Inhibition of adult neurogenesis by inducible and targeted deletion of ERK5 mitogen-activated protein kinase specifically in adult neurogenic regions impairs contextual fear extinction and remote fear memory

Journal of Neuroscience

Volumn 32, Issue 19, 2012, Pages 6444-6455

  Pan, Yung Wei ^a   Chan, Guy C K ^a   Kuo, Chay T ^c   Storm, Daniel R ^a   Xia, Zhengui ^a,b  

^a Department of Pharmacology ^*  (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 7; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONDITIONING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRIC SHOCK; ERK5 GENE; FEAR; GENE; HABITUATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LEARNING; MALE; MAZE TEST; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

AGING; ANIMALS; DENTATE GYRUS; EXTINCTION, PSYCHOLOGICAL; FEAR; GENE DELETION; GENE TARGETING; MALE; MEMORY, LONG-TERM; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEURAL INHIBITION; NEUROGENESIS; RANDOM ALLOCATION; SIGNAL TRANSDUCTION;

EID: 84860668053     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6076-11.2012     Document Type: Article

References (56)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
2. Alvarez-Buylla A, Theelen M, Nottebohm F (1988) Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. Proc Natl Acad Sci U S A 85:8722-8726.
3. Athos J, Impey S, Pineda VV, Chen X, Storm DR (2002) Hippocampal CRE-mediated gene expression is required for contextual memory formation. Nat Neurosci 5:1119-1120.
4. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neu-rosci 1:602-609.
5. Cavanaugh JE, Ham J, Hetman M, Poser S, Yan C, Xia Z (2001) Differential regulation of mitogen-activated protein kinases ERK1/2 and ERK5 by neurotrophins, neuronal activity, and cAMP in neurons. J Neurosci 21:434-443.
6. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213.
7. Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ (2010) Running enhances spatial pattern separation in mice. Proc Natl Acad Sci U S A 107:2367-2372.
8. Cundiff P, Liu L,Wang Y, Zou J, Pan YW, Abel G, Duan X, Ming GL, Englund C, Hevner R, Xia Z (2009) ERK5 MAP kinase regulates Neurogenin1 during cortical neurogenesis. PLoS One 4:e5204.
9. Deng W, Saxe MD, Gallina IS, Gage FH (2009) Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 29:13532-13542.
10. Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339-350.
11. Denis-Donini S, Dellarole A, Crociara P, Francese MT, Bortolotto V, Qua-drato G, Canonico PL, Orsetti M, Ghi P, Memo M, Bonini SA, Ferrari-Toninelli G, Grilli M (2008) Impaired adult neurogenesis associated with short-term memory defects in NF-kappaB p50-deficient mice. J Neurosci 28:3911-3919.
12. Di Benedetto B, Hitz C, Hölter SM, Kühn R, Vogt Weisenhorn DM, Wurst W (2007) Differential mRNA distribution of components of the ERK/ MAPK signalling cascade in the adult mouse brain. J Comp Neurol 500:542-556.
13. Döbrössy MD, Drapeau E, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 8:974-982.
14. Dupret D, Fabre A, Döbrössy MD, Panatier A, Rodríguez JJ, Lamarque S, Lemaire V, Oliet SH, Piazza PV, Abrous DN (2007) Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 5:e214.
15. Dupret D, Revest JM, Koehl M, Ichas F, De Giorgi F, Costet P, Abrous DN, Piazza PV (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 3:e1959.
16. Farioli-Vecchioli S, Saraulli D, Costanzi M, Pacioni S, Cina I, Aceti M, Micheli L, Bacci A, Cestari V, Tirone F (2008) The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol 6:e246.
17. Finegan KG, Wang X, Lee EJ, Robinson AC, Tournier C (2009) Regulation of neuronal survival by the extracellular signal-regulated protein kinase 5. Cell Death Differ 16:674-683.
18. Fischer A, Radulovic M, Schrick C, Sananbenesi F, Godovac-Zimmermann J, Radulovic J (2007) Hippocampal Mek/Erk signaling mediates extinction of contextual freezing behavior. Neurobiol Learn Mem 87:149-158.
19. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6:119-130.
20. Gao Z, Ure K, Ables JL, Lagace DC, Nave KA, Goebbels S, Eisch AJ, Hsieh J (2009) Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci 12:1090-1092.
21. Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 4:e5464.
22. Guo W, Allan AM, Zong R, Zhang L, Johnson EB, Schaller EG, Murthy AC, Goggin SL, Eisch AJ, Oostra BA, Nelson DL, Jin P, Zhao X (2011) Ablation of Fmrp in adult neural stem cells disrupts hippocampus-dependent learning. Nat Med 17:559-565.
23. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult fore-brain. Nat Neurosci 11:1153-1161.
24. Jaholkowski P, Kiryk A, Jedynak P, Ben Abdallah NM, Knapska E, Kowalczyk A, Piechal A, Blecharz-Klin K, Figiel I, Lioudyno V, Widy-Tyszkiewicz E, Wilczynski GM, Lipp HP, Kaczmarek L, Filipkowski RK (2009) New hippocampal neurons are not obligatory for memory formation; cyclin D2 knockout mice with noadult brain neurogenesis show learning. Learn Mem 16:439-451.
25. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16:147-154.
26. Kempermann G, Kuhn HG, Gage FH (1997) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci U S A 94:10409-10414.
27. Kenney AM, Widlund HR, Rowitch DH (2004) Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cere-bellar neuronal precursors. Development 131:217-228.
28. Kitamura T, Saitoh Y, Takashima N, Murayama A, Niibori Y, Ageta H, Seki-guchi M, Sugiyama H, Inokuchi K (2009) Adult neurogenesis modulates the hippocampus-dependent periodof associative fear memory. Cell 139:814-827.
29. Kuo CT, Mirzadeh Z, Soriano-Navarro M, Rasin M, Wang D, Shen J, Sestan N, Garcia-Verdugo J, Alvarez-Buylla A, Jan LY, Jan YN (2006) Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 127:1253-1264.
30. Lee JD, Ulevitch RJ, Han J (1995) Primary structure of BMK1: a new mammalian map kinase. Biochem Biophys Res Commun 213:715-724.
31. Leuner B, Gould E (2010) Structural plasticity and hippocampal function. Annu Rev Psychol 61:111-140, C1-C3.
32. Leuner B, Mendolia-Loffredo S, Kozorovitskiy Y, Samburg D, Gould E, Shors TJ (2004) Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci 24:7477-7481.
33. Lie DC, Colamarino SA, Song HJ, Désiré L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375.
34. Liu L, Cavanaugh JE, Wang Y, Sakagami H, Mao Z, Xia Z (2003) ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons. Proc Natl Acad Sci U S A 100:8532-8537.
35. Liu L, Cundiff P, Abel G, Wang Y, Faigle R, Sakagami H, Xu M, Xia Z (2006) Extracellular signal-regulated kinase (ERK)5isnecessary and sufficient to specify cortical neuronal fate. Proc Natl Acad Sci U S A 103:9697-9702.
36. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110.
37. Meshi D, Drew MR, Saxe M, Ansorge MS, David D, Santarelli L, Malapani C, Moore H, Hen R (2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9:729-731.
38. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250.
39. Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, Monckton JE, Garcia AD, Sofroniew MV, Kandel ER, Santarelli L, Hen R, Drew MR (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci U S A 103:17501-17506.
40. Shalizi A, Lehtinen M, Gaudilliere B, Donovan N, Han J, Konishi Y, Bonni A (2003) Characterization of a neurotrophin signaling mechanism that mediates neuron survival in a temporally specific pattern. J Neurosci 23:7326-7336.
41. Shan Q, Chan GC, Storm DR (2008) Type 1 adenylyl cyclase is essential for maintenance of remote contextual fear memory. J Neurosci 28:12864-12867.
42. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neuro-genesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:578-584.
43. Silva AJ, Stevens CF, Tonegawa S, Wang Y (1992) Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257:201-206.
44. Suh H, Deng W, Gage FH (2009) Signalingin adult neurogenesis. Annu Rev Cell Dev Biol 25:253-275.
45. Taubenfeld SM, Wiig KA, Bear MF, Alberini CM (1999) A molecular correlate of memory and amnesia in the hippocampus. Nat Neurosci 2:309-310.
46. Wang X, Merritt AJ, Seyfried J, Guo C, Papadakis ES, Finegan KG, Kayahara M, Dixon J, Boot-Handford RP, Cartwright EJ, Mayer U, Tournier C (2005) Targeted deletion of mek5 causes early embryonic death and defects in the extracellular signal-regulated kinase 5/myocyte enhancer factor 2 cell survival pathway. Mol Cell Biol 25:336-345.
47. Wang X, Finegan KG, Robinson AC, Knowles L, Khosravi-Far R, Hinchliffe KA, Boot-Handford RP, Tournier C (2006) Activation of extracellular signal-regulated protein kinase 5 downregulates FasL upon osmotic stress. Cell Death Differ 13:2099-2108.
48. Wang Y, Su B, Xia Z (2006) Brain-derived neurotrophic factor activates ERK5 in cortical neurons via a Rap1-MEKK2 signaling cascade. J Biol Chem 281:35965-35974.
49. Watson FL, Heerssen HM, Bhattacharyya A, Klesse L, Lin MZ, Segal RA (2001) Neurotrophins use the Erk5 pathwayto mediate a retrograde survival response. Nat Neurosci 4:981-988.
50. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
51. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, Muglia LJ, Storm DR (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23:787-798.
52. Wu ZL, Thomas SA, Villacres EC, Xia Z, Simmons ML, Chavkin C, Palmiter RD, Storm DR (1995) Altered behavior and long-term potentiation in type I adeny-lyl cyclase mutant mice. Proc Natl Acad Sci U S A 92:220-224.
53. Yin JC, Wallach JS, Del Vecchio M, Wilder EL, Zhou H, Quinn WG, Tully T (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49-58.
54. Zhang CL, Zou Y, He W, Gage FH, Evans RM (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451:1004-1007.
55. Zhang M, Moon C, Chan GC, Yang L, Zheng F, Conti AC, Muglia L, Muglia LJ, Storm DR, Wang H (2008) Ca-stimulated type 8 adenylyl cyclase is required for rapid acquisition of novel spatial information and for working/episodic-like memory. J Neurosci 28:4736-4744.
56. Zhou G, Bao ZQ, Dixon JE (1995) Components of a new human protein kinase signal transduction pathway. J Biol Chem 270:12665-12669.