1128/AAC.01795-13.
21. Leyssen P, De Clercq E, Neyts J. 2006. The anti-yellow fever virus activity of ribavirin is independent of error-prone replication. Mol Pharmacol 69:1461-1467. http://dx.doi.org/10.1124/mol.105.020057.
22. Qing M, Zou G, Wang QY, Xu HY, Dong H, Yuan Z, Shi PY. 2010. Characterization of dengue virus resistance to brequinar in cell culture. Antimicrob Agents Chemother 54:3686-3695. http://dx.doi.org/10.1128 /AAC.00561-10.
23. Lucas-Hourani M, Dauzonne D, Jorda P, Cousin G, Lupan A, Helynck O, Caignard G, Janvier G, Andre-Leroux G, Khiar S, Escriou N, Despres P, Jacob Y, Munier-Lehmann H, Tangy F, Vidalain PO. 2013. Inhibition of pyrimidine biosynthesis pathway suppresses viral growth through innate immunity. PLoS Pathog 9:e1003678. http://dx.doi.org/10.1371 /journal.ppat.1003678.
24. Nelson JA, Carpenter JW, Rose LM, Adamson DJ. 1975. Mechanisms of action of 6-thioguanine, 6-mercaptopurine, and 8-azaguanine. Cancer Res 35:2872-2878.
25. Beardsley GP, Moroson BA, Taylor EC, Moran RG. 1989. A new folate antimetabolite, 5,10-dideaza-5,6,7,8-tetrahydrofolate is a potent inhibitor of de novo purine synthesis. J Biol Chem 264:328-333.
26. Pizzorno G, Moroson BA, Cashmore AR, Beardsley GP. 1991. (6R)- 5,10-Dideaza-5,6,7,8-tetrahydrofolic acid effects on nucleotide metabolism in CCRF-CEM human T-lymphoblast leukemia cells. Cancer Res 51:2291-2295.
27. Budzik GP, Colletti LM, Faltynek CR. 2000. Effects of methotrexate on nucleotide pools in normal human T cells and the CEM T cell line. Life Sci 66:2297-2307. http://dx.doi.org/10.1016/S0024-3205(00)00559-2.
28. Carr SF, Papp E, Wu JC, Natsumeda Y. 1993. Characterization of human type I and type II IMP dehydrogenases. J Biol Chem 268:27286-27290.
29. Silva HT, Jr, Cao W, Shorthouse RA, Loffler M, Morris RE. 1997. In vitro and in vivo effects of leflunomide, brequinar, and cyclosporine on pyrimidine biosynthesis. Transplant Proc 29:1292-1293. http://dx.doi .org/10.1016/S0041-1345(96)00523-4.
30. Greene S, Watanabe K, Braatz-Trulson J, Lou L. 1995. Inhibition of dihydroorotate dehydrogenase by the immunosuppressive agent leflunomide. Biochem Pharmacol 50:861-867. http://dx.doi.org/10.1016/0006-2952(95)00255-X.
31. Lopez JM, Marks CL, Freese E. 1979. The decrease of guanine nucleotides initiates sporulation of Bacillus subtilis. Biochim Biophys Acta 587:238-252. http://dx.doi.org/10.1016/0304-4165(79)90357-X.
32. Seo JY, Yaneva R, Hinson ER, Cresswell P. 2011. Human mtt megalovirus directly induces the antiviral protein viperin to enhance infectivity. Science 332:1093-1097. http://dx.doi.org/10.1126/science.1202007.
33. Rawling DC, Fitzgerald ME, Pyle AM. 2015. Establishing the role of ATP for the function of the RIG-I innate immune sensor. eLife 4:e09391. http: //dx.doi.org/10.7554/eLife.09391.
34. Pawlotsky JM, Dahari H, Neumann AU, Hezode C, Germanidis G, Lonjon I, Castera L, Dhumeaux D. 2004. Antiviral action of ribavirin in chronic hepatitis C. Gastroenterology 126:703-714. http://dx.doi.org/10 .1053/j.gastro.2003.12.002.
35. Poynard T, Marcellin P, Lee SS, Niederau C, Minuk GS, Ideo G, Bain V, Heathcote J, Zeuzem S, Trepo C, Albrecht J. 1998. Randomised trial of interferon alpha2b plus ribavirin for 48 weeks or for 24 weeks versus interferon alpha2b plus placebo for 48 weeks for treatment of chronic infection with hepatitis C virus. International Hepatitis Interventional Therapy Group (IHIT). Lancet 352:1426-1432.
36. Kamar N, Izopet J, Tripon S, Bismuth M, Hillaire S, Dumortier J, Radenne S, Coilly A, Garrigue V, D'Alteroche L, Buchler M, Couzi L, Lebray P, Dharancy S, Minello A, Hourmant M, Roque-Afonso AM, Abravanel F, Pol S, Rostaing L, Mallet V. 2014. Ribavirin for chronic hepatitis E virus infection in transplant recipients. N Engl J Med 370: 1111-1120. http://dx.doi.org/10.1056/NEJMoa1215246.
37. Tam RC, Lau JY, Hong Z. 2001. Mechanisms of action of ribavirin in antiviral therapies. Antivir Chem Chemother 12:261-272. http://dx.doi .org/10.1177/095632020101200501.
38. Paeshuyse J, Dallmeier K, Neyts J. 2011. Ribavirin for the treatment of chronic hepatitis C virus infection: a review of the proposed mechanisms of action. Curr Opin Virol 1:590-598. http://dx.doi.org/10.1016/j.coviro .2011.10.030.
39. Feld JJ, Hoofnagle JH. 2005. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436:967-972. http://dx.doi .org/10.1038/nature04082.
40. Manzia TM, De Liguori Carino N, Orlando G, Toti L, De Luca L, D'Andria D, Cardillo A, Anselmo A, Casciani CU, Tisone G. 2005. Use of mycophenolate mofetil in liver transplantation: a literature review. Transplant Proc 37:2616-2617. http://dx.doi.org/10.1016/j.transproceed .2005.06.073.
41. Pischke S, Stiefel P, Franz B, Bremer B, Suneetha PV, Heim A, Ganzenmueller T, Schlue J, Horn-Wichmann R, Raupach R, Darnedde M, Scheibner Y, Taubert R, Haverich A, Manns MP, Wedemeyer H, Bara CL. 2012. Chronic hepatitis E in heart transplant recipients. Am J Transplant 12:3128-3133. http://dx.doi.org/10.1111/j.1600-6143.2012.04200.x.
42. Kamar N, Lhomme S, Abravanel F, Cointault O, Esposito L, Cardeau-Desangles I, Del Bello A, Dorr G, Lavayssiere L, Nogier MB, Guitard J, Ribes D, Goin AL, Broue P, Metsu D, Saune K, Rostaing L, Izopet J. 2015. An early viral response predicts the virological response to ribavirin in hepatitis E virus organ transplant patients. Transplantation 99:2124-2131. http://dx.doi.org/10.1097/TP .0000000000000850.
43. Hoffmann HH, Kunz A, Simon VA, Palese P, Shaw ML. 2011. Broadspectrum antiviral that interferes with de novo pyrimidine biosynthesis. Proc Natl Acad Sci U S A 108:5777-5782. http://dx.doi.org/10.1073/pnas .1101143108.
44. Chong AS, Rezai K, Gebel HM, Finnegan A, Foster P, Xu X, Williams JW. 1996. Effects of leflunomide and other immunosuppressive agents on T cell proliferation in vitro. Transplantation 61:140-145. http://dx.doi .org/10.1097/00007890-199601150-00026.
45. Xu X, Williams JW, Shen J, Gong H, Yin DP, Blinder L, Elder RT, Sankary H, Finnegan A, Chong AS. 1998. In vitro and in vivo mechanisms of action of the antiproliferative and immunosuppressive agent, brequinar sodium. J Immunol 160:846-853.
46. Cherwinski HM, Cohn RG, Cheung P, Webster DJ, Xu YZ, Caulfield JP, Young JM, Nakano G, Ransom JT. 1995. The immunosuppressant leflunomide inhibits lymphocyte proliferation by inhibiting pyrimidine biosynthesis. J Pharmacol Exp Ther 275:1043-1049.
47. Makowka L, Sher LS, Cramer DV. 1993. The development of brequinar as an immunosuppressive drug for transplantation. Immunol Rev 136: 51-70. http://dx.doi.org/10.1111/j.1600-065X.1993.tb00654.x.
48. Cramer DV, Chapman FA, Makowka L. 1993. The use of brequinar sodium for transplantation. Ann N Y Acad Sci 696:216-226.
49. Cramer DV, Chapman FA, Jaffee BD, Jones EA, Knoop M, Hreha-Eiras G, Makowka L. 1992. The effect of a new immunosuppressive drug, brequinar sodium, on heart, liver, and kidney allograft rejection in the rat. Transplantation 53:303-308. http://dx.doi.org/10.1097/00007890-1992 02010-00009.
50. Chon WJ, Josephson MA. 2011. Leflunomide in renal transplantation. Expert Rev Clin Immunol 7:273-281. http://dx.doi.org/10.1586/eci.11.20.
51. Boa AN, Canavan SP, Hirst PR, Ramsey C, Stead AM, McConkey GA. 2005. Synthesis of brequinar analogue inhibitors of malaria parasite dihydroorotate dehydrogenase. Bioorg Med Chem 13:1945-1967. http://dx .doi.org/10.1016/j.bmc.2005.01.017.
52. Leban J, Vitt D. 2011. Human dihydroorotate dehydrogenase inhibitors, a novel approach for the treatment of autoimmune and inflammatory diseases. Arzneimittelforschung 61:66-72. http://dx.doi.org/10.1055/s -0031-1296169.
53. Baumann P, Mandl-Weber S, Volkl A, Adam C, Bumeder I, Oduncu F, Schmidmaier R. 2009. Dihydroorotate dehydrogenase inhibitor A771726 (leflunomide) induces apoptosis and diminishes proliferation of multiple myeloma cells. Mol Cancer Ther 8:366-375. http://dx.doi.org/10.1158 /1535-7163.MCT-08-0664.
54. Herrmann ML, Schleyerbach R, Kirschbaum BJ. 2000. Leflunomide: an immunomodulatory drug for the treatment of rheumatoid arthritis and other autoimmune diseases. Immunopharmacology 47:273-289. http: //dx.doi.org/10.1016/S0162-3109(00)00191-0.
55. Norman P. 2013. Evaluation of WO2013076170: the use of a dihydroorotate dehydrogenase inhibitor for the treatment of psoriasis. Expert Opin Ther Pat 23:1391-1394. http://dx.doi.org/10.1517/13543776 .2013.831075.
56. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485. http://dx.doi.org/10 .1038/nature09907.
57. Schoggins JW, MacDuff DA, Imanaka N, Gainey MD, Shrestha B, Eitson JL, Mar KB, Richardson RB, Ratushny AV, Litvak V, Dabelic R, Manicassamy B, Aitchison JD, Aderem A, Elliott RM, Garcia- Sastre A, Racaniello V, Snijder EJ, Yokoyama WM, Diamond MS, Virgin HW, Rice CM. 2014. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505:691-695. http://dx.doi.org/10.1038/nature12862.
58. Thomas E, Feld JJ, Li Q, Hu Z, Fried MW, Liang TJ. 2011. Ribavirin potentiates interferon action by augmenting interferon-stimulated gene induction in hepatitis C virus cell culture models. Hepatology 53:32-41. http://dx.doi.org/10.1002/hep.23985.
59. Stewart CE, Randall RE, Adamson CS. 2014. Inhibitors of the interferon response enhance virus replication in vitro. PLoS One 9:e112014. http: //dx.doi.org/10.1371/journal.pone.0112014.
60. Leaman DW, Pisharody S, Flickinger TW, Commane MA, Schlessinger J, Kerr IM, Levy DE, Stark GR. 1996. Roles of JAKs in activation of STATs and stimulation of c-fos gene expression by epidermal growth factor. Mol Cell Biol 16:369-375. http://dx.doi.org/10 .1128/MCB.16.1.369.
61. Shresta S, Sharar KL, Prigozhin DM, Snider HM, Beatty PR, Harris E. 2005. Critical roles for both STAT1-dependent and STAT1-independent pathways in the control of primary dengue virus infection in mice. J Immunol 175:3946-3954. http://dx.doi.org/10.4049/jimmunol.175.6.3946.