Pituitary adenylate cyclase-activating polypeptide induces postsynaptically expressed potentiation in the intra-amygdala circuit

Journal of Neuroscience

Volumn 32, Issue 41, 2012, Pages 14165-14177

  Cho, Jun Hyeong ^a   Zushida, Ko ^b   Shumyatsky, Gleb P ^b   Carlezon, William A ^a   Meloni, Edward G ^a   Bolshakov, Vadim Y ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1;

ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPIKE; SYNAPTIC TRANSMISSION;

EID: 84867249784     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1402-12.2012     Document Type: Article

References (69)

1. Amano T, Unal CT, Paré D (2010) Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13:489-494.
2. Basille M, Vaudry D, Coulouarn Y, Jegou S, Lihrmann I, Fournier A, Vaudry H, Gonzalez B (2000) Comparative distribution of pituitary adenylate cyclase-activating polypeptide (PACAP) binding sites and PACAP receptor mRNAs in the rat brain during development. J Comp Neurol 425:495-509.
3. Cho JH, Bayazitov IT, Meloni EG, Myers KM, Carlezon WA Jr, Zakharenko SS, Bolshakov VY (2012) Coactivation of thalamic and cortical pathways induces input timing-dependent plasticity in amygdala. Nat Neurosci 15:113-122.
4. Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, Müller C, Lüthi A (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277-282.
5. Ciranna L, Cavallaro S (2003) Opposing effects by pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal peptide on hippocampal synaptic transmission. Exp Neurol 184:778-784.
6. Cunha-Reis D, Ribeiro JA, Sebastião AM (2005) VIP enhances synaptic transmission to hippocampal CA1 pyramidal cells through activation of both VPAC1 and VPAC2 receptors. Brain Res 1049:52-60.
7. Das M, Vihlen CS, Legradi G (2007) Hypothalamic and brainstem sources of pituitary adenylate cyclase-activating polypeptide nerve fibers innervating the hypothalamic paraventricular nucleus of the rat. J Comp Neurol 500:761-776.
8. Dickinson T, Fleetwood-Walker SM, Mitchell R, Lutz EM (1997) Evidence for roles of vasoactive intestinal polypeptide (VIP) and pituitary adenylate cyclase activating polypeptide (PACAP) receptors in modulating the responses of rat dorsal horn neurons to sensory inputs. Neuropeptides 31:175-185.
9. Dickson L, Finlayson K (2009) VPAC and PAC receptors: from ligands to function. Pharmacol Ther 121:294-316.
10. Dickson L, Aramori I, McCulloch J, Sharkey J, Finlayson K (2006) Asystematic comparison of intracellular cyclic AMP and calcium signalling highlights complexities in human VPAC/PAC receptor pharmacology. Neuropharmacology 51:1086-1098.
11. Fizanne L, Sigaudo-Roussel D, Saumet JL, Fromy B (2004) Evidence for the involvement of VPAC1 and VPAC2 receptors in pressure-induced vasodilatation in rodents. J Physiol 554:519-528.
12. Gafni J, Munsch JA, Lam TH, Catlin MC, Costa LG, Molinski TF, Pessah IN (1997) Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron 19:723-733.
13. Gourlet P, De Neef P, Cnudde J, Waelbroeck M, Robberecht P (1997) In vitro properties of a high affinity selective antagonist of the VIP1 receptor. Peptides 18:1555-1560.
14. Gray TS, Cassell MD, Nilaver G, Zimmerman EA, Williams TH (1984) The distribution and ultrastructure of VIP-immunoreactivity in the central nucleus of the rat amygdala. Neuroscience 11:399-408.
15. Hammack SE, Roman CW, Lezak KR, Kocho-Shellenberg M, Grimmig B, Falls WA, Braas K, May V (2010) Roles for pituitary adenylate cyclaseactivating peptide (PACAP) expression and signaling in the bed nucleus of the stria terminalis (BNST) in mediating the behavioral consequences of chronic stress. J Mol Neurosci 42:327-340.
16. Hashimoto H, Ishihara T, Shigemoto R, Mori K, Nagata S (1993) Molecular cloning and tissue distribution of a receptor for pituitary adenylate cyclase-activating polypeptide. Neuron 11:333-342.
17. Hashimoto H, Shintani N, Tanaka K, Mori W, Hirose M, Matsuda T, Sakaue M, Miyazaki J, Niwa H, Tashiro F, Yamamoto K, Koga K, Tomimoto S, Kunugi A, Suetake S, Baba A (2001) Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc Natl Acad Sci U S A 98:13355-13360.
18. Hashimoto H, Shintani N, Baba A (2006) New insights into the central PACApergic system from the phenotypes in PACAP- and PACAP receptor-knockout mice. Ann N Y Acad Sci 1070:75-89.
19. Haubensak W, Kunwar PS, Cai H, Ciocchi S, Wall NR, Ponnusamy R, Biag J, Dong HW, Deisseroth K, Callaway EM, Fanselow MS, Lüthi A, Anderson DJ (2010) Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468:270-276.
20. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
21. Herbert JM, Augereau JM, Gleye J, Maffrand JP (1990) Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 172:993-999.
22. Herry C, Ciocchi S, Senn V, Demmou L, Müller C, Lüthi A (2008) Switching on and off fear by distinct neuronal circuits. Nature 454:600-606.
23. Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
24. Ishida A, Kameshita I, Okuno S, Kitani T, Fujisawa H (1995) A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 212:806-812.
25. Ishihara T, Shigemoto R, Mori K, Takahashi K, Nagata S (1992) Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide. Neuron 8:811-819.
26. Joo KM, Chung YH, Kim MK, Nam RH, Lee BL, Lee KH, Cha CI (2004) Distribution of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide receptors (VPAC1, VPAC2, and PAC1 receptor) in the rat brain. J Comp Neurol 476:388-413.
27. Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, Osten P, Schwarz MK, Seeburg PH, Stoop R, Grinevich V (2012) Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73:553-566.
28. Köves K, Arimura A, Görcs TG, Somogyvári-Vigh A (1991) Comparative distribution of immunoreactive pituitary adenylate cyclase activating polypeptide and vasoactive intestinal polypeptide in rat forebrain. Neuroendocrinology 54:159-169.
29. Kozicz T, Arimura A (2002) Dopamine- and cyclic AMP-regulated phosphoprotein-immunoreactive neurons activated by acute stress are innervated by fiber terminals immunopositive for pituitary adenylate cyclase-activating polypeptide in the extended amygdala in the rat. Regul Pept 109:63-70.
30. Kozicz T, Vigh S, Arimura A (1998) The source of origin of PACAP- and VIP-immunoreactive fibers in the laterodorsal division of the bed nucleus of the stria terminalis in the rat. Brain Res 810:211-219.
31. 2+]i increase but not adenylate cyclase stimulation. Cell Signal 17:17-24.
32. Legradi G, Das M, Giunta B, Hirani K, Mitchell EA, Diamond DM (2007) Microinfusion of pituitary adenylate cyclase-activating polypeptide into the central nucleus of amygdala of the rat produces a shift from an active to passive mode of coping in the shock-probe fear/defensive burying test. Neural Plast 2007:79102.
33. Lin MT, Luján R, Watanabe M, Frerking M, Maylie J, Adelman JP (2010) Coupled activity-dependent trafficking of synaptic SK2 channels and AMPA receptors. J Neurosci 30:11726-11734.
34. Lorén I, Emson PC, Fahrenkrug J, Björklund A, Alumets J, Håkanson R, Sundler F (1979) Distribution of vasoactive intestinal polypeptide in the rat and mouse brain. Neuroscience 4:1953-1976.
35. Lutz EM, Sheward WJ, West KM, Morrow JA, Fink G, Harmar AJ (1993) The VIP2 receptor: molecular characterisation of a cDNA encoding a novel receptor for vasoactive intestinal peptide. FEBS Lett 334:3-8.
36. Macdonald DS, Weerapura M, Beazely MA, Martin L, Czerwinski W, Roder JC, Orser BA, MacDonald JF (2005) Modulation of NMDAreceptors by pituitary adenylate cyclase activating peptide in CA1 neurons requires Gαq, protein kinase C, and activation of Src. J Neurosci 25:11374-11384.
37. Masuo Y, Matsumoto Y, Tokito F, Tsuda M, Fujino M (1993) Effects of vasoactive intestinal polypeptide (VIP) and pituitary adenylate cyclase activating polypeptide (PACAP) on the spontaneous release of acethylcholine from hippocampus by brain microdilaysis. Brain Res 611:207-215.
38. Miyata A, Arimura A, Dahl RR, Minamino N, Uehara A, Jiang L, Culler MD, Coy DH (1989) Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 164:567-574.
39. Nielsen KM, Chaverra M, Hapner SJ, Nelson BR, Todd V, Zigmond RE, Lefcort F (2004) PACAP promotes sensory neuron differentiation: blockade by neurotrophic factors. Mol Cell Neurosci 25:629-641.
40. Otto C, Kovalchuk Y, Wolfer DP, Gass P, Martin M, Zuschratter W, Gröne HJ, Kellendonk C, Tronche F, Maldonado R, Lipp HP, Konnerth A, Schütz G (2001a) Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J Neurosci 21:5520-5527.
41. Otto C, Martin M, Wolfer DP, Lipp HP, Maldonado R, Schütz G (2001b) Altered emotional behavior in PACAP-type-I-receptor-deficient mice. Brain Res Mol Brain Res 92:78-84.
42. Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419-463.
43. Piggins HD, Stamp JA, Burns J, Rusak B, Semba K (1996) Distribution of pituitary adenylate cyclase activating polypeptide (PACAP) immunoreactivity in the hypothalamus and extended amygdala of the rat. J Comp Neurol 376:278-294.
44. Pisegna JR, Wank SA (1993) Molecular cloning and functional expression of the pituitary adenylate cyclase-activating polypeptide type I receptor. Proc Natl Acad Sci U S A 90:6345-6349.
45. Polepalli JS, Sullivan RK, Yanagawa Y, Sah P (2010) A specific class of interneuron mediates inhibitory plasticity in the lateral amygdala. J Neurosci 30:14619-14629.
46. Regehr WG, Stevens CF (2001) Physiology of synaptic transmission and short-term plasticity. In: Synapses (Cowan WM, Südhof TC, Stevens CF, eds), pp 135-175. Baltimore, London: Johns Hopkins UP.
47. Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K, Norrholm SD, Kilaru V, Smith AK, Myers AJ, Ramirez M, Engel A, Hammack SE, Toufexis D, Braas KM, Binder EB, May V (2011) Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 470:492-497.
48. Riccio A, Li Y, Moon J, Kim KS, Smith KS, Rudolph U, Gapon S, Yao GL, Tsvetkov E, Rodig SJ, Van't Veer A, Meloni EG, Carlezon WA Jr, Bolshakov VY, Clapham DE (2009) Essential role for TRPC5 in amygdale function and fear-related behavior. Cell 137:761-772.
49. Robberecht P, Gourlet P, De Neef P, Woussen-Colle MC, Vandermeers-Piret MC, Vandermeers A, Christophe J (1992) Structural requirements for the occupancy of pituitary adenylate-cyclase-activating-peptide (PACAP) receptors and adenylate cyclase activation in human neuroblastoma NB-OK-1 cell membranes. Discovery of PACAP(6-38) as a potent antagonist. Eur J Biochem 207:239-246.
50. Roberto M, Brunelli M (2000) PACAP-38 enhances excitatory synaptic transmission in the rat hippocampal CA1 region. Learn Mem 7:303-311.
51. Roberto M, Scuri R, Brunelli M (2001) Differential effects of PACAP-38 on synaptic responses in rat hippocampal CA1 region. Learn Mem 8:265-271.
52. Roberts GW, Woodhams PL, Polak JM, Crow TJ (1982) Distribution of neuropeptides in the limbic system of the rat: the amygdaloid complex. Neuroscience 7:99-131.
53. Royer S, Martina M, Paré D (1999) An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J Neurosci 19:10575-10583.
54. Schaeren-Wiemers N, Gerfin-Moser A (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100:431-440.
55. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
56. Shin RM, Tsvetkov E, Bolshakov VY (2006) Spatiotemporal asymmetry of associative synaptic plasticity in fear conditioning pathways. Neuron 52:883-896.
57. Shioda S, Shuto Y, Somogyvari-Vigh A, Legradi G, Onda H, Coy DH, Nakajo S, Arimura A (1997) Localization and gene expression of the receptor for pituitary adenylate cyclase-activating polypeptide in the rat brain. Neurosci Res 28:345-354.
58. Shumyatsky GP, Malleret G, Shin RM, Takizawa S, Tully K, Tsvetkov E, Zakharenko SS, Joseph J, Vronskaya S, Yin D, Schubart UK, Kandel ER, Bolshakov VY (2005) Stathmin, a gene enriched in the amygdala, controls both learned and innate fear. Cell 123:697-709.
59. Sreedharan SP, Patel DR, Xia M, Ichikawa S, Goetzl EJ (1994) Human vasoactive intestinal peptide1 receptors expressed by stable transfectants couple to two distinct signaling pathways. Biochem Biophys Res Commun 203:141-148.
60. Stella N, Magistretti PJ (1996) Vasoactive intestinal polypeptide (VIP) and pituitary adenylate cyclase activating polypeptide (PACAP) potentiate the glutamate-evoked release of arachidonic acid from mouse cortical neurons. J Biol Chem 271:23705-23710.
61. Sun N, Roberts L, Cassell MD (1991) Rat central amygdaloid nucleus projections to the bed nucleus of the stria terminalis. Brain Res Bull 27:651-662.
62. Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY (2002) Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34:289-300.
63. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358-362.
64. Van Haastert PJ, Van Driel R, Jastorff B, Baraniak J, Stec WJ, De Wit RJ (1984) Competitive cAMP antagonists for cAMP-receptor proteins. J Biol Chem 259:10020-10024.
65. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow BK, Hashimoto H, Galas L, Vaudry H (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61:283-357.
66. Villalba M, Bockaert J, Journot L (1997) Pituitary adenylate cyclaseactivating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J Neurosci 17:83-90.
67. Yang K, Lei G, Jackson MF, Macdonald JF (2010) The involvement of PACAP/VIP system in the synaptic transmission in the hippocampus. J Mol Neurosci 42:319-326.
68. Yang Y, Wang XB, Frerking M, Zhou Q (2008) Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation. Proc Natl Acad Sci U S A 105:11388-11393.
69. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.