1,083
Views
12
CrossRef citations to date
0
Altmetric
Research Paper

Cimetidine synergizes with Praziquantel to enhance the immune response of HBV DNA vaccine via activating cytotoxic CD8+ T cell

, , , , &
Pages 1688-1699 | Received 17 Jan 2014, Accepted 12 Mar 2014, Published online: 18 Mar 2014

References

  • Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol 2005; 5:215 - 29; http://dx.doi.org/10.1038/nri1573; PMID: 15738952
  • Lok AS. Chronic hepatitis B. N Engl J Med 2002; 346:1682 - 3; http://dx.doi.org/10.1056/NEJM200205303462202; PMID: 12037146
  • Chan CY, Lee SD, Lo KJ. Legend of hepatitis B vaccination: the Taiwan experience. J Gastroenterol Hepatol 2004; 19:121 - 6; http://dx.doi.org/10.1111/j.1440-1746.2004.03153.x; PMID: 14731119
  • van Zonneveld M, Honkoop P, Hansen BE, Niesters HG, Darwish Murad S, de Man RA, Schalm SW, Janssen HL. Long-term follow-up of alpha-interferon treatment of patients with chronic hepatitis B. Hepatology 2004; 39:804 - 10; http://dx.doi.org/10.1002/hep.20128; PMID: 14999700
  • Chan HL, Tang JL, Tam W, Sung JJ. The efficacy of thymosin in the treatment of chronic hepatitis B virus infection: a meta-analysis. Aliment Pharmacol Ther 2001; 15:1899 - 905; http://dx.doi.org/10.1046/j.1365-2036.2001.01135.x; PMID: 11736720
  • Papatheodoridis GV, Dimou E, Papadimitropoulos V. Nucleoside analogues for chronic hepatitis B: antiviral efficacy and viral resistance. Am J Gastroenterol 2002; 97:1618 - 28; http://dx.doi.org/10.1111/j.1572-0241.2002.05819.x; PMID: 12135009
  • Wong DK, Cheung AM, O’Rourke K, Naylor CD, Detsky AS, Heathcote J. Effect of alpha-interferon treatment in patients with hepatitis B e antigen-positive chronic hepatitis B. A meta-analysis. Ann Intern Med 1993; 119:312 - 23; http://dx.doi.org/10.7326/0003-4819-119-4-199308150-00011; PMID: 8328741
  • MacGregor RR, Boyer JD, Ugen KE, Lacy KE, Gluckman SJ, Bagarazzi ML, Chattergoon MA, Baine Y, Higgins TJ, Ciccarelli RB, et al. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J Infect Dis 1998; 178:92 - 100; http://dx.doi.org/10.1086/515613; PMID: 9652427
  • Kutzler MA, Weiner DB. DNA vaccines: ready for prime time?. Nat Rev Genet 2008; 9:776 - 88; http://dx.doi.org/10.1038/nrg2432; PMID: 18781156
  • Chow YH, Huang WL, Chi WK, Chu YD, Tao MH. Improvement of hepatitis B virus DNA vaccines by plasmids coexpressing hepatitis B surface antigen and interleukin-2. J Virol 1997; 71:169 - 78; PMID: 8985336
  • Mancini M, Hadchouel M, Davis HL, Whalen RG, Tiollais P, Michel ML. DNA-mediated immunization in a transgenic mouse model of the hepatitis B surface antigen chronic carrier state. Proc Natl Acad Sci USA 1996; 93:12496 - 501; http://dx.doi.org/10.1073/pnas.93.22.12496; PMID: 8901610
  • Davis HL, McCluskie MJ, Gerin JL, Purcell RH. DNA vaccine for hepatitis B: evidence for immunogenicity in chimpanzees and comparison with other vaccines. Proc Natl Acad Sci U S A 1996; 93:7213 - 8; http://dx.doi.org/10.1073/pnas.93.14.7213; PMID: 8692971
  • Tacket CO, Roy MJ, Widera G, Swain WF, Broome S, Edelman R. Phase 1 safety and immune response studies of a DNA vaccine encoding hepatitis B surface antigen delivered by a gene delivery device. Vaccine 1999; 17:2826 - 9; http://dx.doi.org/10.1016/S0264-410X(99)00094-8; PMID: 10438052
  • Greenland JR, Letvin NL. Chemical adjuvants for plasmid DNA vaccines. Vaccine 2007; 25:3731 - 41; http://dx.doi.org/10.1016/j.vaccine.2007.01.120; PMID: 17350735
  • Geng S, Zhong Y, Wang S, Liu H, Zou Q, Xie X, Li C, Yu Q, He Z, Wang B. Amiloride enhances antigen specific CTL by faciliting HBV DNA vaccine entry into cells. PLoS One 2012; 7:e33015; http://dx.doi.org/10.1371/journal.pone.0033015; PMID: 22438887
  • Jin H, Li Y, Ma Z, Zhang F, Xie Q, Gu D, Wang B. Effect of chemical adjuvants on DNA vaccination. Vaccine 2004; 22:2925 - 35; http://dx.doi.org/10.1016/j.vaccine.2003.12.026; PMID: 15246629
  • Cioli D, Pica-Mattoccia L.. Praziquantel. Parasitology Research 2003; 90:Supp 1 S3 9; PMID: 12811543
  • Pearson RD, Guerrant RL. Praziquantel: a major advance in anthelminthic therapy. Ann Intern Med 1983; 99:195 - 8; http://dx.doi.org/10.7326/0003-4819-99-2-195; PMID: 6881777
  • Zou Q, Yao X, Feng J, Yin Z, Flavell R, Hu Y, Zheng G, Jin J, Kang Y, Wu B, et al. Praziquantel facilitates IFN-γ-producing CD8+ T cells (Tc1) and IL-17-producing CD8+ T cells (Tc17) responses to DNA vaccination in mice. PLoS One 2011; 6:e25525; http://dx.doi.org/10.1371/journal.pone.0025525; PMID: 21998665
  • Zou Q, Hu Y, Xue J, Fan X, Jin Y, Shi X, Meng D, Wang X, Feng C, Xie X, et al. Use of praziquantel as an adjuvant enhances protection and Tc-17 responses to killed H5N1 virus vaccine in mice. PLoS One 2012; 7:e34865; http://dx.doi.org/10.1371/journal.pone.0034865; PMID: 22529945
  • Bodemar G, Walan A. Maintenance treatment of recurrent peptic ulcer by cimetidine. Lancet 1978; 1:403 - 7; http://dx.doi.org/10.1016/S0140-6736(78)91200-X; PMID: 75439
  • O’Mahony L, Akdis M, Akdis CA. Regulation of the immune response and inflammation by histamine and histamine receptors. J Allergy Clin Immunol 2011; 128:1153 - 62; http://dx.doi.org/10.1016/j.jaci.2011.06.051; PMID: 21824648
  • Li MJ, Lei JH, Wang T, Lu SJ, Guan F, Liu WQ, Li YL. Cimetidine enhances the protective effect of GST DNA vaccine against Schistosoma japonicum. Exp Parasitol 2011; 128:427 - 32; http://dx.doi.org/10.1016/j.exppara.2011.05.012; PMID: 21624364
  • Wang J, Su B, Ding Z, Du X, Wang B. Cimetidine enhances immune response of HBV DNA vaccination via impairment of the regulatory function of regulatory T cells. Biochem Biophys Res Commun 2008; 372:491 - 6; http://dx.doi.org/10.1016/j.bbrc.2008.04.191; PMID: 18502198
  • Steiner K, Garbe A, Diekmann HW, Nowak H. The fate of praziquantel in the organism I. Pharmacokinetics in animals. Eur J Drug Metab Pharmacokinet 1976; 1:85 - 95; http://dx.doi.org/10.1007/BF03189262
  • Knodell RG, Browne DG, Gwozdz GP, Brian WR, Guengerich FP. Differential inhibition of individual human liver cytochromes P-450 by cimetidine. Gastroenterology 1991; 101:1680 - 91; PMID: 1955133
  • Dachman WD, Adubofour KO, Bikin DS, Johnson CH, Mullin PD, Winograd M. Cimetidine-induced rise in praziquantel levels in a patient with neurocysticercosis being treated with anticonvulsants. J Infect Dis 1994; 169:689 - 91; http://dx.doi.org/10.1093/infdis/169.3.689; PMID: 8158054
  • Grabbe S, Schwarz T. Immunoregulatory mechanisms involved in elicitation of allergic contact hypersensitivity. Immunol Today 1998; 19:37 - 44; http://dx.doi.org/10.1016/S0167-5699(97)01186-9; PMID: 9465487
  • Maini MK, Boni C, Ogg GS, King AS, Reignat S, Lee CK, Larrubia JR, Webster GJM, McMichael AJ, Ferrari C, et al. Direct ex vivo analysis of hepatitis B virus-specific CD8(+) T cells associated with the control of infection. Gastroenterology 1999; 117:1386 - 96; http://dx.doi.org/10.1016/S0016-5085(99)70289-1; PMID: 10579980
  • Alatrakchi N, Koziel M. Regulatory T cells and viral liver disease. J Viral Hepat 2009; 16:223 - 9; http://dx.doi.org/10.1111/j.1365-2893.2009.01081.x; PMID: 19222744
  • Xu D, Fu J, Jin L, Zhang H, Zhou C, Zou Z, Zhao JM, Zhang B, Shi M, Ding X, et al. Circulating and liver resident CD4+CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B. J Immunol 2006; 177:739 - 47; PMID: 16785573
  • Furuichi Y, Tokuyama H, Ueha S, Kurachi M, Moriyasu F, Kakimi K. Depletion of CD25+CD4+T cells (Tregs) enhances the HBV-specific CD8+ T cell response primed by DNA immunization. World J Gastroenterol 2005; 11:3772 - 7; PMID: 15968737
  • Chisari FV, Pinkert CA, Milich DR, Filippi P, McLachlan A, Palmiter RD, Brinster RL. A transgenic mouse model of the chronic hepatitis B surface antigen carrier state. Science 1985; 230:1157 - 60; http://dx.doi.org/10.1126/science.3865369; PMID: 3865369
  • Kakimi K, Isogawa M, Chung J, Sette A, Chisari FV. Immunogenicity and tolerogenicity of hepatitis B virus structural and nonstructural proteins: implications for immunotherapy of persistent viral infections. J Virol 2002; 76:8609 - 20; http://dx.doi.org/10.1128/JVI.76.17.8609-8620.2002; PMID: 12163580
  • Liang M, Ma S, Hu X, Zhou B, Zhang J, Chen J, Wang Z, Sun J, Zhu X, Abbott W, et al. Cellular immune responses in patients with hepatitis B surface antigen seroclearance induced by antiviral therapy. Virol J 2011; 8:69; http://dx.doi.org/10.1186/1743-422X-8-69; PMID: 21320337
  • Carey I, D’Antiga L, Bansal S, Longhi MS, Ma Y, Mesa IR, Mieli-Vergani G, Vergani D. Immune and viral profile from tolerance to hepatitis B surface antigen clearance: a longitudinal study of vertically hepatitis B virus-infected children on combined therapy. J Virol 2011; 85:2416 - 28; http://dx.doi.org/10.1128/JVI.01449-10; PMID: 21147914
  • Rehermann B, Lau D, Hoofnagle JH, Chisari FV. Cytotoxic T lymphocyte responsiveness after resolution of chronic hepatitis B virus infection. J Clin Invest 1996; 97:1655 - 65; http://dx.doi.org/10.1172/JCI118592; PMID: 8601631
  • Thimme R, Wieland S, Steiger C, Ghrayeb J, Reimann KA, Purcell RH, Chisari FV. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 2003; 77:68 - 76; http://dx.doi.org/10.1128/JVI.77.1.68-76.2003; PMID: 12477811
  • Maini MK, Boni C, Lee CK, Larrubia JR, Reignat S, Ogg GS, King AS, Herberg J, Gilson R, Alisa A, et al. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J Exp Med 2000; 191:1269 - 80; http://dx.doi.org/10.1084/jem.191.8.1269; PMID: 10770795
  • Sad S, Marcotte R, Mosmann TR. Cytokine-induced differentiation of precursor mouse CD8+ T cells into cytotoxic CD8+ T cells secreting Th1 or Th2 cytokines. Immunity 1995; 2:271 - 9; http://dx.doi.org/10.1016/1074-7613(95)90051-9; PMID: 7697544
  • Intlekofer AM, Banerjee A, Takemoto N, Gordon SM, Dejong CS, Shin H, Hunter CA, Wherry EJ, Lindsten T, Reiner SL. Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 2008; 321:408 - 11; http://dx.doi.org/10.1126/science.1159806; PMID: 18635804
  • Phillips S, Chokshi S, Riva A, Evans A, Williams R, Naoumov NV. CD8(+) T cell control of hepatitis B virus replication: direct comparison between cytolytic and noncytolytic functions. J Immunol 2010; 184:287 - 95; http://dx.doi.org/10.4049/jimmunol.0902761; PMID: 19949099
  • Guidotti LG, Ishikawa T, Hobbs MV, Matzke B, Schreiber R, Chisari FV. Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity 1996; 4:25 - 36; http://dx.doi.org/10.1016/S1074-7613(00)80295-2; PMID: 8574849
  • Appay V, Nixon DF, Donahoe SM, Gillespie GM, Dong T, King A, Ogg GS, Spiegel HM, Conlon C, Spina CA, et al. HIV-specific CD8(+) T cells produce antiviral cytokines but are impaired in cytolytic function. J Exp Med 2000; 192:63 - 75; http://dx.doi.org/10.1084/jem.192.1.63; PMID: 10880527
  • Tagawa Y, Sekikawa K, Iwakura Y. Suppression of concanavalin A-induced hepatitis in IFN-gamma(-/-) mice, but not in TNF-alpha(-/-) mice: role for IFN-gamma in activating apoptosis of hepatocytes. J Immunol 1997; 159:1418 - 28; PMID: 9233639
  • Roth E, Pircher H. IFN-γ promotes Fas ligand- and perforin-mediated liver cell destruction by cytotoxic CD8 T cells. J Immunol 2004; 172:1588 - 94; PMID: 14734739
  • Roth E, Pircher H. IFN-gamma promotes Fas ligand- and perforin-mediated liver cell destruction by cytotoxic CD8 T cells. J Immunol 2004; 172:1588 - 94; PMID: 14734739
  • Spanaus KS, Schlapbach R, Fontana A. TNF-alpha and IFN-gamma render microglia sensitive to Fas ligand-induced apoptosis by induction of Fas expression and down-regulation of Bcl-2 and Bcl-xL. Eur J Immunol 1998; 28:4398 - 408; http://dx.doi.org/10.1002/(SICI)1521-4141(199812)28:12<4398::AID-IMMU4398>3.0.CO;2-Y; PMID: 9862377
  • Yeh N, Glosson NL, Wang N, Guindon L, McKinley C, Hamada H, Li Q, Dutton RW, Shrikant P, Zhou B, et al. Tc17 cells are capable of mediating immunity to vaccinia virus by acquisition of a cytotoxic phenotype. J Immunol 2010; 185:2089 - 98; http://dx.doi.org/10.4049/jimmunol.1000818; PMID: 20624947
  • Hinrichs CS, Kaiser A, Paulos CM, Cassard L, Sanchez-Perez L, Heemskerk B, Wrzesinski C, Borman ZA, Muranski P, Restifo NP. Type 17 CD8+ T cells display enhanced antitumor immunity. Blood 2009; 114:596 - 9; http://dx.doi.org/10.1182/blood-2009-02-203935; PMID: 19471017
  • Wu B, Zou Q, Hu Y, Wang B. Interleukin-22 as a molecular adjuvant facilitates IL-17-producing CD8+ T cell responses against a HBV DNA vaccine in mice. Hum Vaccin Immunother 2013; 9:2133 - 41; http://dx.doi.org/10.4161/hv.26047; PMID: 23941891
  • Workman CJ, Szymczak-Workman AL, Collison LW, Pillai MR, Vignali DA. The development and function of regulatory T cells. Cell Mol Life Sci 2009; 66:2603 - 22; http://dx.doi.org/10.1007/s00018-009-0026-2; PMID: 19390784
  • Stoop JN, van der Molen RG, Baan CC, van der Laan LJ, Kuipers EJ, Kusters JG, Janssen HL. Regulatory T cells contribute to the impaired immune response in patients with chronic hepatitis B virus infection. Hepatology 2005; 41:771 - 8; http://dx.doi.org/10.1002/hep.20649; PMID: 15791617
  • Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8:523 - 32; http://dx.doi.org/10.1038/nri2343; PMID: 18566595
  • Elenkov IJ, Webster E, Papanicolaou DA, Fleisher TA, Chrousos GP, Wilder RL. Histamine potently suppresses human IL-12 and stimulates IL-10 production via H2 receptors. J Immunol 1998; 161:2586 - 93; PMID: 9725260
  • Watanabe K, Mwinzi PN, Black CL, Muok EM, Karanja DM, Secor WE, Colley DG. T regulatory cell levels decrease in people infected with Schistosoma mansoni on effective treatment. Am J Trop Med Hyg 2007; 77:676 - 82; PMID: 17978070
  • Zou Q, Zhong Y, Su H, Kang Y, Jin J, Liu Q, Geng S, Zhao G, Wang B. Enhancement of humoral and cellular responses to HBsAg DNA vaccination by immunization with praziquantel through inhibition TGF-beta/Smad2,3 signaling. Vaccine 2010; 28:2032 - 8; http://dx.doi.org/10.1016/j.vaccine.2009.10.101; PMID: 20188260
  • Li J, Qiu SJ, She WM, Wang FP, Gao H, Li L, Tu CT, Wang JY, Shen XZ, Jiang W. Significance of the balance between regulatory T (Treg) and T helper 17 (Th17) cells during hepatitis B virus related liver fibrosis. PLoS One 2012; 7:e39307; http://dx.doi.org/10.1371/journal.pone.0039307; PMID: 22745730
  • Li J, Wu W, Peng G, Chen F, Bai M, Zheng M, Chen Z. HBcAg induces interleukin-10 production, inhibiting HBcAg-specific Th17 responses in chronic hepatitis B patients. Immunol Cell Biol 2010; 88:834 - 41; http://dx.doi.org/10.1038/icb.2010.63; PMID: 20498672
  • Zhang JY, Song CH, Shi F, Zhang Z, Fu JL, Wang FS. Decreased ratio of Treg cells to Th17 cells correlates with HBV DNA suppression in chronic hepatitis B patients undergoing entecavir treatment. PLoS One 2010; 5:e13869; http://dx.doi.org/10.1371/journal.pone.0013869; PMID: 21079784
  • Zhang W, Wang J, Su B, Li R, Ding Z, Kang Y, Wang B. Cimetidine augments Th1/Th2 dual polarized immune responses to recombinant HBV antigens. Vaccine 2011; 29:4862 - 8; http://dx.doi.org/10.1016/j.vaccine.2011.03.091; PMID: 21481324
  • Babinet C, Farza H, Morello D, Hadchouel M, Pourcel C. Specific expression of hepatitis B surface antigen (HBsAg) in transgenic mice. Science 1985; 230:1160 - 3; http://dx.doi.org/10.1126/science.3865370; PMID: 3865370
  • Du X, Zheng G, Jin H, Kang Y, Wang J, Xiao C, Zhang S, Zhao L, Chen A, Wang B. The adjuvant effects of co-stimulatory molecules on cellular and memory responses to HBsAg DNA vaccination. J Gene Med 2007; 9:136 - 46; http://dx.doi.org/10.1002/jgm.1004; PMID: 17310492

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.