Enhancement in Motor Learning through Genetic Manipulation of the Lynx1 Gene

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Miwa, Julie M ^a   Walz, Andreas ^b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b Ophidion Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LYNX1 PROTEIN; NICOTINE; TOXIN; UNCLASSIFIED DRUG;

ADULT ANIMAL; AGED; ANIMAL EXPERIMENT; ARTICLE; CHOLINERGIC SYSTEM; CONTROLLED STUDY; GENE; GENETIC ENGINEERING; GENETIC MANIPULATION; LEARNING; LYNX1 GENE; MOTOR COORDINATION; MOTOR LEARNING; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; ROTAROD TEST; TRANSGENIC MOUSE;

ANIMALS; GENE KNOCKOUT TECHNIQUES; LEARNING; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MOTOR ACTIVITY; NEUROPEPTIDES; RECEPTORS, NICOTINIC; ROTAROD PERFORMANCE TEST; SYNAPSES;

LYNX; MUS;

EID: 84868347589     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043302     Document Type: Article

References (57)

1. Jones S, Sudweeks S, Yakel JL, (1999) Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 22: 555-561.
2. Davis JA, Kenney JW, Gould TJ, (2007) Hippocampal alpha4beta2 nicotinic acetylcholine receptor involvement in the enhancing effect of acute nicotine on contextual fear conditioning. J Neurosci 27: 10870-10877.
3. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, et al. (2011) A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480: 331-335.
4. Picciotto MR, Zoli M, Lena C, Bessis A, Lallemand Y, et al. (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374: 65-67.
5. Decker MW, Majchrzak MJ, Arneric SP, (1993) Effects of lobeline, a nicotinic receptor agonist, on learning and memory. Pharmacol Biochem Behav 45: 571-576.
6. Socci DJ, Sanberg PR, Arendash GW, (1995) Nicotine enhances Morris water maze performance of young and aged rats. Neurobiol Aging 16: 857-860.
7. Collins AC, Burch JB, de Fiebre CM, Marks MJ, (1988) Tolerance to and cross tolerance between ethanol and nicotine. Pharmacol Biochem Behav 29: 365-373.
8. Labarca C, Schwarz J, Deshpande P, Schwarz S, Nowak MW, et al. (2001) Point mutant mice with hypersensitive α4 nicotinic receptors show dopaminergic deficits and increased anxiety. Proc Natl Acad Sci U S A 98: 2786-2791.
9. Miwa JM, Freedman R, Lester HA, (2011) Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron 70: 20-33.
10. Hasselmo ME, Sarter M, (2011) Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36: 52-73.
11. Lin L, Jeanclos EM, Treuil M, Braunewell KH, Gundelfinger ED, et al. (2002) The calcium sensor protein visinin-like protein-1 modulates the surface expression and agonist sensitivity of the α4β2 nicotinic acetylcholine receptor. J Biol Chem 277: 41872-41878.
12. Cheng SB, Amici SA, Ren XQ, McKay SB, Treuil MW, et al. (2009) Presynaptic targeting of α4β2 nicotinic acetylcholine receptors is regulated by neurexin-1β. J Biol Chem 284: 23251-23259.
13. Jeanclos EM, Lin L, Treuil MW, Rao J, DeCoster MA, et al. (2001) The chaperone protein 14-3-3η interacts with the nicotinic acetylcholine receptor α4 subunit. Evidence for a dynamic role in subunit stabilization. J Biol Chem 276: 28281-28290.
14. Miwa JM, Ibanez-Tallon I, Crabtree GW, Sanchez R, Sali A, et al. (1999) lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 23: 105-114.
15. Ibanez-Tallon I, Miwa JM, Wang HL, Adams NC, Crabtree GW, et al. (2002) Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron 33: 893-903.
16. Miwa JM, Stevens TR, King SL, Caldarone BJ, Ibanez-Tallon I, et al. (2006) The Prototoxin lynx1 Acts on Nicotinic Acetylcholine Receptors to Balance Neuronal Activity and Survival In Vivo. Neuron 51: 587-600.
17. Morishita H, Miwa JM, Heintz N, Hensch T, (2010) Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 330: 1238-1240.
18. Crawley JN, (1999) Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res 835: 18-26.
19. Liu SJ, Lachamp P, Liu Y, Savtchouk I, Sun L, (2008) Long-term synaptic plasticity in cerebellar stellate cells. Cerebellum 7: 559-562.
20. Thompson RF, Steinmetz JE, (2009) The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162: 732-755.
21. Raymond JL, Lisberger SG, Mauk MD, (1996) The cerebellum: a neuronal learning machine? Science 272: 1126-1131.
22. Lisberger SG, Raymond JL, (1996) Neural recordings and behavioral observations in the monkey vestibulo-ocular reflex constrain the cellular mechanisms for cerebellum-dependent behavioral learning. J Physiol Paris 90: 381-382.
23. Zheng N, Raman IM, (2010) Synaptic inhibition, excitation, and plasticity in neurons of the cerebellar nuclei. Cerebellum 9: 56-66.
24. Reno LA, Zago W, Markus RP, (2004) Release of [(3)H]-L-glutamate by stimulation of nicotinic acetylcholine receptors in rat cerebellar slices. Neuroscience 124: 647-653.
25. Sher E, Chen Y, Sharples TJ, Broad LM, Benedetti G, et al. (2004) Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity. Curr Top Med Chem 4: 283-297.
26. De Filippi G, Baldwinson T, Sher E, (2001) Evidence for nicotinic acetylcholine receptor activation in rat cerebellar slices. Pharmacol Biochem Behav 70: 447-455.
27. De Filippi G, Baldwinson T, Sher E, (2005) Nicotinic receptor modulation of neurotransmitter release in the cerebellum. Prog Brain Res 148: 307-320.
28. Rossi DJ, Hamann M, Attwell D, (2003) Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548: 97-110.
29. Taslim N, Soderstrom K, Dar MS, (2011) Role of mouse cerebellar nicotinic acetylcholine receptor (nAChR) alpha(4)beta(2)- and alpha(7) subtypes in the behavioral cross-tolerance between nicotine and ethanol-induced ataxia. Behav Brain Res 217: 282-292.
30. Court JA, Perry EK, Johnson M, Piggott MA, Kerwin JA, et al. (1993) Regional patterns of cholinergic and glutamate activity in the developing and aging human brain. Brain Res Dev Brain Res 74: 73-82.
31. Middleton SJ, Racca C, Cunningham MO, Traub RD, Monyer H, et al. (2008) High-frequency network oscillations in cerebellar cortex. Neuron 58: 763-774.
32. Lee M, Martin-Ruiz C, Graham A, Court J, Jaros E, et al. (2002) Nicotinic receptor abnormalities in the cerebellar cortex in autism. Brain 125: 1483-1495.
33. Jaarsma D, Ruigrok TJ, Caffe R, Cozzari C, Levey AI, et al. (1997) Cholinergic innervation and receptors in the cerebellum. Prog Brain Res 114: 67-96.
34. Nakayama H, Shioda S, Nakajo S, Ueno S, Nakashima T, et al. (1997) Immunocytochemical localization of nicotinic acetylcholine receptor in the rat cerebellar cortex. Neurosci Res 29: 233-239.
35. Caruncho HJ, Guidotti A, Lindstrom J, Costa E, Pesold C, (1997) Subcellular localization of the alpha 7 nicotinic receptor in rat cerebellar granule cell layer. Neuroreport 8: 1431-1433.
36. Turner JR, Kellar KJ, (2005) Nicotinic cholinergic receptors in the rat cerebellum: multiple heteromeric subtypes. J Neurosci 25: 9258-9265.
37. Luetje CW, Wada K, Rogers S, Abamson SN, Tsuji K, (1990) Neurotoxins distinguish between different neuronal nicotinic acetylcholine receptor subunit combinations. J Neurochem 55: 632-640.
38. Nirthanan S, Gwee MC, (2004) Three-finger alpha-neurotoxins and the nicotinic acetylcholine receptor, forty years on. J Pharmacol Sci 94: 1-17.
39. Tsuji H, Okamoto K, Matsuzaka Y, Iizuka H, Tamiya G, et al. (2003) SLURP-2, a novel member of the human Ly-6 superfamily that is up-regulated in psoriasis vulgaris. Genomics 81: 26-33.
40. Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JD, et al. (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10: 483-511.
41. Chimienti F, Hogg RC, Plantard L, Lehmann C, Brakch N, et al. (2003) Identification of SLURP-1 as an epidermal neuromodulator explains the clinical phenotype of Mal de Meleda. Hum Mol Genet 12: 3017-3024.
42. Tsetlin V, Utkin Y, Kasheverov I, (2009) Polypeptide and peptide toxins, magnifying lenses for binding sites in nicotinic acetylcholine receptors. Biochem Pharmacol 78: 720-731.
43. Darvas M, Morsch M, Racz I, Ahmadi S, Swandulla D, et al. (2009) Modulation of the Ca2+ conductance of nicotinic acetylcholine receptors by Lypd6. Eur Neuropsychopharmacol 19: 670-681.
44. Hruska M, Keefe J, Wert D, Tekinay AB, Hulce JJ, et al. (2009) Prostate stem cell antigen is an endogenous lynx1-like prototoxin that antagonizes α7-containing nicotinic receptors and prevents programmed cell death of parasympathetic neurons. J Neurosci 29: 14847-14854.
45. Tekinay AB, Nong Y, Miwa JM, Lieberam I, Ibanez-Tallon I, et al. (2009) A role for LYNX2 in anxiety-related behavior. Proc Natl Acad Sci U S A 106: 4477-4482.
46. Dessaud E, Salaun D, Gayet O, Chabbert M, deLapeyriere O, (2006) Identification of lynx2, a novel member of the ly-6/neurotoxin superfamily, expressed in neuronal subpopulations during mouse development. Mol Cell Neurosci 31: 232-242.
47. Horie M, Okutomi K, Taniguchi Y, Ohbuchi Y, Suzuki M, et al. (1998) Isolation and characterization of a new member of the human Ly6 gene family (LY6H). Genomics 53: 365-368.
48. Friedman S, Palfree RG, Sirlin S, Hammerling U, (1990) Analysis of three distinct Ly6-A-related cDNA sequences isolated from rat kidney. Immunogenetics 31: 104-111.
49. Bonnon C, Wendeler MW, Paccaud JP, Hauri HP, (2010) Selective export of human GPI-anchored proteins from the endoplasmic reticulum. J Cell Sci 123: 1705-1715.
50. Levitin F, Weiss M, Hahn Y, Stern O, Papke RL, et al. (2008) PATE gene clusters code for multiple, secreted TFP/Ly-6/uPAR proteins that are expressed in reproductive and neuron-rich tissues and possess neuromodulatory activity. J Biol Chem 283: 16928-16939.
51. Dizon MJ, Khodakhah K, (2011) The role of interneurons in shaping Purkinje cell responses in the cerebellar cortex. J Neurosci 31: 10463-10473.
52. Mittmann W, Hausser M, (2007) Linking synaptic plasticity and spike output at excitatory and inhibitory synapses onto cerebellar Purkinje cells. J Neurosci 27: 5559-5570.
53. Wulff P, Schonewille M, Renzi M, Viltono L, Sassoe-Pognetto M, et al. (2009) Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci 12: 1042-1049.
54. Cendelin J, Korelusova I, Vozeh F, (2008) The effect of repeated rotarod training on motor skills and spatial learning ability in Lurcher mutant mice. Behav Brain Res 189: 65-74.
55. van Zanten TS, Cambi A, Koopman M, Joosten B, Figdor CG, et al. (2009) Hotspots of GPI-anchored proteins and integrin nanoclusters function as nucleation sites for cell adhesion. Proc Natl Acad Sci U S A 106: 18557-18562.
56. Lyukmanova EN, Shenkarev ZO, Shulepko MA, Mineev KS, D'Hoedt D, et al. (2011) NMR structure and action on nicotinic acetylcholine receptors of water-soluble domain of human lynx1. J Biol Chem.
57. Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, van Der Oost J, et al. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411: 269-276.