Drug-dependent behaviors and nicotinic acetylcholine receptor expressions in Caenorhabditis elegans following chronic nicotine exposure

NeuroToxicology

Volumn 47, Issue , 2015, Pages 27-36

  Polli, Joseph R ^a   Dobbins, Dorothy L ^a   Kobet, Robert A ^a   Farwell, Mary A ^a   Zhang, Baohong ^a   Lee, Myon Hee ^b   Pan, Xiaoping ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

Author keywords

C. elegans; Drug dependent behaviors; Gene expression; NAChRs; Nicotine

Indexed keywords

NICOTINE; NICOTINIC RECEPTOR; NICOTINIC AGENT;

ACR 11 GENE; ACR 14 GENE; ACR 20 GENE; ACR 21 GENE; ACR 6 GENE; ACR 7 GENE; ADAPTATION; ARC 16 GENE; ARTICLE; CAENORHABDITIS ELEGANS; COMPUTER PROGRAM; CONTROLLED STUDY; DRUG DEPENDENCE; DRUG STIMULATION; DRUG TOLERANCE; GENE EXPRESSION; GENE FUNCTION; LEV 1 GENE; LEV 8 GENE; LOCOMOTION; LONG TERM EXPOSURE; MEDICAL INFORMATION; MOVEMENT (PHYSIOLOGY); NACHR GENE; NONHUMAN; PATHOGENESIS; QUANTITATIVE STUDY; REAL TIME POLYMERASE CHAIN REACTION; RIC 3 GENE; UNC 29 GENE; UPREGULATION; VELOCITY; WITHDRAWAL REFLEX; ANIMAL; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; TOBACCO DEPENDENCE;

CAENORHABDITIS ELEGANS; NICOTIANA TABACUM;

ANIMALS; CAENORHABDITIS ELEGANS; MOTOR ACTIVITY; NICOTINE; NICOTINIC AGONISTS; RECEPTORS, NICOTINIC; TOBACCO USE DISORDER;

EID: 84921521355     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2014.12.005     Document Type: Article

References (57)

1. Anderson G.L., Boyd W.A., Williams P.L. Assessment of sublethal endpoints for toxicity testing with the nematode Caenorhabditis elegans. Environ Toxicol Chem 2001, 20:833-838.
2. Anderson G.L., Cole R.D., Williams P.L. Assessing behavioral toxicity with Caenorhabditis elegans. Environ Toxicol Chem 2004, 23:1235-1240.
3. Azam L., Winzer-Serhan U., Leslie F.M. Co-expression of alpha7 and beta2 nicotinic acetylcholine receptor subunit mRNAs within rat brain cholinergic neurons. Neuroscience 2003, 119:965-977.
4. Ballivet M., Alliod C., Bertrand S., Bertrand D. Nicotinic acetylcholine receptors in the nematode Caenorhabditis elegans. J Mol Biol 1996, 258:261-269.
5. Belluzzi J.D., Lee A.G., Oliff H.S., Leslie F.M. Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology (Berl) 2004, 174:389-395.
6. Benowitz N.L. Drug therapy: pharmacologic aspects of cigarette smoking and nicotine addition. N Engl J Med 1988, 319:1318-1330.
7. Brenner S. The genetics of Caenorhabidits elegans. Genetics 1974, 77:71-94.
8. Cahir E., Pillidge K., Drago J., Lawrence A.J. The necessity of alpha 4* nicotinic receptors in nicotine-driven behaviors: dissociation between reinforcing and motor effects of nicotine. Neuropsychopharmacology 2011, 36:1505-1517.
9. Castillo M., Mulet J., Gutierrez L.M., Ortiz J.A., Castelan F., Gerber S., et al. Dual role of the RIC-3 protein in trafficking of serotonin and nicotinic acetylcholine receptors. J Biol Chem 2005, 280:27062-27068.
10. Changeux J.P., Edelstein S.J. Allosteric receptors after 30 years. Neuron 1998, 21:959-980.
11. Culetto E., Baylis H.A., Richmond J.E., Jones A.K., Fleming J.T., Squire M.D., et al. The Caenorhabditis elegans unc-63 gene encodes a Levamisole-sensitive nicotinic acetylcholine receptor alpha subunit. J Biol Chem 2004, 279:42476-42483.
12. Cutter A.D., Dey A., Murray R.L. Evolution of the Caenorhabditis elegans genome. Mol Biol Evol 2009, 26:1199-1234.
13. Faraday M.M., Elliott B.M., Grunberg N.E. Adult vs. adolescent rats differ in biobehavioral responses to chronic nicotine administration. Pharmacol Biochem Behav 2001, 70:475-489.
14. Feng Z., Li W., Ward A., Piggott B.J., Larkspur E.R., Sternberg P.W., et al. A C. elegans model of nicotine-dependent behavior: regulation by TRP-family channels. Cell 2006, 127:621-633.
15. Francis M.M., Evans S.P., Jensen M., Madsen D.M., Mancuso J., Norman K.R., et al. The Ror receptor tyrosine kinase CAM-1 is required for ACR-16-mediated synaptic transmission at the C. elegans neuromuscular junction. Neuron 2005, 46:581-594.
16. Gerzanich V., Wang F., Kuryatov A., Lindstrom J. Alpha 5 subunit alters desensitization, pharmacology, Ca++ permeability and Ca++ modulation of human neuronal alpha 3 nicotinic receptors. J Pharmacol Exp Ther 1998, 286:311-320.
17. Gottschalk A., Almedom R.B., Schedletzky T., Anderson S.D., Yates J.R., Schafer W.R. Identification and characterization of novel nicotinic receptor-associated proteins in Caenorhabditis elegans. EMBO J 2005, 24:2566-2578.
18. Halevi S., McKay J., Palfreyman M., Yassin L., Eshel M., Jorgensen E., et al. The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J 2002, 21:1012-1020.
19. Henningfield J.E., Shiffman S., Ferguson S.G., Gritz E.R. Tobacco dependence and withdrawal: science base, challenges and opportunities for pharmacotherapy. Pharmacol Ther 2009, 123:1-16.
20. Hernando G., Berge I., Rayes D., Bouzat C. Contribution of subunits to Caenorhabditis elegans levamisole-sensitive nicotinic receptor function. Mol Pharmacol 2012, 82:550-560.
21. Jones A.K., Davis P., Hodgkin J., Sattelle D.B. The nicotinic acetylcholine receptor gene family of the nematode Caenorhabditis elegans: an update on nomenclature. Invert Neurosci 2007, 7:129-131.
22. Jones A.K., Sattelle D.B. Functional genomics of the nicotinic acetylcholine receptor gene family of the nematode, Caenorhabditis elegans. Bioessays 2003, 26:39-49.
23. Jospin M., Qi Y.B., Stawicki T.M., Boulin T., Schuske K.R., Horvitz H.R., et al. A neuronal acetylcholine receptor regulates the balance of muscle excitation and inhibition in Caenorhabditis elegans. PLoS Biol 2009, 7.
24. Karlin A. Emerging structure of the nicotinic acetylcholine receptors. Nat Rev Neurosci 2002, 3:102-114.
25. Lansdell S.J., Gee V.J., Harkness P.C., Doward A.I., Baker E.R., Gibb A.J., et al. RIC-3 enhances functional expression of multiple nicotinic acetylcholine receptor subtypes in mammalian cells. Mol Pharmacol 2005, 68:1431-1438.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 2001, 25:402-408.
27. Marks M.J. Genetic matters: thirty years of progress using mouse models in nicotinic research. Biochem Pharmacol 2013, 86:1105-1113.
28. Matta S.G., Balfour D.J., Benowitz N.L., Boyd R.T., Buccafusco J.J., Caggiula A.R., et al. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 2007, 190:269-319.
29. Millar N.S. RIC-3: a nicotinic acetylcholine receptor chaperone. Br J Pharmacol 2008, 153(Suppl. 1):S177-S183.
30. Mineur Y.S., Picciotto M.R. Genetics of nicotinic acetylcholine receptors: relevance to nicotine addiction. Biochem Pharmacol 2008, 75:323-333.
31. Mongan N.P., Baylis H.A., Adcock C., Smith G.R., Sansom M.S., Sattelle D.B. An extensive and diverse gene family of nicotinic acetylcholine receptor alpha subunits in Caenorhabditis elegans. Receptors Channels 1998, 6:213-228.
32. Mongan N.P., Jones A.K., Smith G.R., Sansom M.S.P., Sattelle D.B. Novel alpha 7-like nicotinic acetylcholine receptor subunits in the nematode Caenorhabditis elegans. Protein Sci 2002, 11:1162-1171.
33. Petrash H.A., Philbrook A., Haburcak M., Barbagallo B., Francis M.M. ACR-12 ionotropic acetylcholine receptor complexes regulate inhibitory motor neuron activity in Caenorhabditis elegans. J Neurosci 2013, 33:5524-5532.
34. Pidoplichko V.I., DeBiasi M., Williams J.T., Dani J.A. Nicotine activates and desensitizes midbrain dopamine neurons. Nature 1997, 390:401-404.
35. Ramot D., Johnson B.E., Berry T.L., Carnell L., Goodman M.B. The parallel worm tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PLoS ONE 2008, 3.
36. Rand J.B. Acetylcholine. WormBook: the online review of C. elegans biology 2007, 1-21.
37. Riddle D.L., Blumenthal T., Meyer B.J., Priess J.R. Introduction to C. elegans. C. elegans II 1997, Cold Spring Harbor, New York. D.L. Riddle, T. Blumenthal, B.J. Meyer, J.R. Priess (Eds.).
38. Roh J.Y., Choi P.Y.J. A cadmium toxicity assay using stress responsive Caenorhabditis elgans mutant strains. Environ Toxicol Pharmacol 2009, 28:409-413.
39. Rose J.K., Miller M.K., Crane S.A., Hope K.A., Pittman P.G. Parental and larval exposure to nicotine modulate spontaneous activity as well as cholinergic and GABA receptor expression in adult C. elegans. Neurotoxicol Teratol 2013, 39:122-127.
40. Sattelle D.B., Culetto E., Grauso M., Raymond V., Franks C.J., Towers P. Functional genomics of ionotropic acetylcholine receptors in Caenorhabditis elegans and Drosophila melanogaster. Novartis Found Symp 2002, 245:240-260.
41. Saur T., DeMarco S.E., Ortiz A., Sliwoski G.R., Hao L.M., Wang X., et al. A genome-wide RNAi screen in Caenorhabditis elegans identifies the nicotinic acetylcholine receptor subunit ACR-7 as an antipsychotic drug target. PLoS Genet 2013, 9.
42. Schafer W.R. Addiction research in a simple animal model: the nematode Caenorhabditis elegans. Neuropharmacology 2004, 47(Suppl. 1):123-131.
43. Sellings L., Pereira S., Qian C., Dixon-McDougall T., Nowak C., Zhao B., et al. Nicotine-motivated behavior in Caenorhabditis elegans requires the nicotinic acetylcholine receptor subunits acr-5 and acr-15. Eur J Neurosci 2013, 37:743-756.
44. Sherlekar A.L., Janssen A., Siehr M.S., Koo P.K., Caflisch L., Boggess M., et al. The C. elegans male exercises directional control during mating through cholinergic regulation of sex-shared command interneurons. PLOS ONE 2013, 8:e60597.
45. Slawecki C.J., Ehlers C.L. Lasting effects of adolescent nicotine exposure on the electroencephalogram, event related potentials, and locomotor activity in the rat. Dev Brain Res 2002, 138:15-25.
46. Slotkin T.A. Nicotine and the adolescent brain: insights from an animal model. Neurotoxicol Teratol 2002, 24:369-384.
47. Smith M.A., Zhang Y., Polli J.R., Wu H., Zhang B., Xiao P., et al. Impacts of chronic low-level nicotine exposure on Caenorhabditis elegans reproduction: identification of novel gene targets. Reprod Toxicol 2013, 40:69-75.
48. Sobkowiak R., Kowalski M., Lesicki A. Concentration- and time-dependent behavioral changes in Caenorhabditis elegans after exposure to nicotine. Pharmacol Biochem Behav 2011, 99:365-370.
49. Taki F.A., Zhang B. Determination of reliable reference genes for multi-generational gene expression analysis on C. elegans exposed to abused drug nicotine. Psychopharmacology (Berl) 2013, 230:77-88.
50. Touroutine D., Fox R.M., Von Stetina S.E., Burdina A., Miller D.M., Richmond J.E. acr-16 encodes an essential subunit of the levamisole-resistant nicotinic receptor at the Caenorhabditis elegans neuromuscular junction. J Biol Chem 2005, 280:27013-27021.
51. Towers P.R., Edwards B., Richmond J.E., Sattelle D.B. The Caenorhabditis elegans lev-8 gene encodes a novel type of nicotinic acetylcholine receptor alpha subunit. J Neurochem 2005, 93:1-9.
52. Treinin M., Gillo B., Liebman L., Chalfie M. Two functionally dependent acetylcholine subunits are encoded in a single Caenorhabditis elegans operon. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15492-15495.
53. Waggoner L.E., Dickinson K.A., Poole D.S., Tabuse Y., Miwa J., Schafer W.R. Long-term nicotine adaptation in Caenorhabditis elegans involves PKC-dependent changes in nicotinic receptor abundance. J Neurosci 2000, 20:8802-8811.
54. Wolf F.W., Heberlein U. Invertebrate models of drug abuse. J Neurobiol 2003, 54:161-178.
55. Wonnacott S. The paradox of nicotinic acetylcholine receptor upregulation by nicotine. Trends Pharmacol Sci 1990, 11:216-219.
56. Wormatlas. Wormbook. http://www.wormbook.org/.
57. Zhang Y., Chen D., Smith M.A., Zhang B., Pan X. Selection of reliable reference genes in Caenorhabditis elegans for analysis of nanotoxicity. PLoS ONE 2012, 7:e31849.