CaBPs and other immunohistochemical markers of the human vomeronasal system: A comparison with other mammals

Microscopy Research and Technique

Volumn 41, Issue 6, 1998, Pages 530-541

  Johnson, Edward W ^a  

^a Nucl Eng Idaho State University   (United States)

Author keywords

Calbindin; Calretinin; Neurocalcin; NSE; Olfactory marker protein; Parvalbumin; PGP 9.5

Indexed keywords

BIOCHEMISTRY;

CALBINDIN; CALRETININ; IMMUNOHISTOCHEMICAL MARKERS; IMMUNOHISTOCHEMISTRY; MARKER PROTEINS; NEUROCALCIN; NSE; OLFACTORY MARKER PROTEIN; PARVALBUMIN; PGP 9.5;

MAMMALS;

CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; GENE PRODUCT; NEUROCALCIN; NEURON SPECIFIC ENOLASE; PARVALBUMIN;

ADULT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; COMPARATIVE STUDY; CONTROLLED STUDY; EPITHELIUM CELL; FETUS; HEDGEHOG; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAMMAL; MOUSE; NERVE PROJECTION; NEWBORN; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RAT; VOMERONASAL ORGAN;

ANIMALIA; ERINACEIDAE; MAMMALIA;

EID: 0031879808     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19980615)41:6<530::AID-JEMT8>3.0.CO;2-Q     Document Type: Article

References (126)

1. Abe, H., Watanabe, M., and Kondo H. (1992) Developmental changes in expression of a calcium-binding protein (Spot 35-calbindin) in the nervus terminalis and the vomeronasal and olfactory receptor cells. Acta Otolaryngol. (Stockh.), 112:862-871.
2. Alonso, J.R., Arévalo, R., Crespo, C., García-Ojeda, E., Porteros, A., Briñ́n, J.G., and Aijón, J. (1995) NADPH-diaphorase active and calbindin D-28k-immunoreactive neurons and fibers in the olfactory bulb of the Hedgehog (Erinaceus europaeus). J. Comp. Neurol., 351:307-327.
3. Andressen, C., Blümcke, I., and Celio., M.R. (1993) Calcium-binding proteins: Selective markers of nerve cells. Cell Tissue Res., 271:181-208.
4. Baker, H. (1990) Unilateral, neonatal olfactory deprivation alters tyrosine hydroxylase expression but not aromatic amino acid decarboxylase or GABA immunoreactivity. Neuroscience 36:761-771.
5. Barber, P.C., and Raisman, G. (1974) An autoradiographic investigation of the projection of the vomeronasal organ to the accessory olfactory bulb in the mouse. Brain Res., 81:21-30.
6. 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.
7. Berliner, D.L., Monti-Bloch, L., Jenning-White, C., and Diaz-Sanchez, V. (1996) The functionality of the human vomeronasal organ (VNO): evidence for steroid receptors. J. Steroid Biochem. Mol. Biol., 58:259-265.
8. Boehm, N., and Gasser, B. (1993) Sensory receptor-like cells in the human foetal vomeronasal organ. NeuroReport, 4:867-870.
9. Bossy, J. (1980) Development of olfactory and related structures in staged human embryos. Anat. Embryol., 161:225-236.
10. Buck, L., and Axel, R. (1991) A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell, 65:175-187.
11. Buffa, R., Mare, P., Salvadore, M., Solcia, E., Furness, J.B. and Lawson, D.E.M. (1989) Calbindin 28 kDa in endocrine cells of known or putative calcium-regulating function. Histochemistry, 91:107-113.
12. Buiakova, O.I., Rama Krishna, N.S., Getchell, T.V., and Margolis, F.L. (1994) Human and rodent OMP genes: Conservation of structural and regulatory motifs and cellular localization. Genomics, 20:452-462.
13. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35:375-475.
14. Celio, M.R., Baier, W., Sch[00e4]rer, L., Gregersen, H.J., de Viragh, P.A., and Norman, A.W. (1990) Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. Cell Calcium, 11:599-602.
15. Chuah, M.I., and Zheng, D.R (1987) Olfactory marker protein is present in olfactory receptor cells of human fetuses. Neuroscience, 23:363-370.
16. Coppola, D.M., and Millar, L.C. (1994) Stimulus access to the accessory olfactory system in the prenatal and perinatal rat. Neuroscience, 60:463-468.
17. Coppola, D.M., and O'Connell, K.J. (1989) Stimulus access to olfactory and vomeronasal receptors in utero. Neurosci. Lett., 106:241-248.
18. Coppola, D.M., Budde, J., and Millar, L.C. (1993) The vomeronasal duct has a protracted postnatal development in the mouse. J. Morphol. 218:59-64.
19. Crosby, E.C., and Humphrey, T. (1939) Studies of the vertebrate telencephalon. I. The nuclear configuration of the olfactory and accessory olfactory formations and the nucleus olfactorius anterior of certain reptiles, birds and mammals. J. Comp. Neurol., 71:121-213.
20. Cutz, E., Chan, W., Wong, V., and Conen, P.E. (1975) Ultrastructure and fluorescence histochemistry of endocrine (APUD-type) cells in tracheal mucosa of human and various animal species. Cell Tissue Res., 158:425-437.
21. Domes, K.M, Adkins-Regan, E., and Halpern, B.P. (1997) Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in the pig. Brain Behav. Evol., 49:53-62.
22. Dulac, C., and Axel, R. (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell, 83:195-206.
23. Eisthen, H.L. (1992) Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates. Microsc. Res. Tech., 23:1-21.
24. Farbman, A.I., and Margolis F.L. (1980) Olfactory marker protein during ontogeny: immunohistochemical localization. Dev. Biol., 74:205-215.
25. Garcia-Velasco J., and Mondragon M. (1991) The incidence of the vomeronasal organ in 1000 human subjects and its possible clinical significance. J. Steroid Biochem. Mol. Biol., 39:561-563.
26. Garrosa, M., Coca, S., and Mora, O.A. (1986) Histological development of the vomeronasal complex in the pre- and postnatal rat. Acta Otolaryngol. (Stockh.), 102:291-301.
27. Garrosa, M., Iñiguez, Fernandez, J.M., and Gayoso, M.J. (1992) Developmental stages of the vomeronasal organ in the rat: A light and electron microscopic study. J. Hirnforsch., 33:123-132.
28. Halpern, M. (1987) The organization and function of the vomeronasal system. Ann. Rev. Neurosci., 10:325-362.
29. Herrada, G., and Dulac, C. (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell, 90:763-773.
30. Houghton, P.E., Buchan, A.M.J., and Challis, J.R.G. (1992) Ontogeny of the distribution and colocalization of Calbindin D28k within neural and endocrine cells of the gastrointestinal tract of fetal and neonatal sheep. Regulat. Pept., 37:73-83.
31. Humphrey, T. (1940) The development of the olfactory and the accessory olfactory formations in human embryos and fetuses. J. Comp. Neurol., 73:431-468.
32. Humphrey, T., and Crosby, B.C. (1938) The human olfactory bulb. Univ. (of Mich.) Hosp. Bull., 4:61-62.
33. Iino, S., Kobayashi, S., Okazaki, K., and Hidaka, H. (1995) Neurocalcin-immunoreactive receptor cells in the rat olfactory epithelium and vomeronasal organ. Neurosci. Lett. 191:91-94.
34. Ito, T., Udaka, N., Inayama, Y., Kitamura, H., and Kanisawa, M. (1998) Hamster pulmonary endocrine cells with positive immuno-staining for calbindin-D28k. Histochem. Cell Biol., 109:67-73.
35. Jacobowitz, D.M., and Winsky, L. (1991) Immunocytochemical localization of calretmin in the forebrain of the rat. J. Comp. Neurol., 304:198-218.
36. Johnson, A., Josephson, R., and Hawke, M. (1985) Clinical and histological evidence for the presence of the vomeronasal (Jacobson's) organ in adult humans. J. Otolaryngol., 14:71-79.
37. Johnson, E.W., Eller, P.M., and Jafek, B.W. (1992) Calbindin-like immunoreactivity in two peripheral chemosensory tissues of the rat: Taste buds and the vomeronasal organ. Brain Res., 572:319-324.
38. Johnson, E.W., Eller, P.M., and Jafek, B.W. (1993) An immuno-electron microscopic comparison of olfactory marker protein localization in the supranuclear regions of the rat olfactory epithelium and vomeronasal organ neuroepithelium. Acta Otolaryngol. (Stockh.), 113:766-771.
39. Johnson, E.W., Eller, P.M., and Jafek, B.W. (1994a) Calbindin-like immunoreactivity in epithelial cells of the newborn and adult human vomeronasal organ. Brain Res., 638:329-333.
40. Johnson, E.W., Eller, P.M., and Jafek, B.W. (1994b) Protein gene product 9.5 in the developing and mature rat vomeronasal organ. Dev. Brain Res., 78:259-264.
41. Johnson, E.W., Eller, P.M., and Jafek, B.W. (1995a) Distribution of OMP-, PGP 9.5- and CaBP-like immunoreactive chemoreceptor neurons in the developing human olfactory epithelium. Anat. Embryol., 191:311-317.
42. Johnson, E.W., Eller, P.M., and Jafek, B.W. (1995b) More evidence that the human vomeronasal organ has unique epithelial cells: Calbindin-, NSE-, OMP-, and PGP-like immunoreactivity in two fetuses. Chem. Senses, 20:714-715.
43. Johnson, E.W., Eller, P.M., and Jafek, B.W. (1997) Protein gene product 9.5-like and calbmdin-like immunoreactivity in the nasal respiratory mucosa of perinatal human. Anat. Rec., 247:38-45.
44. Kishimoto, J., Keverne, E.B., and Emson, P.C. (1993) Calretinin, calbindin-D28k and parvalbumin-like immunoreactivity in mouse chemoreceptor neurons. Brain Res., 610:325-329.
45. Kjær, I., and Fischer Hansen, B. (1996) The human vomeronasal organ: prenatal development stages and distribution of luteinizing hormone-releasing hormone. Eur. J. Oral Sci., 104:34-40.
46. Kosaka, K., Heizmann, C.W., and Kosaka, T. (1994a) Calcium-binding protein parvalbumin-immunoreactive neurons in the rat olfactory bulb. 1. Distribution and structural features in adult rat. Exp. Brain Res., 99:191-204.
47. Kosaka, K., Heizmann, C.W., and Kosaka, T. (1994b) Calcium-binding protein parvalbumin-immunoreactive neurons in the rat olfactory bulb. 2. Postnatal development. Exp. Brain Res., 99:205-213.
48. Kreutzer, E.W., and Jafek, B.W. (1980) The vomeronasal organ of Jacobson in the human embryo and fetus. Otolaryngol. Head Neck Surg., 88:119-123.
49. Kroner, C., Breer, H., Singer, A.G., and O'Connell, R.J. (1996) Pheromone-induced second messenger signalling in the hamster vomeronasal organ. NeuroReport, 7:2989-2992.
50. Labella, T., and Ciges, M. (1975) Ontogenia y estudio comparative del órgano de Jacobson en el hombre. Acta Otorrinolar. Esp., 26:167-182.
51. Larriva-Sahd, J., Rondan, A., Orozco-Estevez, H., and Sanchez-Robles, M.R. (1993) Evidence of a direct projection of the vomeronasal organ to the medial preoptic nucleus and hypothalamus. Neurosci. Lett, 163:45-49.
52. Lauweryns, J.M., and Seldeslagh, K.A. (1993) Immunocytochemical expression of protein gene product (PGP) 9.5 in the cat bronchopulmonary neuroendocrine cells and nerves. Anat Rec., 236:191-197.
53. Lévy, F., Locatelli, A., Piketty, V., Tillet, Y, and Poindron, P. (1995) Involvement of the main but not the accessory olfactory system in maternal behavior or primiparous and multiparous ewes. Physiol. Behav., 57:97-104.
54. Liman, E.R. (1996) Pheromone transduction in the vomeronasal organ. Curr. Opin. Neurobiol., 6:487-493.
55. Liman, E.R., and Corey, D.P. (1996) Electrophysiological characterization of chemosensory neurons from the mouse vomeronasal organ. J. Neurosci., 16:4625-4637.
56. Marangos, P.J., and Schmechel, D.E. (1987) Neuron specific enolase, a clinically useful marker for neurons and neuroendocrine cells. Ann. Rev. Neurosci., 10:269-295.
57. Margolis, F.L. (1972) A brain protein unique to the olfactory bulb: Isolation and immunological studies. Proc. Natl. Acad. Sci. U.S.A., 69:1221-1224.
58. Margolis, F.L. (1980) A marker protein for the olfactory chemoreceptor neuron. In: Proteins of the Nervous System, 2nd ed. R.A. Bradshaw, and D.M. Schneider, eds. Raven Press, New York, pp. 59-84.
59. Margolis, F.L. (1985) Olfactory marker protein: from PAGE band to cDNAclone. Trends Neurosci., Dec:542-546.
60. Matsunami, H., and Buck, L.B. (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell, 90:775-784.
61. McClintock, M.K. (1971) Menstrual synchrony and suppression. Nature, 229:244-245.
62. Menco, B.Ph.M. (1989) Electron-microscopic demonstration of olfactory-marker protein with protein G-gold in freeze-substituted, Lowicryl K11M-embedded rat olfactory-receptor cells. Cell Tissue Res., 256:275-281.
63. Monti-Bloch, L., and Grosser, B.I (1991) Effect of putative pheromones on the electrical activity of the human vomeronasal organ and olfactory epithelium. J. Steroid Biochem Mol. Biol., 39:573-582.
64. Monti-Bloch, L., Jennings-White, C., Dolberg, D.S., and Berliner, D.L. (1994) The human vomeronasal system. Psychoneuroendocrinology, 19:673-686.
65. Monti Graziadei, U.A., Margolis, F.L, Harding, J.W., and Graziadei, P.P.C. (1977) Immunocytochemistry of the olfactory marker protein. J. Histochem. Cytochem., 25:1311-1316.
66. Monti Graziadei, G.A., Stanley, R.S, and Graziadei, P.P.C. (1980) The olfactory marker protein in the olfactory system of the mouse during development. Neuroscience, 5:1239-1252.
67. Moran, D.T., Jafek, B.W., and Rowley, J.C.III (1991) The vomeronasal (Jacobson's) organ in man: ultrastructure and frequency of occurrence. J. Steroid Biochem. Mol. Biol., 39:545-552.
68. Moss, R.L., Dudley, C.A., and Condon, K. (1993) Direct projections of bipolar cells of the vomeronasal (VNO) organ to the accessory olfactory bulb (AOB). Soc. Neurosci. Abstr., 19:120 (Abstr. 53.17).
69. Nakashima, T., Kimmelman, C.P., and Snow, J.B. (1985a) Olfactory marker protein in the human olfactory pathway. Arch. Otolaryngol., 111:294-297.
70. Nakashima, T., Kimmelman, C.P., and Snow J.B. (1985b) Immunohistopathology of human olfactory epithelium, nerve and bulb. Laryngoscope, 95:391-396.
71. Nakashima, T., Kimmelman, C.P., and Snow J.B. (1985c) Vomeronasal organs and nerves of Jacobson in the human fetus. Acta Otolaryngol. (Stockh), 99:266-271.
72. Ohm, T.G., Braak, E., and Probst, A. (1988) Somatostatin-14-like immunoreactive neurons and fibres in the human olfactory bulb. Anat. Embryol., 179:165-172.
73. Ohm, T.G., Braak, E., Probst, A., and Weindl, A. (1989) Neuropeptide Y-like immunoreactive neurons in the human olfactory bulb. Brain Res., 451:295-300.
74. Ohm, T.G., Müller, H., and Braak, E. (1990) Glutamic-acid-decarboxylase- and parvalbumin-like-immunoreactive structures in the olfactory bulb of the adult human. J. Comp. Neurol., 291:1-8.
75. Ohm, T.G., Müller, H., and Braak, E. (1991) Calbindin-D-28k-like immunoreactive structures in the olfactory bulb and anterior olfactory nucleus of the human adult: Distribution and cell typology, partial complementarity with parvalbumin. Neuroscience, 42:823-840.
76. O'Rahilly, R., Muller, F., Hutchins, G.M., and Moore, G.W. (1988) Computer ranking of the sequence of appearance of 40 features of the brain and related structures in staged human embryos during the seventh week of development. Am. J. Anat., 182:295-317.
77. Ortmann, R. (1989) Über sinneszellen am fetalen vomeronasalen organ des menschen. HNO, 37:191-197.
78. Parmentier, M. (1990) Structure of the human cDNAs and genes coding for calbindin D28K and calretinin. Adv. Exp. Med. Biol. 269:27-34.
79. Parmentier, M., Ghysens, M., Rypens, F., Lawson, D.E.M., Pasteels, J.L., and Pochet, R. (1987) Calbindin in vertebrate classes: Immunohistochemical localization and Western blot analysis. Gen. Comp. Endocrinol., 65:399-107.
80. Pasteels, J.L., Rogers, J., Blachier, F., and Pochet, R. (1990) Calbindin and calretinin localization in retina from different species. Vis. Neurosci., 5:1-16.
81. Pearson, A.A. (1942) The development of the olfactory nerve, the nervus terminalis, and the vomeronasal nerve in man. Ann. Otol. Rhinol. Laryngol., 51:317-332.
82. Pedersen, P.E., Stewart, W.B., Greer, C.A., and Shepherd, G.M. (1983) Evidence for olfactory function in utero. Science, 221:478-480.
83. Persechini, A., Moncrief, N.D., and Kretsinger, R.H. (1989) The EF-hand family of calcium-modulated proteins. Trends Neurosci., 12:462-467.
84. Pochet, R., Parmentier, M., Lawson, D.E.M., and Pasteel, J.L. (1985) Rat brain synthesizes two Vitamin D-dependent' calcium-binding proteins. Brain Res., 345:251-256.
85. Porteros, A., Arévalo, R., Crespo, C., García-Ojeda, E., Briñón, J.G., Aijón, J., and Alonso, J.R. (1995) Calbindin D-28k immunoreactivity in the rat accessory olfactory bulb. Brain Res., 689:93-100.
86. Porteros, A., Briñón, J.G., Crespo, C., Okazaki, K., Hidaka, H., Aijón. J., and Alonso, J.R. (1996) Neurocalcin immunoreactivity in the rat accessory olfactory bulb. Brain Res., 729:82-89.
87. Rama Krishna, N.S, Getchell, M.L., Buiakova, O.I., Margolis, F.L., and Getchell, TV. (1995) Human olfactory receptor neurons contain OMP mRNA in their dendritic and axonal processes. NeuroReport, 6:817-821.
88. Résibois, A., and Rogers, J.H. (1992) Calretinin in rat brain: an immunohistochemical study. Neuroscience, 46:101-134.
89. 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.
90. Rogers, J.H. (1987) Calretinin: A gene for a novel calcium-binding protein expressed principally in neurons. J. Cell Biol., 105:1343-1353.
91. Rogers, J.H. (1989a) Two calcium-binding proteins mark many chick sensory neurons. Neuroscience, 31:697-709.
92. Rogers, J.H. (1989b) Immunoreactivity for calretinin and other calcium-binding proteins in cerebellum. Neuroscience 31:711-721.
93. Rogers, J.H., and Résibois, A. (1992) Calretinin and calbindin-D28k in rat brain: Patterns of partial co-localization. Neuroscience, 51:843-865.
94. Russell, M.J. (1976) Human olfactory communication. Nature, 260:522-524.
95. Russell, M.J, Switz, G.M., Thompson, K. (1980) Olfactory influences on the human menstrual cycle. Pharmacol. Biochem. Behav., 13:737-738.
96. Ryba, N.J., and Tirindelli, R. (1997) A new multigene family of putative pheromone receptors. Neuron, 19:371-379.
97. Salazar, I., Barber, P.C., and Cifuentes, J.M. (1992) Anatomical and immunohistochemical demonstration of the primary neural connections of the vomeronasal organ in the dog. Anat. Rec., 233:309-313.
98. Salazar, I., Quinteiro, P.C., Cifuentes, J.M., and Caballero, T.G. (1996) The vomeronasal organ of the cat. J. Anat., 188: 445-454.
99. Schwarting, G.A., Drinkwater, D., and Crandall, J.E. (1994) A unique neuronal glycolipid defines rostrocaudal compartmentalization in the accessory olfactory system of rats. Dev. Brain Res., 78:191-200.
100. Shamley, D.R., Opperman, L.A., Buffenstein, R., and Ross, F.P. (1992) Ontogeny of calbindin-D28k and calbindin-D9k in the mouse kidney, duodenum, cerebellum and placenta. Development 116:491-496.
101. Shnayder, L., Schwanzel-Fukuda, M., and Halpern, M. (1993) Differential OMP expression in opossum accessory olfactory bulb. NeuroReport, 5:193-196.
102. Sipos, M.L., Wysocki, C.J., Nyby, J.G., Wysocki, L., and Nemura, TA. (1995) An ephemeral pheromone of female house mice: Perception via the main and accessory olfactory systems. Physiol Behav., 58:529-534.
103. Smith, R.L., Baker, H., Kolstad, K., Spencer, D.D., and Greer, C.A. (1991) Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivities in the human and macaque olfactory bulbs. Brain Res., 548:140-148.
104. Smith, R.L., Baker, H., and Greer, C.A. (1993) Immunohistochemical analyses of the human olfactory bulb. J. Comp. Neurol., 333:519-530.
105. Smith, T.D., Siegel, M.I., Mooney, M.P., Burdi, A.R., Burrows, A.M., and Todhunter, J.S. (1997) Prenatal growth of the human vomeronasal organ. Anat. Rec., 248:447-455.
106. Stensaas, L.J., Lavker, R.M., Monti-Bloch, L., Grosser, B.I., and Berliner, D.L. (1991) The vomeronasal (Jacobson's) organ in man: ultrastructure and frequency of occurrence. J. Ster. Biochem. Mol. Biol., 39:553-560.
107. Stern, K., and McClintock, M.K. (1998) Regulation of ovulation by human pheromones. Nature, 392:177-179.
108. Swann, J., and Fiber, J.M. (1997) Sex differences in function of a pheromonally stimulated pathway: Role of steroids and the main olfactory system. Brain Res. Bull., 44:409-413.
109. Takami, S., Getchell, M.L., Chen, Y., Monti-Bloch, L., Berliner, D.L., Stensaas, L.J., and Getchell, T.V. (1993) Vomeronasal epithelial cells of the adult human express neuron-specific molecules, Neuroreport, 4:375-378.
110. Talamo, B.R., Rudel, R.A., Kosik, K.S., Lee, V.M.-Y., Neff, S., Adelman, L., and Kauer, J.S. (1989) Pathological changes in olfactory neurons in patients with Alzheimer's disease. Nature, 337:736-739.
111. Taniguchi, K., Saito, H., Okamura, M., and Ogawa, K. (1993) Immunohistochemical demonstration of protein gene product 9.5 (PGP 9.5) in the primary olfactory system of the rat. Neurosci. Lett., 156:24-26.
112. Tarozzo, G., Cappello, P., De Andrea, M., Walters, E., Margolis, F.L., Oestreicher, B., and Fasolo, A. (1998) Prenatal differentiation of mouse vomeronasal neurones. Eur. J. Neurosci., 10:392-396.
113. Thompson, R.J., Doran, J.F., Jackson, P., Dhillon, A.P., and Rode, J. (1983) PGP 9.5, a new marker for vertebrate neurons and neuroendocrine cells. Brain Res., 278:224-228
114. Veith, J.L , Buck, M., Getzlaf, S., Van Dalfsen, P., and Slade, S (1983) Exposure to men influences the occurrence of ovulation in women Physiol. Behav., 31:313-315.
115. Wang R., Jiang S , and Gu R. (1994) [Immunohistochemical study of the olfactory mucosa and vomeronasal organ in rat, guinea pig and human fetus] published in Chinese. Chung. Hua. Erh. Pi. Yen. Hou. Ko. Tsa. Chih., 29:23-26.
116. Weller, A., and Weller, L. (1997) Menstrual synchrony under optimal conditions: Bedouin families. J. Comp. Psychol. 111:143-151.
117. Wekesa, K.S , and Anholt, R.R.H. (1997) Pheromone regulated produc- tion of inositol-(1, 4, 5)-triphosphate in the mammalian vomeronasal organ. Endocrinology, 138:3497-3504.
118. Wensley, C.H., Stone, D.M., Baker, H., Kauer, J.S., Margolis, F.L., and Chikaraishi, D.M. (1995) Olfactory marker protein mRNA is found in axons of olfactory receptor neurons. J. Neurosci., 15:4827-4837.
119. Wharton, J., Polak, J.M., Cole, G.A., Marangos, P.J., and Pearse, A.O.E. (1981) Neuron-specific enolase as an immunocytochemical marker for diffuse neuroendocrine system in human fetal lung. J. Histochem. Cytochem., 29:1359-1364.
120. Winsky, L., Nakata, H., Martin, B.M., and Jacobowitz, D.M. (1989) Isolation, partial amino acid sequence, and immunohistochemical localization of a brain-specific calcium-binding protein Proc. Natl. Acad. Sci. U.S.A., 86:10139-10143.
121. Wysocki, C.J. (1979) Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci. Biobehav. Rev., 3:301-341.
122. Yamagishi, M., Ishizuka, Y., Fujiwara, M., Nakamura, H., Igarashi, S., Nakano, Y., and Kuwano, R. (1993) Distribution of calcium binding proteins in sensory organs of the ear, nose and throat. Acta Otolaryngol. (Stockh.) Suppl., 506:85-89.
123. Yamagishi, M., Okazoe, R., and Ishizuka, Y. (1994) Olfactory mucosa of patients with olfactory disturbance following head trauma. Ann. Otol. Rhinol. Laryngol., 103:279-284.
124. Yamagishi, M., Takami, S., and Getchell, T.V. (1996) Ontogenetic expression of spot 35 protein (calbindin-D28k) in human olfactory receptor neurons and its decrease in Alzheimer's disease patients. Ann. Otol. Rhinol. Laryngol., 105:132-139.
125. Yoshida, J., Kimura, J., Tsukise, A., and Okano, M. (1993) Developmental study on the vomeronasal organ in the rat fetus. J. Reprod. Dev., 39:47-54.
126. Zhou, A., and Moss, R.L. (1997) Effect of urine-derived compounds on cAMP accumulation in mouse vomeronasal cells. NeuroReport, 8:2173-2177.