In vivo and in vitro analyses of amygdalar function reveal a role for copper

Journal of Neurophysiology

Volumn 111, Issue 10, 2014, Pages 1927-1939

  Gaier, E D ^a   Rodriguiz, R M ^b   Zhou, J ^b   Ralle, M ^c   Wetsel, W C ^b   Eipper, B A ^a   Mains, R E ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Fear; GABA; Learning and memory; Peptidylglycine alpha amidating monooxygenase; Synaptic plasticity

Indexed keywords

ALPHA AMIDATING ENZYME; COPPER; MIXED FUNCTION OXIDASE; MULTIENZYME COMPLEX; PEPTIDYLGLYCINE MONOOXYGENASE;

AMNESIA; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BRAIN LEVEL; COMPARATIVE STUDY; CONDITIONING; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEAR; GABAERGIC TRANSMISSION; GENOTYPE; HIPPOCAMPUS; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; LATERAL AMYGDALA; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SECRETORY PATHWAY; SIGNAL TRANSDUCTION; SUPPLEMENTATION; SYNAPSE; SYNAPTIC EFFICACY; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP; WILD TYPE; ANIMAL; C57BL MOUSE; DIET; FEMALE; GENETICS; METABOLISM; NERVE CELL INHIBITION; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; THALAMUS; TISSUE CULTURE TECHNIQUE; TRANSGENIC MOUSE;

AMYGDALA; ANIMALS; CONDITIONING (PSYCHOLOGY); COPPER; DIET; FEAR; FEMALE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIXED FUNCTION OXYGENASES; MULTIENZYME COMPLEXES; NEURAL INHIBITION; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; SYNAPSES; SYNAPTIC TRANSMISSION; THALAMUS; TISSUE CULTURE TECHNIQUES;

EID: 84900795254     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00631.2013     Document Type: Article

References (72)

1. Akatsu H, Hori A, Yamamoto T, Yoshida M, Mimuro M, Hashizume Y, Tooyama I, Yezdimer EM. Transition metal abnormalities in progressive dementias. Biometals 25: 337-350, 2012.
2. Anagnostaras SG, Josselyn SA, Frankland PW, Silva AJ. Computerassisted behavioral assessment of Pavlovian fear conditioning in mice. Learn Mem 7: 58-72, 2000.
3. Bauer EP, Schafe GE, Ledoux JE. NMDA receptors and L-type voltagegated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 22: 5239-5249, 2002.
4. Bousquet-Moore D, Ma XM, Nillni EA, Czyzyk TA, Pintar JE, Eipper BA, Mains RE. Reversal of physiological deficits caused by diminished levels of peptidylglycine alpha-amidating monooxygenase by dietary copper. Endocrinology 150: 1739-1747, 2009.
5. Bousquet-Moore D, Prohaska JR, Nillni EA, Czyzyk T, Wetsel WC, Mains RE, Eipper BA. Interactions of peptide amidation and copper: novel biomarkers and mechanisms of neural dysfunction. Neurobiol Dis 37: 130-140, 2010.
6. 2+ channels in rat palaeocortical neurons. J Membr Biol 195: 121-136, 2003.
7. Chrosniak LD, Smith LN, McDonald CG, Jones BF, Flinn JM. Effects of enhanced zinc and copper in drinking water on spatial memory and fear conditioning. J Geochem Explor 88: 91-94, 2006.
8. Czyzyk TA, Ning Y, Hsu MS, Peng B, Mains RE, Eipper BA, Pintar JE. Deletion of peptide amidation enzymatic activity leads to edema and embryonic lethality in the mouse. Dev Biol 287: 301-313, 2005.
9. Davis M. Pharmacological and anatomical analysis of fear conditioning. NIDA Res Monogr 97: 126-162, 1990.
10. De M, Ciccotosto GD, Mains RE, Eipper BA. Trafficking of a secretory granule membrane protein is sensitive to copper. J Biol Chem 282: 23362-23371, 2007.
11. Dodani SC, Domaille DW, Nam CI, Miller EW, Finney LA, Vogt S, Chang CJ. Calcium-dependent copper redistributions in neuronal cells revealed by a fluorescent copper sensor and X-ray fluorescence microscopy. Proc Natl Acad Sci USA 108: 5980-5985, 2011.
12. Doreulee N, Yanovsky Y, Haas HL. Suppression of long-term potentiation in hippocampal slices by copper. Hippocampus 7: 666-669, 1997.
13. Duvarci S, Pare D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 27: 4482-4491, 2007.
14. Fisher JL, Macdonald RL. The role of an alpha subtype M2-M3 His in regulating inhibition of GABAA receptor current by zinc and other divalent cations. J Neurosci 18: 2944-2953, 1998.
15. Fujiwara N, Iso H, Kitanaka N, Kitanaka J, Eguchi H, Ookawara T, Ozawa K, Shimoda S, Yoshihara D, Takemura M, Suzuki K. Effects of copper metabolism on neurological functions in Wistar and Wilson's disease model rats. Biochem Biophys Res Commun 349: 1079-1086, 2006.
16. Gaier ED, Eipper BA, Mains RE. Copper signaling in the mammalian nervous system: synaptic effects. J Neurosci Res 91: 2-19, 2013a.
17. Gaier ED, Miller MB, Ralle M, Aryal D, Wetsel WC, Mains RE, Eipper BA. Peptidylglycine alpha-amidating monooxygenase heterozygosity alters brain copper handling with region specificity. J Neurochem 127: 605-619, 2013b.
18. Gaier ED, Rodriguiz RM, Ma XM, Sivaramakrishnan S, Bousquet-Moore D, Wetsel WC, Eipper BA, Mains RE. Haploinsufficiency in peptidylglycine alpha-amidating monooxygenase leads to altered synaptic transmission in the amygdala and impaired emotional responses. J Neurosci 30: 13656-13669, 2010.
19. Goldschmith A, Infante C, Leiva J, Motles E, Palestini M. Interference of chronically ingested copper in long-term potentiation (LTP) of rat hippocampus. Brain Res 1056: 176-182, 2005.
20. Gonzalez M, Reyes-Jara A, Suazo M, Jo WJ, Vulpe C. Expression of copper-related genes in response to copper load. Am J Clin Nutr 88: 830S-834S, 2008.
21. Gybina AA, Prohaska JR. Copper deficiency results in AMP-activated protein kinase activation and acetylCoA carboxylase phosphorylation in rat cerebellum. Brain Res 1204: 69-76, 2008.
22. Hawkins CJ, Perrin DD. Oxidation-reduction potentials of metal complexes in water. Part II. Copper complexes with 2,9-dimethyl-and 2-chloro-1,10-phenanthroline. J Chem Soc (Lond) 1963: 2996-3002, 1963.
23. Jackson B, Harper S, Smith L, Flinn J. Elemental mapping and quantitative analysis of Cu, Zn, and Fe in rat brain sections by laser ablation ICP-MS. Anal Bioanal Chem 384: 951-957, 2006.
24. Kardos J, Kovacs I, Hajos F, Kalman M, Simonyi M. Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability. Neurosci Lett 103: 139-144, 1989.
25. Kim BE, Turski ML, Nose Y, Casad M, Rockman HA, Thiele DJ. Cardiac copper deficiency activates a systemic signaling mechanism that communicates with the copper acquisition and storage organs. Cell Metab 11: 353-363, 2010.
26. 2+ sensitivity of alphabeta3gamma2L GABA(A) receptors. Mol Pharmacol 64: 1145-1152, 2003.
27. Kim JJ, Jung MW. Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 30: 188-202, 2006.
28. Klinman JP. The copper-enzyme family of dopamine beta-monooxygenase and peptidylglycine alpha-hydroxylating monooxygenase: resolving the chemical pathway for substrate hydroxylation. J Biol Chem 281: 3013-3016, 2006.
29. Korte S, Vassallo N, Kramer ML, Kretzschmar HA, Herms J. Modulation of L-type voltage-gated calcium channels by recombinant prion protein. J Neurochem 87: 1037-1042, 2003.
30. Kuramoto N, Wilkins ME, Fairfax BP, Revilla-Sanchez R, Terunuma M, Tamaki K, Iemata M, Warren N, Couve A, Calver A, Horvath Z, Freeman K, Carling D, Huang L, Gonzales C, Cooper E, Smart TG, Pangalos MN, Moss SJ. Phospho-dependent functional modulation of GABA(B) receptors by the metabolic sensor AMP-dependent protein kinase. Neuron 53: 233-247, 2007.
31. La Fontaine S, Mercer JF. Trafficking of the copper-ATPases, ATP7A and ATP7B: role in copper homeostasis. Arch Biochem Biophys 463: 149-167, 2007.
32. LeDoux J. The amygdala. Curr Biol 17: R868-R874, 2007.
33. Ledoux JE. Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184, 2000.
34. Ledoux JE, Cicchetti P, Xagoraris A, Romanski LM. The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10: 1062-1069, 1990.
35. Leiva J, Gaete P, Palestini M. Copper interaction on the long-term potentiation. Arch Ital Biol 141: 149-155, 2003.
36. Leiva J, Palestini M, Infante C, Goldschmidt A, Motles E. Copper suppresses hippocampus LTP in the rat, but does not alter learning or memory in the morris water maze. Brain Res 1256: 69-75, 2009.
37. Leiva J, Palestini M, Tetas M, Lopez J. Copper sensitivity in dorsal hippocampus slices. Arch Ital Biol 138: 175-184, 2000.
38. Levenson CW. Trace metal regulation of neuronal apoptosis: from genes to behavior. Physiol Behav 86: 399-406, 2005.
39. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY. Function and regulation of human copper-transporting ATPases. Physiol Rev 87: 1011-1046, 2007.
40. Lynch SM, Frei B. Reduction of copper, but not iron, by human low density lipoprotein (LDL). Implications for metal ion-dependent oxidative modification of LDL. J Biol Chem 270: 5158-5163, 1995.
41. Ma XM, Kiraly DD, Gaier ED, Wang Y, Kim EJ, Levine ES, Eipper BA, Mains RE. Kalirin-7 is required for synaptic structure and function. J Neurosci 28: 12368-12382, 2008.
42. Mains RE, Eipper BA. Peptides. In: Basic Neurochemistry: Molecular, Cellular and Medical Aspects, edited by Siegal GJ, Agranoff BW, Albers RW, Fisher SK, and Uhler MD. Philidelphia, PA: Lippincott-Raven, 1999, p. 363-382.
43. Mains RE, Park LP, Eipper BA. Inhibition of peptide amidation by disulfiram and diethyldithiocarbamate. J Biol Chem 261: 11938-11941, 1986.
44. Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat Rev Neurosci 5: 844-852, 2004.
45. Maret W, Sandstead HH. Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 20: 3-18, 2006.
46. Mathie A, Sutton GL, Clarke CE, Veale EL. Zinc and copper: pharmacological probes and endogenous modulators of neuronal excitability. Pharmacol Ther 111: 567-583, 2006.
47. McDonald AJ, Mascagni F. Parvalbumin-containing interneurons in the basolateral amygdala express high levels of the alpha1 subunit of the GABAA receptor. J Comp Neurol 473: 137-146, 2004.
48. McDonald AJ, Mascagni F, Muller JF. Immunocytochemical localization of GABABR1 receptor subunits in the basolateral amygdala. Brain Res 1018: 147-158, 2004.
49. McGee TP, Houston CM, Brickley SG. Copper block of extrasynaptic GABAA receptors in the mature cerebellum and striatum. J Neurosci 33: 13431-13435, 2013.
50. Morrisett RA, Mott DD, Lewis DV, Swartzwelder HS, Wilson WA. GABAB-receptor-mediated inhibition of the N-methyl-D-aspartate component of synaptic transmission in the rat hippocampus. J Neurosci 11: 203-209, 1991.
51. Nathan T, Jensen MS, Lambert JD. The slow inhibitory postsynaptic potential in rat hippocampal CA1 neurones is blocked by intracellular injection of QX-314. Neurosci Lett 110: 309-313, 1990.
52. Pan BX, Dong Y, Ito W, Yanagawa Y, Shigemoto R, Morozov A. Selective gating of glutamatergic inputs to excitatory neurons of amygdala by presynaptic GABAb receptor. Neuron 61: 917-929, 2009.
53. Peters C, Munoz B, Sepulveda FJ, Urrutia J, Quiroz M, Luza S, De Ferrari GV, Aguayo LG, Opazo C. Biphasic effects of copper on neurotransmission in rat hippocampal neurons. J Neurochem 119: 78-88, 2011.
54. Porton B, Rodriguiz RM, Phillips LE, Gilbert JW, Feng J, Greengard P, Kao HT, Wetsel WC. Mice lacking synapsin III show abnormalities in explicit memory and conditioned fear. Genes Brain Behav 9: 257-268, 2010.
55. Prigge ST, Mains RE, Eipper BA, Amzel LM. New insights into copper monooxygenases and peptide amidation: structure, mechanism and function. Cell Mol Life Sci 57: 1236-1259, 2000.
56. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284: 805-808, 1999.
57. Railey AM, Micheli TL, Wanschura PB, Flinn JM. Alterations in fear response and spatial memory in pre-and post-natal zinc supplemented rats: remediation by copper. Physiol Behav 100: 95-100, 2010.
58. Sah P, Faber ES, Lopez De AM, Power J. The amygdaloid complex: anatomy and physiology. Physiol Rev 83: 803-834, 2003.
59. Salazar-Weber NL, Smith JP. Copper inhibits NMDA receptor-independent LTP and modulates the paired-pulse ratio after LTP in mouse hippocampal slices. Int J Alzheimers Dis 2011: 864753, 2011.
60. Schlief ML, Craig AM, Gitlin JD. NMDA receptor activation mediates copper homeostasis in hippocampal neurons. J Neurosci 25: 239-246, 2005.
61. Schlief ML, West T, Craig AM, Holtzman DM, Gitlin JD. Role of the Menkes copper-transporting ATPase in NMDA receptor-mediated neuronal toxicity. Proc Natl Acad Sci USA 103: 14919-14924, 2006.
62. Shaban H, Humeau Y, Herry C, Cassasus G, Shigemoto R, Ciocchi S, Barbieri S, van der PH, Kaupmann K, Bettler B, Luthi A. Generalization of amygdala LTP and conditioned fear in the absence of presynaptic inhibition. Nat Neurosci 9: 1028-1035, 2006.
63. Tamano H, Takeda A. Dynamic action of neurometals at the synapse. Metallomics 3: 656-661, 2011.
64. Taylor GA, Rodriguiz RM, Greene RI, Daniell X, Henry SC, Crooks KR, Kotloski R, Tessarollo L, Phillips LE, Wetsel WC. Behavioral characterization of P311 knockout mice. Genes Brain Behav 7: 786-795, 2008.
65. Terunuma M, Pangalos MN, Moss SJ. Functional modulation of GABAB receptors by protein kinases and receptor trafficking. Adv Pharmacol 58: 113-122, 2010.
66. Tully K, Li Y, Tsvetkov E, Bolshakov VY. Norepinephrine enables the induction of associative long-term potentiation at thalamo-amygdala synapses. Proc Natl Acad Sci USA 104: 14146-14150, 2007.
67. Verhaegh GW, Richard MJ, Hainaut P. Regulation of p53 by metal ions and by antioxidants: dithiocarbamate down-regulates p53 DNA-binding activity by increasing the intracellular level of copper. Mol Cell Biol 17: 5699-5706, 1997.
68. Vlachova V, Zemkova H, Vyklicky L Jr. Copper modulation of NMDA responses in mouse and rat cultured hippocampal neurons. Eur J Neurosci 8: 2257-2264, 1996.
69. Weisskopf MG, Bauer EP, Ledoux JE. L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. J Neurosci 19: 10512-10519, 1999.
70. Weisskopf MG, Ledoux JE. Distinct populations of NMDA receptors at subcortical and cortical inputs to principal cells of the lateral amygdala. J Neurophysiol 81: 930-934, 1999.
71. Yin P, Bousquet-Moore D, Annangudi SP, Southey BR, Mains RE, Eipper BA, Sweedler JV. Probing the production of amidated peptides following genetic and dietary copper manipulations. PLoS One 6: e28679, 2011.
72. Zhou WL, Yan P, Wuskell JP, Loew LM, Antic SD. Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons. Eur J Neurosci 27: 923-936, 2008.