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Research Paper

Alum adjuvant is more effective than MF59 at prompting early germinal center formation in response to peptide-protein conjugates and enhancing efficacy of a vaccine against opioid use disorders

, ORCID Icon, ORCID Icon, , & ORCID Icon
Pages 909-917 | Received 28 Sep 2018, Accepted 05 Dec 2018, Published online: 20 Feb 2019

References

  • Florence CS, Zhou C, Luo F, Xu L. The economic burden of prescription opioid overdose, abuse, and dependence in the United States, 2013. Med Care. 2016;54:901–906. doi:10.1097/MLR.0000000000000625.
  • Pravetoni M, Le Naour M, Harmon TM, Tucker AM, Portoghese PS, Pentel PR. An oxycodone conjugate vaccine elicits drug-specific antibodies that reduce oxycodone distribution to brain and hot-plate analgesia. J Pharmacol Exp Ther. 2012;341:225–232. doi:10.1124/jpet.111.189506.
  • Pravetoni M, Le Naour M, Tucker AM, Harmon TM, Hawley TM, Portoghese PS, Pentel PR. Reduced antinociception of opioids in rats and mice by vaccination with immunogens containing oxycodone and hydrocodone haptens. J Med Chem. 2013;56:915–923. doi:10.1021/jm3013745.
  • Pravetoni M, Pentel PR, Potter DN, Chartoff EH, Tally L, LeSage MG. Effects of an oxycodone conjugate vaccine on oxycodone self-administration and oxycodone-induced brain gene expression in rats. PLoS One. 2014;9:e101807. doi:10.1371/journal.pone.0101807.
  • Hwang CS, Smith LC, Natori Y, Ellis B, Zhou B, Janda KD. Efficacious vaccine against heroin contaminated with fentanyl. ACS Chem Neurosci. 2018. doi: 10.1021/acschemneuro.8b00079.
  • Bremer PT, Schlosburg JE, Banks ML, Steele FF, Zhou B, Poklis JL, Janda KD. Development of a clinically viable heroin vaccine. J Am Chem Soc. 2017;139:8601–8611. doi:10.1021/jacs.7b03334.
  • Raleigh MD, Laudenbach M, Baruffaldi F, Peterson SJ, Roslawski MJ, Birnbaum AK, Carroll FI, Runyon SP, Winston S, Pentel PR, et al. Opioid dose- and route-dependent efficacy of oxycodone and heroin vaccines in rats. J Pharmacol Exp Ther. 2018. doi: 10.1124/jpet.117.247049.
  • Sulima A, Jalah R, Antoline JFG, Torres OB, Imler GH, Deschamps JR, Beck Z, Alving CR, Jacobson AE, Rice KC, et al. A stable heroin analogue that can serve as a vaccine hapten to induce antibodies that block the effects of heroin and its metabolites in rodents and that cross-react immunologically with related drugs of abuse. J Med Chem. 2018;61:329–343. doi:10.1021/acs.jmedchem.7b01427.
  • Torres OB, Matyas GR, Rao M, Peachman KK, Jalah R, Beck Z, Michael NL, Rice KC, Jacobson AE, Alving CR. Heroin-HIV-1 (H2) vaccine: induction of dual immunologic effects with a heroin hapten-conjugate and an HIV-1 envelope V2 peptide with liposomal lipid A as an adjuvant. NPJ Vaccines. 2017;2:13. doi:10.1038/s41541-017-0013-9.
  • Raleigh MD, Pravetoni M, Harris AC, Birnbaum AK, Pentel PR. Selective effects of a morphine conjugate vaccine on heroin and metabolite distribution and heroin-induced behaviors in rats. J Pharmacol Exp Ther. 2013;344:397–406. doi:10.1124/jpet.112.201194.
  • Laudenbach M, Baruffaldi F, Vervacke JS, Distefano MD, Titcombe PJ, Mueller DL, et al. The frequency of naive and early-activated hapten-specific B cell subsets dictates the efficacy of a therapeutic vaccine against prescription opioid abuse. J Immunol. 2015;194:5926–5936. doi:10.4049/jimmunol.1500385.
  • Taylor JJ, Laudenbach M, Tucker AM, Jenkins MK, Pravetoni M. Hapten-specific naive B cells are biomarkers of vaccine efficacy against drugs of abuse. J Immunol Methods. 2014;405:74–86. doi:10.1016/j.jim.2014.01.010.
  • Pravetoni M, Vervacke JS, Distefano MD, Tucker AM, Laudenbach M, Pentel PR. Effect of currently approved carriers and adjuvants on the pre-clinical efficacy of a conjugate vaccine against oxycodone in mice and rats. PLoS One. 2014;9:e96547.
  • Baruffaldi F, Kelcher AH, Laudenbach M, Gradinati V, Limkar A, Roslawski M, et al. Preclinical efficacy and characterization of candidate vaccines for treatment of opioid use disorders using clinically viable carrier proteins. Mol Pharm. 2018;15:4947–4962. doi:10.1021/acs.molpharmaceut.8b00592.
  • Laudenbach M, Baruffaldi F, Robinson C, Carter P, Seelig D, Baehr C, Pravetoni M. Blocking interleukin-4 enhances efficacy of vaccines for treatment of opioid abuse and prevention of opioid overdose. Sci Rep. 2018;8:5508. doi:10.1038/s41598-018-23777-6.
  • HogenEsch H. Mechanisms of stimulation of the immune response by aluminum adjuvants. Vaccine. 2002;20:S34–9.
  • Guy B. The perfect mix: recent progress in adjuvant research. Nat Rev Microbiol. 2007;5:505–517. doi:10.1038/nrmicro1681.
  • Wille-Reece U, Flynn BJ, Lore K, Koup RA, Miles AP, Saul A, Kedl RM, Mattapallil JJ, Weiss WR, Roederer M, et al. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med. 2006;203:1249–1258. doi:10.1084/jem.20052433.
  • Vajdy M, Selby M, Medina-Selby A, Coit D, Hall J, Tandeske L, et al. Hepatitis C virus polyprotein vaccine formulations capable of inducing broad antibody and cellular immune responses. J Gen Virol. 2006;87:2253–2262. doi:10.1099/vir.0.81849-0.
  • McKee AS, Munks MW, Marrack P. How do adjuvants work? Important considerations for new generation adjuvants. Immunity. 2007;27:687–690. doi:10.1016/j.immuni.2007.11.003.
  • Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting innate immunity to work. Immunity. 2010;33:492–503. doi:10.1016/j.immuni.2010.10.002.
  • Nakaya HI, Clutterbuck E, Kazmin D, Wang L, Cortese M, Bosinger SE, et al. Systems biology of immunity to MF59-adjuvanted versus nonadjuvanted trivalent seasonal influenza vaccines in early childhood. Proc Natl Acad Sci U S A. 2016;113:1853–1858. doi:10.1073/pnas.1519690113.
  • Block SL, Ruiz-Palacios GM, Guerrero ML, Beygo J, Sales V, Holmes SJ. Dose-range study of MF59-adjuvanted versus nonadjuvanted monovalent A/H1N1 pandemic influenza vaccine in six- to less than thirty-six-month-old children. Pediatr Infect Dis J. 2012;31:e92–8. doi:10.1097/INF.0b013e318257644f.
  • Della CG, Nicolay U, Lindert K, Leroux-Roels G, Clement F, Castellino F, Galli C, Groth N, Levin Y, Del Giudice G. A dose-ranging study in older adults to compare the safety and immunogenicity profiles of MF59(R)-adjuvanted and non-adjuvanted seasonal influenza vaccines following intradermal and intramuscular administration. Hum Vaccin Immunother. 2014;10:1701–1710. doi:10.4161/hv.28618.
  • Lofano G, Mancini F, Salvatore G, Cantisani R, Monaci E, Carrisi C, et al. Oil-in-water emulsion MF59 increases germinal center b cell differentiation and persistence in response to vaccination. J Immunol. 2015;195:1617–1627. doi:10.4049/jimmunol.1402604.
  • Mastelic Gavillet B, Eberhardt CS, Auderset F, Castellino F, Seubert A, Tregoning JS, Lambert P-H, de Gregorio E, Del Giudice G, Siegrist C-A. MF59 mediates its B cell adjuvanticity by promoting T follicular helper cells and thus germinal center responses in adult and early life. J Immunol. 2015;194:4836–4845. doi:10.4049/jimmunol.1402071.
  • Mosca F, Tritto E, Muzzi A, Monaci E, Bagnoli F, Iavarone C, O’Hagan D, Rappuoli R, De Gregorio E. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci U S A. 2008;105:10501–10506. doi:10.1073/pnas.0804699105.
  • Seubert A, Monaci E, Pizza M, O’Hagan DT, Wack A. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J Immunol. 2008;180:5402–5412. doi:10.4049/jimmunol.180.8.5402.
  • 2018 Annual Surveillance Report of Drug-Related Risks and Outcomes-United States. Centers for disease control and prevention. US Department of Health and Human Services; 2018. https://www.cdc.gov/drugoverdose/pdf/pubs/2018-cdc-drug-surveillance-report.pdf
  • Moon JJ, Chu HH, Hataye J, Pagan AJ, Pepper M, McLachlan JB, Zell T, Jenkins MK. Tracking epitope-specific T cells. Nat Protoc. 2009;4:565–581. doi:10.1038/nprot.2009.9.
  • Raleigh MD, Peterson SJ, Laudenbach M, Baruffaldi F, Carroll FI, Comer SD, Navarro HA, Langston TL, Runyon SP, Winston S, et al. Safety and efficacy of an oxycodone vaccine: addressing some of the unique considerations posed by opioid abuse. PLoS One. 2017;12:e0184876. doi:10.1371/journal.pone.0184876.
  • Backonja M, Webster LR, Setnik B, Bass A, Sommerville KW, Matschke K, Malhotra BK, Wolfram G. Intravenous abuse potential study of oxycodone alone or in combination with naltrexone in nondependent recreational opioid users. Am J Drug Alcohol Abuse. 2016;42:539–549. doi:10.3109/00952990.2016.1167215.
  • Harris SC, Perrino PJ, Smith I, Shram MJ, Colucci SV, Bartlett C, Sellers EM. Abuse potential, pharmacokinetics, pharmacodynamics, and safety of intranasally administered crushed oxycodone HCl abuse-deterrent controlled-release tablets in recreational opioid users. J Clin Pharmacol. 2013;54:468–477. doi:10.1002/jcph.235.
  • FDA approves first seasonal influenza vaccine containing an adjuvant. U.S. food and drug administration, 2015 https://www.fda.gov/biologicsbloodvaccines/safetyavailability/vaccinesafety/ucm473989.htm:.
  • Schmiel SE, Yang JA, Jenkins MK, Mueller DL. Cutting edge: adenosine A2a receptor signals inhibit germinal center T follicular helper cell differentiation during the primary response to vaccination. J Immunol. 2017;198:623–628. doi:10.4049/jimmunol.1601686.
  • Yang JA, Tubo NJ, Gearhart MD, Bardwell VJ, Jenkins MK. Cutting edge: bcl6-interacting corepressor contributes to germinal center T follicular helper cell formation and B cell helper function. J Immunol. 2015;194:5604–5608. doi:10.4049/jimmunol.1500201.
  • Wang C, Hart M, Chui C, Ajuogu A, Brian IJ, de Cassan SC, et al. Germinal center B cell and T follicular helper cell responses to viral vector and protein-in-adjuvant vaccines. J Immunol. 2016;197:1242–1251. doi:10.4049/jimmunol.1502472.

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