Interactions between mitochondria and the transcription factor myocyte enhancer factor 2 (MEF2) regulate neuronal structural and functional plasticity and metaplasticity

Journal of Physiology

Volumn 593, Issue 16, 2015, Pages 3471-3481

  Brusco, Janaina ^a   Haas, Kurt ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; HYDROGEN PEROXIDASE; MITOCHONDRIAL PROTEIN; MYOCYTE ENHANCER FACTOR 2; OXIDOREDUCTASE; PEROXIDASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ENZYME SYNTHESIS; HUMAN; INTRACELLULAR SIGNALING; METAPLASTICITY; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL GENOME; MITOCHONDRION; MOLECULAR INTERACTION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FUNCTION; NERVOUS SYSTEM PARAMETERS; NEUROANATOMY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION; ANIMAL; NERVE CELL; PHYSIOLOGY;

ANIMALS; MEF2 TRANSCRIPTION FACTORS; MITOCHONDRIA; NEURONAL PLASTICITY; NEURONS;

EID: 84939000993     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.282459     Document Type: Article

References (103)

1. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, Moore A, Rodriguez M, Kellner U, Leo-Kottler B, Auburger G, Bhattacharya SS & Wissinger B (2000). OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26, 211-215.
2. Attwell D & Laughlin SB (2001). An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21, 1133-1145.
3. Bai Y & Attardi G (1998). The mtDNA-encoded ND6 subunit of mitochondrial NADH dehydrogenase is essential for the assembly of the membrane arm and the respiratory function of the enzyme. EMBO J 17, 4848-4858.
4. Bertolotto C, Ricci JE, Luciano F, Mari B, Chambard JC & Auberger P (2000). Cleavage of the serum response factor during death receptor-induced apoptosis results in an inhibition of the c-FOS promoter transcriptional activity. J Biol Chem 275, 12941-12947.
5. Black BL & Olson EN (1998). Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14, 167-196.
6. 2+-dependent gene expression mediated by MEF2 transcription factors. J Biol Chem 275, 197-209.
7. Brancolini C, Benedetti M & Schneider C (1995). Microfilament reorganization during apoptosis: the role of Gas2, a possible substrate for ICE-like proteases. EMBO J 14, 5179-5190.
8. Cameron HA, Kaliszewski CK & Greer CA (1991). Organization of mitochondria in olfactory bulb granule cell dendritic spines. Synapse 8, 107-118.
9. Campbell DS & Holt CE (2003). Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37, 939-952.
10. Cereghetti GM, Stangherlin A, Martins de Brito O, Chang CR, Blackstone C, Bernardi P & Scorrano L (2008). Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci U S A 105, 15803-15808.
11. Chan SL, Griffin WS & Mattson MP (1999). Evidence for caspase-mediated cleavage of AMPA receptor subunits in neuronal apoptosis and Alzheimer's disease. J Neurosci Res 57, 315-323.
12. Chang DT, Honick AS & Reynolds IJ (2006). Mitochondrial trafficking to synapses in cultured primary cortical neurons. J Neurosci 26, 7035-7045.
13. Chang DT & Reynolds IJ (2006). Mitochondrial trafficking and morphology in healthy and injured neurons. Prog Neurobiol 80, 241-268.
14. Chang MY, Sun W, Ochiai W, Nakashima K, Kim SY, Park CH, Kang JS, Shim JW, Jo AY, Kang CS, Lee YS, Kim JS & Lee SH (2007). Bcl-xL/Bax proteins direct the fate of embryonic cortical precursor cells. Mol Cell Biol 27, 4293-4305.
15. Charvet C, Alberti I, Luciano F, Jacquel A, Bernard A, Auberger P & Deckert M (2003). Proteolytic regulation of Forkhead transcription factor FOXO3a by caspase-3-like proteases. Oncogene 22, 4557-4568.
16. Chawla S, Vanhoutte P & Arnold F (2003). Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J Neurochem 85, 151-159.
17. Chen SX, Cherry A, Tari PK, Podgorski K, Kwong YK & Haas K (2012). The transcription factor MEF2 directs developmental visually driven functional and structural metaplasticity. Cell 151, 41-55.
18. Chen C & Regehr WG (2000). Developmental remodeling of the retinogeniculate synapse. Neuron 28, 955-966.
19. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL & Worley PF (2006). Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52, 445-459.
20. Cole CJ, Mercaldo V, Restivo L, Yiu AP, Sekeres MJ, Han JH, Vetere G, Pekar T, Ross PJ, Neve RL, Frankland PW & Josselyn SA (2012). MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nature Neurosci 15, 1255-1264.
21. Colledge M, Snyder EM, Crozier RA, Soderling JA, Jin Y, Langeberg LK, Lu H, Bear MF & Scott JD (2003). Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression, Neuron 40, 595-607.
22. Cribbs JT & Strack S (2007). Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 8, 939-944.
23. Cryns VL, Bergeron L, Zhu H, Li H & Yuan J (1996). Specific cleavage of α-fodrin during Fas- and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1β-converting enzyme/Ced-3 protease distinct from the poly(ADP-ribose) polymerase protease. J Biol Chem 271, 31277-31282.
24. D'Amelio M, Cavallucci V, Middei S, Marchetti C, Pacioni S, Ferri A, Diamantini A, DeZio D, Carrara P, Battistini L, Moreno S, Bacci A, Ammassari-Teule M, Marie H & Cecconi F (2011). Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat Neurosci 14, 69-76.
25. Elmer B & McAllister A (2013). Major histocompatibility complex class I proteins in brain development and plasticity. Trends Neurosci 35, 660-670.
26. Ertürk A, Wang Y & Sheng M (2014). Local pruning of dendrites and spines by caspase-3-dependent and proteasome-limited mechanisms. J Neurosci 34, 1672-1688.
27. Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME & Schratt G (2009). Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 28, 697-710.
28. Flavell SW, Cowan CW, Kim TK, Greer PL, Lin Y, Paradis S, Griffith EC, Hu LS, Chen C & Greenberg ME (2006). Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311, 1008-1012.
29. Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M, Hong EJ, Markenscoff-Papadimitriou E, Bear DM & Greenberg ME (2008). Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60, 1022-1038.
30. François F, Godinho MJ & Grimes ML (2000). CREB is cleaved by caspases during neural cell apoptosis. FEBS Lett 486, 281-284.
31. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F, Smith CL & Youle RJ (2001). The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 1, 515-525.
32. Fukata Y, Adesnik H, Iwanaga T, Bredt DS, Nicoll RA & Fukata M (2006). Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science 313, 1792-1795.
33. Gamblin TC, Chen F, Zambrano A, Abraha A, Lagalwar S, Guillozet AL, Lu M, Fu Y, Garcia-Sierra F, LaPointe N, Miller R, Berry RW, Binder LI & Cryns VL (2003). Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci U S A 100, 10032-10037.
34. Glazner GW, Chan SL, Lu C & Mattson MP (2000). Caspase-mediated degradation of AMPA receptor subunits: a mechanism for preventing excitotoxic necrosis and ensuring apoptosis. J Neurosci 20, 3641-3649.
35. Gong X, Tang X, Wiedmann M, Wang X, Peng J, Zheng D, Blair LA, Marshall J & Mao Z (2003). Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron 38, 33-46.
36. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfield M, Marin L, Charlton MP, Atwood HL & Zinsmaier KE (2005). The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47, 379-393.
37. Haas KF, Miller S & Friedman DB (2007). The ubiquitin-proteasome system postsynaptically regulates glutamatergic synaptic function. Mol Cell Neurosci 35, 64-75.
38. Hongpaisan J, Winters CA & Andrews SB (2004). Strong calcium entry activates mitochondrial superoxide generation, upregulating kinase signaling in hippocampal neurons. J Neurosci 24, 10878-10887.
39. Huesmann GR & Clayton DF (2006). Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation. Neuron 52, 1061-1072.
40. Jiao S & Li Z (2011). Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron 70, 758-772.
41. 1-42 inhibition of LTP is mediated by a signaling pathway involving caspase-3, Akt1 and GSK-3β. Nat Neurosci 14, 545-547.
42. Jonas E ( 2014). Contributions of Bcl-xL to acute and long term changes in bioenergetics during neuronal plasticity. Biochim Biophys Acta 1842, 1168-1178.
43. Kato Y, Zhao M, Morikawa A, Sugiyama T, Chakravortty D, Koide N, Yoshida T, Tapping RI, Yang Y, Yokochi T & Lee JD (2000). Big mitogen-activated kinase regulates multiple members of the MEF2 protein family. J Biol Chem 275, 18534-18540.
44. Keith D & El-Husseini A (2008). Excitation control: balancing PSD-95 function at the synapse. Front Mol Neurosci 4, 1-12.
45. Kothakota S1, Azuma T, Reinhard C, Klippel A, Tang J, Chu K, McGarry TJ, Kirschner MW, Koths K, Kwiatkowski DJ & Williams LT (1997). Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278, 294-298.
46. Kuo CT, Zhu S, Younger S, Jan LY & Jan YN (2006). Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51, 283-290.
47. Labi V, Grespi F, Baumgartner F & Villunger A (2008). Targeting the Bcl-2-regulated apoptosis pathway by BH3 mimetics: a breakthrough in anticancer therapy? Cell Death Differ 15, 977-987.
48. Lazaro JB, Bailey PJ & Lassar AB (2002). Cyclin D-cdk4 activity modulates the subnuclear localization and interaction of MEF2 with SRC-family coactivators during skeletal muscle differentiation. Genes Dev 16, 1792-1805.
49. Levy M, Faas GC, Saggau P, Craigen WJ & Sweatt JD (2003). Mitochondrial regulation of synaptic plasticity in the hippocampus. J Biol Chem 278, 17727-17734.
50. Li Z, Jo J, Jia JM, Lo SC, Whitcomb DJ, Jiao S, Cho K & Sheng M (2010). Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141, 859-871.
51. Li M, Linseman DA, Allen MP, Meintzer JK, Wang X, Laessig T, Wierman ME & Heidenreich KA (2001). Myocyte enhancer factor 2A and 2D undergo phosphorylation and caspase-mediated degradation during apoptosis of rat cerebellar granule neurons. J Neurosci 21, 6544-6552.
52. Li Z, Okamoto K, Hayashi Y & Sheng M (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873-887.
53. Li Z & Sheng M (2012). Caspases in synaptic plasticity. Mol Brain 5, 15.
54. Liu J, Chang L, Roselli F, Almeida OF, Gao X, Wang X, Yew DT & Wu Y (2010). Amyloid-β induces caspase-dependent loss of PSD-95 and synaptophysin through NMDA receptors. J Alzheimers Dis 22, 541-556.
55. Lu C, Fu W, Salvesen GS & Mattson MP (2002). Direct cleavage of AMPA receptor subunit GluR1 and suppression of AMPA currents by caspase-3: implications for synaptic plasticity and excitotoxic neuronal death. Neuromol Med 1, 69-79.
56. MacAskill, AF, Rinholm JE & Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009). Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61, 541-555.
57. Malenka RC & Bear MF (2004). LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
58. Mao, Z (1999). Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286, 785-790.
59. Martin JF, Miano JM, Hustad CM, Copeland NG, Jenkins NA & Olson EN (1994). A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol Cell Biol 14, 1647-1656.
60. Mattson MP, Gleichmann M & Cheng A (2008). Mitochondria in neuroplasticity and neurological disorders. Neuron 60, 748-766.
61. McKinsey TA, Zhang CL & Olson EN (2002). MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27, 4047.
62. Miska EA, Karlsson C, Langley E, Nielsen SJ, Pines J & Kouzarides T (1999). HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J 18, 5099-5107.
63. Morin S, Charron F, Robitaille L & Nemer M (2000). GATA-dependent recruitment of MEF2 proteins to target promoters. EMBO J 19, 2046-2055.
64. Morris RL & Hollenbeck PJ (1995). Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J Cell Biol 131, 1315-1326.
65. Naya FJ, Black BL, Wu H, Bassel-Duby R, Richardson JA, Hill JA & Olson EN (2002). Mitochondrial deficiency and cardiac sudden death in mice lacking the MEF2A transcription factor. Nat Med 8, 1303-1309.
66. Ohsawa S, Hamada S, Kuida K, Yoshida H, Igaki T & Miura M (2010). Maturation of the olfactory sensory neurons by Apaf-1/caspase-9-mediated caspase activity. Proc Natl Acad Sci U S A 107, 13366-13371.
67. Ohtsubo T, Kamada S, Mikami T, Murakami H & Tsujimoto Y (1999). Identification of NRF2, a member of the NF-E2 family of transcription factors, as a substrate for caspase-3(-like) proteases. Cell Death Differ 6, 865-872.
68. Okamoto S, Li Z, Ju C, Scholzke MN, Mathews E, Cui J, Salvesen GS, Bossy-Wetzel E & Lipton SA (2002). Dominant-interfering forms of MEF2 generated by caspase cleavage contribute to NMDA-induced neuronal apoptosis. Proc Natl Acad Sci U S A 99, 3974-3979.
69. Olsen KM & Sheng M (2012). NMDA receptors and BAX are essential for Aβ impairment of LTP. Sci Rep 2, 225.
70. Olson EN, Perry M & Schulz RA (1995). Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev Biol 172, 2-14.
71. Opazo P, Sainlos M & Choquet D (2012). Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol 22, 453-460.
72. Paroni G, Mizzau M, Henderson C, Del Sal G, Schneider C & Brancolini C (2004). Caspase-dependent regulation of histone deacetylase 4 nuclear-cytoplasmic shuttling promotes apoptosis. Mol Biol Cell 15, 2804-2818.
73. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Lo E, Wu D, Saule E, Bouschet T, Matthews P, Isaac JT, Bortolotto ZA, Wang YT & Collingridge GL (2007). LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53, 703-717.
74. Pfeiffer BE1, Zang T, Wilkerson JR, Taniguchi M, Maksimova MA, Smith LN, Cowan CW & Huber KM (2010). Fragile X mental retardation protein is required for synapse elimination by the activity-dependent transcription factor MEF2. Neuron 66, 191-197.
75. Pivovarova NB, Pozzo-Miller LD, Hongpaisan J & Andrews SB (2002). Correlated calcium uptake and release by mitochondria and endoplasmic reticulum of CA3 hippocampal dendrites after afferent synaptic stimulation. J Neurosci 22, 10653-10661.
76. Pop C & Salvesen GS (2009). Human caspases: activation, specificity, and regulation. J Biol Chem 284, 21777-21781.
77. Popov V, Medvedev NI, Davies HA & Stewart MG (2005). Mitochondria form a filamentous reticular network in hippocampal dendrites but are present as discrete bodies in axons: a three-dimensional ultrastructural study. J Comp Neurol 492, 50-65.
78. Potthoff MJ & Olson EN (2007). MEF2: a central regulator of diverse developmental programs. Development 134, 4131-4140.
79. Rangaraju V, Calloway N & Ryan TA (2014). Activity-driven local ATP synthesis is required for synaptic function. Cell 156, 825-835.
80. Rashid A, Cole C & Josselyn S (2014). Emerging roles for MEF2 transcription factors in memory. Genes Brain Behav 13, 118-125.
81. Rudel T & Bokoch GM (1997). Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276, 1571-1574.
82. Sala C, Futai K, Yamamoto K, Worley PF, Hayashi Y & Sheng M (2003). Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein Homer1a. J Neurosci 23, 6327-6337.
83. Sartorelli V, Huang J, Hamamori Y & Kedes L (1997). Molecular mechanisms of myogenic coactivation by p300: direct interaction with the activation domain of MyoD and with the MADS box of MEF2C. Mol Cell Biol 17, 1010-1026.
84. Shalizi AK & Bonni A (2005). Brawn for brains: the role of MEF2 proteins in the developing nervous system. Curr Top Dev Biol 69, 239-266.
85. Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW & Bonni A (2006). A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311, 1012-1017.
86. She H, Yang Q, Shepherd K, Smith Y, Miller G, Testa C & Mao Z (2011). Direct regulation of complex I by mitochondrial MEF2D is disrupted in a mouse model of Parkinson disease and in human patients. J Clin Invest 121, 930-940.
87. Snigdha S, Smith ED, Prieto GA & Cotman CW (2012). Caspase-3 activation as a bifurcation point between plasticity and cell death. Neurosci Bull 28, 14-24.
88. Stowers RS, Megeath LJ, Górska-Andrzejak J, Meinertzhagen IA & Schwarz TL (2002). Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 36, 1063-1077.
89. Sung JY, Engmann O, Teylan MA, Nairn AC, Greengard P & Kim Y (2008). WAVE1 controls neuronal activity-induced mitochondrial distribution in dendritic spines. Proc Natl Acad Sci U S A 105, 3112-3116.
90. Suzuki Y, Nakabayashi Y, Nakata K, Reed JC & Takahashi R (2001). X-linked inhibitor of apoptosis protein (XIAP) inhibits caspase-3 and -7 in distinct modes. J Biol Chem 276, 27058-27063.
91. Tsai N-P, Wilkerson J, Guo W, Maksimova M, DeMartino G, Cowan C & Huber K (2012). Multiple autism-linked genes mediate synapse elimination via proteasomal degradation of a synaptic scaffold PSD-95. Cell 151, 1581-1594.
92. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y & Bellen HJ (2005). Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47, 365-378.
93. Wang JX, Jiao JQ, Li Q, Long B, Wang K, Liu JP, Li YR & Li PF (2011). miR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat Med 17, 71-78.
94. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284, 339-343.
95. Wang H, Pineda VV, Chan GC, Wong ST, Muglia LJ & Storm DR (2003). Type 8 adenylyl cyclase is targeted to excitatory synapses and required for mossy fiber long-term potentiation. J Neurosci 23, 9710-9718.
96. Weber GF & Menko AS (2005). The canonical intrinsic mitochondrial death pathway has a non-apoptotic role in signaling lens cell differentiation. J Biol Chem 280, 22135-22145.
97. Westphal D, Sytnyk V, Schachner M & Leshchynska I (2010). Clustering of the neural cell adhesion molecule (NCAM) at the neuronal cell surface induces caspase-8- and -3-dependent changes of the spectrin meshwork required for NCAM-mediated neurite outgrowth. J Biol Chem 285, 42046-42057.
98. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y & Truman JW (2006). Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9, 1234-1236.
99. Woods GF, Oh WC & Boudewyn LC (2011). Loss of PSD-95 enrichment is not a prerequisite for spine retraction. J Neurosci 31, 12129-12138.
100. Yamada T, Yang Y, Huang J, Coppola G, Geschwind DH & Bonni A (2013). Sumoylated MEF2A coordinately eliminates orphan presynaptic sites and promotes maturation of presynaptic boutons. J Neurosci 33, 4726-4740.
101. Zhang Xh & Poo MM (2002). Localized synaptic potentiation by BDNF requires local protein synthesis in the developing axon. Neuron 36, 675-688.
102. Zhao M, New L, Kravchenko VV, Kato Y, Gram H, di Padova F, Olson EN, Ulevitch RJ & Han J (1999). Regulation of the MEF2 family of transcription factors by p38. Mol Cell Biol 19, 21-30.
103. Zhu Y, Pak D, Qin Y, McCormack SG, Kim MJ, Baumgart JP, Velamoor V, Auberson YP, Osten P, vanAelst L, Sheng M & Zhu JJ (2005). Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 46, 905-916.