Genetic disruptions of O/E2 and O/E3 genes reveal involvement in olfactory receptor neuron projection

Development

Volumn 131, Issue 6, 2004, Pages 1377-1388

  Wang, Song S ^a   Lewcock, Joseph W ^a   Feinstein, Paul ^b   Mombaerts, Peter ^b   Reed, Randall R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Axon targeting; Olfactory; Transcription factor

Indexed keywords

BETA GALACTOSIDASE; BIOLOGICAL MARKER; GREEN FLUORESCENT PROTEIN; HELIX LOOP HELIX PROTEIN; TAU PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; B LYMPHOCYTE DIFFERENTIATION; BRAIN REGION; CELL DAMAGE; CELL LINEAGE; CONTROLLED STUDY; FEMALE; GENE CONTROL; GENE DISRUPTION; GENE TARGETING; HETEROZYGOSITY; KNOCKOUT MOUSE; MALE; MOUSE; MOUSE MUTANT; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; TISSUE DISTRIBUTION;

ANIMALS; GENES, REPORTER; MICE; OLFACTORY RECEPTOR NEURONS; PHENOTYPE; RECEPTORS, ODORANT; RECOMBINANT FUSION PROTEINS; TAU PROTEINS; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA;

EID: 1842611581     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01009     Document Type: Review

References (65)

1. 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.
2. Bally-Cuif, L., Dubois, L. and Vincent, A. (1998). Molecular cloning of Zcoe2, the zebrafish homolog of Xenopus Xcoe2 and mouse EBF-2, and its expression during primary neurogenesis. Mech. Dev. 77, 85-90.
3. Belluscio, L., Koentges, G., Axel, R. and Dulac, C. (1999). A map of pheromone receptor activation in the mammalian brain. Cell 97, 209-220.
4. Belluscio, L., Lodovichi, C., Feinstein, P., Mombaerts, P. and Katz, L. C. (2002). Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature 419, 296-300.
5. Bozza, T., Feinstein, P., Zheng, C. and Mombaerts, P. (2002). Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22, 3033-3043.
6. Carr, V. M. and Farbman, A. I. (1993). The dynamics of cell death in the olfactory epithelium. Exp. Neurol. 124, 308-314.
7. Cau, E., Casarosa, S. and Guillemot, F. (2002). Mash1 and Ngn1 control distinct steps of determination and differentiation in the olfactory sensory neuron lineage. Development 129, 1871-1880.
8. Cau, E., Gradwohl, G., Casarosa, S., Kageyama, R. and Guillemot, F. (2000). Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development 127, 2323-2332.
9. Cau, E., Gradwohl, G., Fode, C. and Guillemot, F. (1997). Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124, 1611-1621.
10. Cho, J. Y., Min, N., Franzen, L. and Baker, H. (1996). Rapid down-regulation of tyrosine hydroxylase expression in the olfactory bulb of naris-occluded adult rats. J. Comp. Neurol. 369, 264-276.
11. Corradi, A., Croci, L., Broccoli, V., Zecchini, S., Previtali, S., Wurst, W., Amadio, S., Maggi, R., Quattrini, A. and Consalez, G. G. (2003). Hypogonadotropic hypogonadism and peripheral neuropathy in Ebf2-null mice. Development 130, 401-410.
12. Couper Leo, J. M., Devine, A. H. and Brunjes, P. C. (2000). Focal denervation alters cellular phenotypes and survival in the rat olfactory bulb: A developmental analysis. J. Comp. Neurol. 425, 409-421.
13. Crozatier, M., Valle, D., Dubois, L., Ibnsouda, S. and Vincent, A. (1996). Collier, a novel regulator of Drosophila head development, is expressed in a single mitotic domain. Curr. Biol. 6, 707-718.
14. Crozatier, M. and Vincent, A. (1999). Requirement for the Drosophila COE transcription factor Collier in formation of an embryonic muscle: Transcriptional response to notch signalling. Development 126, 1495-1504.
15. Davis, J. A. and Reed, R. R. (1996). Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J. Neurosci. 16, 5082-5094.
16. Dubois, L., Bally-Cuif, L., Crozatier, M., Moreau, J., Paquereau, L. and Vincent, A. (1998). XCoe2, a transcription factor of the Col/Olf-1/EBF family involved in the specification of primary neurons in Xenopus. Curr. Biol. 8, 199-209.
17. Ebneth, A., Godemann, R., Stamer, K., Illenberger, S., Trinczek, B. and Mandelkow, E. (1998). Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: Implications for Alzheimer's disease. J. Cell Biol. 143, 777-794.
18. Fiske, B. K. and Brunjes, P. C. (2001). Cell death in the developing and sensory-deprived rat olfactory bulb. J. Comp. Neurol. 431, 311-319.
19. Garcia, M. L. and Cleveland, D. W. (2001). Going new places using an old MAP: Tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 13, 41-48.
20. Garel, S., Marin, F., Grosschedl, R. and Charnay, P. (1999). Ebf1 controls early cell differentiation in the embryonic striatum. Development 126, 5285-5294.
21. Garel, S., Garcia-Dominguez, M. and Charnay, P. (2000). Control of the migratory pathway of facial branchiomotor neurones. Development 127, 5297-5307.
22. Garel, S., Maria, F., Mattei, M. G., Vesque, C., Vincent, A. and Charnay, P. (1997). Family of Ebf/Olf-1-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev. Dyn. 210, 191-205.
23. Garel, S., Yun, K., Grosschedl, R. and Rubenstein, J. L. (2002). The early topography of thalamocortical projections is shifted in Ebf1 and Dlx1/2 mutant mice. Development 129, 5621-5634.
24. Gisler, R., Jacobsen, S. E. and Sigvardsson, M. (2000). Cloning of human early B-cell factor and identification of target genes suggest a conserved role in B-cell development in man and mouse. Blood 96, 1457-1464.
25. Grant, P., Sharma, P. and Pant, H. C. (2001). Cyclin-dependent protein kinase 5 (Cdk5) and the regulation of neurofilament metabolism. Eur. J. Biochem. 268, 1534-1546.
26. Grundke-Iqbal, I. and Iqbal, K. (1999). Tau pathology generated by overexpression of tau. Am. J. Pathol. 155, 1781-1785.
27. Hagman, J., Belanger, C., Travis, A., Turck, C. W. and Grosschedl, R. (1993). Cloning and functional characterization of early B-cell factor, a regulator of lymphocyte-specific gene expression. Genes Dev. 7, 760-773.
28. Iwema, C. L. and Schwob, J. E. (2003). Odorant receptor expression as a function of neuronal maturity in the adult rodent olfactory system. J. Comp. Neurol. 459, 209-222.
29. Konzelmann, S., Saucier, D., Strotmann, J., Breer, H. and Astic, L. (1998). Decline and recovery of olfactory receptor expression following unilateral bulbectomy. Cell Tissue Res. 294, 421-430.
30. Kudrycki, K., Stein-Izsak, C., Behn, C., Grillo, M., Akeson, R. and Margolis, F. L. (1993). Olf-1-binding site: Characterization of an olfactory neuron-specific promoter motif. Mol. Cell Biol. 13, 3002-3014.
31. Kudrycki, K. E., Buiakova, O., Tarozzo, G., Grillo, M., Walters, E. and Margolis, F. L. (1998). Effects of mutation of the Olf-1 motif on transgene expression in olfactory receptor neurons. J. Neurosci. Res. 52, 159-172.
32. Lin, H. and Grosschedl, R. (1995). Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376, 263-267.
33. Mackay-Sim, A. and Kittel, P. (1991). Cell dynamics in the adult mouse olfactory epithelium: A quantitative autoradiographic study. J. Neurosci. 11, 979-984.
34. Mombaerts, P. (1999). Molecular biology of odorant receptors in vertebrates. Annu. Rev. Neurosci. 22, 487-509.
35. 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.
36. Mori, K., Nagao, H. and Yoshihara, Y. (1999). The olfactory bulb: Coding and processing of odor molecule information. Science 286, 711-715.
37. Mori, K., von Campenhause, H. and Yoshihara, Y. (2000). Zonal organization of the mammalian main and accessory olfactory systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1801-1812.
38. Nadi, N. S., Head, R., Grillo, M., Hempstead, J., Grannot-Reisfeld, N. and Margolis, F. L. (1981). Chemical deafferentation of the olfactory bulb: Plasticity of the levels of tyrosine hydroxylase, dopamine and norepinephrine. Brain Res. 213, 365-377.
39. Nagy, Z., Maccioni, R. B. and Cambiazo, V. (2000). Cell cycle regulatory failure in neurones: Causes and consequences. Role of microtubule-associated proteins in the control of microtubule assembly. Neurobiol. Aging 21, 761-769.
40. Paglini, G., Peris, L., Mascotti, F., Quiroga, S. and Caceres, A. (2000). Tau protein function in axonal formation. Neurochem Res. 25, 37-42.
41. Pasterkamp, R. J., Ruitenberg, M. J. and Verhaagen, J. (1999). Semaphorins and their receptors in olfactory axon guidance. Cell. Mol. Biol. (Noisy-le-grand) 45, 763-779.
42. Pozzoli, O., Bosetti, A., Croci, L., Consalez, G. G. and Vetter, M. L. (2001). Xebf3 is a regulator of neuronal differentiation during primary neurogenesis in xenopus. Dev. Biol. 233, 495-512.
43. Prasad, B. C., Ye, B., Zackhary, R., Schrader, K., Seydoux, G. and Reed, R. R. (1998). unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors. Development 125, 1561-1568.
44. Probst, A., Gotz, J., Wiederhold, K. H., Tolnay, M., Mistl, C., Jaton, A. L., Hong, M., Ishihara, T., Lee, V. M., Trojanowski, J. Q. et al. (2000). Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol (Berl) 99, 469-481.
45. Qasba, P. and Reed, R. R. (1998). Tissue and zonal-specific expression of an olfactory receptor transgene. J. Neurosci. 18, 227-236.
46. Renzi M. J., Wexler, T. L. and Raper, J. A. (2000). Olfactory sensory axons expressing a dominant-negative semaphorin receptor enter the CNS early and overshoot their target. Neuron 28, 437-447.
47. Ressler, K. J., Sullivan, S. L. and Buck, L. B. (1993). A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597-609.
48. Royal, S. J. and Key, B. (1999). Development of P2 olfactory glomeruli in P2-internal ribosome entry site-tau-lacZ transgenic mice. J. Neurosci. 19, 9856-9864.
49. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: In situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
50. Schwarting, G. A., Kostek, C., Ahmad, N., Dibble, C., Pays, L. and Puschel, A. W. (2000). Semaphorin 3A is required for guidance of olfactory axons in mice. J. Neurosci. 20, 7691-7697.
51. Schwob, J. E., Szumowski, K. E. and Stasky, A. A. (1992). Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J. Neurosci. 12, 3896-3919.
52. Strotmann, J., Conzelmann, S., Beck, A., Feinstein, P., Breer, H. and Mombaerts, P. (2000). Local permutations in the glomerular array of the mouse olfactory bulb. J. Neurosci. 20, 6927-6938.
53. Travis, A., Hagman, J., Hwang, L. and Grosschedl, R. (1993). Purification of early-B-cell factor and characterization of its DNA-binding specificity. Mol. Cell. Biol. 13, 3392-3400.
54. Vassalli, A., Rothman, A., Feinstein, P., Zapotocky, M. and Mombaerts, P. (2002). Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35, 681-696.
55. Vassar, R., Ngai, J. and Axel, R. (1993). Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309-318.
56. Vervoort, M., Crozatier, M., Valle, D. and Vincent, A. (1999). The COE transcription factor Collier is a mediator of short-range Hedgehog-induced patterning of the Drosophila wing. Curr. Biol. 9, 632-639.
57. Walters, E., Grillo, M., Tarozzo, G., Stein-Izsak, C., Corbin, J., Bocchiaro, C. and Margolis, F. L. (1996). Proximal regions of the olfactory marker protein gene promoter direct olfactory neuron-specific expression in transgenic mice. J. Neurosci. Res. 43, 146-160.
58. Wang, F., Nemes, A., Mendelsohn, M. and Axel, R. (1998). Odorant receptors govern the formation of a precise topographic map. Cell 93, 47-60.
59. Wang, M. M. and Reed, R. R. (1993). Molecular cloning of the olfactory neuronal transcription factor Olf-1 by genetic selection in yeast. Nature 364, 121-126.
60. Wang, M. M., Tsai, R. Y., Schrader, K. A. and Reed, R. R. (1993). Genes encoding components of the olfactory signal transduction cascade contain a DNA binding site that may direct neuronal expression. Mol. Cell. Biol. 13, 5805-5813.
61. Wang, S. S., Betz, A. G. and Reed, R. R. (2002). Cloning of a Novel Olf-1/EBF-like Gene, O/E-4, by degenerate oligo-based direct selection. Mol. Cell Neurosci. 20, 404-414.
62. Wang, S. S., Tsai, R. Y. and Reed, R. R. (1997). The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 17, 4149-4158.
63. Weintraub, H. (1993). The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75, 1241-1244.
64. 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.
65. 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.