Protocols for two- and three-color fluorescent RNA in situ hybridization of the main and accessory olfactory epithelia in mouse

Journal of Neurocytology

Volumn 33, Issue 6, 2004, Pages 657-669

  Ishii, Tomohiro ^a   Omura, Masayo ^a   Mombaerts, Peter ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE;

ANIMAL TISSUE; ARTICLE; GENOMIC IN SITU HYBRIDIZATION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY EPITHELIUM; PRIORITY JOURNAL; RNA HYBRIDIZATION;

EID: 26444495013     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11068-005-3334-y     Document Type: Article

References (69)

1. ALENIUS, M. & BOHM, S. (1997) Identification of a novel neural cell adhesion molecule-related gene with a potential role in selective axonal projection. Journal of Biological Chemistry 272, 26083-26086.
2. BERGHARD, A. & BUCK, L. B. (1996) Sensory transduction in vomeronasal neurons: Evidence for Gαo, Gαi2, and adenylyl cyclase II as major components of a pheromone signaling cascade. The Journal of Neuroscience 16, 909-918.
3. BUCK, L. & AXEL, R. (1991) A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell 65, 175-187.
4. CARR, V. MCM. & FARBMAN, A. I. (1992) Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Experimental Neurology 115, 55-59.
5. CAU, E., CASAROSA, S. & GUILLEMOT, E. (2002) Mash1 and Ngn1 control distinct steps of determination and differentiation in the olfactory sensory neuron lineage. Development 129, 1871-1880.
6. CHERRY, J. A. & PHO, V. (2002) Characterization of cAMP degradation by phosphodiesterases in the accessory olfactory system. Chemical Senses 27, 643-652.
7. CHESS, A., SIMON, I., CEDAR, H. & AXEL, R. (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78, 823-834.
8. CLOUTIER, J. F., GIGER, R. J., KOENTGES, G., DULAC, C., KOLODKIN, A. L. & GINTY, D. D. (2002) Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons. Neuron 33, 877-892.
9. CLOUTIER, J. F., SAHAY, A., CHANG, E. C., TESSIER-LAVIGNE, M., DULAC, C., KOLODKIN, A. L. & GINTY, D. D. (2004) Differential requirements for semaphorin 3F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections. The Journal of Neuroscience 24, 9087-9096.
10. DEL PUNTA, K., PUCHE, A., ADAMS, N.C., RODRIGUEZ, I. & MOMBAERTS, P. (2002) A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35, 1057-1066.
11. DULAC, C. & AXEL, R. (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83, 195-206.
12. ESUMI, S., KAKAZU, N., TAGUCHI, Y., HIRAYAMA, T., SASAKI, A., HIRABAYASHI, T., KOIDE, T., KITSUKAWA, T., HAMADA, S. & YAGI, T. (2005) Monoallelic yet combinatorial expression of variable exons of the protocadherin-α gene cluster in single neurons. Nature Genetics 37, 171-176.
13. FARBMAN, A. I. (1990) Olfactory neurogenesis: Genetic or environmental controls? Trends in Neurosciences 13, 362-365.
14. FARBMAN, A. I. (1992) Cell Biology of Olfaction (Developmental and Cell Biology Series) Cambridge: Cambridge University Press.
15. GIACOBINI, P., BENEDETTO, A., TIRINDELLI, R. & FASOLO, A. (2000) Proliferation and migration of receptor neurons in the vomeronasal organ of the adult mouse. Developmental Brain Research 123, 33-40.
16. GUILLEMOT, F., LO, L. C., JOHNSON, J. E., AUERBACH, A., ANDERSON, D. J. & JOYNER, A. L. (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476.
17. GUSSING, F. & BOHM, S. (2004) NQO1 activity in the main and the accessory olfactory systems correlates with the zonal topography of projection maps. European Journal of Neuroscience 19, 2511-2518.
18. HALPERN, M. & MARTINEZ-MARCOS, A. (2003) Structure and function of the vomeronasal system: An update. Progress in Neurobiology 70, 245-318.
19. HAUPTMANN, G. (2001) One-, two-, and three-color whole-mount in situ hybridization to Drosophila embryos. Methods 23, 359-372.
20. HERRADA, G. & DULAC, C. (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90, 763-773.
21. HIROTA, J. & MOMBAERTS, P. (2004) The LIM-homeodomain protein Lhx2 is required for complete development of mouse olfactory sensory neurons. Proceedings of the National Academy of Sciences USA 101, 8751-8755.
22. HIROTA, S., ITO, A., MORII, E., WANAKA, A., TOHYAMA, M., KITAMURA, Y. & NOMURA, S. (1992) Localization of mRNA for c-kit receptor and its ligand in the brain of adult rats: An analysis using in situ hybridizationhistochemistry. Molecular Brain Research 15, 47-54.
23. HUARD, J. M., YOUNGENTOB, S. L., GOLDSTEIN, B. J., LUSKIN, M. B. & SCHWOB, J. E. (1998) Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. The Journal of Comparative Neurology 400, 469-486.
24. ISHII, T., HIROTA, J. & MOMBAERTS, P. (2003) Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Current Biology 13, 394-400.
25. ISHII, T., SERIZAWA, S., KOHDA, A., NAKATANI, H., SHIROISHI, T., OKUMURA, K., IWAKURA, Y., NAGAWA, F., TSUBOI, A. & SAKANO, H. (2001) Monoallelic expression of the odourant receptor gene and axonal projection of olfactory sensory neurons. Genes to Cells 6, 71-78.
26. ISHII, Y., NAKAMURA, S. & OSUMI, N. (2000) Demarcation of early mammalian cortical development by differential expression of fringe genes. Developmental Brain Research 119, 307-320.
27. JIA, C. & HALPERN, M. (1996) Subclasses of vomeronasal receptor neurons: Differential expression of G proteins (Gia2 and Goa) and segregated projections to the accessory olfactory bulb. Brain Research 719, 117-128.
28. KALUZA, J. F., GUSSING, F., BOHM, S., BREER, H. & STROTMANN, J. (2004) Olfactory receptors in the mouse septal organ. Journal of Neuroscience Research 76, 442-452.
29. KEVERNE, E. B. (1999) The vomeronasal organ. Science 286, 716-720.
30. KNOLL, B., SCHMIDT, H., ANDREWS, W., GUTHRIE, S., PINI, A., SUNDARESAN, V. & DRESCHER, U. (2003) On the topographic targeting of basal vomeronasal axons through Slit-mediated chemorepulsion. Development 130, 5073-5082.
31. KNOLL, B., ZARBALIS, K., WURST, W. & DRESCHER, U. (2001) A role for the EphA family in the topographic targeting of vomeronasal axons. Development 128, 895-906.
32. KOHMURA, N., SENZAKI, K., HAMADA, S., KAI, N., YASUDA, R., WATANABE, M., ISHII, H., YASUDA, M., MISHINA, M. & YAGI, T. (1998) Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20, 1137-1151.
33. KOSMAN, D., MIZUTANI, C. M., LEMONS, D., COX, W. G., MCGINNIS, W. & BIER, E. (2004) Multiplex detection of RNA expression in Drosophila embryos. Science 305, 846.
34. LAU, Y. E. & CHERRY, J. A. (2000) Distribution of PDE4A and Goa immunoreactivity in the accessory olfactory system of the mouse. Neuroreport 11, 27-32.
35. LEVSKY, J. M., SHENOY, S. M., PEZO, R. C. & SINGER, R. H. (2002) Single-cell gene expression profiling. Science 297, 836-840.
36. LI, J., ISHII, T., FEINSTEIN, P. & MOMBAERTS, P. (2004) Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428, 393-399.
37. LOCONTO, J., PAPES, F., CHANG, E., STOWERS, L., JONES, E. P., TAKADA, T., KUMANOVICS, A., FISCHER LINDAHL, K. & DULAC, C. (2003) Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112, 607-618.
38. MA, Q., KINTNER, C. & ANDERSON, D. J. (1996) Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87, 43-52.
39. MARTINEZ-MARCOS, A., UBEDA-BANON, I., DENG, L. & HALPERN, M. (2000) Neurogenesis in the vomeronasal epithelium of adult rats: Evidence for different mechanisms for growth and neuronal turnover. Journal of Neurobiology 44, 423-435.
40. MARTINI, S., SILVOTTI, L., SHIRAZI, A., RYBA, N. J. & TIRINDELLI, R. (2001) Co-expression of putative pheromone receptors in the sensory neurons of the vomeronasal organ. The Journal of Neuroscience 21, 843-848.
41. MATARAZZO, V., COHEN, D., PALMER, A. M., SIMPSON, P. J., KHOKHAR, B., PAN, S. J. & RONNETT, G. V. (2004) The transcriptional repressor Mecp2 regulates terminal neuronal differentiation. Molecular and Cellular Neuroscience 27, 44-58.
42. MATSUNAMI, H. & BUCK, L. B. (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90, 775-784.
43. MOMBAERTS, P. (2004a) Genes and ligands for odorant, vomeronasal and taste receptors. Nature Reviews Neuroscience 5, 263-278.
44. MOMBAERTS, P. (2004b) Odorant receptor gene choice in olfactory sensory neurons: The one receptor-one neuron hypothesis revisited. Current Opinion in Neurobiology 14, 31-36.
45. MONTMAYEUR, J. P., LIBERLES, S. D., MATSUNAMI, H. & BUCK, L. B. (2001) A candidate taste receptor gene near a sweet taste locus. Nature Neuroscience 4, 492-498.
46. NORLIN, E. M. & BERGHARD, A. (2001) Spatially restricted expression of regulators of G-protein signaling in primary olfactory neurons. Molecular and Cellular Neuroscience 17, 872-882.
47. OKA, Y., KOBAYAKAWA, K., NISHIZUMI, H., MIYAMICHI, K., HIROSE, S., TSUBOI, A. & SAKANO, H. (2003) O-MACS, a novel member of the medium-chain acyl-CoA synthetase family, specifically expressed in the olfactory epithelium in a zone-specific manner. European Journal of Biochemistry 270, 1995-2004.
48. PANTAGES, E. & DULAC, C. (2000) A novel family of candidate pheromone receptors in mammals. Neuron 28, 835-845.
49. PARATORE, C., SUTER, U. & SOMMER, L. (1999) Embryonic gene expression resolved at the cellular level by fluorescence in situ hybridization. Histochemistry and Cell Biology 111, 435-443.
50. RAWSON, N. E., EBERWINE, J., DOTSON, R., JACKSON, J., ULRICH, P. & RESTREPO, D. (2000) Expression of mRNAs encoding for two different olfactory receptors in a subset of olfactory receptor neurons. Journal of Neurochemistry 75, 185-195.
51. RODRIGUEZ, I., FEINSTEIN, P. & MOMBAERTS, P. (1999) Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97, 199-208.
52. ROTHMAN, A., FEINSTEIN, P., HIROTA, J. & MOMBAERTS, P. (2005) The promoter of the mouse odorant receptor gene M71. Molecular and Cellular Neuroscience 28, 535-546.
53. RUNNENBURGER, K., BREER, H. & BOEKHOFF, I. (2002) Selective G protein β-subunit compositions mediate phospholipase C activation in the vomeronasal organ. European Journal of Cell Biology 81, 539-547.
54. RYBA, N. J. & TIRINDELLI, R. (1997) A new multigene family of putative pheromone receptors. Neuron 19, 371-379.
55. SCHWARZENBACHER, K., FLEISCHER, J., BREER, H. & CONZELMANN, S. (2004) Expression of olfactory receptors in the cribriform mesenchyme during prenatal development. Gene Expression Patterns 4, 543-552.
56. SCHWOB, J. E. (2002) Neural regeneration and the peripheral olfactory system. The Anatomical Record 269, 33-49.
57. SERIZAWA, S., MIYAMICHI, K., NAKATANI, H., SUZUKI, M., SAITO, M., YOSHIHARA, Y. & SAKANO, H. (2003) Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302, 2088-2094.
58. SHYKIND, B. M., ROHANI, S. C., O'DONNELL, S., NEMES, A., MENDELSOHN, M., SUN, Y., AXEL, R. & BARNEA, G. (2004) Gene switching and the stability of odorant receptor gene choice. Cell 117, 801-815.
59. STROTMANN, J., CONZELMANN, S., BECK, A., FEINSTEIN, P., BREER, H. & MOMBAERTS, P. (2000) Local permutations in the glomerular array of the mouse olfactory bulb. The Journal of Neuroscience 20, 6927-6938.
60. TIAN, H. & MA, M. (2004) Molecular organization of the olfactory septal organ. The Journal of Neuroscience 24, 8383-8390.
61. TSUBOI, A., YOSHIHARA, S., YAMAZAKI, N., KASAI, H., ASAI-TSUBOI, H., KOMATSU, M., SERIZAWA, S., ISHII, T., MATSUDA, Y., NAGAWA, F. & SAKANO, H. (1999) Olfactory neurons expressing closely linked and homologous odorant receptor genes tend to project their axons to neighboring glomeruli on the olfactory bulb. The Journal of Neuroscience 19, 8409-8418.
62. WALZ, A., RODRIGUEZ, I. & MOMBAERTS, P. (2002) Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. The Journal of Neuroscience 22, 4025-4035.
63. WEILER, E. & FARBMAN, A. I. (1997) Proliferation in the rat olfactory epithelium: Age-dependent changes. The Journal of Neuroscience 17, 3610-3622.
64. WEILER, E., MCCULLOCH, M. A. & FARBMAN, A. I. (1999) Proliferation in the vomeronasal organ of the rat during postnatal development. European Journal of Neuroscience 11, 700-711.
65. WILKIE, G. S. & DAVIS, I. (1998) Visualizing mRNA by in situ hybridization using high resolution and sensitive tyramide signal amplification. Elsevier Trends Journals, Technical Tips Online:T01458.
66. YOSHIHARA, Y., KAWASAKI, M., TAMADA, A., FUJITA, H., HAYASHI, H., KAGAMIYAMA, H. & MORI, K. (1997) OCAM: A new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. The Journal of Neuroscience 17, 5830-5842.
67. YU, T. T., MCINTYRE, J. C., BOSE, S. C., HARDIN, D., OWEN, M. C. & MCCLINTOCK, T. S. (2005) Differentially expressed transcripts from phenotypically identified olfactory sensory neurons. The Journal of Comparative Neurology 483, 251-262.
68. ZAIDI, A. U., ENOMOTO, H., MILBRANDT, J. & ROTH, K. A. (2000) Dual fluorescent in situ hybridization and immunohistochemical detection with tyramide signal amplification. Journal of Histochemistry & Cytochemistry 48, 1369-1375.
69. ZHANG, X., RODRIGUEZ, I., MOMBAERTS, P. & FIRESTEIN, S. (2004) Odorant and vomeronasal receptor genes in two mouse genome assemblies. Genomics 83, 802-811.