Retinoic acid receptor and CNGA2 channel signaling are part of a regulatory feedback loop controlling axonal convergence and survival of olfactory sensory neurons

FASEB Journal

Volumn 26, Issue 2, 2012, Pages 617-627

  Öztokatli, Hande ^a   Hörnberg, Maria ^a   Berghard, Anna ^a   Bohm, Staffan ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

Caspase 3; Kirrel 2; Neuronal activity; Neuropilin 1; Retinoids

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL A2; NEUROPILIN 1; RETINOIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL DEATH; CELL SURVIVAL; FEEDBACK SYSTEM; FEMALE; GENE EXPRESSION; MOUSE; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY NERVE; OLFACTORY RECEPTOR; PHENOTYPE; PRIORITY JOURNAL; SENSORY NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CELL SURVIVAL; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; CYTOCHROME P-450 ENZYME SYSTEM; FEEDBACK, PHYSIOLOGICAL; FEMALE; GENE EXPRESSION; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; RECEPTORS, RETINOIC ACID; SIGNAL TRANSDUCTION;

MUS;

EID: 84856545944     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-192450     Document Type: Article

References (47)

1. Maden, M. (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 8, 755-765
2. Chambon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954
3. Hagglund, M., Berghard, A., Strotmann, J., and Bohm, S. (2006) Retinoic acid receptor-dependent survival of olfactory sensory neurons in postnatal and adult mice. J. Neurosci. 26, 3281-3291
4. Hornberg, M., Gussing, F., Berghard, A., and Bohm, S. (2009) Retinoic acid selectively inhibits death of basal vomeronasal neurons during late stage of neural circuit formation. J. Neurochem. 110, 1263-1275
5. Ressler, K. J., Sullivan, S. L., and Buck, L. B. (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245-1255
6. Vassar, R., Chao, S. K., Sitcheran, R., Nunez, J. M., Vosshall, L. B., and Axel, R. (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981-991
7. Mombaerts, P., Wang, F., Dulac, C., Chao, S. K., Nemes, A., Mendelsohn, M., Edmondson, J., and Axel, R. (1996) Visualizing an olfactory sensory map. Cell 87, 675-686 (Pubitemid 26386941)
8. Zou, D. J., Chesler, A., and Firestein, S. (2009) How the olfactory bulb got its glomeruli: a just so story? Nat. Rev. Neurosci. 10, 611-618
9. Firestein, S. (2001) How the olfactory system makes sense of scents. Nature 413, 211-218
10. Munger, S. D., Leinders-Zufall, T., and Zufall, F. (2009) Subsystem organization of the mammalian sense of smell. Annu. Rev. Physiol. 71, 115-140
11. Pun, R. Y., and Kleene, S. J. (2003) Contribution of cyclic-nucleotide- gated channels to the resting conductance of olfactory receptor neurons. Biophys. J. 84, 3425-3435 (Pubitemid 36531787)
12. Murphy, G. J., and Isaacson, J. S. (2003) Presynaptic cyclic nucleotide-gated ion channels modulate neurotransmission in the mammalian olfactory bulb. Neuron 37, 639-647 (Pubitemid 36262985)
13. Maritan, M., Monaco, G., Zamparo, I., Zaccolo, M., Pozzan, T., and Lodovichi, C. (2009) Odorant receptors at the growth cone are coupled to localized cAMP and Ca2+ increases. Proc. Natl. Acad. Sci. U. S. A. 106, 3537-3542
14. Imai, T., Suzuki, M., and Sakano, H. (2006) Odorant receptor-derived cAMP signals direct axonal targeting. Science 314, 657-661 (Pubitemid 44646392)
15. Zhao, H., and Reed, R. R. (2001) X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104, 651-660 (Pubitemid 32241016)
16. Yu, C. R., Power, J., Barnea, G., O'Donnell, S., Brown, H. E., Osborne, J., Axel, R., and Gogos, J. A. (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42, 553-566 (Pubitemid 38639876)
17. Zou, D. J., Chesler, A. T., Le Pichon, C. E., Kuznetsov, A., Pei, X., Hwang, E. L., and Firestein, S. (2007) Absence of adenylyl cyclase 3 perturbs peripheral olfactory projections in mice. J. Neurosci. 27, 6675-6683 (Pubitemid 46983434)
18. Chesler, A. T., Zou, D. J., Le Pichon, C. E., Peterlin, Z. A., Matthews, G. A., Pei, X., Miller, M. C., and Firestein, S. (2007) A G protein/cAMP signal cascade is required for axonal convergence into olfactory glomeruli. Proc. Natl. Acad. Sci. U. S. A. 104, 1039-1044 (Pubitemid 46154732)
19. Col, J. A., Matsuo, T., Storm, D. R., and Rodriguez, I. (2007) Adenylyl cyclase-dependent axonal targeting in the olfactory system. Development 134, 2481-2489 (Pubitemid 47074142)
20. Henion, T. R., Faden, A. A., Knott, T. K., and Schwarting, G. A. (2011) β3GnT2 maintains adenylyl cyclase-3 signaling and axon guidance molecule expression in the olfactory epithelium. J. Neurosci. 31, 6576-6586
21. Baker, H., Cummings, D. M., Munger, S. D., Margolis, J. W., Franzen, L., Reed, R. R., and Margolis, F. L. (1999) Targeted deletion of a cyclic nucleotide-gated channel subunit (OCNC1): biochemical and morphological consequences in adult mice. J. Neurosci. 19, 9313-9321 (Pubitemid 30228085)
22. Lin, D. M., Wang, F., Lowe, G., Gold, G. H., Axel, R., Ngai, J., and Brunet, L. (2000) Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26, 69-80
23. Zheng, C., Feinstein, P., Bozza, T., Rodriguez, I., and Mombaerts, P. (2000) Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit. Neuron 26, 81-91
24. Brunet, L. J., Gold, G. H., and Ngai, J. (1996) General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17, 681-693 (Pubitemid 26365347)
25. Serizawa, S., Miyamichi, K., Takeuchi, H., Yamagishi, Y., Suzuki, M., and Sakano, H. (2006) A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127, 1057-1069 (Pubitemid 44792252)
26. Damm, K., Heyman, R. A., Umesono, K., and Evans, R. M. (1993) Functional inhibition of retinoic acid response by dominant negative retinoic acid receptor mutants. Proc. Natl. Acad. Sci. U. S. A. 90, 2989-2993 (Pubitemid 23113543)
27. Conzelmann, S., Levai, O., Bode, B., Eisel, U., Raming, K., Breer, H., and Strotmann, J. (2000) A novel brain receptor is expressed in a distinct population of olfactory sensory neurons. Eur. J. Neurosci. 12, 3926-3934
28. Ishii, T., Omura, M., and Mombaerts, P. (2004) Protocols for two- and three-color fluorescent RNA in situ hybridization of the main and accessory olfactory epithelia in mouse. J. Neurocytol. 33, 657-669 (Pubitemid 41434138)
29. Berghard, A., Buck, L. B., and Liman, E. R. (1996) Evidence for distinct signaling mechanisms in two mammalian olfactory sense organs. Proc. Natl. Acad. Sci. U. S. A. 93, 2365-2369 (Pubitemid 26104356)
30. Berghard, A., and Buck, L. B. (1996) Sensory transduction in vomeronasal neurons: evidence for G alpha o, G alpha i2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J. Neurosci. 16, 909-918 (Pubitemid 26140846)
31. Norlin, E. M., Alenius, M., Gussing, F., Hägglund, M., Vedin, V., and Bohm, S. (2001) Evidence for gradients of gene expression correlating with zonal topography of the olfactory sensory map. Mol. Cell. Neurosci. 18, 283-295 (Pubitemid 33027933)
32. Strotmann, J., Levai, O., Fleischer, J., Schwarzenbacher, K., and Breer, H. (2004) Olfactory receptor proteins in axonal processes of chemosensory neurons. J. Neurosci. 24, 7754-7761 (Pubitemid 39186831)
33. Zou, D. J., Feinstein, P., Rivers, A. L., Mathews, G. A., Kim, A., Greer, C. A., Mombaerts, P., and Firestein, S. (2004) Postnatal refinement of peripheral olfactory projections. Science 304, 1976-1979 (Pubitemid 38822191)
34. Kerr, M. A., and Belluscio, L. (2006) Olfactory experience accelerates glomerular refinement in the mammalian olfactory bulb. Nat. Neurosci. 9, 484-486
35. Cutforth, T., Moring, L., Mendelsohn, M., Nemes, A., Shah, N. M., Kim, M. M., Frisen, J., and Axel, R. (2003) Axonal ephrin-As and odorant receptors: coordinate determination of the olfactory sensory map. Cell 114, 311-322 (Pubitemid 36962930)
36. Schwarting, G. A., Raitcheva, D., Crandall, J. E., Burkhardt, C., and Puschel, A. W. (2004) Semaphorin 3A-mediated axon guidance regulates convergence and targeting of P2 odorant receptor axons. Eur. J. Neurosci. 19, 1800-1810 (Pubitemid 38482567)
37. Imai, T., Yamazaki, T., Kobayakawa, R., Kobayakawa, K., Abe, T., Suzuki, M., and Sakano, H. (2009) Pre-target axon sorting establishes the neural map topography. Science 325, 585-590
38. Verhaagen, J., Oestreicher, A. B., Gispen, W. H., and Margolis, F. L. (1989) The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J. Neurosci. 9, 683-691 (Pubitemid 19069512)
39. Billig, G. M., Pal, B., Fidzinski, P., and Jentsch, T. J. Ca(2+)-activated Cl(-) currents are dispensable for olfaction. Nat. Neurosci. 14, 763-769
40. Brunjes, P. C. (1994) Unilateral naris closure and olfactory system development. Brain Res. Brain Res. Rev. 19, 146-160
41. Di Schiavi, E., Riano, E., Heye, B., Bazzicalupo, P., and Rugarli, E. I. (2005) UMODL1/Olfactorin is an extracellular membrane-bound molecule with a restricted spatial expression in olfactory and vomeronasal neurons. Eur. J. Neurosci. 21, 3291-3300 (Pubitemid 40961424)
42. Greer, P. L., and Greenberg, M. E. (2008) From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59, 846-860
43. Langton, S., and Gudas, L. J. (2008) CYP26A1 knockout embryonic stem cells exhibit reduced differentiation and growth arrest in response to retinoic acid. Dev. Biol. 315, 331-354
44. Lin, C. W., Sim, S., Ainsworth, A., Okada, M., Kelsch, W., and Lois, C. (2010) Genetically increased cell-intrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 65, 32-39
45. Aoto, J., Nam, C. I., Poon, M. M., Ting, P., and Chen, L. (2008) Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 60, 308-320
46. Jones, S. V., Choi, D. C., Davis, M., and Ressler, K. J. (2008) Learning-dependent structural plasticity in the adult olfactory pathway. J. Neurosci. 28, 13106-13111
47. Niederreither, K., Fraulob, V., Garnier, J. M., Chambon, P., and Dolle, P. (2002) Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech. Dev. 110, 165-171 (Pubitemid 34020635)