Epidermal growth factor receptor mRNA and protein are expressed in progenitor cells of the olfactory epithelium

Journal of Comparative Neurology

Volumn 373, Issue 2, 1996, Pages 297-307

  Krishna, N S Rama ^a   Little, Susan S ^a   Getchell, Thomas V ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

basal cells; cell cycle; in situ RT PCR; mitogens; neurogenesis

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; MITOGENIC AGENT; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; MALE; MITOGENESIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

ANIMALS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C3H; OLFACTORY MUCOSA; POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; STEM CELLS; TRANSCRIPTION, GENETIC;

EID: 0029785848     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960916)373:2<297::AID-CNE11>3.0.CO;2-I     Document Type: Article

References (79)

1. Anchan, R.M., T.A. Reh, J. Angello, A. Balliet, and M. Walker (1991) EGF and TGF-α stimulate retinal neuroepithelial cell proliferation in vitro. Neuron 6:923-936.
2. Avivi, A., I. Lax, A. Ullrich, J. Schlessinger, D. Givol, and B. Morse (1991) Comparison of EGF receptor sequences as a guide to study the ligand binding site. Oncogene 6:673-676.
3. Buiakova, O.I., N.S. Rama Krishna, T.V. Getchell, and F.L. Margolis (1994) Human and rodent OMP genes: conservation of structural and regulatory motifs and cellular localization. Genomics 20:452-462.
4. Caggiano, M., J.S Kauer, and D.D. Hunter (1994) Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using replication-incompetent retrovirus. Neuron 13:339-352.
5. Calof, A.L., and D.M. Chikaraishi (1989) Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3:115-127.
6. Carpenter, G., and S. Cohen (1990) Epidermal growth factor. J. Biol. Chem. 265:770-782.
7. Cassel, D., and L. Glaser (1982) Proteolytic cleavage of epidermal growth factor receptor. J. Biol. Chem. 257:9845-9848.
8. Cohen, S., G. Carpenter, and L. King, Jr. (1980) Epidermal growth factor-receptor-protein kinase interactions. J. Biol. Chem. 255:4834-4842.
9. Cohen, S., H. Ushiro, C. Stoscheck, and M. Chinkers (1982) A native 170,000 epidermal growth factor receptor-kinase complex from shed plasma membrane vesicles. J. Biol. Chem. 257:1523-1531.
10. Deckner, M.L., J. Frisen, V.M.K. Verge, T. Hökfelt, and M. Risling (1993) Localization of neurotrophin receptors in olfactory epithelium and bulb. NeuroReport 5:301-304.
11. DeHamer, M.K., J.L. Guerva, K. Hannon, B.P. Olwin, and A.L. Calof (1994) Genesis of olfactory receptor neurons in vitro: regulation of progenitor cell divisions by fibroblast growth factors. Neuron 13:1083-1097.
12. Derynck, R. (1988) Transforming growth factor α. Cell 54:593-595.
13. Derynck, R., A.B. Roberts, M.E. Winkler, E.Y. Chen, and D.V. Goeddel (1984) Human transforming growth factor-α: precursor structure and expression in E. coli Cell 38:287-297.
14. Farbman, A.I. (1994) Developmental biology of olfactory sensory neurons. Semin. Cell Biol. 5:3-10.
15. Farbman, A.I., and J.A. Buchholz (1996) Transforming growth factor-α and other growth factors stimulate cell division in olfactory epithelium in vitro. J. Neurobiol. 30:267-280.
16. Farbman, A.I., J.A. Buchholz, and R.C. Bruch (1994a) Growth factor regulation of olfactory cell proliferation. In K. Kurihara, N. Suzuki, and H. Ogawa (eds): Olfaction and Taste XI. Tokyo: Springer-Verlag, pp. 45-48.
17. Farbman, A.I., R.C. Bruch, and J.A. Buchholz (1994b) Epidermal growth factor-receptor (EGFR-R) and EGF and/or transforming growth factor-α (TGF-α) may play a role in regulating olfactory cell proliferation. Chem. Senses 18:553.
18. Gardner, R.M., G. Verner, J.L. Kirkland, and G.M. Stancel (1989) Regulation of uterine epidermal growth factor (EGF) receptor by estrogen in the mature rat and during the estrous cycle. J. Steroid Biochem. 32:339-343.
19. Gamella, L.G., E.R. Sargent, and T.P. Wade (1989) Expression of transforming growth factor-α in normal human adult kidney and enhanced expression of transforming growth factor-α and β1 in renal cell carcinoma. Cancer Res. 49:6972-6978.
20. Getchell, M.L., A. Kulkarni-Narla, S. Takami, and T.V. Getchell (1995) Age-dependent phenotypic switching of mast cells in NGF-transgenic mice. NeuroReport 6:1261-1266.
21. Getchell, T.V., M.L. Getchell, and N.S. Rama Krishna (1996) Human olfactory receptor neurons and their central targets in the bulb differentially express BDNF and its receptor trk B. Assoc. Chemoreception Sci XVIII. Abstr. No. 95.
22. Graziadei, P.P.C., and G.A. Monti Graziadei (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8:1-18.
23. Gullick, W.J., J. Downward, and M.D. Waterfield (1985) Antibodies to the autophosphorylation sites of the epidermal growth factor receptor protein-tyrosine kinase as probes of structure and function. EMBO J. 4:2869-2877.
24. Heinford, B.W., A. Shum-Siu, M. Leonberger, and F.J. Hendler (1993) Variation in cellular EGF receptor mRNA expression demonstrated by in situ reverse transcriptase polymerase chain reaction. Nucleic Acids Res. 21:3159-3166.
25. Holbrook, E.H., K.E. Mieleszko Szumowski, and J.E. Schwob (1995) An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium. J. Comp. Neurol. 363:129-146.
26. Huard, J.M.T., and J.E. Schwob (1995) Cell cycle of globose basal cells in rat olfactory epithelium. Dev. Dyn. 203:17-26.
27. Key, B., H.B. Treloar, L. Wangerek, M.D. Ford, and V. Nurcombe (1996) Expression and localization of EGF-1 in the developing rat olfactory system. J. Comp. Neurol. 366:197-206.
28. Lee, K.H., D.F. Bowen-Pope, and R.R. Reed (1990) Isolation and characterization of the a platelet-derived growth factor receptor from rat olfactory epithelium. Mol. Cell Biol. 10:2237-2246.
29. Lee, D.C., S.E. Fenton, E.A. Berkowitz, and M.A. Hissong (1995) Transforming growth factor α: expression, regulation, and biological activities. Pharmacol. Rev. 47:51-85.
30. Lingham, R.B., G.M. Stancel, and D.S. Loose-Mitchell (1988) Estrogen regulation of epidermal growth factor receptor messenger ribonucleic acid. Mol. Endocrinol. 2:230-235.
31. Little, S.S., N.S. Rama Krishna, and T.V. Getchell (1996) RT-PCR identification of cell cycle-related expression of cyclin D1 and retinoblastoma genes in the mouse olfactory mucosa. Assoc. Res. Otolaryngol. Abstr. 580:145.
32. Mackay-Sim, A., and P. Kittel (1991) Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J. Neurosci. 11:979-984.
33. Madhukar, B.V., D.W. Brewster, and F. Matsumura (1984) Effects of in vivo administered 2,3,7,8-tetrachlorodibenzo-p-dixon on receptor binding of epidermal growth factor in the hepatic plasma membrane of rat, guinea pig, mouse, and hamster. Proc. Natl. Acad. Sci. USA 81:7407-7411.
34. Mahanthappa, N.K., and G.A. Schwarting (1993) Peptide growth factor control of olfactory neurogenesis and neuron survival in vitro: roles of EGF and TGF-βs. Neuron 10:293-305.
35. Margolis, F.L. (1980) A marker protein for the olfactory chemoreceptor neurons. In R.A. Bradhaw and D.M. Schneider (eds): Proteins of the Nervous System. New York: Raven Press, pp. 59-84.
36. Margolis, F.L. (1988) Molecular cloning of olfactory-specific gene products. In F.L. Margolis and T.V. Getchell (eds): Molecular Neurobiology of the Olfactory System. New York: Plenum Press, pp. 237-265.
37. Martinez, A., M.J. Miller, K. Quinn, E.J. Unsworth, M. Ebina, and F. Cuttita (1995) Non-radioactive localization of nucleic acids by direct in situ PCR and in situ RT-PCR in paraffin-embedded sections. J. Histochem. Cytochem. 43:739-747.
38. Mead, J.E., and N. Fausto (1989) Transforming growth factor-α may be a physiological regulator of liver regeneration by means of an autocrine mechanism. Proc. Natl. Acad. Sci. USA 86:1558-1562.
39. Miller, W.E., H.S. Earp, and N. Raab-Traub (1995) The epstein-Barr virus latent membrane 1 induces expression of the epidermal growth factor receptor. J. Virol. 69:4390-4398.
40. Moulton, D.G., G. Celebi, and R.P. Fink (1970) Olfaction in mammals - two aspects: proliferation of cells in the olfactory epithelium and sensitivity to odors. In G.E.W. Wolstenholme and J. Knight (eds): Taste and Smell in Vertebrates, CIBA Foundation Symposium. London: Churchill, pp. 227-250.
41. Newberry, E.P., and L.J. Pike (1995) Cell-cycle-dependent modulation of EGF-receptor-mediated signaling. Biochem. Biophys. Res. Com. 205:253-259.
42. Nuovo, G.J. (1994) PCR In Situ Hybridization: Protocols and Applications. New York: Raven Press.
43. Nuovo, G.J., P.B. MacConnell, A. Simsir, F. Valea, and D.L. French (1995) Correlation of the in situ detection of polymerase chain reaction-amplified metalloproteinase complementary DNAs and their inhibitors with prognosis in cervical carcinoma. Cancer Res. 55:267-275.
44. Orellana, S.A., W.E. Sweeney, C.D. Neff, and E.D. Avner (1995) Epidermal growth factor receptor expression is abnormal in murine polycystic kidney. Kidney Int. 47:490-499.
45. Palata-Salaman, C.R. (1991) Epidermal growth factor and the nervous system. Peptides 12:653-663.
46. 1 events and regulation of cell proliferation. Science 246:603-608.
47. Paria, B.C., S.K. Das, G.K. Andrews, and S.K. Dey (1993) Expression of the epidermal growth factor receptor gene is regulated in mouse blastocysts during delayed implantation. Proc. Natl. Acad. Sci. USA 90:55-59.
48. Pixley, S.K. (1992) Purified cultures of keratin positive cells: identification of a subset as neuronal supporting (sustentacular) cells. J. Neurosci. Res. 31:693-707.
49. Rama Krishna, N.S., M.L. Getchell, S.S. Tate, F.L. Margolis, and T.V. Getchell (1992) Glutathione and γ-glutamyl transpeptidase are differentially distributed in the olfactory mucosa of rats. Cell Tissue Res. 270:475-484.
50. Rama Krishna, N.S., T.V. Getchell, and M.L. Getchell (1994) Differential expression of alpha, mu, and pi classes of glutathione S-transferases in chemosensory mucosae of rats during development. Cell Tissue Res. 275:435-150.
51. Rama Krishna, N.S., M.L. Getchell, T.V. Getchell (1995a) Expression and induction of cyclin D1 and PCNA during cell cycle progression and apoptosis in the rat olfactory epithelium. Chem. Senses 20:725.
52. Rama Krishna, N.S., M.L. Getchell, F.L. Margolis, and T.V. Getchell (1995b) Differential expression of vomeromodulin and odorant-binding protein, putative pheromone and odorant transporters, in the developing rat nasal chemosensory mucosae. J. Neurosci. Res. 40:54-71.
53. Reynolds, B.A., W. Tetzlaff, and A. Weiss (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12:4565-4574.
54. Ronsin, B., C. Brisson, H.C. Mertani, B. Grandclement, and G. Morel (1995) Detection of growth hormone receptor mRNA using RT in situ PCR on frozen sections of rat pituitary. Biochemica 4:33-36.
55. Roskams, A.J.I., M. Angelyn Bethel, K. Joseph Hurt, and G.V. Ronnett (1996) Sequential expression of trks A, B, and C in the regenerating olfactory neuroepithelium. J. Neurosci. 16:1294-1307.
56. Salehi-Ashtiani, K., and A.I. Farbman (1995) Expression of the EGF family of receptors and ligands in the olfactory mucosa. Chem. Senses 20:771.
57. Sambrook, J., E.F. Fritsch, and T. Maniatis (1989) Molecular Cloning: A Laboratory Manual. 2nd Edition, Vol. 1. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
58. Schwob, J.E. (1992) The biochemistry of olfactory neurons: stages of differentiation and neuronal subsets. In M.L. Serby and K.L. Chodor (eds): Science of Olfaction. New York: Springer-Verlag, pp. 80-125.
59. Schwob, J.E., K.E. Mieleszko Szumowski, and A.A. Stasky (1992) Olfactory sensory neurons are topically dependent on the olfactory bulb for their prolonged survival. J. Neurosci. 12:3896-3919.
60. Schwob, J.E., J.M.T. Huard, M.B. Luskin, and S.L. Youngentob (1994) Retroviral lineage studies of the rat olfactory epithelium. Chem. Senses 19:671-682.
61. Schwob, J.E., S.L. Youngentob, and R.C. Mezza (1995) The reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. Comp. Neurol. 359:15-37.
62. Schwartz Levey, M.A., D.M. Chikaraishi, and J.S. Kauer (1991) Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J. Neurosci. 11:3556-3564.
63. Seroogy, K.B., C.M. Gall, D.C. Lee, and H.I. Kornblum (1995) Proliferative zones of postnatal rat brain express epidermal growth factor receptor mRNA. Brain Res. 670:157-164.
64. Sewall, C.H., G.C. Clark, and G.W. Lucier (1995) TCDD reduces rat hepatic epidermal growth factor receptor: comparison of binding, immunodetection, and autophosphorylation. Toxicol. Appl. Pharmacol. 132:263-272.
65. 1 phase progression: Cycling on cue. Cell 79:551-555.
66. Simmons, P.A., and T.V. Getchell (1981) Physiological activity of newly differentiated olfactory receptor neurons correlated with morphological recovery from olfactory nerve section in the salamander. J. Neurophysiol. 45:529-549.
67. Simmons, P.A., J.A. Rafols, and T.V. Getchell (1981) Ultrastructural changes in olfactory receptor neurons following olfactory nerve section. J. Comp. Neurol. 197:237-257.
68. Staecker, H., M. Cammer, T.R. Van De Water (1994) A procedure for RT-PCR amplification of mRNAs on histological specimens. Biotechniques 16:76-80.
69. Suzuki, Y., and M. Takeda (1991a) Basal cells in the mouse olfactory epithelium after axotomy: immunohistochemical and electron-microscopic studies. Cell Tissue Res. 266:239-245.
70. Suzuki, Y., and M. Takeda (1991b) Keratins in the developing olfactory epithelia. Dev. Brain Res. 59:171-178.
71. Takami, S., M.L. Getchell, and T.V. Getchell (1994) Lectin histochemical localization of galactose, N-acetylgalactosamine, and N-acetylglucosamine in glycoconjugates of the rat vomeronasal organ, with comparison to the olfactory and septal mucosae. Cell Tissue Res. 277:211-230.
72. Takami, S., M.L. Getchell, M. Yamagishi, K.M. Albers, and T.V. Getchell (1995) Enhanced extrinsic innervation of nasal and oral chemosensory mucosae in keratin 14-NGF transgenic mice. Cell Tissue Res. 282:481-491.
73. Thompson, J.F., M.V.D. Berg, and P.C.F. Stokkers (1994) Developmental regulation of epidermal growth factor receptor kinase in rat intestine. Gasteroenterology 107:1278-1287.
74. NGFR in the olfactory system following peripheral differentiation. NeuroReport 4:1023-1026.
75. Ushiro, H., and S. Cohen (1980) Identification of phosphotyrosine as a product of epidermal growth factor-activated protein kinase in A-431 cell membranes. J. Biol. Chem. 255:8363-8365.
76. Verhaagen, J., A.B. Oestreicher, M. Grille, Y.-S. Khew-Goodall, W.H. Gispen, and F.L. Margolis (1990) Neuroplasticity in the olfactory system: differential effects of central and peripheral lesions of the primary olfactory pathway on the expression of B-50/GAP43 and the olfactory marker protein. J. Neurosci. Res. 26:31-44.
77. Wang, S.L., C.Y. Wu-Wang, A. Slomiany, and B.L. Slomiany (1994) Effect of acute ethanol treatment on epidermal growth factor receptor in the rat stomach. Alcohol 11:11-15.
78. Weickert, C.S., and M. Blum (1995) Striatal TGFα: Postnatal developmental expression and evidence for a role in the proliferation of subependymal cells. Dev. Brain Res. 86:203-216.
79. Yamagishi, M., S. Hasegawa, S. Takahashi, Y. Nakano, and T. Iwanaga (1989) Immunohistochemical analysis of the olfactory mucosa by use of antibodies to brain proteins and cytokeratin. Ann. Otol. Rhinol. Laryngol. 98:384-388.