Cocaine hydrolase gene therapy for cocaine abuse

Future Medicinal Chemistry

Volumn 4, Issue 2, 2012, Pages 151-162

  Brimijoin, Stephen ^a   Gao, Yang ^a  

^a MAYO GRADUATE SCHOOL   (United States)

Author keywords

including cocaine (but at low efficiency); Plasma enzyme capable of hydrolyzing acetylcholine and numerous other bioactive esters

Indexed keywords

ANTITOXIN; CHOLINESTERASE; COCAINE; COCAINE HYDROLASE; UNCLASSIFIED DRUG;

BEHAVIOR; COCAINE DEPENDENCE; DRUG ABUSE; DRUG HALF LIFE; DRUG USE; GENE LOCUS; GENE THERAPY; HUMAN; NONHUMAN; PRIORITY JOURNAL; RELAPSE; REVIEW; REWARD; TRANSGENE; VIRAL GENE DELIVERY SYSTEM;

COCAINE; COCAINE-RELATED DISORDERS; GENE THERAPY; GENETIC VECTORS; HUMANS; HYDROLASES;

EID: 84863053088     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.11.183     Document Type: Review

References (80)

1. Duysen EG, Li B, Darvesh S, Lockridge O. Sensitivity of butyrylcholinesterase knockout mice to (-)-huperzine A and donepezil suggests humans with butyrylcholinesterase deficiency may not tolerate these Alzheimer's disease drugs and indicates butyrylcholinesterase function in neurotransmission. Toxicology 233(1-3), 60-69 (2007). (Pubitemid 46509686)
2. Gorelick DA. Enhancing cocaine metabolism with butyrylcholinesterase as a treatment strategy. Drug Alcohol Depend. 48(3), 159-165 (1997). (Pubitemid 27526022)
3. Bresler MM, Rosser SJ, Basran A, Bruce NC. Gene cloning and nucleotide sequencing and properties of a cocaine esterase from Rhodococcus sp. strain MB1. Appl. Environ. Microbiol. 66(3), 904-908 (2000). (Pubitemid 30130004)
4. Larsen NA, de Prada P, Deng SX et al. Crystallographic and biochemical analysis of cocaine-degrading antibody 15A10. Biochemistry 43(25), 8067-8076 (2004). (Pubitemid 38808261)
5. Turner JM, Larsen NA, Basran A et al. Biochemical characterization and structural analysis of a highly proficient cocaine esterase. Biochemistry 41(41), 12297-12307 (2002).
6. Cooper ZD, Narasimhan D, Sunahara RK et al. Rapid and robust protection against cocaine-induced lethality in rats by the bacterial cocaine esterase. Mol. Pharmacol. 70, 1885-1891 (2006). (Pubitemid 44771904)
7. Collins GT, Brim RL, Narasimhan D et al. Cocaine esterase prevents cocaine-induced toxicity and the ongoing intravenous self-administration of cocaine in rats. J. Pharmacol. Exp. Ther. 331(2), 445-455 (2009).
8. Collins GT, Carey KA, Narasimhan D et al. Amelioration of the cardiovascular effects of cocaine in rhesus monkeys by a long-acting mutant form of cocaine esterase. Neuropsychopharmacology 36(5), 1047-1059 (2011).
9. Ko MC, Narasimhan D, Berlin AA, Lukacs NW, Sunahara RK, Woods JH. Effects of cocaine esterase following its repeated administration with cocaine in mice. Drug Alcohol Depend. 101(3), 202-209 (2009).
10. Xie W, Altamirano CV, Bartels CF, Speirs RJ, Cashman JR, Lockridge O. An improved cocaine hydrolase: the A328Y mutant of human butyrylcholinesterase is 4-fold more efficient. Mol. Pharmacol. 55(1), 83-91 (1999). (Pubitemid 29042525)
11. Sun H, Shen ML, Pang YP, Lockridge O, Brimijoin S. Cocaine metabolism accelerated by a re-engineered human butyrylcholinesterase. J. Pharmacol. Exp. Ther. 302(2), 710-716 (2002). (Pubitemid 34787239)
12. Sun H, El Yazal J, Lockridge O, Schopfer LM, Brimijoin S, Pang YP. Predicted Michaelis-Menten complexes of cocaine-butyrylcholinesterase. Engineering effective butyrylcholinesterase mutants for cocaine detoxication. J. Biol. Chem. 276(12), 9330-9336 (2001).
13. Pan Y, Gao D, Yang W, Cho H, Zhan CG. Free energy perturbation (FEP) simulation on the transition states of cocaine hydrolysis catalyzed by human butyrylcholinesterase and its mutants. J. Am. Chem. Soc. 129(44), 13537-13543 (2007). (Pubitemid 350071782)
14. Yang W, Xue L, Fang L, Chen X, Zhan CG. Characterization of a high-activity mutant of human butyrylcholinesterase against (-)-cocaine. Chem. Biol. Interact. 187(1-3), 148-152 (2010).
15. Xue L, Ko MC, Tong M et al. Design, preparation, and characterization of high-activity mutants of human butyrylcholinesterase specific for detoxification of cocaine. Mol. Pharmacol. 79(2), 290-297 (2011).
16. Sun H, Pang Y-P, Lockridge O, Brimijoin S. Re-engineering butyrylcholinesterase as a cocaine hydrolase. Mol. Pharmacol. 621, 220-224 (2002). (Pubitemid 34804100)
17. Gao Y, Brimijoin S. An engineered cocaine hydrolase blunts and reverses cardiovascular responses to cocaine in rats. J. Pharmacol. Exp. Ther. 310, 1046-1052 (2004). (Pubitemid 39108926)
18. Gao Y, LaFleur D, Shah R, Zhao Q, Singh M, Brimijoin S. An albumin-butyrylcholinesterase for cocaine toxicity and addiction: catalytic and pharmacokinetic properties. Chem. Biol. Interact. 175(1-3), 83-87 (2008).
19. Brimijoin S, Gao Y, Anker JJ et al. A cocaine hydrolase engineered from human butyrylcholinesterase selectively blocks cocaine toxicity and reinstatement of drug seeking in rats. Neuropsychopharmacology 33(11), 2715-2725 (2008).
20. Ostergaard D, Viby-Mogensen J, Hanel HK, Skovgaard LT. Half-life of plasma cholinesterase. Acta Anaesthesiol. Scand. 32(3), 266-269 (1988). (Pubitemid 18098974)
21. Gao Y, Atanasova E, Sui N, Pancook JD, Watkins JD, Brimijoin S. Gene transfer of cocaine hydrolase suppresses cardiovascular responses to cocaine in rats. Mol. Pharmacol. 67(1), 204-211 (2005). (Pubitemid 40069980)
22. Papadakis ED, Nicklin SA, Baker AH, White SJ. Promoters and control elements: designing expression cassettes for gene therapy. Curr. Gene Ther. 4(1), 89-113 (2004). (Pubitemid 38854948)
23. Pancook JD, Pecht G, Ader M, Mosko M, Lockridge O, Watkins JD. Application of directed evolution technology to optimize the cocaine hydrolase activity of human butyrylcholinesterase. FASEB J. 17, A565 (2003).
24. Morral N, O'Neal W, Rice K et al. Administration of helper-dependent adenoviral vectors and sequential delivery of different vector serotype for long-term liver-directed gene transfer in baboons. Proc. Natl Acad. Sci. USA 96(22), 12816-12821 (1999). (Pubitemid 29513585)
25. Mitani K, Graham FL, Caskey CT, Kochanek S. Rescue, propagation, and partial purification of a helper virus-dependent adenovirus vector. Proc. Natl Acad. Sci. USA 92(9), 3854-3858 (1995).
26. Kochanek S, Clemens PR, Mitani K, Chen HH, Chan S, Caskey CT. A new adenoviral vector: replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and b-galactosidase. Proc. Natl Acad. Sci. USA 93(12), 5731-5736 (1996).
27. Parks RJ, Chen L, Anton M, Sankar U, Rudnicki MA, Graham FL. A helper-dependent adenovirus vector system: removal of helper virus by Cre-mediated excision of the viral packaging signal. Proc. Natl Acad. Sci. USA 93(24), 13565-13570 (1996). (Pubitemid 26424159)
28. Kim IH, Jozkowicz A, Piedra PA, Oka K, Chan L. Lifetime correction of genetic deficiency in mice with a single injection of helper-dependent adenoviral vector. Proc. Natl Acad. Sci. USA 98(23), 13282-13287 (2001). (Pubitemid 33051354)
29. Brunetti-Pierri N, Nichols TC, McCorquodale S et al. Sustained phenotypic correction of canine hemophilia B after systemic administration of helper-dependent adenoviral vector. Hum. Gene Ther. 16(7), 811-820 (2005). (Pubitemid 40982330)
30. Muruve DA, Cotter MJ, Zaiss AK et al. Helper-dependent adenovirus vectors elicit intact innate but attenuated adaptive host immune responses in vivo. J. Virol. 78(11), 5966-5972 (2004). (Pubitemid 38661684)
31. Gao Y, Brimijoin S. Lasting reduction of cocaine action in neostriatum - a hydrolase gene therapy approach. J. Pharmacol. Exp. Ther. 330(2), 449-457 (2009).
32. Heffron PF. Actions of the selective inhibitor of cholinesterase tetramonoisopropyl pyrophosphortetramide on the rat phrenic nerve-diaphragm preparation. Br. J. Pharmacol. 46(4), 714-724 (1972).
33. La Du BN, Lockridge O. Molecular biology of human serum cholinesterase. Fed. Proc. 45(13), 2965-2969 (1986). (Pubitemid 17233737)
34. Nachon F, Nicolet Y, Viguie N, Masson P, Fontecilla-Camps JC, Lockridge O. Engineering of a monomeric and low-glycosylated form of human butyrylcholinesterase: expression, purification, characterization and crystallization. Eur. J. Biochem. 269(2), 630-637 (2002). (Pubitemid 34128021)
35. Lockridge O, Eckerson HW, La Du BN. Interchain disulfide bonds and subunit organization in human serum cholinesterase. J. Biol. Chem. 254(17), 8324-8330 (1979).
36. Lockridge O, Bartels CF, Vaughan TA, Wong CK, Norton SE, Johnson LL. Complete amino acid sequence of human serum cholinesterase. J. Biol. Chem. 262(2), 549-557 (1987). (Pubitemid 17005217)
37. Scott EM. Inheritance of two types of deficiency of human serum cholinesterase. Ann. Hum. Genet. 37(2), 139-143 (1973).
38. Hodgkin W, Giblett ER, Levine H, Bauer W, Motulsky AG. Complete pseudocholinesterase deficiency: genetic and immunologic characterization. J. Clin. Invest. 44, 486-493 (1965).
39. Silver A. The Biology of Cholinesterases. North-Holland Publishing Co., Amsterdam, The Netherlands (1974).
40. Saxena A, Sun W, Fedorko JM, Koplovitz I, Doctor BP. Prophylaxis with human serum butyrylcholinesterase protects guinea pigs exposed to multiple lethal doses of soman or VX. Biochem. Pharmacol. 81(1), 164-169 (2011).
41. Saxena A, Sun W, Luo C, Doctor BP. Human serum butyrylcholinesterase: in vitro and in vivo stability, pharmacokinetics, and safety in mice. Chem. Biol. Interact. 157-158, 199-203 (2005). (Pubitemid 41757651)
42. Anker JJ, Brimijoin S, Gao Y et al. Cocaine hydrolase encoded in viral vector blocks the reinstatement of cocaine seeking in rats for 6 months. Biol. Psychiatry DOI: 10.1016/j. biopsych.2011.11.014 (2012) (Epub ahead of print).
43. Jufer RA, Walsh SL, Cone EJ. Cocaine and metabolite concentrations in plasma during repeated oral administration: development of a human laboratory model of chronic cocaine use. J. Anal. Toxicol. 22(6), 435-444 (1998). (Pubitemid 28457816)
44. Walsh SL, Stoops WW, Moody DE, Lin SN, Bigelow GE. Repeated dosing with oral cocaine in humans: assessment of direct effects, withdrawal, and pharmacokinetics. Exp. Clin. Psychopharmacol. 17(4), 205-216 (2009).
45. Jozkowicz A, Dulak J. Helper-dependent adenoviral vectors in experimental gene therapy. Acta Biochim. Pol. 52(3), 589-599 (2005). (Pubitemid 41571704)
46. Brunetti-Pierri N, Ng P. Helper-dependent adenoviral vectors for liver-directed gene therapy. Hum. Mol. Genet. 20(R1), R7-R13 (2011).
47. Vetrini F, Ng P. Liver-directed gene therapy with helper-dependent adenoviral vectors: current state of the art and future challenges. Curr. Pharm. Design 17(24), 2488-2499 (2011).
48. Wang L, Wang H, Morizono H et al. Sustained correction of OTC deficiency in spf(ash) mice using optimized self-complementary AAV2/8 vectors. Gene Ther. doi:10.1038/gt.2011.111 (2011) (Epub ahead of print).
49. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat. Rev. Genet. 12(5), 341-355 (2011).
50. Berns KI, Hauswirth WW. Adeno-associated viruses. Adv. Virus Res. 25, 407-449 (1979). (Pubitemid 10097827)
51. Muruve DA. The innate immune response to adenovirus vectors. Hum. Gene Ther. 15(12), 1157-1166 (2004). (Pubitemid 40052429)
52. Brunetti-Pierri N, Palmer DJ, Beaudet al. Carey KD, Finegold M, Ng P. Acute toxicity after high-dose systemic injection of helper-dependent adenoviral vectors into nonhuman primates. Hum. Gene Ther. 15(1), 35-46 (2004). (Pubitemid 38147187)
53. Raper SE, Chirmule N, Lee FS et al. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol. Genet. Metab. 80(1-2), 148-158 (2003). (Pubitemid 37272241)
54. Seregin SS, Appledorn DM, McBride AJ et al. Transient pretreatment with glucocorticoid ablates innate toxicity of systemically delivered adenoviral vectors without reducing efficacy. Mol. Ther. 17(4), 685-696 (2009).
55. Dong JY, Fan PD, Frizzell RA. Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum. Gene Ther. 7(17), 2101-2112 (1996). (Pubitemid 26400735)
56. Wang AY, Peng PD, Ehrhardt A, Storm TA, Kay MA. Comparison of adenoviral and adeno-associated viral vectors for pancreatic gene delivery in vivo. Hum. Gene Ther. 15(4), 405-413 (2004). (Pubitemid 38469782)
57. Kaplitt MG, Leone P, Samulski RJ et al. Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat. Genet. 8(2), 148-154 (1994). (Pubitemid 24308362)
58. Koornneef A, Maczuga P, van Logtenstein R et al. Apolipoprotein B knockdown by AAV-delivered shRNA lowers plasma cholesterol in mice. Mol. Ther. 19(4), 731-740 (2011).
59. Choi SH, Lee HC. Long-term, antidiabetogenic effects of GLP-1 gene therapy using a double-stranded, adeno-associated viral vector. Gene Ther. 18(2), 155-163 (2011).
60. Brantly ML, Chulay JD, Wang L et al. Sustained transgene expression despite T lymphocyte responses in a clinical trial of rAAV1-AAT gene therapy. Proc. Natl Acad. Sci. USA 106(38), 16363-16368 (2009).
61. Manno CS, Pierce GF, Arruda VR et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12(3), 342-347 (2006). (Pubitemid 43355084)
62. Wagner JA, Messner AH, Moran ML et al. Safety and biological efficacy of an adeno-associated virus vector-cystic fibrosis transmembrane regulator (AAV-CFTR) in the cystic fibrosis maxillary sinus. Laryngoscope 109(2 Pt 1), 266-274 (1999). (Pubitemid 29075570)
63. Christine CW, Starr PA, Larson PS et al. Safety and tolerability of putaminal AADC gene therapy for Parkinson disease. Neurology 73(20), 1662-1669 (2009).
64. Jaski BE, Jessup ML, Mancini DM et al. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID Trial), a first-in-human Phase I/II clinical trial. J. Card. Fail 15(3), 171-181 (2009).
65. Mease PJ, Wei N, Fudman EJ et al. Safety, tolerability, and clinical outcomes after intraarticular injection of a recombinant adeno-associated vector containing a tumor necrosis factor antagonist gene: results of a Phase I/II study. J. Rheumatol. 37(4), 692-703 (2010).
66. McCarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ. Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther. 10(26), 2112-2118 (2003). (Pubitemid 37536760)
67. Michelfelder S, Trepel M. Adeno-associated viral vectors and their redirection to cell-type specific receptors. Adv. Genet. 67, 29-60 (2009).
68. Gill DR, Pringle IA, Hyde SC. Progress and prospects: the design and production of plasmid vectors. Gene Ther. 16(2), 165-171 (2009).
69. Dorer DE, Nettelbeck DM. Targeting cancer by transcriptional control in cancer gene therapy and viral oncolysis. Adv. Drug Deliv. Rev. 61(7-8), 554-571 (2009).
70. Leevy CM, Mendenhall CL, Lesko W, Howard MM. Estimation of hepatic blood flow with indocyanine green. J. Clin. Invest. 41, 1169-1179 (1962).
71. Pien GC, Basner-Tschakarjan E, Hui DJ et al. Capsid antigen presentation flags human hepatocytes for destruction after transduction by adeno-associated viral vectors. J. Clin. Invest. 119(6), 1688-1695 (2009).
72. Nathwani AC, Gray JT, McIntosh J et al. Safe and efficient transduction of the liver after peripheral vein infusion of self-complementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 109(4), 1414-1421 (2007). (Pubitemid 46239572)
73. Kreppel F, Kochanek S. Long-term transgene expression in proliferating cells mediated by episomally maintained high-capacity adenovirus vectors. J. Virol. 78(1), 9-22 (2004). (Pubitemid 37549715)
74. Hepatology: Textbook and Atlas: History, Morphology, Biochemistry, Diagnostics, Clinic, Therapy. Kuntz E, Kuntz H-D (Eds). Springer, Heidelberg, NY, USA (2008).
75. Spalding KL, Bhardwaj RD, Buchholz BA, Druid H, Frisen J. Retrospective birth dating of cells in humans. Cell 122(1), 133-143 (2005). (Pubitemid 40977946)
76. Gao Y, Orson FM, Kinsey B, Kosten T, Brimijoin S. The concept of pharmacologic cocaine interception as a treatment for drug abuse. Chem. Biol. Interact. 187(1-3), 421-424 (2010).
77. Thome J, Hassler F, Zachariou V. Gene therapy for psychiatric disorders. World J. Biol. Psychiatry 12(Suppl. 1), 16-18 (2011).
78. Ferguson SM, Mitchell ES, Neumaier JF. Increased expression of 5-HT6 receptors in the nucleus accumbens blocks the rewarding but not psychomotor activating properties of cocaine. Biol. Psychiatry 63(2), 207-213 (2008). (Pubitemid 350299315)
79. Neumaier JF, Vincow ES, Arvanitogiannis A, Wise RA, Carlezon WA Jr. Elevated expression of 5-HT1B receptors in nucleus accumbens efferents sensitizes animals to cocaine. J. Neurosci. 22(24), 10856-10863 (2002). (Pubitemid 36005160)
80. Iniguez SD, Warren BL, Neve RL, Russo SJ, Nestler EJ, Bolanos-Guzman CA. Viral-mediated expression of extracellular signal-regulated kinase-2 in the ventral tegmental area modulates behavioral responses to cocaine. Behav. Brain Res. 214(2), 460-464 (2010).