Local CRH Signaling Promotes Synaptogenesis and Circuit Integration of Adult-Born Neurons

Developmental Cell

Volumn 30, Issue 6, 2014, Pages 645-659

  Garcia, Isabella ^a   Quast, KathleenB ^a   Huang, Longwen ^a   Herman, AlexanderM ^a   Selever, Jennifer ^a   Deussing, JanM ^b   Justice, NicholasJ ^c   Arenkiel, BenjaminR ^a,d  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GRANULE CELL; HORMONE RELEASE; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY BULB; OPTOGENETICS; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTOGENESIS; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; SYNAPSE;

ANIMALS; CORTICOTROPIN-RELEASING HORMONE; INTERNEURONS; MICE; MICE, INBRED C57BL; NEUROGENESIS; NEURONAL PLASTICITY; OLFACTORY BULB; SYNAPSES;

EID: 84908210690     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.07.001     Document Type: Article

References (82)

1. Abraham N.M., Egger V., Shimshek D.R., Renden R., Fukunaga I., Sprengel R., Seeburg P.H., Klugmann M., Margrie T.W., Schaefer A.T., Kuner T. Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 2010, 65:399-411.
2. Abrous D.N., Koehl M., Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 2005, 85:523-569.
3. Alvarez-Buylla A., Temple S. Stem cells in the developing and adult nervous system. J.Neurobiol. 1998, 36:105-110.
4. Arenkiel B.R., Hasegawa H., Yi J.J., Larsen R.S., Wallace M.L., Philpot B.D., Wang F., Ehlers M.D. Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS ONE 2011, 6:e29423.
5. Atasoy D., Aponte Y., Su H.H., Sternson S.M. A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J.Neurosci. 2008, 28:7025-7030.
6. Bale T.L., Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 2004, 44:525-557.
7. Balu R., Pressler R.T., Strowbridge B.W. Multiple modes of synaptic excitation of olfactory bulb granule cells. J.Neurosci. 2007, 27:5621-5632.
8. Barinka F., Salaj M., Rybář J., Krajčovičová E., Kubová H., Druga R. Calretinin, parvalbumin and calbindin immunoreactive interneurons in perirhinal cortex and temporal area Te3V of the rat brain: qualitative and quantitative analyses. Brain Res. 2012, 1436:68-80.
9. Batista-Brito R., Close J., Machold R., Fishell G. The distinct temporal origins of olfactory bulb interneuron subtypes. J.Neurosci. 2008, 28:3966-3975.
10. Bayatti N., Zschocke J., Behl C. Brain region-specific neuroprotective action and signaling of corticotropin-releasing hormone in primary neurons. Endocrinology 2003, 144:4051-4060.
11. Berger H., Heinrich N., Wietfeld D., Bienert M., Beyermann M. Evidence that corticotropin-releasing factor receptor type 1 couples to Gs- and Gi-proteins through different conformations of its J-domain. Br. J. Pharmacol. 2006, 149:942-947.
12. Blank T., Nijholt I., Grammatopoulos D.K., Randeva H.S., Hillhouse E.W., Spiess J. Corticotropin-releasing factor receptors couple to multiple G-proteins to activate diverse intracellular signaling pathways in mouse hippocampus: role in neuronal excitability and associative learning. J.Neurosci. 2003, 23:700-707.
13. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8:1263-1268.
14. Breton-Provencher V., Lemasson M., Peralta M.R., Saghatelyan A. 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. 2009, 29:15245-15257.
15. Carleton A., Petreanu L.T., Lansford R., Alvarez-Buylla A., Lledo P.M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 2003, 6:507-518.
16. Chen W.R., Greer C.A. Olfactory bulb. The Synaptic Organization of the Brain 2004, 165-216. Oxford University Press, New York. Fifth Edition. G.M. Shepherd (Ed.).
17. Chen Y., Bender R.A., Brunson K.L., Pomper J.K., Grigoriadis D.E., Wurst W., Baram T.Z. Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc. Natl. Acad. Sci. USA 2004, 101:15782-15787.
18. de Andrade J.S., Céspedes I.C., Abrão R.O., Dos Santos T.B., Diniz L., Britto L.R., Spadari-Bratfisch R.C., Ortolani D., Melo-Thomas L., da Silva R.C., Viana M.B. Chronic unpredictable mild stress alters an anxiety-related defensive response, Fos immunoreactivity and hippocampal adult neurogenesis. Behav. Brain Res. 2013, 250:81-90.
19. De Marco García N.V., Karayannis T., Fishell G. Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 2011, 472:351-355.
20. Eyre M.D., Antal M., Nusser Z. Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J.Neurosci. 2008, 28:8217-8229.
21. Favero M., Castro-Alamancos M.A. Synaptic cooperativity regulates persistent network activity in neocortex. J.Neurosci. 2013, 33:3151-3163.
22. Fenoglio K.A., Chen Y., Baram T.Z. Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J.Neurosci. 2006, 26:2434-2442.
23. Gracia-Llanes F.J., Crespo C., Blasco-Ibáñez J.M., Marqués-Marí A.I., Martínez-Guijarro F.J. VIP-containing deep short-axon cells of the olfactory bulb innervate interneurons different from granule cells. Eur. J. Neurosci. 2003, 18:1751-1763.
24. Hanstein R., Lu A., Wurst W., Holsboer F., Deussing J.M., Clement A.B., Behl C. Transgenic overexpression of corticotropin releasing hormone provides partial protection against neurodegeneration in an invivo model of acute excitotoxic stress. Neuroscience 2008, 156:712-721.
25. Hensch T.K., Fagiolini M., Mataga N., Stryker M.P., Baekkeskov S., Kash S.F. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 1998, 282:1504-1508.
26. Hitoshi S., Maruta N., Higashi M., Kumar A., Kato N., Ikenaka K. Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J.Neurosci. Res. 2007, 85:3574-3585.
27. Huang L., Garcia I., Jen H.I., Arenkiel B.R. Reciprocal connectivity between mitral cells and external plexiform layer interneurons in the mouse olfactory bulb. Front Neural Circuits 2013, 7:32.
28. Isaacson J.S., Strowbridge B.W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 1998, 20:749-761.
29. Jacobson L., Muglia L.J., Weninger S.C., Pacák K., Majzoub J.A. CRH deficiency impairs but does not block pituitary-adrenal responses to diverse stressors. Neuroendocrinology 2000, 71:79-87.
30. Justice N.J., Yuan Z.F., Sawchenko P.E., Vale W. Type 1 corticotropin-releasing factor receptor expression reported in BAC transgenic mice: implications for reconciling ligand-receptor mismatch in the central corticotropin-releasing factor system. J.Comp. Neurol. 2008, 511:479-496.
31. Kato H.K., Gillet S.N., Peters A.J., Isaacson J.S., Komiyama T. Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 2013, 80:1218-1231.
32. Kelsch W., Lin C.W., Mosley C.P., Lois C. A critical period for activity-dependent synaptic development during olfactory bulb adult neurogenesis. J.Neurosci. 2009, 29:11852-11858.
33. Kosaka T., Kosaka K. Heterogeneity of parvalbumin-containing neurons in the mouse main olfactory bulb, with special reference to short-axon cells and betaIV-spectrin positive dendritic segments. Neurosci. Res. 2008, 60:56-72.
34. Kühne C., Puk O., Graw J., Hrabě de Angelis M., Schütz G., Wurst W., Deussing J.M. Visualizing corticotropin-releasing hormone receptor type 1 expression and neuronal connectivities in the mouse using a novel multifunctional allele. J.Comp. Neurol. 2012, 520:3150-3180.
35. Le Magueresse C., Monyer H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 2013, 77:388-405.
36. Le Roux N., Cabezas C., Böhm U.L., Poncer J.C. Input-specific learning rules at excitatory synapses onto hippocampal parvalbumin-expressing interneurons. J.Physiol. 2013, 591:1809-1822.
37. Lemasson M., Saghatelyan A., Olivo-Marin J.C., Lledo P.M. Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J.Neurosci. 2005, 25:6816-6825.
38. Lepousez G., Csaba Z., Bernard V., Loudes C., Videau C., Lacombe J., Epelbaum J., Viollet C. Somatostatin interneurons delineate the inner part of the external plexiform layer in the mouse main olfactory bulb. J.Comp. Neurol. 2010, 518:1976-1994.
39. Lepousez G., Mouret A., Loudes C., Epelbaum J., Viollet C. Somatostatin contributes to invivo gamma oscillation modulation and odor discrimination in the olfactory bulb. J.Neurosci. 2010, 30:870-875.
40. Lipschitz D.L., Crowley W.R., Armstrong W.E., Bealer S.L. Neurochemical bases of plasticity in the magnocellular oxytocin system during gestation. Exp. Neurol. 2005, 196:210-223.
41. Lledo P.M., Merkle F.T., Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 2008, 31:392-400.
42. Ma Y., Hu H., Berrebi A.S., Mathers P.H., Agmon A. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J.Neurosci. 2006, 26:5069-5082.
43. Madisen L., Mao T., Koch H., Zhuo J.M., Berenyi A., Fujisawa S., Hsu Y.W., Garcia A.J., Gu X., Zanella S., et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 2012, 15:793-802.
44. Maras P.M., Baram T.Z. Sculpting the hippocampus from within: stress, spines, and CRH. Trends Neurosci. 2012, 35:315-324.
45. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 2005, 28:223-250.
46. Miyamichi K., Shlomai-Fuchs Y., Shu M., Weissbourd B.C., Luo L., Mizrahi A. Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 2013, 80:1232-1245.
47. Mori K., Kishi K., Ojima H. Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory bulb. J.Comp. Neurol. 1983, 219:339-355.
48. Mouret A., Gheusi G., Gabellec M.M., de Chaumont F., Olivo-Marin J.C., Lledo P.M. Learning and survival of newly generated neurons: when time matters. J.Neurosci. 2008, 28:11511-11516.
49. Mouret A., Lepousez G., Gras J., Gabellec M.M., Lledo P.M. Turnover of newborn olfactory bulb neurons optimizes olfaction. J.Neurosci. 2009, 29:12302-12314.
50. Muglia L., Jacobson L., Dikkes P., Majzoub J.A. Corticotropin-releasing hormone deficiency reveals major fetal but not adult glucocorticoid need. Nature 1995, 373:427-432.
51. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 2003, 100:13940-13945.
52. Nielsen S.M., Nielsen L.Z., Hjorth S.A., Perrin M.H., Vale W.W. Constitutive activation of tethered-peptide/corticotropin-releasing factor receptor chimeras. Proc. Natl. Acad. Sci. USA 2000, 97:10277-10281.
53. Panzanelli P., Bardy C., Nissant A., Pallotto M., Sassoè-Pognetto M., Lledo P.M., Fritschy J.M. Early synapse formation in developing interneurons of the adult olfactory bulb. J.Neurosci. 2009, 29:15039-15052.
54. Perrin M.H., Vale W.W. Corticotropin releasing factor receptors and their ligand family. Ann. N Y Acad. Sci. 1999, 885:312-328.
55. Perrin M.H., Donaldson C.J., Chen R., Lewis K.A., Vale W.W. Cloning and functional expression of a rat brain corticotropin releasing factor (CRF) receptor. Endocrinology 1993, 133:3058-3061.
56. Perrin M., Donaldson C., Chen R., Blount A., Berggren T., Bilezikjian L., Sawchenko P., Vale W. Identification of a second corticotropin-releasing factor receptor gene and characterization of a cDNA expressed in heart. Proc. Natl. Acad. Sci. USA 1995, 92:2969-2973.
57. Pressler R.T., Strowbridge B.W. Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 2006, 49:889-904.
58. Price J.L., Powell T.P. An electron-microscopic study of the termination of the afferent fibres to the olfactory bulb from the cerebral hemisphere. J.Cell Sci. 1970, 7:157-187.
59. Price J.L., Powell T.P. The synaptology of the granule cells of the olfactory bulb. J.Cell Sci. 1970, 7:125-155.
60. Refojo D., Schweizer M., Kuehne C., Ehrenberg S., Thoeringer C., Vogl A.M., Dedic N., Schumacher M., von Wolff G., Avrabos C., et al. Glutamatergic and dopaminergic neurons mediate anxiogenic and anxiolytic effects of CRHR1. Science 2011, 333:1903-1907.
61. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J.Neurosci. 2002, 22:2679-2689.
62. Roozendaal B., Schelling G., McGaugh J.L. Corticotropin-releasing factor in the basolateral amygdala enhances memory consolidation via an interaction with the beta-adrenoceptor-cAMP pathway: dependence on glucocorticoid receptor activation. J.Neurosci. 2008, 28:6642-6651.
63. Rudy B., Fishell G., Lee S., Hjerling-Leffler J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 2011, 71:45-61.
64. Schmolesky M.T., De Ruiter M.M., De Zeeuw C.I., Hansel C. The neuropeptide corticotropin-releasing factor regulates excitatory transmission and plasticity at the climbing fibre-Purkinje cell synapse. Eur. J. Neurosci. 2007, 25:1460-1466.
65. Schoenfeld T.J., Gould E. Differential effects of stress and glucocorticoids on adult neurogenesis. Curr. Top. Behav. Neurosci. 2013, 15:139-164.
66. Sheng H., Xu Y., Chen Y., Zhang Y., Xu X., He C., Ni X. CRH-R1 and CRH-R2 differentially modulate dendritic outgrowth of hippocampal neurons. Endocrine 2012, 41:458-464.
67. Shepherd G.M., Greer C.A. Olfactory Bulb in the Synaptic Organization of the Brain 2004, 159-204. Oxford University Press, New York. G.M. Shepherd (Ed.).
68. Smith G.W., Aubry J.M., Dellu F., Contarino A., Bilezikjian L.M., Gold L.H., Chen R., Marchuk Y., Hauser C., Bentley C.A., et al. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 1998, 20:1093-1102.
69. Takatoh J., Nelson A., Zhou X., Bolton M.M., Ehlers M.D., Arenkiel B.R., Mooney R., Wang F. New modules are added to vibrissal premotor circuitry with the emergence of exploratory whisking. Neuron 2013, 77:346-360.
70. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
71. Thiel G., Cibelli G. Corticotropin-releasing factor and vasoactive intestinal polypeptide activate gene transcription through the cAMP signaling pathway in a catecholaminergic immortalized neuron. Neurochem. Int. 1999, 34:183-191.
72. Tobin V.A., Hashimoto H., Wacker D.W., Takayanagi Y., Langnaese K., Caquineau C., Noack J., Landgraf R., Onaka T., Leng G., et al. An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 2010, 464:413-417.
73. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 2004, 5:97-107.
74. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391:892-896.
75. Ung K., Arenkiel B.R. Fiber-optic implantation for chronic optogenetic stimulation of brain tissue. J.Vis. Exp. 2012, e50004.
76. Vale W., Spiess J., Rivier C., Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213:1394-1397.
77. Vale W., Rivier C., Brown M.R., Spiess J., Koob G., Swanson L., Bilezikjian L., Bloom F., Rivier J. Chemical and biological characterization of corticotropin releasing factor. Recent Prog. Horm. Res. 1983, 39:245-270.
78. Whitman M.C., Greer C.A. Synaptic integration of adult-generated olfactory bulb granule cells: basal axodendritic centrifugal input precedes apical dendrodendritic local circuits. J.Neurosci. 2007, 27:9951-9961.
79. Wickersham I.R., Finke S., Conzelmann K.K., Callaway E.M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 2007, 4:47-49.
80. Wickersham I.R., Lyon D.C., Barnard R.J., Mori T., Finke S., Conzelmann K.K., Young J.A., Callaway E.M. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 2007, 53:639-647.
81. Xu H., Jeong H.Y., Tremblay R., Rudy B. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 2013, 77:155-167.
82. Yamaguchi M., Mori K. Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc. Natl. Acad. Sci. USA 2005, 102:9697-9702.