Temporal patterns of gene expression during calyx of held development

Developmental Neurobiology

Volumn 76, Issue 2, 2016, Pages 166-189

  Kolson, Douglas R ^a   Wan, Jun ^b   Wu, Jonathan ^a   Dehoff, Marlin ^a   Brandebura, Ashley N ^a   Qian, Jiang ^b   Mathers, Peter H ^a   Spirou, George A ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Calyx of held; Development; Microarray; MNTB; Perineuronal net

Indexed keywords

AGGRECAN; ALDOLASE C; BONE MORPHOGENETIC PROTEIN 5; BREVICAN; CADHERIN; CADHERIN 20; CALBINDIN 1; CD24 ANTIGEN; CD24A ANTIGEN; CEREBELLIN 1 PRECURSOR PROTEIN; DOUBLECORTIN; ENDOTHELIN B RECEPTOR; ENDOTHELIN RECEPTOR; FRUCTOSE BISPHOSPHATE ALDOLASE; HYALURONIC ACID; LINK PROTEIN; MUSCULAR LMNA INTERACTING PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROTEIN DACT1; PROTEIN HAPLN1; PROTEIN PRECURSOR; PROTEOGLYCAN; RECEPTOR ACTIVITY MODIFYING PROTEIN 3; SEMAPHORIN; SEMAPHORIN 4D; TENASCIN; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG; UNINDEXED DRUG; VESICULAR GLUTAMATE TRANSPORTER 3; XENOPUS PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALIX OF HELD; CELL ADHESION; CELL DIFFERENTIATION; CELL MATURATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE ONTOLOGY; MEDIAL NUCLEUS OF THE TRAPEZOID BODY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL; NERVE ENDING; NERVE FIBER; NONHUMAN; PERINEURONAL NET; POLYMERASE CHAIN REACTION; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SYNAPSE; TEMPORAL EXPRESSION; TRAPEZOID BODY; ANIMAL; AUDITORY NERVOUS SYSTEM; AXON; BRAIN STEM; GENE EXPRESSION REGULATION; GLIA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

ANIMALS; AUDITORY PATHWAYS; AXONS; BRAIN STEM; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NEUROGLIA; NEURONS; SYNAPSES;

EID: 84953637869     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22306     Document Type: Article

References (87)

1. Allen NJ. 2013. Role of glia in developmental synapse formation. Curr Opin Neurobiol 23:1027-1033.
2. Bahr SM, Borgschulte T, Kayser KJ, Lin N. 2009. Using microarray technology to select housekeeping genes in Chinese hamster ovary cells. Biotechnol Bioeng 104:1041-1046.
3. Barry J, Gu Y, Gu C. 2010. Polarized targeting of L1-CAM regulates axonal and dendritic bundling in vitro. Eur J Neurosci 32:1618-1631.
4. Bekku Y, Saito M, Moser M, Fuchigami M, Maehara A, Nakayama M, Kusachi S, Ninomiya Y, Oohashi T. 2012. Bral2 is indispensable for the proper localization of brevican and the structural integrity of the perineuronal net in the brainstem and cerebellum. J Comp Neurol 520:1721-1736.
5. Blosa M, Sonntag M, Bruckner G, Jager C, Seeger G, Matthews RT, Rubsamen R, Arendt T, Morawski M. 2013. Unique features of extracellular matrix in the mouse medial nucleus of trapezoid body-implications for physiological functions. Neuroscience 228:215-234.
6. Borst JG, Soria van Hoeve J. 2012. The calyx of held synapse: From model synapse to auditory relay. Annu Rev Physiol 74:199-224.
7. Bouzioukh F, Daoudal G, Falk J, Debanne D, Rougon G, Castellani V. 2006. Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. Eur J Neurosci 23:2247-2254.
8. Bozdagi O, Valcin M, Poskanzer K, Tanaka H, Benson DL. 2004. Temporally distinct demands for classic cadherins in synapse formation and maturation. Mol Cell Neurosci 27:509-521.
9. Brigidi GS, Bamji SX. 2011. Cadherin-catenin adhesion complexes at the synapse. Curr Opin Neurobiol 21:208-214.
10. Bruses JL. 2010. Identification of gene transcripts expressed by postsynaptic neurons during synapse formation encoding cell surface proteins with presumptive synaptogenic activity. Synapse 64:47-60.
11. Bukalo O, Dityatev A. 2012. Synaptic cell adhesion molecules. Adv Exp Med Biol 970:97-128.
12. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA. 2008. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci 28:264-278.
13. Campbell DS, Holt CE. 2001. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-1026.
14. Carulli D, Pizzorusso T, Kwok JC, Putignano E, Poli A, Forostyak S, Andrews MR, Deepa SS, Glant TT, Fawcett JW. 2010. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133:2331-2347.
15. Carulli D, Rhodes KE, Brown DJ, Bonnert TP, Pollack SJ, Oliver K, Strata P, Fawcett JW. 2006. Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J Comp Neurol 494:559-577.
16. Chang BD, Watanabe K, Broude EV, Fang J, Poole JC, Kalinichenko TV, Roninson IB. 2000. Effects of p21Waf1/Cip1/Sdi1 on cellular gene expression: Implications for carcinogenesis, senescence, and age-related diseases. Proc Natl Acad Sci USA 97:4291-4296.
17. Clarke LE, Barres BA. 2013. Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14:311-321.
18. Demyanenko GP, Siesser PF, Wright AG, Brennaman LH, Bartsch U, Schachner M, Maness PF. 2011. L1 and CHL1 cooperate in thalamocortical axon targeting. Cereb Cortex 21:401-412.
19. Ehmann H, Hartwich H, Salzig C, Hartmann N, Clement-Ziza M, Ushakov K, Avraham KB, Bininda-Emonds OR, Hartmann AK, Lang P, Friauf E, Nothwang HG. 2013. Time-dependent gene expression analysis of the developing superior olivary complex. J Biol Chem 288:25865-25879.
20. Ehret G. 1976. Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1:179-184.
21. Faissner A, Pyka M, Geissler M, Sobik T, Frischknecht R, Gundelfinger ED, Seidenbecher C. 2010. Contributions of astrocytes to synapse formation and maturation-Potential functions of the perisynaptic extracellular matrix. Brain Res Rev 63:26-38.
22. Felmy F, Schneggenburger R. 2004. Developmental expression of the Ca2+-binding proteins calretinin and parvalbumin at the calyx of held of rats and mice. Eur J Neurosci 20:1473-1482.
23. Fournier AE, Nakamura F, Kawamoto S, Goshima Y, Kalb RG, Strittmatter SM. 2000. Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J Cell Biol 149:411-422.
24. Friauf E. 2000. Development of chondroitin sulfate proteoglycans in the central auditory system of rats correlates with acquisition of mature properties. Audiol Neurootol 5:251-262.
25. Friauf E, Rust MB, Schulenborg T, Hirtz JJ. 2011. Chloride cotransporters, chloride homeostasis, and synaptic inhibition in the developing auditory system. Hear Res 279:96-110.
26. Futai K, Okada M, Matsuyama K, Takahashi T. 2001. High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21:3342-3349.
27. Gao G, Plaas A, Thompson VP, Jin S, Zuo F, Sandy JD. 2004. ADAMTS4 (aggrecanase-1) activation on the cell surface involves C-terminal cleavage by glycosylphosphatidyl inositol-anchored membrane type 4-matrix metalloproteinase and binding of the activated proteinase to chondroitin sulfate and heparan sulfate on syndecan-1. J Biol Chem 279:10042-10051.
28. Giamanco KA, Matthews RT. 2012. Deconstructing the perineuronal net: Cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience 218:367-384.
29. Gumy LF, Yeo GS, Tung YC, Zivraj KH, Willis D, Coppola G, Lam BY, Twiss JL, Holt CE, Fawcett JW. 2011. Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17:85-98.
30. Gutierrez L, Mauriat M, Guenin S, Pelloux J, Lefebvre JF, Louvet R, Rusterucci C, Moritz T, Guerineau F, Bellini C, Van Wuytswinkel O. 2008. The lack of a systematic validation of reference genes: A serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotechnol J 6:609-618.
31. Harris JA, Hardie NA, Bermingham-McDonogh O, Rubel EW. 2005. Gene expression differences over a critical period of afferent-dependent neuron survival in the mouse auditory brainstem. J Comp Neurol 493:460-474.
32. Hartig W, Bruckner G, Brauer K, Schmidt C, Bigl V. 1995. Allocation of perineuronal nets and parvalbumin-, calbindin-D28k- and glutamic acid decarboxylase-immunoreactivity in the amygdala of the rhesus monkey. Brain Res 698:265-269.
33. Hartig W, Singer A, Grosche J, Brauer K, Ottersen OP, Bruckner G. 2001. Perineuronal nets in the rat medial nucleus of the trapezoid body surround neurons immunoreactive for various amino acids, calcium-binding proteins and the potassium channel subunit Kv3.1b. Brain Res 899:123-133.
34. Hoffpauir BK, Grimes JL, Mathers PH, Spirou GA. 2006. Synaptogenesis of the calyx of Held: Rapid onset of function and one-to-one morphological innervation. J Neurosci 26:5511-5523.
35. Hoffpauir BK, Kolson DR, Mathers PH, Spirou GA. 2010. Maturation of synaptic partners: Functional phenotype and synaptic organization tuned in synchrony. J Physiol 588:4365-4385.
36. Holcomb PS, Hoffpauir BK, Hoyson MC, Jackson DR, Deerinck TJ, Marrs GS, Dehoff M, Wu J, Ellisman MH, Spirou GA. 2013. Synaptic inputs compete during rapid formation of the calyx of Held: A new model system for neural development. J Neurosci 33:12954-12969.
37. Howell DM, Morgan WJ, Jarjour AA, Spirou GA, Berrebi AS, Kennedy TE, Mathers PH. 2007. Molecular guidance cues necessary for axon pathfinding from the ventral cochlear nucleus. J Comp Neurol 504:533-549.
38. Hsieh CY, Cramer KS. 2006. Deafferentation induces novel axonal projections in the auditory brainstem after hearing onset. J Comp Neurol 497:589-599.
39. Hsieh CY, Hong CT, Cramer KS. 2007. Deletion of EphA4 enhances deafferentation-induced ipsilateral sprouting in auditory brainstem projections. J Comp Neurol 504:508-518.
40. Hsieh CY, Nakamura PA, Luk SO, Miko IJ, Henkemeyer M, Cramer KS. 2010. Ephrin-B reverse signaling is required for formation of strictly contralateral auditory brainstem pathways. J Neurosci 30:9840-9849.
41. Huggett J, Dheda K, Bustin S, Zumla A. 2005. Real-time RT-PCR normalisation; strategies and considerations. Genes Immun 6:279-284.
42. Joshi I, Wang LY. 2002. Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol 540:861-873.
43. Jung H, Gkogkas CG, Sonenberg N, Holt CE. 2014. Remote control of gene function by local translation. Cell 157:26-40.
44. Kandler K, Friauf E. 1993. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328:161-184.
45. Kaneko-Goto T, Yoshihara S, Miyazaki H, Yoshihara Y. 2008. BIG-2 mediates olfactory axon convergence to target glomeruli. Neuron 57:834-846.
46. Kang H, Schuman EM. 1996. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402-1406.
47. Kim G, Kandler K. 2003. Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6:282-290.
48. Koehl A, Schmidt N, Rieger A, Pilgram SM, Letunic I, Bork P, Soto F, Friauf E, Nothwang HG. 2004. Gene expression profiling of the rat superior olivary complex using serial analysis of gene expression. Eur J Neurosci 20:3244-3258.
49. Korber C, Dondzillo A, Eisenhardt G, Herrmannsdorfer F, Wafzig O, Kuner T. 2014. Gene expression profile during functional maturation of a central mammalian synapse. Eur J Neurosci. 40:2867-2877.
50. Kucukdereli H, Allen NJ, Lee AT, Feng A, Ozlu MI, Conatser LM, Chakraborty C, Workman G, Weaver M, Sage EH, Barres BA, Eroglu C. 2011. Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc Natl Acad Sci USA 108:E440-449.
51. Lee SK, Hollenbeck PJ. 2003. Organization and translation of mRNA in sympathetic axons. J Cell Sci 116:4467-4478.
52. Lohmann C, Friauf E. 1996. Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J Comp Neurol 367:90-109.
53. Lurie DI, Pasic TR, Hockfield SJ, Rubel EW. 1997. Development of Cat-301 immunoreactivity in auditory brainstem nuclei of the gerbil. J Comp Neurol 380:319-334.
54. Malinverno M, Carta M, Epis R, Marcello E, Verpelli C, Cattabeni F, Sala C, Mulle C, Di Luca M, Gardoni F. 2010. Synaptic localization and activity of ADAM10 regulate excitatory synapses through N-cadherin cleavage. J Neurosci 30:16343-16355.
55. Maness PF, Schachner M. 2007. Neural recognition molecules of the immunoglobulin superfamily: Signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
56. Marrs GS, Morgan WJ, Howell DM, Spirou GA, Mathers PH. 2013. Embryonic origins of the mouse superior olivary complex. Dev Neurobiol 73:384-398.
57. Masahira N, Takebayashi H, Ono K, Watanabe K, Ding L, Furusho M, Ogawa Y, Nabeshima Y, Alvarez-Buylla A, Shimizu K, Ikenaka K. 2006. Olig2-positive progenitors in the embryonic spinal cord give rise not only to motoneurons and oligodendrocytes, but also to a subset of astrocytes and ependymal cells. Dev Biol 293:358-369.
58. Michalski N, Babai N, Renier N, Perkel DJ, Chedotal A, Schneggenburger R. 2013. Robo3-driven axon midline crossing conditions functional maturation of a large commissural synapse. Neuron 78:855-868.
59. Mikaelian D, Alford BR, Ruben RJ. 1965. Cochlear potentials and 8 nerve action potentials in normal and genetically deaf mice. Ann Otol Rhinol Laryngol 74:146-157.
60. Milev P, Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU. 1998. Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: Aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 247:207-212.
61. Mutch DM, Berger A, Mansourian R, Rytz A, Roberts MA. 2002. The limit fold change model: A practical approach for selecting differentially expressed genes from microarray data. BMC Bioinformatics 3:17
62. Myers AK, Ray J, Kulesza RJ. Jr. 2012. Neonatal conductive hearing loss disrupts the development of the Cat-315 epitope on perineuronal nets in the rat superior olivary complex. Brain Res 1465:34-47.
63. Nakamura PA, Cramer KS. 2013. EphB2 signaling regulates lesion-induced axon sprouting but not critical period length in the postnatal auditory brainstem. Neural Dev 8:2
64. Noh J, Seal RP, Garver JA, Edwards RH, Kandler K. 2010. Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map. Nat Neurosci 13:232-238.
65. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
66. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. 2002. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248-1251.
67. Redies C, Neudert F, Lin J. 2011. Cadherins in cerebellar development: Translation of embryonic patterning into mature functional compartmentalization. Cerebellum 10:393-408.
68. Renier N, Schonewille M, Giraudet F, Badura A, Tessier-Lavigne M, Avan P, De Zeeuw CI, Chedotal A. 2010. Genetic dissection of the function of hindbrain axonal commissures. PLoS Biol 8:e1000325
69. Rodriguez-Contreras A, de Lange RP, Lucassen PJ, Borst JG. 2006. Branching of calyceal afferents during postnatal development in the rat auditory brainstem. J Comp Neurol 496:214-228.
70. Rusu SI, Borst JG. 2011. Developmental changes in intrinsic excitability of principal neurons in the rat medial nucleus of the trapezoid body. Dev Neurobiol 71:284-295.
71. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T. 2006. The RIN: An RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7:3
72. Shelly M, Cancedda L, Lim BK, Popescu AT, Cheng PL, Gao H, Poo MM. 2011. Semaphorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 71:433-446.
73. Stanton H, Melrose J, Little CB, Fosang AJ. 2011. Proteoglycan degradation by the ADAMTS family of proteinases. Biochim Biophys Acta 1812:1616-1629.
74. Steward O, Levy WB. 1982. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2:284-291.
75. Tcherkezian J, Brittis PA, Thomas F, Roux PP, Flanagan JG. 2010. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141:632-644.
76. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M. 2002. Cadherin regulates dendritic spine morphogenesis. Neuron 35:77-89.
77. Toyoshima M, Sakurai K, Shimazaki K, Takeda Y, Shimoda Y, Watanabe K. 2009. Deficiency of neural recognition molecule NB-2 affects the development of glutamatergic auditory pathways from the ventral cochlear nucleus to the superior olivary complex in mouse. Dev Biol 336:192-200.
78. Tran TS, Kolodkin AL, Bharadwaj R. 2007. Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol 23:263-292.
79. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121.
80. Vanderhaeghen P, Cheng HJ. 2010. Guidance molecules in axon pruning and cell death. Cold Spring Harb Perspect Biol 2:a001859
81. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034
82. Vo T, Carulli D, Ehlert EM, Kwok JC, Dick G, Mecollari V, Moloney EB, Neufeld G, de Winter F, Fawcett JW, Verhaagen J. 2013. The chemorepulsive axon guidance protein semaphorin3A is a constituent of perineuronal nets in the adult rodent brain. Mol Cell Neurosci 56:186-200.
83. Wang D, Fawcett J. 2012. The perineuronal net and the control of CNS plasticity. Cell Tissue Res 349:147-160.
84. Willis DE, Twiss JL. 2010. Regulation of protein levels in subcellular domains through mRNA transport and localized translation. Mol Cell Proteomics 9:952-962.
85. Xiao L, Michalski N, Kronander E, Gjoni E, Genoud C, Knott G, Schneggenburger R. 2013. BMP signaling specifies the development of a large and fast CNS synapse. Nat Neurosci 16:856-864.
86. Yao J, Sasaki Y, Wen Z, Bassell GJ, Zheng JQ. 2006. An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat Neurosci 9:1265-1273.
87. Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, Yeo GS, Holt CE. 2010. Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J Neurosci 30:15464-15478.