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

Journal of Neuroscience

Volumn 32, Issue 12, 2012, Pages 4118-4132

  Zou, Junhui ^a   Pan, Yung Wei ^a   Wang, Zhenshan ^b   Chang, Shih Yu ^a   Wang, Wenbin ^a   Wang, Xin ^c   Tournier, Cathy ^c   Storm, Daniel R ^b   Xia, Zhengui ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

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

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CASPASE 3; GLUTAMATE DECARBOXYLASE 67; MITOGEN ACTIVATED PROTEIN KINASE 7; NERVE CELL ADHESION MOLECULE; POLYSIALIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ERK5 GENE; FEMALE; FLUORESCENCE MICROSCOPE; GENE; GENE DELETION; HABITUATION; IMMUNOHISTOCHEMISTRY; INTERNEURON; KNOCKOUT MOUSE; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NICK END LABELING; NONHUMAN; OLFACTOMETRY; OLFACTORY BULB; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMELLING; SUBVENTRICULAR ZONE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BROMODEOXYURIDINE; CELL MOVEMENT; DISEASE MODELS, ANIMAL; ELECTROOCULOGRAPHY; EMBRYO, MAMMALIAN; GABAERGIC NEURONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DECARBOXYLASE; IN SITU NICK-END LABELING; LATERAL VENTRICLES; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEURAL CELL ADHESION MOLECULE L1; NEURAL STEM CELLS; NEUROGENESIS; ODORS; OLFACTORY BULB; PERCEPTUAL DISORDERS; PHOSPHOPYRUVATE HYDRATASE; SIALIC ACIDS; SIGNAL TRANSDUCTION; SMELL; SOXB1 TRANSCRIPTION FACTORS;

EID: 84863348110     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6260-11.2012     Document Type: Article

References (79)

1. Abraham NM, Egger V, Shimshek DR, Renden R, Fukunaga I, Sprengel R, Seeburg PH, Klugmann M, Margrie TW, Schaefer AT, Kuner T (2010) Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 65:399-411.
2. Adam Y, Mizrahi A (2010) Circuit formation and maintenance-perspectives from the mammalian olfactory bulb. Curr Opin Neurobiol 20:134-140.
3. Allen ZJ 2nd, Waclaw RR, Colbert MC, Campbell K (2007) Molecular identity of olfactory bulb interneurons: transcriptional codes of periglomeru-lar neuron subtypes. J Mol Histol 38:517-525.
4. Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult sub-ventricular zone. J Neurosci 22:629-634.
5. Batista-Brito R, Close J, Machold R, Fishell G (2008) The distinct temporal origins of olfactory bulb interneuron subtypes. J Neurosci 28:3966-3975.
6. Blanchart A, De Carlos JA, López-Mascaraque L (2006) Time frame of mitral cell development in the mice olfactory bulb. J Comp Neurol 496:529-543.
7. 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.
8. Brill MS, Snapyan M, Wohlfrom H, Ninkovic J, Jawerka M, Mastick GS, Ashery-Padan R, Saghatelyan A, Berninger B, Götz M (2008) A dlx2-and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J Neurosci 28:6439-6452.
9. 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.
10. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S (1994) Inactivation of the N-CAM gene in mice results insize reduction of the olfactory bulb and deficitsin spatial learning. Nature 367:455-459.
11. Cude K, Wang Y, Choi HJ, Hsuan SL, Zhang H, Wang CY, Xia Z (2007) Regulation of the G2-M cell cycle progression by the ERK5-NF{kappa}B signaling pathway. J Cell Biol 177:253-264.
12. 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.
13. Dellovade TL, Pfaff DW, Schwanzel-Fukuda M (1998) Olfactory bulb development is altered in small-eye (Sey) mice. J Comp Neurol 402:402-418.
14. 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.
15. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging resultsin reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24:8354-8365.
16. Esparís-Ogando A, Díaz-Rodríguez E, Montero JC, Yuste L, Crespo P, Pand-iella A (2002) Erk5 participates in neuregulin signal transduction and is constitutively active in breast cancer cells overexpressing ErbB2. Mol Cell Biol 22:270-285.
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. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, Lledo PM (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci U S A 97:1823-1828.
19. Haberly LB, Price JL (1977) The axonal projection patterns ofthe mitral and tufted cells of the olfactory bulb in the rat. Brain Res 129:152-157.
20. Hartman BK, Margolis FL (1975) Immunofluorescence localization of the olfactory marker protein. Brain Res 96:176-180.
21. Hayashi M, Lee JD (2004) Role of the BMK1/ERK5 signaling pathway: lessons from knockout mice. J Mol Med 82:800-808.
22. Hinds JW (1968) Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287-304.
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. Kato Y, Tapping RI, Huang S, Watson MH, Ulevitch RJ, Lee JD (1998) Bmk1/Erk5 isrequired for cell proliferation inducedby epidermal growth factor. Nature 395:713-716.
25. Kim H, Greer CA (2000) The emergence of compartmental organization in olfactory bulb glomeruli during postnatal development. J Comp Neurol 422:297-311.
26. 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.
27. Lee JD, Ulevitch RJ, Han J (1995) Primary structure of BMK1: a new mammalian map kinase. Biochem Biophys Res Commun 213:715-724.
28. Lévai O, Strotmann J (2003) Projection pattern of nerve fibers from the septal organ: DiI-tracing studies with transgenic OMP mice. Histochem Cell Biol 120:483-492.
29. Li X, Tang X, Jablonska B, Aguirre A, Gallo V, Luskin MB (2009) P27(KIP1) regulates neurogenesis in the rostral migratory stream and olfactory bulb of the postnatal mouse. J Neurosci 29:2902-2914.
30. Linster C, Cleland TA (2009) Glomerular microcircuits in the olfactory bulb. Neural Netw 22:1169-1173.
31. 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.
32. 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.
33. Lledo PM, Saghatelyan A, Lemasson M (2004) Inhibitory interneurons in the olfactory bulb: from development to function. Neuroscientist 10:292-303.
34. Lledo PM, Merkle FT, Alvarez-Buylla A (2008) Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31:392-400.
35. Long JE, Garel S, Depew MJ, Tobet S, Rubenstein JL (2003) DLX5 regulates development of peripheral and central components of the olfactory system. J Neurosci 23:568-578.
36. Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein JL (2007) Dlx-dependent and -independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27:3230-3243.
37. Luskin MB (1998) Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J Neurobiol 36:221-233.
38. Lyons GE, Moore R, Yahara O, Buckingham ME, Walsh FS (1992) Expression ofNCAM isoforms during skeletal myogenesis inthe mouse embryo. Dev Dyn 194:94-104.
39. Mehta PB, Jenkins BL, McCarthy L, Thilak L, Robson CN, Neal DE, Leung HY (2003) MEK5 overexpression is associated with metastatic prostate cancer, and stimulates proliferation, MMP-9 expression and invasion. On-cogene 22:1381-1389.
40. Mihalick SM, Langlois JC, Krienke JD, Dube WV (2000) An olfactory discrimination procedure for mice. J Exp Anal Behav 73:305-318.
41. Miller AM, Maurer LR, Zou DJ, Firestein S, Greer CA (2010) Axon fascicu-lation in the developing olfactory nerve. Neural Dev 5:20.
42. Moreno MM, Linster C, Escanilla O, Sacquet J, Didier A, Mandairon N (2009) Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci U S A 106:17980-17985.
43. Mugnaini E, Oertel WH, Wouterlood FF (1984a) Immunocytochemical localization of GABA neurons and dopamine neurons in the rat main and accessory olfactory bulbs. Neurosci Lett 47:221-226.
44. Mugnaini E, Wouterlood FG, Dahl AL, Oertel WH (1984b) Immunocyto-chemical identification of GABAergic neurons in the main olfactory bulb of the rat. Arch Ital Biol 122:83-113.
45. Newbern JM, Li X, Shoemaker SE, Zhou J, Zhong J, Wu Y, Bonder D, Hol-lenback S, Coppola G, Geschwind DH, Landreth GE, Snider WD (2011) Specific functions for ERK/MAPK signaling during PNS development. Neuron 69:91-105.
46. Panzanelli P, Fritschy JM, Yanagawa Y, Obata K, Sassoé-Pognetto M (2007) GABAergic phenotype of periglomerular cells in the rodent olfactory bulb. J Comp Neurol 502:990-1002.
47. Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC (2007) Quantitative analysisofneuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825-836.
48. Pearson G, English JM, White MA, Cobb MH (2001) ERK5 and ERK2 cooperate to regulate NF-kappaB and cell transformation. J Biol Chem 276:7927-7931.
49. Regan CP, Li W, Boucher DM, Spatz S, Su MS, Kuida K (2002) Erk5 null mice display multiple extraembryonic vascular and embryonic cardiovascular defects. Proc Natl Acad Sci U S A 99:9248-9253.
50. Reyes AA, Small SJ, Akeson R (1991) At least 27 alternatively spliced forms of the neural cell adhesion molecule mRNA are expressed during rat heart development. Mol Cell Biol 11:1654-1661.
51. Rioux L, Gelber EI, Parand L, Kazi HA, Yeh J, Wintering R, Bilker W, Arnold SE (2005) Characterization of olfactory bulb glomeruli in schizophrenia. Schizophr Res 77:229-239.
52. Rosselli-Austin L, Altman J (1979) The postnatal development of the main olfactory bulb of the rat. J Dev Physiol 1:295-313.
53. Schwob JE, Price JL (1978) The cortical projection of the olfactory bulb: development in fetal and neonatal rats correlated with quantitative variations in adult rats. Brain Res 151:369-374.
54. 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.
55. Shepherd GM, Chen WR, Willhite D, Migliore M, Greer CA (2007) The olfactory granule cell: from classical enigma to central role in olfactory processing. Brain Res Rev 55:373-382.
56. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S (2003) Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299:117-120.
57. Sohn SJ, Sarvis BK, Cado D, Winoto A (2002) ERK5 MAPK regulates embryonic angiogenesis and acts as a hypoxia-sensitive repressor of vascular endothelial growth factor expression. J Biol Chem 277:43344-43351.
58. Stenman J, Toresson H, Campbell K (2003) Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167-174.
59. Sundberg H, Døving K, Novikov S, Ursin H (1982) A method for studying responses and habituation to odorsinrats. Behav Neural Biol 34:113-119.
60. Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, Rutishauser U, Magnuson T (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163-1174.
61. Trinh K, Storm DR (2003) Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat Neurosci 6:519-525.
62. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, SchützG (1999) Disruptionofthe glucocorticoid receptor genein the nervous system results in reduced anxiety. Nat Genet 23:99-103.
63. van Velthoven CT, Kavelaars A, van Bel F, Heijnen CJ (2010) Repeated mesenchymal stem cell treatment after neonatal hypoxia-ischemia has distinct effects on formation and maturation of new neurons and oligo-dendrocytes leading to restoration of damage, corticospinal motor tract activity, and sensorimotor function. J Neurosci 30:9603-9611.
64. Wachowiak M, Shipley MT (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 17:411-423.
65. Waclaw RR, Allen ZJ 2nd, Bell SM, Erdélyi F, Szabó G, Potter SS, Campbell K (2006) The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49:503-516.
66. Wang X, Tournier C (2006) Regulation of cellular functions by the ERK5 signalling pathway. Cell Signal 18:753-760.
67. Wang Y, Su B, Xia Z (2006a) Brain-derived neurotrophic factor activates ERK5 in cortical neurons via a rap1-MEKK2 signaling cascade. J Biol Chem 281:35965-35974.
68. Wang Z, Balet Sindreu C, Li V, Nudelman A, Chan GC, Storm DR (2006b) Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J Neurosci 26:7375-7379.
69. Wang X, Finegan KG, Robinson AC, Knowles L, Khosravi-Far R, Hinchliffe KA, Boot-Handford RP, Tournier C (2006c) Activation of extracellular signal-regulated protein kinase 5 downregulates FasL upon osmotic stress. Cell Death Differ 13:2099-2108.
70. Wang Y, Kaneko N, Asai N, Enomoto A, Isotani-Sakakibara M, Kato T, Asai M, Murakumo Y, Ota H, Hikita T, Namba T, Kuroda K, Kaibuchi K, Ming GL, Song H, Sawamoto K, Takahashi M (2011) Girdin is an intrinsic regulator of neuroblast chain migration in the rostral migratory stream of the postnatal brain. J Neurosci 31:8109-8122.
71. 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.
72. Wesson DW, Donahou TN, Johnson MO, Wachowiak M (2008) Sniffing behavior of mice during performance in odor-guided tasks. Chem Senses 33:581-596.
73. White LE (1965) Olfactory bulb projections of the rat. The Anatomical Record 152:465-479.
74. Whitman MC, Greer CA (2009) Adult neurogenesis and the olfactory system. Prog Neurobiol 89:162-175.
75. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759-3771.
76. Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27:487-497.
77. Yan L, Carr J, Ashby PR, Murry-Tait V, Thompson C, Arthur JS (2003) Knockout of ERK5 causes multiple defects in placental and embryonic development. BMC Dev Biol 3:11.
78. Yun K, Potter S, Rubenstein JL (2001) Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128:193-205.
79. Zhou G, Bao ZQ, Dixon JE (1995) Components of a new human protein kinase signal transduction pathway. J Biol Chem 270:12665-12669.