Active and Passive Immunization with an Anti-Methamphetamine Vaccine Attenuates the Behavioral and Cardiovascular Effects of Methamphetamine
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals, Housing, and Drug
2.2. Vaccine Preparation and Administration
2.3. Quantification of Anti-Methamphetamine Antibody Levels
2.4. Methamphetamine-Induced Locomotor Activity in Mice
2.5. Passive Immunization
2.6. Intravenous Cannula and Telemetry Probe Implantation
2.7. Tests Following Methamphetamine Administration
2.8. Intravenous Catheter Implantation and Methamphetamine Self-Administration Training
2.9. Reinstatement Tests
2.10. Data Analysis
3. Results
3.1. Anti-MA Response to Different Entolimod Doses
3.2. MA Induced Locomotor Activity
3.3. Passive Immunization and MA Cardiovascular Effects
3.4. Passive Immunization and Drug-Induced Reinstatement
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Substance Abuse and Mental Health Services Administration. Key substance use and mental health indicators in the United States: Results from the 2020 National Survey on Drug Use and Health; (HHS Publication No. PEP21-07-01-003, NSDUH Series H-56); Center for Behavioral Health Statistics and Quality; Substance Abuse and Mental Health Services Administration: Rockville, MD, USA, 2021; Available online: https://www.samhsa.gov/data/ (accessed on 14 August 2022).
- Han, B.; Compton, W.M.; Jones, C.M.; Einstein, E.B.; Volkow, N.D. Methamphetamine Use, Methamphetamine Use Disorder, and Associated Overdose Deaths Among US Adults. JAMA Psychiatry 2021, 78, 1329–1342. [Google Scholar] [CrossRef] [PubMed]
- Ellis, M.S.; Kasper, Z.A.; Cicero, T.J. Twin epidemics: The surging rise of methamphetamine use in chronic opioid users. Drug Alcohol Depend. 2018, 193, 14–20. [Google Scholar] [CrossRef] [PubMed]
- Siefried, K.J.; Acheson, L.S.; Lintzeris, N.; Ezard, N. Pharmacological Treatment of Methamphetamine/Amphetamine Dependence: A Systematic Review. CNS Drugs 2020, 34, 337–365. [Google Scholar] [CrossRef] [PubMed]
- Twillman, R.K.; Dawson, E.; LaRue, L.; Guevara, M.G.; Whitley, P.; Huskey, A. Evaluation of Trends of Near-Real-Time Urine Drug Test Results for Methamphetamine, Cocaine, Heroin, and Fentanyl. JAMA Netw. Open 2020, 3, e1918514. [Google Scholar] [CrossRef]
- Kamp, F.; Proebstl, L.; Hager, L.; Schreiber, A.; Riebschlager, M.; Neumann, S.; Straif, M.; Schacht-Jablonowsky, M.; Manz, K.; Soyka, M.; et al. Effectiveness of methamphetamine abuse treatment: Predictors of treatment completion and comparison of two residential treatment programs. Drug Alcohol Depend. 2019, 201, 8–15. [Google Scholar] [CrossRef]
- Soares, E.; Pereira, F.C. Pharmacotherapeutic strategies for methamphetamine use disorder: Mind the subgroups. Expert Opin. Pharmacother. 2019, 20, 2273–2293. [Google Scholar] [CrossRef]
- Byrnes-Blake, K.A.; Carroll, F.I.; Abraham, P.; Owens, S.M. Generation of anti-(+)methamphetamine antibodies is not impeded by (+)methamphetamine administration during active immunization of rats. Int. Immunopharmacol. 2001, 1, 329–338. [Google Scholar] [CrossRef]
- Duryee, M.J.; Bevins, R.A.; Reichel, C.M.; Murray, J.E.; Dong, Y.; Thiele, G.M.; Sanderson, S.D. Immune responses to methamphetamine by active immunization with peptide-based, molecular adjuvant-containing vaccines. Vaccine 2009, 27, 2981–2988. [Google Scholar] [CrossRef]
- Carroll, F.I.; Blough, B.E.; Pidaparthi, R.R.; Abraham, P.; Gong, P.K.; Deng, L.; Huang, X.; Gunnell, M.; Lay, J.O., Jr.; Peterson, E.C.; et al. Synthesis of mercapto-(+)-methamphetamine haptens and their use for obtaining improved epitope density on (+)-methamphetamine conjugate vaccines. J. Med. Chem. 2011, 54, 5221–5228. [Google Scholar] [CrossRef]
- Moreno, A.Y.; Mayorov, A.V.; Janda, K.D. Impact of distinct chemical structures for the development of a methamphetamine vaccine. J. Am. Chem. Soc. 2011, 133, 6587–6595. [Google Scholar] [CrossRef] [Green Version]
- Miller, M.L.; Moreno, A.Y.; Aarde, S.M.; Creehan, K.M.; Vandewater, S.A.; Vaillancourt, B.D.; Wright, M.J.; Janda, K.D.; Taffe, M.A. A methamphetamine vaccine attenuates methamphetamine-induced disruptions in thermoregulation and activity in rats. Biol. Psychiatry 2013, 73, 721–728. [Google Scholar] [CrossRef] [PubMed]
- Ruedi-Bettschen, D.; Wood, S.L.; Gunnell, M.G.; West, C.M.; Pidaparthi, R.R.; Carroll, F.I.; Blough, B.E.; Owens, S.M. Vaccination protects rats from methamphetamine-induced impairment of behavioral responding for food. Vaccine 2013, 31, 4596–4602. [Google Scholar] [CrossRef] [PubMed]
- Shen, X.Y.; Kosten, T.A.; Lopez, A.Y.; Kinsey, B.M.; Kosten, T.R.; Orson, F.M. A vaccine against methamphetamine attenuates its behavioral effects in mice. Drug Alcohol Depend. 2013, 129, 41–48. [Google Scholar] [CrossRef] [PubMed]
- Collins, K.C.; Janda, K.D. Investigating hapten clustering as a strategy to enhance vaccines against drugs of abuse. Bioconjug. Chem. 2014, 25, 593–600. [Google Scholar] [CrossRef]
- Collins, K.C.; Schlosburg, J.E.; Lockner, J.W.; Bremer, P.T.; Ellis, B.A.; Janda, K.D. Lipid tucaresol as an adjuvant for methamphetamine vaccine development. Chem. Commun. 2014, 50, 4079–4081. [Google Scholar] [CrossRef]
- Haile, C.N.; Kosten, T.A.; Shen, X.Y.; O’Malley, P.W.; Winoske, K.J.; Kinsey, B.M.; Wu, Y.; Huang, Z.; Lykissa, E.D.; Naidu, N.; et al. Altered methamphetamine place conditioning in mice vaccinated with a succinyl-methamphetamine-tetanus-toxoid vaccine. Am. J. Addict. 2015, 24, 748–755. [Google Scholar] [CrossRef]
- Miller, M.L.; Aarde, S.M.; Moreno, A.Y.; Creehan, K.M.; Janda, K.D.; Taffe, M.A. Effects of active anti-methamphetamine vaccination on intravenous self-administration in rats. Drug Alcohol Depend. 2015, 153, 29–36. [Google Scholar] [CrossRef]
- Collins, K.C.; Schlosburg, J.E.; Bremer, P.T.; Janda, K.D. Methamphetamine Vaccines: Improvement through Hapten Design. J. Med. Chem. 2016, 59, 3878–3885. [Google Scholar] [CrossRef]
- Gooyit, M.; Miranda, P.O.; Wenthur, C.J.; Ducime, A.; Janda, K.D. Influencing Antibody-Mediated Attenuation of Methamphetamine CNS Distribution through Vaccine Linker Design. ACS Chem. Neurosci. 2017, 8, 468–472. [Google Scholar] [CrossRef]
- Arora, R.; Haile, C.N.; Kosten, T.A.; Wu, Y.; Ramakrishnan, M.; Hawkins, L.D.; Orson, F.M.; Kosten, T.R. Preclinical efficacy of an anti-methamphetamine vaccine using E6020 adjuvant. Am. J. Addict. 2019, 28, 119–126. [Google Scholar] [CrossRef]
- Olson, M.E.; Sugane, T.; Zhou, B.; Janda, K.D. Consequence of Hapten Stereochemistry: An Efficacious Methamphetamine Vaccine. J. Am. Chem. Soc. 2019, 141, 14089–14092. [Google Scholar] [CrossRef]
- Keller, C.M.; Spence, A.L.; Stevens, M.W.; Owens, S.M.; Guerin, G.F.; Goeders, N.E. Effects of a methamphetamine vaccine, IXT-v100, on methamphetamine-related behaviors. Psychopharmacology 2020, 237, 655–667. [Google Scholar] [CrossRef] [PubMed]
- Gentry, W.B.; Laurenzana, E.M.; Williams, D.K.; West, J.R.; Berg, R.J.; Terlea, T.; Owens, S.M. Safety and efficiency of an anti-(+)-methamphetamine monoclonal antibody in the protection against cardiovascular and central nervous system effects of (+)-methamphetamine in rats. Int. Immunopharmacol. 2006, 6, 968–977. [Google Scholar] [CrossRef]
- Kosten, T.R.; Domingo, C.B.; Shorter, D.; Orson, F.; Green, C.; Somoza, E.; Sekerka, R.; Levin, F.R.; Mariani, J.J.; Stitzer, M.; et al. Vaccine for cocaine dependence: A randomized double-blind placebo-controlled efficacy trial. Drug Alcohol Depend. 2014, 140, 42–47. [Google Scholar] [CrossRef] [PubMed]
- Martell, B.A.; Orson, F.M.; Poling, J.; Mitchell, E.; Rossen, R.D.; Gardner, T.; Kosten, T.R. Cocaine vaccine for the treatment of cocaine dependence in methadone-maintained patients: A randomized, double-blind, placebo-controlled efficacy trial. Arch. Gen. Psychiatry 2009, 66, 1116–1123. [Google Scholar] [CrossRef] [PubMed]
- O’Neill, L.A.; Bryant, C.E.; Doyle, S.L. Therapeutic targeting of Toll-like receptors for infectious and inflammatory diseases and cancer. Pharmacol. Rev. 2009, 61, 177–197. [Google Scholar] [CrossRef]
- Hennessy, E.J.; Parker, A.E.; O’Neill, L.A. Targeting Toll-like receptors: Emerging therapeutics? Nat. Rev. Drug Discov. 2010, 9, 293–307. [Google Scholar] [CrossRef]
- Duthie, M.S.; Windish, H.P.; Fox, C.B.; Reed, S.G. Use of defined TLR ligands as adjuvants within human vaccines. Immunol. Rev. 2011, 239, 178–196. [Google Scholar] [CrossRef] [PubMed]
- Garaude, J.; Kent, A.; van Rooijen, N.; Blander, J.M. Simultaneous targeting of toll- and nod-like receptors induces effective tumor-specific immune responses. Sci. Transl. Med. 2012, 4, 120ra116. [Google Scholar] [CrossRef]
- Bremer, P.T.; Schlosburg, J.E.; Lively, J.M.; Janda, K.D. Injection route and TLR9 agonist addition significantly impact heroin vaccine efficacy. Mol. Pharm. 2014, 11, 1075–1080. [Google Scholar] [CrossRef]
- Ishizaka, S.T.; Hawkins, L.D. E6020: A synthetic Toll-like receptor 4 agonist as a vaccine adjuvant. Expert Rev. Vaccines 2007, 6, 773–784. [Google Scholar] [CrossRef] [PubMed]
- Morefield, G.L.; Hawkins, L.D.; Ishizaka, S.T.; Kissner, T.L.; Ulrich, R.G. Synthetic Toll-like receptor 4 agonist enhances vaccine efficacy in an experimental model of toxic shock syndrome. Clin. Vaccine Immunol. 2007, 14, 1499–1504. [Google Scholar] [CrossRef] [PubMed]
- Lockner, J.W.; Ho, S.O.; McCague, K.C.; Chiang, S.M.; Do, T.Q.; Fujii, G.; Janda, K.D. Enhancing nicotine vaccine immunogenicity with liposomes. Bioorg. Med. Chem. Lett. 2013, 23, 975–978. [Google Scholar] [CrossRef] [PubMed]
- Stevens, M.W.; Gunnell, M.G.; Tawney, R.; Owens, S.M. Optimization of a methamphetamine conjugate vaccine for antibody production in mice. Int. Immunopharmacol. 2016, 35, 137–141. [Google Scholar] [CrossRef]
- Yang, F.; Kosten, T.R. Psychopharmacology: Neuroimmune signaling in psychiatric disease-developing vaccines against abused drugs using toll-like receptor agonists. Psychopharmacology 2019, 236, 2899–2907. [Google Scholar] [CrossRef]
- Al Ustwani, O.; Gupta, N.; Bakhribah, H.; Griffiths, E.; Wang, E.; Wetzler, M. Clinical updates in adult acute lymphoblastic leukemia. Crit. Rev. Oncol./Hematol. 2016, 99, 189–199. [Google Scholar] [CrossRef]
- deWit, H.; Stewart, J. Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology 1981, 75, 134–143. [Google Scholar] [CrossRef]
- Shalev, U.; Highfield, D.; Yap, J.; Shaham, Y. Stress and relapse to drug seeking in rats: Studies on the generality of the effect. Psychopharmacology 2000, 150, 337–346. [Google Scholar] [CrossRef]
- Shaham, Y.; Shalev, U.; Lu, L.; DeWit, H. The reinstatement model of drug relapse: History, methodology and major findings. Psychopharmacology 2003, 168, 3–20. [Google Scholar] [CrossRef]
- Haile, C.N.; Kosten, T.A. Differential effects of D1- and D2-like compounds on cocaine self-administration in Lewis and Fischer 344 inbred rats. J. Pharmacol. Exp. Ther. 2001, 299, 509–518. [Google Scholar]
- Zhang, X.Y.; Kosten, T.A. Prazosin, an a-1 adrenergic antagonist, reduces cocaine-induced reinstatement of drug-seeking. Biol. Psychiatry 2005, 57, 1202–1204. [Google Scholar] [CrossRef] [PubMed]
- Lockner, J.W.; Eubanks, L.M.; Choi, J.L.; Lively, J.M.; Schlosburg, J.E.; Collins, K.C.; Globisch, D.; Rosenfeld-Gunn, R.J.; Wilson, I.A.; Janda, K.D. Flagellin as carrier and adjuvant in cocaine vaccine development. Mol. Pharm. 2015, 12, 653–662. [Google Scholar] [CrossRef]
- Byrnes-Blake, K.A.; Laurenzana, E.M.; Carroll, F.I.; Abraham, P.; Gentry, W.B.; Lanes, R.D.; Owens, S.M. Pharmacodynamic mechanisms of monoclonal antibody-based antagonism of (+)-methamphetamine in rats. Eur. J. Pharmacol. 2003, 461, 119–128. [Google Scholar] [CrossRef]
- Hambuchen, M.D.; Rüedi-Bettschen, D.; Gunnell, M.G.; Hendrickson, H.; Owens, S.M. Chronic treatment of (+)-methamphetamine-induced locomotor effects in rats using one or a combination of two high affinity anti-methamphetamine monoclonal antibodies. Hum. Vaccines Immunother. 2016, 12, 2240–2248. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, J.D.; Bremer, P.T.; Hwang, C.S.; Vandewater, S.A.; Collins, K.C.; Creehan, K.M.; Janda, K.D.; Taffe, M.A. Effective active vaccination against methamphetamine in female rats. Drug Alcohol Depend. 2017, 175, 179–186. [Google Scholar] [CrossRef]
- Singh, R.A.K.; Kosten, T.A.; Kinsey, B.M.; Shen, X.; Lopez, A.L.; Kosten, T.R.; Orson, F.M. Dose-dependent changes in the locomotor responses to methamphetamine in BALB/c mice: Low doses induce hypolocomotion. Pharmacol. Biochem. Behav. 2012, 103, 230–236. [Google Scholar] [CrossRef]
- Good, R.L.; Radcliffe, R.A. Methamphetamine-induced locomotor changes are dependent on age, dose and genotype. Pharmacol. Biochem. Behav. 2011, 98, 101–111. [Google Scholar] [CrossRef]
- Kosten, T.R.; Newton, T.F.; DeLaGarza, R.; Haile, C.N. Cocaine and Methamphetamine Dependence: Advances in Treatment; American Psychiatric Publishing: Arlington, VA, USA, 2012. [Google Scholar]
- Kantak, K.M.; Collins, S.L.; Lipman, E.G.; Bond, J.; Giovanoni, K.; Fox, B.S. Evaluation of anti-cocaine antibodies and a cocaine vaccine in a rat self-administration model. Psychopharmacology 2000, 148, 251–262. [Google Scholar] [CrossRef]
- Carrera, M.R.; Ashley, J.A.; Zhou, B.; Wirsching, P.; Koob, G.F.; Janda, K.D. Cocaine vaccines: Antibody protection against relapse in a rat model. Proc. Natl. Acad. Sci. USA 2000, 97, 6202–6206. [Google Scholar] [CrossRef]
- McMillan, D.E.; Hardwick, W.C.; Li, M.; Gunnell, M.G.; Carroll, F.I.; Abraham, P.; Owens, S.M. Effects of murine-derived anti-methamphetamine monoclonal antibodies on (+)-methamphetamine self-administration in the rat. J. Pharmacol. Exp. Ther. 2004, 309, 1248–1255. [Google Scholar] [CrossRef]
- Barrett, A.C.; Miller, J.R.; Dohrmann, J.M.; Caine, S.B. Effects of dopamine indirect agonists and selective D1-like and D2-like agonists and antagonists on cocaine self-administration and food maintained responding in rats. Neuropharmacology 2004, 47 (Suppl. 1), 256–273. [Google Scholar] [CrossRef] [PubMed]
- Weissenborn, R.; Deroche, V.; Koob, G.F.; Weiss, F. Effects of dopamine agonists and antagonists on cocaine-induced operant responding for a cocaine-associated stimulus. Psychopharmacology 1996, 126, 311–322. [Google Scholar] [CrossRef] [PubMed]
- Lindenstrøm, T.; Woodworth, J.; Dietrich, J.; Aagaard, C.; Andersen, P.; Agger, E.M. Vaccine-induced th17 cells are maintained long-term postvaccination as a distinct and phenotypically stable memory subset. Infect. Immun. 2012, 80, 3533–3544. [Google Scholar] [CrossRef] [PubMed]
- Køllgaard, T.; Ugurel-Becker, S.; Idorn, M.; Andersen, M.H.; Becker, J.C.; Straten, P.T. Pre-Vaccination Frequencies of Th17 Cells Correlate with Vaccine-Induced T-Cell Responses to Survivin-Derived Peptide Epitopes. PLoS ONE 2015, 10, e0131934. [Google Scholar] [CrossRef] [PubMed]
- Murdaca, G.; Greco, M.; Tonacci, A.; Negrini, S.; Borro, M.; Puppo, F.; Gangemi, S. IL-33/IL-31 Axis in Immune-Mediated and Allergic Diseases. Int. J. Mol. Sci. 2019, 20, 5856. [Google Scholar] [CrossRef] [Green Version]
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Haile, C.N.; Varner, K.J.; Huijing, X.; Arora, R.; Orson, F.M.; Kosten, T.R.; Kosten, T.A. Active and Passive Immunization with an Anti-Methamphetamine Vaccine Attenuates the Behavioral and Cardiovascular Effects of Methamphetamine. Vaccines 2022, 10, 1508. https://doi.org/10.3390/vaccines10091508
Haile CN, Varner KJ, Huijing X, Arora R, Orson FM, Kosten TR, Kosten TA. Active and Passive Immunization with an Anti-Methamphetamine Vaccine Attenuates the Behavioral and Cardiovascular Effects of Methamphetamine. Vaccines. 2022; 10(9):1508. https://doi.org/10.3390/vaccines10091508
Chicago/Turabian StyleHaile, Colin N., Kurt J. Varner, Xia Huijing, Reetakshi Arora, Frank M. Orson, Thomas R. Kosten, and Therese A. Kosten. 2022. "Active and Passive Immunization with an Anti-Methamphetamine Vaccine Attenuates the Behavioral and Cardiovascular Effects of Methamphetamine" Vaccines 10, no. 9: 1508. https://doi.org/10.3390/vaccines10091508