Epac2 mediates cAMP-dependent potentiation of neurotransmission in the hippocampus

Journal of Neuroscience

Volumn 35, Issue 16, 2015, Pages 6544-6553

  Fernandes, Herman B ^a   Riordan, Sean ^a   Nomura, Toshihiro ^a   Remmers, Christine L ^a   Kraniotis, Stephen ^a   Marshall, John J ^a   Kukreja, Lokesh ^a   Vassar, Robert ^a   Contractor, Anis ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

cAMP; Epac2; Mossy fiber; Readily releasable pool

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CAMP 2; FORSKOLIN; PROTEIN; RAB PROTEIN; UNCLASSIFIED DRUG; CYCLIC AMP; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAPGEF4 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENSITOMETRY; ELECTROPHYSIOLOGICAL PROCEDURES; EXOCYTOSIS; HIPPOCAMPAL CA1 REGION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MOSSY FIBER; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; KNOCKOUT MOUSE; MALE; METABOLISM; PHYSIOLOGY; SYNAPTOSOME;

ANIMALS; CA3 REGION, HIPPOCAMPAL; COLFORSIN; CYCLIC AMP; EXCITATORY POSTSYNAPTIC POTENTIALS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; LONG-TERM POTENTIATION; MALE; MICE; MICE, KNOCKOUT; MOSSY FIBERS, HIPPOCAMPAL; PRESYNAPTIC TERMINALS; SYNAPTIC TRANSMISSION;

EID: 84929353459     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0314-14.2015     Document Type: Article

References (46)

1. Armstrong JN, Saganich MJ, Xu NJ, Henkemeyer M, Heinemann SF, Contractor A (2006) B-ephrin reverse signaling is required for NMDA-independent long-term potentiation of mossy fibers in the hippocampus. J Neurosci 26:3474-3481. CrossRef Medline
2. Bagri A, Cheng HJ, Yaron A, Pleasure SJ, Tessier-Lavigne M (2003) Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113:285-299. CrossRef Medline
3. Bekkers JM, Clements JD (1999) Quantal amplitude and quantal variance of strontium-induced asynchronous EPSCs in rat dentate granule neurons. J Physiol 516:227-248. CrossRef Medline
4. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39. CrossRef Medline
5. Branham MT, Bustos MA, De Bias GA, Rehmann H, Zarelli VE, Trevino CL, Darszon A, Mayorga LS, Tomes CN (2009) Epac activates the small G proteins Rap 1 and Rab3A to achieve exocytosis. J Biol Chem 284:24825-24839. CrossRef Medline
6. Castillo PE, Janz R, Südhof TC, Tzounopoulos T, Malenka RC, Nicoll RA (1997) Rab3A is essential for mossy fibre long-term potentiation in the hippocampus. Nature 388:590-593. CrossRef Medline
7. Castillo PE, Schoch S, Schmitz F, Südhof TC, Malenka RC (2002) RIMlalpha is required for presynaptic long-term potentiation. Nature 415:327-330. CrossRef Medline
8. Cheung U, Atwood HL, Zucker RS (2006) Presynaptic effectors contributing to cAMP-induced synaptic potentiation in Drosophila. J Neurobiol 66:273-280. CrossRef Medline
9. Chevaleyre V, Castillo PE (2002) Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci U S A 99:9538-9543. CrossRef Medline
10. Contractor A, Swanson G, Heinemann SF (2001) Kainate receptors are involved in short-and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29:209-216. CrossRef Medline
11. de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, Bos JL (1998) Epac is a Rapl guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474-477. CrossRef Medline
12. de Rooij J, Rehmann H, van Triest M, Cool RH, Wittinghofer A, Bos JL (1998) Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J Biol Chem 275:20829-20836. CrossRef Medline
13. Fernandes HB, Catches JS, Petralia RS, Copits BA, Xu J, Russell TA, Swanson GT, Contractor A (2009) High-affinity kainate receptor subunits are necessary for ionotropic but not metabotropic signaling. Neuron 63:818-829. CrossRef Medline
14. Gekel I, Neher E (2008) Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J Neurosci 28:7991-8002. CrossRef Medline
15. Gloerich M, Bos JL (2010) Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50:355-375. CrossRef Medline
16. Huang CC, Hsu KS (2003) Reexamination of the role of hyperpolarizationactivated cation channels in short-and long-term plasticity at hippocampal mossy fiber synapses. Neuropharmacology 44:968-981. CrossRef Medline
17. Huang YY, Li XC, Kandel ER (1994) cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69-79. CrossRef Medline
18. Huang YY, Kandel ER, Varshavsky L, Brandon EP, Qi M, Idzerda RL, McK-night GS, Bourtchouladze R (1995) A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83:1211-1222. CrossRef Medline
19. Kaeser-Woo YJ, Younts TJ, Yang X, Zhou P, Wu D, Castillo PE, Südhof TC (2010) Synaptotagmin-12 phosphorylation by cAMP-dependent protein kinase is essential for hippocampal mossy fiber LTP. J Neurosci 33:9769-9780. CrossRef Medline
20. Kaneko M, Takahashi T (2004) Presynaptic mechanism underlying cAMP-dependent synaptic potentiation. J Neurosci 24:5202-5208. CrossRef Medline
21. Kashima Y, Miki T, Shibasaki T, Ozaki N, Miyazaki M, Yano H, Seino S (1999) Critical role of cAMP-GEFII-Rim2 complex in incretin-potentiated insulin secretion. J Biol Chem 276:46046-46053. CrossRef Medline
22. Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakaya M, Matsuda M, Housman DE, Graybiel AM (1998) A family of cAMP-binding proteins that directly activate Rapl. Science 282:2275-2279. CrossRef Medline
23. Kwan EP, Xie L, Sheu L, Ohtsuka T, Gaisano HY (2007) Interaction between Muncl3-1 and RIM is critical for glucagon-like peptide-1 mediated rescue of exocytotic defects in Muncl3-1 deficient pancreatic beta-cells. Diabetes 56:2579-2588. CrossRef Medline
24. Lawrence JJ, Grinspan ZM, McBain CJ (2004) Quantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus. J Physiol 554:175-193. CrossRef Medline
25. Lonart G, Janz R, Johnson KM, Südhof TC (1998) Mechanism of action of rab3A in mossy fiber LTP. Neuron 21:1141-1150. CrossRef Medline
26. Marie H, Morishita W, Yu X, Calakos N, Malenka RC (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741-752. CrossRef Medline
27. Mellor J, Nicoll RA, Schmitz D (2002) Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science 295:143-147. CrossRef Medline
28. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, MatsuuraY, Iwanaga T, Takai Y, Seino S (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2:805-811. CrossRef Medline
29. Regehr WG, Delaney KR, Tank DW (1994) The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci 14:523-537. Medline
30. Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262:754-757. CrossRef Medline
31. Salin PA, Scanziani M, Malenka RC, Nicoll RA (1996) Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci U S A 93:13304-13309. CrossRef Medline
32. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409. CrossRef Medline
33. Sedej S, Rose T, Rupnik M (2005) cAMP increases Ca2 +-dependent exocytosis through both PKA and Epac2 in mouse melanotrophs from pituitary tissue slices. J Physiol 567:799-813. CrossRef Medline
34. Seino S, Shibasaki T (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85:1303-1342. CrossRef Medline
35. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, Yamanaka M, Zhang C, Tamamoto A, Satoh T, Miyazaki J, Seino S (2007) Essential role of Epac2/Rapl signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci USA 104:19333-19338. CrossRef Medline
36. Song HJ, Ming GL, Poo MM (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature 388:275-279. CrossRef Medline
37. Ster J, de Bock F, Bertaso F, Abitbol K, Daniel H, Bockaert J, Fagni L (2009) Epac mediates PACAP-dependent long-term depression in the hippocampus. J Physiol 587:101-113. CrossRef Medline
38. Suyama S, Hikima T, Sakagami H, Ishizuka T, Yawo H (2007) Synaptic vesicle dynamics in the mossy fiber-CA3 presynaptic terminals of mouse hippocampus. Neurosci Res 59:481-490. CrossRef Medline
39. Terrian DM, Johnston D, Claiborne BJ, Ansah-Yiadom R, Strittmatter WJ, Rea MA (1988) Glutamate and dynorphin release from a subcellular fraction enriched in hippocampal mossy fiber synaptosomes. Brain Res Bull 21:343-351. CrossRef Medline
40. Vandecasteele G, Rochais F, Abi-Gerges A, Fischmeister R (2006) Functional localization of cAMP signalling in cardiac myocytes. Biochem Soc Trans 34:484-488. CrossRef Medline
41. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1994) Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265:1878-1882. CrossRef Medline
42. Woolfrey KM, Srivastava DP, Photowala H, Yamashita M, Barbolina MV, Cahill ME, Xie Z, Jones KA, Quilliam LA, Prakriya M, Penzes P (2009) Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat Neurosci 12:1275-1284. CrossRef Medline
43. Yang Y, Calakos N (2011) Muncl3-1 is required for presynaptic long-term potentiation. J Neurosci 31:12053-12057. CrossRef Medline
44. Yang Y, Shu X, Liu D, Shang Y, Wu Y, Pei L, Xu X, Tian Q, Zhang J, Qian K, Wang YX, Petralia RS, Tu W, Zhu LQ, Wang JZ, Lu Y (2012) EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73:774-788. CrossRef Medline
45. Zhong N, Zucker RS (2005) cAMP acts on exchange protein activated by cAMP/cAMP-regulated guanine nucleotide exchange protein to regulate transmitter release at the crayfish neuromuscular junction. J Neurosci 25:208-214. CrossRef Medline
46. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405. CrossRef