Targeted Deletion of the ERK5 MAP Kinase Impairs Neuronal Differentiation, Migration, and Survival during Adult Neurogenesis in the Olfactory Bulb

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Li, Tan ^a,b   Pan, Yung Wei ^a   Wang, Wenbin ^a   Abel, Glen ^a   Zou, Junhui ^a   Xu, Lihong ^b   Storm, Daniel R ^c   Xia, Zhengui ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 7; SHORT HAIRPIN RNA;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL REGULATED KINASE 5 GENE; GENE DELETION; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLFACTORY BULB; OLFACTORY SYSTEM; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; ROSTRAL MIGRATORY STREAM; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE;

ANIMALS; CELL CYCLE; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL VENTRICLES; GENE KNOCKOUT TECHNIQUES; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; OLFACTORY BULB; PRIMARY CELL CULTURE;

MUS;

EID: 84876429721     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061948     Document Type: Article

References (84)

1. Altman J, (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137: 433-457.
2. Ming GL, Song H, (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70: 687-702.
3. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A, (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716.
4. Gage FH, (2000) Mammalian neural stem cells. Science 287: 1433-1438.
5. Whitman MC, Greer CA, (2009) Adult neurogenesis and the olfactory system. Prog Neurobiol 89: 162-175.
6. Ma DK, Kim WR, Ming GL, Song H, (2009) Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann N Y Acad Sci 1170: 664-673.
7. Belvindrah R, Lazarini F, Lledo PM, (2009) Postnatal neurogenesis: from neuroblast migration to neuronal integration. Rev Neurosci 20: 331-346.
8. Hsieh J, (2012) Orchestrating transcriptional control of adult neurogenesis. Genes Dev 26: 1010-1021.
9. Ming GL, Song H, (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223-250.
10. Doetsch F, Hen R, (2005) Young and excitable: the function of new neurons in the adult mammalian brain. Curr Opin Neurobiol 15: 121-128.
11. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, et al. (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci U S A 97: 1823-1828.
12. Breton-Provencher V, Lemasson M, Peralta MR 3rd, Saghatelyan A (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29: 15245-15257.
13. Lazarini F, Mouthon MA, Gheusi G, de Chaumont F, Olivo-Marin JC, et al. (2009) Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS One 4: e7017.
14. Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, et al. (2010) Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. Faseb J 24: 2355-2363.
15. Pan YW, Kuo CT, Storm DR, Xia Z, (2012) Inducible and Targeted Deletion of the ERK5 MAP Kinase in Adult Neurogenic Regions Impairs Adult Neurogenesis in the Olfactory Bulb and Several Forms of Olfactory Behavior. PLoS One 7: e49622.
16. Petreanu L, Alvarez-Buylla A, (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22: 6106-6113.
17. Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG, (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16: 1681-1689.
18. Yokoyama TK, Mochimaru D, Murata K, Manabe H, Kobayakawa K, et al. (2011) Elimination of adult-born neurons in the olfactory bulb is promoted during the postprandial period. Neuron 71: 883-897.
19. Yamaguchi M, Mori K, (2005) Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci U S A 102: 9697-9702.
20. English JM, Vanderbilt CA, Xu S, Marcus S, Cobb MH, (1995) Isolation of MEK5 and differential expression of alternatively spliced forms. J Biol Chem 270: 28897-28902.
21. Zhou G, Bao ZQ, Dixon JE, (1995) Components of a new human protein kinase signal transduction pathway. J Biol Chem 270: 12665-12669.
22. Kuo CT, Mirzadeh Z, Soriano-Navarro M, Rasin M, Wang D, et al. (2006) Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 127: 1253-1264.
23. Wang X, Merritt AJ, Seyfried J, Guo C, Papadakis ES, et al. (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.
24. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
25. Pan YW, Chan GCK, Kuo CT, Storm DR, Xia Z, (2012) 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. J Neurosci 32: 6444-6455.
26. Pan YW, Zou J, Wang W, Sakagami H, Garelick MG, et al. (2012) Inducible and conditional deletion of extracellular signal-regulated kinase 5 disrupts adult hippocampal neurogenesis. J Biol Chem 287: 23306.
27. Wang W, Pan YW, Wietecha T, Zou J, Abel GM, et al. (2013) Extracellular Signal-regulated Kinase 5 (ERK5) Mediates Prolactin-stimulated Adult Neurogenesis in the Subventricular Zone and Olfactory Bulb. J Biol Chem 288: 2623-2631.
28. Bath KG, Mandairon N, Jing D, Rajagopal R, Kapoor R, et al. (2008) Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J Neurosci 28: 2383-2393.
29. Ducruet AF, Zacharia BE, Sosunov SA, Gigante PR, Yeh ML, et al. (2012) Complement inhibition promotes endogenous neurogenesis and sustained anti-inflammatory neuroprotection following reperfused stroke. PLoS One 7: e38664.
30. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, et al. (2011) Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8: 59-71.
31. Kempermann G (2006) Adult Neurogenesis. In: Neurogenesis in the Adult Olfactory System. New York: Oxford University Press 140-167.
32. Cundiff P, Liu L, Wang Y, Zou J, Pan YW, et al. (2009) ERK5 MAP kinase regulates Neurogenin1 during cortical neurogenesis. PLoS ONE 4: e5204.
33. Raponi E, Agenes F, Delphin C, Assard N, Baudier J, et al. (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55: 165-177.
34. Kato Y, Tapping RI, Huang S, Watson MH, Ulevitch RJ, et al. (1998) Bmk1/Erk5 is required for cell proliferation induced by epidermal growth factor. Nature 395: 713-716.
35. Akerblom M, Sachdeva R, Barde I, Verp S, Gentner B, et al. (2012) MicroRNA-124 is a subventricular zone neuronal fate determinant. J Neurosci 32: 8879-8889.
36. Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, et al. (2002) Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci U S A 99: 13211-13216.
37. Belvindrah R, Nissant A, Lledo PM, (2011) Abnormal neuronal migration changes the fate of developing neurons in the postnatal olfactory bulb. J Neurosci 31: 7551-7562.
38. Battista D, Rutishauser U, (2010) Removal of polysialic acid triggers dispersion of subventricularly derived neuroblasts into surrounding CNS tissues. J Neurosci 30: 3995-4003.
39. Lledo PM, Alonso M, Grubb MS, (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7: 179-193.
40. Emsley JG, Mitchell BD, Kempermann G, Macklis JD, (2005) Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 75: 321-341.
41. Imura T, Wang X, Noda T, Sofroniew MV, Fushiki S, (2010) Adenomatous polyposis coli is essential for both neuronal differentiation and maintenance of adult neural stem cells in subventricular zone and hippocampus. Stem Cells 28: 2053-2064.
42. Cude K, Wang Y, Choi HJ, Hsuan SL, Zhang H, et al. (2007) Regulation of the G2-M cell cycle progression by the ERK5-NF{kappa}B signaling pathway. J Cell Biol 177: 253-264.
43. Zou J, Pan YW, Wang Z, Chang SY, Wang W, et al. (2012) Targeted Deletion of ERK5 MAP Kinase in the Developing Nervous System Impairs Development of GABAergic Interneurons in the Main Olfactory Bulb and Behavioral Discrimination between Structurally Similar Odorants. J Neurosci 32: 4118-4132.
44. Liu L, Cundiff P, Abel G, Wang Y, Faigle R, et al. (2006) Extracellular signal-regulated kinase (ERK) 5 is necessary and sufficient to specify cortical neuronal fate. Proc Natl Acad Sci U S A 103: 9697-9702.
45. Anton ES, Ghashghaei HT, Weber JL, McCann C, Fischer TM, et al. (2004) Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci 7: 1319-1328.
46. Mejia-Gervacio S, Murray K, Sapir T, Belvindrah R, Reiner O, et al. (2012) MARK2/Par-1 guides the directionality of neuroblasts migrating to the olfactory bulb. Mol Cell Neurosci 49: 97-103.
47. Rolando C, Parolisi R, Boda E, Schwab ME, Rossi F, et al. (2012) Distinct roles of nogo-a and nogo receptor 1 in the homeostatic regulation of adult neural stem cell function and neuroblast migration. J Neurosci 32: 17788-17799.
48. Saha B, Ypsilanti AR, Boutin C, Cremer H, Chedotal A, (2012) Plexin-b2 regulates the proliferation and migration of neuroblasts in the postnatal and adult subventricular zone. J Neurosci 32: 16892-16905.
49. Miwa N, Storm DR, (2005) Odorant-induced activation of extracellular signal-regulated kinase/mitogen-activated protein kinase in the olfactory bulb promotes survival of newly formed granule cells. J Neurosci 25: 5404-5412.
50. Giachino C, De Marchis S, Giampietro C, Parlato R, Perroteau I, et al. (2005) cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J Neurosci 25: 10105-10118.
51. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, et al. (2009) GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci 29: 7966-7977.
52. Herold S, Jagasia R, Merz K, Wassmer K, Lie DC (2010) CREB signalling regulates early survival, neuronal gene expression and morphological development in adult subventricular zone neurogenesis. Mol Cell Neurosci.
53. Liu L, Cavanaugh JE, Wang Y, Sakagami H, Mao Z, et al. (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 USA 100: 8532-8537.
54. Watson FL, Heerssen HM, Bhattacharyya A, Klesse L, Lin MZ, et al. (2001) Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat Neurosci 4: 981-988.
55. Shalizi A, Lehtinen M, Gaudilliere B, Donovan N, Han J, et al. (2003) Characterization of a neurotrophin signaling mechanism that mediates neuron survival in a temporally specific pattern. J Neurosci 23: 7326-7336.
56. 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.
57. Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, et al. (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131: 3805-3819.
58. Liu HK, Belz T, Bock D, Takacs A, Wu H, et al. (2008) The nuclear receptor tailless is required for neurogenesis in the adult subventricular zone. Genes Dev 22: 2473-2478.
59. Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A, (2005) Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25: 6997-7003.
60. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, et al. (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8: 865-872.
61. Brill MS, Snapyan M, Wohlfrom H, Ninkovic J, Jawerka M, et al. (2008) A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J Neurosci 28: 6439-6452.
62. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, et al. (2009) Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12: 1524-1533.
63. Ninkovic J, Pinto L, Petricca S, Lepier A, Sun J, et al. (2010) The transcription factor Pax6 regulates survival of dopaminergic olfactory bulb neurons via crystallin alphaA. Neuron 68: 682-694.
64. Adachi K, Mirzadeh Z, Sakaguchi M, Yamashita T, Nikolcheva T, et al. (2007) Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25: 2827-2836.
65. Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R, (2010) Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 30: 3489-3498.
66. Ahn S, Joyner AL, (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437: 894-897.
67. Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, et al. (2005) Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132: 335-344.
68. Chiara Rolando RP, Enrica Boda, Martin E Schwab, Ferdinando Rossi, Annalisa Buffo, (2012) Distinct Roles of Nogo-A and Nogo Receptor 1 in the Homeostatic Regulation of Adult Neural Stem Cell Function and Neuroblast Migration. J Neurosci 32: 17788-17799.
69. Marinissen MJ, Chiariello M, Pallante M, Gutkind JS, (1999) A network of mitogen-activated protein kinases links G protein-coupled receptors to the c-jun promoter: a role for c-Jun NH2-terminal kinase, p38 s, and extracellular signal-regulated kinase 5. Mol Cell Biol 19: 4289-4301.
70. Obara Y, Nakahata N, (2010) The signaling pathway leading to extracellular signal-regulated kinase 5 (ERK5) activation via G-proteins and ERK5-dependent neurotrophic effects. Mol Pharmacol 77: 10-16.
71. Kendrick TS, Bogoyevitch MA, (2007) Activation of mitogen-activated protein kinase pathways by the granulocyte colony-stimulating factor receptor: mechanisms and functional consequences. Front Biosci 12: 591-607.
72. Ghashghaei HT, Weber J, Pevny L, Schmid R, Schwab MH, et al. (2006) The role of neuregulin-ErbB4 interactions on the proliferation and organization of cells in the subventricular zone. Proc Natl Acad Sci U S A 103: 1930-1935.
73. Tang M, Miyamoto Y, Huang EJ, (2009) Multiple roles of beta-catenin in controlling the neurogenic niche for midbrain dopamine neurons. Development 136: 2027-2038.
74. Favaro R, Valotta M, Ferri AL, Latorre E, Mariani J, et al. (2009) Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat Neurosci 12: 1248-1256.
75. Jiao J, Chen DF, (2008) Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells 26: 1221-1230.
76. Kenney AM, Widlund HR, Rowitch DH, (2004) Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131: 217-228.
77. Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, et al. (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39: 937-950.
78. Pozniak CD, Pleasure SJ, (2006) A tale of two signals: Wnt and Hedgehog in dentate neurogenesis. Sci STKE 2006: pe5.
79. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, et al. (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437: 1370-1375.
80. Ma DK, Ponnusamy K, Song MR, Ming GL, Song H, (2009) Molecular genetic analysis of FGFR1 signalling reveals distinct roles of MAPK and PLCgamma1 activation for self-renewal of adult neural stem cells. Mol Brain 2: 16.
81. Nichols JT, Miyamoto A, Weinmaster G, (2007) Notch signaling-constantly on the move. Traffic 8: 959-969.
82. Gobeske KT, Das S, Bonaguidi MA, Weiss C, Radulovic J, et al. (2009) BMP signaling mediates effects of exercise on hippocampal neurogenesis and cognition in mice. PLoS One 4: e7506.
83. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, et al. (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16: 147-154.
84. Shook BA, Manz DH, Peters JJ, Kang S, Conover JC, (2012) Spatiotemporal changes to the subventricular zone stem cell pool through aging. J Neurosci 32: 6947-6956.