lynx1 supports neuronal health in the mouse dorsal striatum during aging: An ultrastructural investigation

Journal of Molecular Neuroscience

Volumn 53, Issue 3, 2014, Pages 525-536

  Kobayashi, Atsuko ^a,b   Parker, Rell L ^a   Wright, Ashley P ^c   Brahem, Hajer ^c   Ku, Pauline ^c   Oliver, Katherine M ^d   Walz, Andreas ^c   Lester, Henry A ^a   Miwa, Julie M ^a,d  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c Ophidion Inc   (United States)

^d LEHIGH UNIVERSITY   (United States)

Author keywords

Cholinergic system; Learning and memory; Neurodegeneration; Neurotoxins; Nicotinic acetylcholine receptors; Plasticity; Prototoxins

Indexed keywords

BINDING PROTEIN; NICOTINIC RECEPTOR; PROTEIN LYNX1; UNCLASSIFIED DRUG; LYNX1 PROTEIN, MOUSE; MEMBRANE PROTEIN; NEUROPEPTIDE;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; CORPUS STRIATUM; MOLECULAR INTERACTION; MOUSE; MYELIN SHEATH; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE FIBER; NEUROPROTECTION; NONHUMAN; PHENOTYPE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; ULTRASTRUCTURE;

LYNX; MUS;

AGING; ANIMALS; CORPUS STRIATUM; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MYELIN SHEATH; NEURONS; NEUROPEPTIDES;

EID: 84905019070     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0352-1     Document Type: Article

References (44)

1. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73-120
2. Berger F, Gage FH, Vijayaraghavan S (1998) Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J Neurosci 18:6871-6881
3. Bordia T, Campos C, Huang L, Quik M(2008) Continuous and intermittent nicotine treatment reduces L-3,4-dihydroxyphenylalanine (L-DOPA)-induced dyskinesias in a rat model of Parkinson's disease. J Pharmacol Exp Ther 327:239-247
4. Colquhoun LM, Patrick JW (1997) Pharmacology of neuronal nicotinic acetylcholine receptor subtypes. Adv Pharmacol 39:191-220
5. Costa G, Abin-Carriquiry JA, Dajas F (2001) Nicotine prevents striatal dopamine loss produced by 6-hydroxydopamine lesion in the substantia nigra. Brain Res 888:336-342 (Pubitemid 32058803)
6. Court J, Clementi F (1995) Distribution of nicotinic subtypes in human brain. Alzheimer Dis Assoc Disord 9(Suppl 2):6-14
7. Cragg B (1980) Preservation of extracellular space during fixation of the brain for electron microscopy. Tissue Cell 12:63-72
8. Dajas F, Costa G, Abin-Carriquiry JA, McGregor R, Urbanavicius J (2001) Involvement of nicotinic acetylcholine receptors in the protection of dopamine terminals in experimental parkinsonism. Funct Neurol 16:113-123 (Pubitemid 34295902)
9. Dajas-Bailador FA, Lima PA, Wonnacott S (2000) The alpha7 nicotinic acetylcholine receptor subtype mediates nicotine protection against NMDA excitotoxicity in primary hippocampal cultures through a Ca(2+) dependent mechanism. Neuropharmacology 39:2799-2807
10. Decker MW, McGaugh JL (1991) The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse 7:151-168
11. Geula C, Nagykery N, Nicholas A, Wu CK (2008) Cholinergic neuronal and axonal abnormalities are present early in aging and in Alzheimer disease. J Neuropathol Exp Neurol 67:309-318 (Pubitemid 351507486)
12. Hill JA Jr, Zoli M, Bourgeois J-P, Changeux J-P (1993) Immunocytochemical localization of a neuronal nicotinic receptor: The β2 subunit. J Neurosci 13:1551-1568 (Pubitemid 23095398)
13. Huang LZ, Abbott LC, Winzer-Serhan UH (2007) Effects of chronic neonatal nicotine exposure on nicotinic acetylcholine receptor binding, cell death and morphology in hippocampus and cerebellum. Neuroscience 146:1854-1868 (Pubitemid 46783205)
14. Ibanez-Tallon I, Miwa JM, Wang HL, Adams NC, Crabtree GW, Sine SM, Heintz N (2002) Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron 33:893-903 (Pubitemid 34246355)
15. Kaneko S, Maeda T, Kume T, Kochiyama H, Akaike A, Shimohama S, Kimura J (1997) Nicotine protects cultured cortical neurons against glutamate-induced cytotoxicity via alpha7-neuronal receptors and neuronal CNS receptors. Brain Res 765:135-140 (Pubitemid 27374924)
16. Khwaja M, McCormack A, McIntosh JM, DiMonte DA, Quik M (2007) Nicotine partially protects against paraquat-induced nigrostriatal damage in mice; link to α6β2*nAChRs. J Neurochem 100:180-190 (Pubitemid 46085848)
17. Levin ED, McClernon FJ, Rezvani AH (2005) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl) 1-17
18. McCallum SE, Parameswaran N, Bordia T, Fan H, Tyndale RF, Langston JW, McIntosh JM, Quik M (2006) Increases in α4*but not α3*/α6*nicotinic receptor sites and function in the primate striatum following chronic oral nicotine treatment. J Neurochem 96:1028-1041
19. Miwa JM, Ibanez-Tallon I, Crabtree GW, Sanchez R, Sali A, Role LW, Heintz N (1999) lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 23:105-114 (Pubitemid 29262468)
20. Miwa JM, Stevens TR, King SL, Caldarone BJ, Ibanez-Tallon I, Xiao C, Fitzsimonds RM, Pavlides C, Lester HA, Picciotto MR et al (2006) The prototoxin lynx1 acts on nicotinic acetylcholine receptors to balance neuronal activity and survival in vivo. Neuron 51:587-600 (Pubitemid 44301826)
21. Miwa JM, Freedman R, Lester HA (2011) Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron 70:20-33
22. Miwa JM, Lester HA, Walz A (2012) Optimizing cholinergic tone through lynx modulators of nicotinic receptors: implications for plasticity and nicotine addiction. Physiology (Bethesda) 4:187-199
23. Morishita H, Miwa JM, Heintz N, Hensch TK (2010) Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 330:1238-1240
24. O'NeillMJ, Murray TK, Lakics V, Visanji NP, Duty S (2002) The role of neuronal nicotinic acetylcholine receptors in acute and chronic neurodegeneration. Curr Drug Targets CNS Neurol Disord 1:399-411
25. Orb S, Wieacker J, Labarca C, Fonck C, Lester HA, Schwarz J (2004) Knockinmicewith Leu9'Ser α4 nicotinic receptors: substantia nigra dopaminergic neurons are hypersensitive to agonist and lost postnatally. Physiol Genomics 18:299-307 (Pubitemid 39319513)
26. Orr-Urtreger A, Broide RS, Kasten MR, Dang H, Dani JA, Beaudet AL, Patrick JW (2000) Mice homozygous for the L250T mutation in the α7 nicotinic acetylcholine receptor show increased neuronal apoptosis and die within 1 day of birth. J Neurochem 74:2154-2166 (Pubitemid 30217673)
27. Perez XA, Bordia T, McItosh JM, Grady SR, Quik, M (2008) Long-term nicotine treatment differentially regulates striatal α6α4β 2*and α6 (non-α4) β2*nAChR expression and function. Mol Pharmacol 74:844-853
28. Pfeffer CK, SteinV, Keating DJ, Maier H, Rinke I, Rudhard Y, Hentschke M, Rune GM, Jentsch TJ, Huebner CA (2009) NKCC1- dependent GABAergic excitation drives synaptic network maturation during early hippocampal development. J Neurosci 29: 3419-3430
29. Picciotto MR (2003) Nicotine as a modulator of behavior: beyond the inverted U. Trends Pharmacol Sci 24:493-499
30. Picciotto MR, Zoli M (2008) Neuroprotection via nAChRs: the role of nAChRs in neurodegenerative disorders such as Alzheimer 's and Parkinson's disease. Front Biosci 13:492-504 (Pubitemid 351599760)
31. Picciotto MR, Zoli M, Lena C, Bessis A, Lallemand Y, LeNovere N, Vincent P, Pich EM, Brulet P, Changeux JP (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374:65-67
32. Quik M, Kulak JM (2002) Nicotine and nicotinic receptors; relevance to Parkinson's disease. Neurotoxicology 23:581-594 (Pubitemid 36527678)
33. Quik M, Cox H, Parameswaran N, O'Leary K, Langston JW, DiMonte D (2007) Nicotine reduces levodopa-induced dyskinesias in lesioned monkeys. Ann Neurol 62:588-596
34. Ryan RE, Ross SA, Drago J, Loiacono RE (2001) Dose-related neuroprotective effects of chronic nicotine in 6-hydroxydopamine treated rats, and loss of neuroprotection in α4 nicotinic receptor subunit knockout mice. Br J Pharmacol 132:1650-1656 (Pubitemid 32397956)
35. Schliebs R, Arendt T (2011) The cholinergic system in aging and neuronal degeneration. Behav Brain Res 221:555-563
36. Sekhon HS, Song P, Jia Y, Lindstrom J, Spindel ER (2005) Expression of lynx1 in developing lung and its modulation by prenatal nicotine exposure. Cell Tissue Res 320: 287-297 (Pubitemid 40684755)
37. Spencer-Segal JL, Waters EM, Bath KG, Chao MV, McEwen BS, Milner TA (2011) Distribution of phosphorylated TrkB receptor in the mouse hippocampa; formation depends on sex and estrous cycle stage. J Neurosci 31: 6780-6790
38. Stevens TR, Krueger SR, Fitzsimonds RM, Picciotto MR (2003) Neuroprotection by nicotine in mouse primary cortical cultures involves activation of calcineurin and L-type calcium channel inactivation. J Neurosci 23:10093-10099 (Pubitemid 37392556)
39. Tekinay AB, Nong Y, Miwa JM, Lieberam I, Ibanez-Tallon I, Greengard P, Heintz N (2009) A role for LYNX2 in anxiety-related behavior. Proc Natl Acad Sci U S A 106:4477-4482
40. Terry AV Jr, Buccafusco JJ (2003) The cholinergic hypothesis of age and Alzheimer 's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J Pharmacol Exp Ther 306:821-827
41. Toulorge D, Guerreiro S, Hild A, Maskos U, Hirsch EC, Michel PP (2011) Neuroprotection of midbrain dopamine neurons by nicotine is gated by cytoplasmic Ca2+. FASEB J 25:2563-2573
42. 2+. Neuron 8:353-362
43. Yamauchi JG, Nemecz A, Nguyen QT, Muller A, Schroeder LF, Talley TT, Lindstrom J, Kleinfeld D, Taylor P (2011) Characterizing ligand-gated ion channel receptors with genetically encoded Ca2++ sensors. PLoS One 6:e16519
44. Zoli M, Picciotto MR, Ferrari R, Cocchi D, Changeux JP (1999) Increased neurodegeneration during ageing in mice lacking high-affinity nicotine receptors. Embo J 18:1235-1244 (Pubitemid 29110308)