Carotid labyrinth of amphibians

Microscopy Research and Technique

Volumn 59, Issue 3, 2002, Pages 207-226

  Kusakabe, Tatsumi ^a  

^a KOKUSHIKAN UNIVERSITY   (Japan)

Author keywords

Amphibia; Carotid body; Carotid labyrinth; Chemoreceptor; Immunohistochemistry; Ontogeny; Peptidergic innervation; Ultrastructure

Indexed keywords

ARCHES; BIOCHEMISTRY; COLLAGEN; CYTOLOGY; ENDOTHELIAL CELLS; FLUORESCENCE; MAMMALS; MUSCLE; PEPTIDES;

AMPHIBIUM; CAROTID BODY; CAROTID LABYRINTH; EXTERNAL CAROTID ARTERIES; FINE STRUCTURES; GLOMUS CELLS; IMMUNOHISTOCHEMISTRY; ONTOGENY; PEPTIDERGIC INNERVATION; ULTRASTRUCTURE;

CHEMOSENSOR;

AMPHIBIA; ANTIBODY LABELING; ARTICLE; BLOOD FLOW; BLOOD VESSEL INNERVATION; BLOOD VESSEL TONE; BRAIN REGION; CAROTID ARTERY; CAROTID BODY; CAROTID SINUS; CELL ULTRASTRUCTURE; COMMON CAROTID ARTERY; CORROSION; CYTOPLASM; EFFERENT NERVE; ENDOTHELIUM CELL; EXTERNAL CAROTID ARTERY; FROG; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; INTERNAL CAROTID ARTERY; LARVAL DEVELOPMENT; METAMORPHOSIS; MORPHOGENESIS; NONHUMAN; PERICYTE; PRIORITY JOURNAL; SENSORY NERVE; SMOOTH MUSCLE FIBER; THREE DIMENSIONAL IMAGING;

AMPHIBIA; ANURA; GLOMUS; MAMMALIA;

EID: 0036828105     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jemt.10195     Document Type: Article

References (109)

1. Adams WE. 1958. The Comparative Morphology of the Carotid Body and Carotid Sinus. Springfield, IL: Charles V Thomas. p 202-214.
2. Banister RJ, Mann SP. 1965. An investigation of the adrenergic innervation of the heart and major blood vessels of the frog by Falck's method of fluorescence microscopy. J Physiol 181:13P-15P.
3. Banister RJ, Portig PJ, Vogt M. 1967. The content and localization of catecholamines in the carotid labyrinths and aortic arches of Rana temporaria. J Physiol 192:529-535.
4. Barer GR, Edwards C, Jolly AI. 1976. Changes in the carotid body and ventilatory response to hypoxia in chronically hypoxic rats. Clin Sci 50:311-313.
5. Bennett T. 1971. The neuronal and extra-neuronal localizations of biogenic amines in the cervical ganglion of the domestic fowl (Gallus gallus domesticus L.). Z Zellforsch 112:443-464.
6. Biscoe TJ, Stehbens WE. 1966. Ultrastructure of the carotid labyrinth. J Cell Biol 30:563-578.
7. Blessing MH, Wolff H. 1973. Befunde an glomus caroticum der ratte nach aufenhalt im einer simulierten Höhe von 7500m. Virchows Arch Pathol Anat Physiol 360:78-97.
8. Böck P, Gorgas K. 1976. Catecholamines anf granule content of the carotid body type-I cells. In: Coupland RE, Fujita T, editors. Chromaffin, Enterochromaffin and Related Cells. Amsterdam: Elsevier. p 355-374.
9. Boissezon P. 1939. Le labyrinthe carotidien de la grenouille rouse adulte. Bull Soc Hist Nat Tolouse 73:145-152.
10. Brain SD, Williams TJ, Tippins JR, Moris HR, McIntyre I. 1985. Calcitonin gene-related peptide is a potent vasodilator. Nature 313:54-56.
11. Cannatella DC, Treub L. 1988. Evolution of pipoid frogs: Intergeneric relationships of the aquatic frog family Pipidae (Anura). Zool J Linn Soc 94:1-38.
12. Carman JB. 1955. The carotid labyrinth in Hyla aurea, with a note on that in Leiopelma hochstettri. J Anat 89:503-525.
13. Carman JB. 1967a. The carotid labyrinth in the anuran Breviceps mossambicys. Trans R Soc New Zeal Zool 10:1-15.
14. Carman JB. 1967b. The morphology on the carotid labyrinth in Bufo bufo and Leiopelma hochstetteri. Trans R Soc New Zeal Zool 10:71-76.
15. Chiocchio SR, Biscardi AM, Tramezzani JH. 1966. Catecholamines in the carotid body of the cat. Nature 212:834-835.
16. Chowdhary DS. 1951. The carotid labyrinth of Rana tigrina. Nature 167:1074.
17. Cuello AC, McQeen DS. 1980. Substance P: A carotid body peptide. Neurosci Lett 17:215-219.
18. Dhillon DP, Barer GR, Walsh M. 1984. The enlarged carotid body of the chronically hypoxic and chronically hypoxic and hypercapnic rat: A morphometric analysis. Q J Exp Physiol 69:301-317.
19. Dual DE. 1980. The origin of nuclear bodies: A study of the undifferentiated epithelial cells of the equine small intestine. Am J Anat 157:61-70.
20. Duellman WE, Trueb L. 1986. Biology of Amphibians. New York: McGraw-Hill. p 397-405.
21. Edvinsson L, Uddman R. 1982. Immunohistochemical localization and dilatatory effect of substance P on cerebral vessels. Brain Res 232:466-471.
22. Edvinsson L, McCulloch J, Uddman R. 1981. Substance P: Immunohistochemical localization and effect upon feline pial arteries in vitro and in situ. J Physiol 318:251-258.
23. Edvinsson L, Emson P, McCulloch J, Teramoto K, Uddman R. 1983. Neuropeptide Y: Cerebrovascular innervation and vasomotor effects in the cat. Neurosci Lett 43:79-84.
24. Foster CL, Young BA, Allason M, Cameron E. 1965. Nuclear inclusions in the adenohypophysis of the rabbit. J Endocrinol 33:159-160.
25. Grifond B, Boer HH, Wijedens J. 1986. Localization and function of an FMRFamide-like substance in the aorta of Helix aspera. Cell Tissue Res 246:303-307.
26. Hallberg D, Pernow B. 1975. Effect of substance P of various vascular beds in the dog. Acta Physiol Scand 93:277-285.
27. Heath D, Edwards C, Winson M, Smith P. 1973. Effects on the right ventricle, pulmonary vasculature, and carotid bodies of the rat exposed to, and recovery from, simulated high altitude. Thorax 28:24-28.
28. Hirakawa H, Nakamura T, Hayashida Y. 1997. Effect of carbon dioxide on autonomic cardiovascular responses to systemic hypoxia in conscious rats. Am J Physiol 273:R747-R754.
29. Ishida S. 1954. So-called carotic body of the Amphibia. Igaku Kenkyu 24:1024-1050.
30. Ishii K, Ishii K. 1973. Fiber composition and derivation of afferent and efferent nerve fibers in the carotid nerve innervating the carotid labyrinth of the toad. Tohoku J Exp Med 109:323-337.
31. Ishii K, Kusakabe T. 1982. The glomus cell of the carotid labyrinth of Xenopus laevis. Cell Tissue Res 224:459-463.
32. Ishii K, Oosaki T. 1966. Electron microscopy of the chemoreceptor cells of the carotid labyrinth of the toad. Nature 212:1499-1500.
33. Ishii K, Oosaki T. 1969. Fine structure of the chemoreceptor cell in the amphibian carotid labyrinth. J Anat 104:263-280.
34. Ishii K, Honda K, Ishii K. 1966. The function of the carotid labyrinth in the toad. Tohoku J Exp Med 88:103-116.
35. Jakobowitz DM, Helke CJ. 1980. Localization of substance P immunoreactive nerves in the carotid body. Brain Res Bull 5:195-197.
36. Kameda Y. 1989. Distribution of CGRP-, somatostatin-, galanin-, VIP-, and substance P-immunoreactive nerve fibers in the chicken carotid body. Cell Tissue Res 257:623-629.
37. Kameda Y. 1990a. Innervation of the serotonin-immunoreactive cells distributed in the wall of the common carotid artery and its branches in the chicken. J Comp Neurol 292:537-550.
38. Kameda Y. 1990b. Distribution of serotonin-immunoreactive cells around arteries arising from the common carotid artery in the chicken. Anat Rec 227:87-96.
39. Kameda Y. 1994. Electron microscopic study on the development of the carotid body and glomus cell group distributed in the wall of the common carotid artery and its branches in the chicken. J Comp Neurol 348:544-555.
40. Kameda Y. 1999. Ultrastructural localization of neuropeptide Y and expression of its mRNA in the glomus cells distributed in the wall of the common carotid artery of the chicken. J Comp Neurol 413:232-240.
41. Kawakami T, Kusakabe T, Takenaka T. 1995. Distribution of immunoreactive neuropeptides in the pancreas of the bullfrog, Rana catesbeiana, demonstrated by immunofluorescence. Cell Tissue Res 280:307-311.
42. Kawakami T, Kusakabe T, Matsuda H, Gono Y, Hiruma H, Kurihara K, Takenaka T. 1998. Distribution of neuropeptide-containing nerve fibers in the salamander taste organs. Histol Histopathol 13:115-119.
43. Kobayashi S. 1971a. Comparative cytological studies of the carotid body. 1. Demonstration of monoamine-storing cells by correlated chromaffin reaction and fluorescence histochemistry. Arch Histol Jpn 33:319-339.
44. Kobayashi S. 1971b. Comparative cytological studies of the carotid body. 2. Ultrastructure of the synapses on the chief cell. Arch Histol Jpn 33:387-420.
45. Kobayashi S, Murakami T. 1975. Scanning electron microscopic observation of the fine three-dimensional distribution of the blood vessels in the frog carotid labyrinth. In: Purxes MJ, editor, The Peripheral Chemoreceptors. Cambridge, UK: Cambridge University Press. p 301-313.
46. 8 in the carotid body chief cells of the dog. Arch Histol Jpn 46:716-722.
47. Kondo H. 1974. On the granule-containing cells in the aortic wall of the young chick. Anat Rec 178:253-266.
48. Kondo H, Kuramoto H, Fujita T. 1986. Neuropeptide tyrosine-like immunoreactive nerve fibers in the carotid body chemoreceptor of rats. Brain Res 372:353-356.
49. Kusakabe T. 1990a. Comparative studies of the vascular organization of carotid labyrinths of anurans and caudates. J Morphol 204:47-55.
50. Kusakabe T. 1990b. Ultrastructural studies of the carotid labyrinth in the newt Cynops pyrrhogaster. Zool Sci 7:201-208.
51. Kusakabe T. 1991a. The occurrence of melanosomes in the newt glomus cell. Arch Histol Cytol 54:81-87.
52. Kusakabe T. 1991b. Morphogenesis of the carotid labyrinth in the bullfrog, Rana catesbeiana, during larval development and metamorphosis. Anat Embryol 184:133-139.
53. Kusakabe T. 1992a. Intimate apposition of the glomus and smooth muscle cells (g-s connection) in the carotid labyrinth of juvenile bullfrogs. Anat Embryol 185:39-44.
54. Kusakabe T. 1992b. Ultrastructural characteristics of glomus cells in the external carotid artery during larval development and metamorphosis in the bullfrogs, Rana catesbeiana. Anat Rec 233:461-466.
55. Kusakabe T. 1992c. Ontogeny of substance P-, CGRP-, and VIP-containing nerve fibers in the amphibian carotid labyrinth of the bullfrog, Rana catesbeiana: An immunohistochemical study. Cell Tissue Res 269:79-85.
56. Kusakabe T, Ishii K, Ishii K. 1987. A possible role of the glomus cell in the controlling vascular tone of the carotid labyrinth of Xenopus laevis. Tohoku J Exp Med 151:395-408.
57. Kusakabe T, Anglade P, Tsuji S. 1991. Localization of substance P, CGRP, VIP, neuropeptide Y, and somatostatin immunoreactive nerve fibers in the carotid labyrinths of some amphibian species. Histochemistry 96:255-260.
58. Kusakabe T, Kawakami T, Takenaka T. 1993a. Distribution of FMRFamide-immunoreactive nerve fibers in the carotid labyrinth of the bullfrog, Rana catesbeiana in corresponding differential interference-contrast (Nomarski) images. Arch Histol Cytol 56:277-282.
59. Kusakabe T, Powell FL, Ellisman MH. 1993b. Ultrastructure of the glomus cells in the carotid body of chronically hypoxic rats: With a special reference of the similarity of the amphibian glomus cells. Anat Rec 237:220-227.
60. Kusakabe T, Kawakami T, Tanabe Y, Fujii S, Bandou Y, Takenaka T. 1993c. Coexistence of substance P and calcitonin gene-related peptide in the nerve fibers of the carotid labyrinth of the bullfrog, Rana catesbeiana. Brain Res 603:153-156.
61. Kusakabe T, Kawakami T, Takenaka T. 1994a. Coexistence of substance P, neuropeptide Y, VIP, and CGRP in the nerve fibers of the carotid labyrinth of the bullfrog, Rana catesbeiana: A double labelling immunofluorescence study in combination with alternate consecutive sections. Cell Tissue Res 276:91-97.
62. Kusakabe T, Kawakami T, Takenaka T. 1994b. Localization of immunoreactive neuropeptides in the kidney of the bullfrog, Rana catesbeiana, by immunofluorescence. Cell Tissue Res 278:41-44.
63. Kusakabe T, Kawakami T, Tanabe Y, Fujii S, Takenaka T. 1994c. Distribution of substance P-containing and catecholaminergic fibers in the rabbit carotid body: An immunohistochemical study in combination with catecholamine fluorescent histochemistry. Arch Histol Cytol 57:193-199.
64. Kusakabe T, Kawakami T, Takenaka T. 1995a. Calcitonin gene-related peptide and substance P in the pharynx and lung of the bullfrog, Rana catesbeiana. Cell Tissue Res 279:115-121.
65. Kusakabe T, Kawakami T, Takenaka T. 1995b. Peptidergic innervation in the amphibian carotid labyrinth. Histol Histopathol 10:185-202.
66. Kusakabe T, Kawakami T, Ono M, Hori H, Takenaka T. 1995c. Localization of galanin-immunoreactive nerve fibers in the carotid labyrinth of the bullfrog, Rana catesbeiana: Comparison with substance P-immunoreactive fibers. Cell Tissue Res 281:63-67.
67. Kusakabe T, Kawakami T, Ono M, Takenaka T. 1996a. Distribution of peptidergic nerve fibers in the bullfrog lingual papillae demonstrated by a combination of double immunofluorescence labelling and a multiple dye filter. Histochem J 28:289-297.
68. Kusakabe T, Matsuda H, Kawakami T, Syoui N, Kurihara K, Takenaka T. 1996b. Ontogeny of neuropeptide-containing fibers in the bullfrog taste organ. Dev Brain Res 96:285-289.
69. Kusakabe T, Kawakami T, Ono M, Syoui N, Kurihara K, Takenaka T. 1996c. Precise coexistence of regulatory peptides in the nerve fibers of the amphibian carotid labyrinth demonstrated by a combination of double immunofluorescence labelling and a multiple dye filter. Brain Res 735:307-310.
70. Kusakabe T, Kawakami T, Takenaka T. 1996d. Coexistence of neuropeptides in the amphibian carotid labyrinth: An application of double immunolabelling in combination with a multiple dye filter. Adv Exp Med Biol 410:325-328.
71. Kusakabe T, Hayashida Y, Matsuda H, Gono Y, Kawakami T, Powell FL, Ellisman MH, Takenaka T. 1998. Hypoxic adaptation of the peptidergic innervation in the rat carotid body. Brain Res 806:165-174.
72. Laidler P, Kay JM. 1975a. The effect of chronic hypoxia on the number and nuclear diameter of type I cells in the carotid bodies of the rats. J Pathol 79:311-320.
73. Laidler P, Kay JM. 1975b. A quantitative morphological study of the carotid bodies of the rats living at a simulated altitude of 4300 meters. J Pathol 117:183-191.
74. Laidler P, Kay JM. 1978. A quantitative study of some ultrastructural features of the type I cells in carotid bodies of rats living at a simulated altitude of 4300 meters. J Neurocytol 7:183-192.
75. Lundberg JM, Hökfelt T, Fahrenkrug J, Nilsson G, Terenius, L. 1979. Peptides in the carotid body (glomus caroticum): VIP-, enkephalin- and substance P-like immunoreactivity. Acta Physiol Scand 107:279-281.
76. Lundberg JM, Anggard A, Fahrenkrug J, Hökfelt T, Mutt V. 1980. Vasoactive intestinal polypeptide in cholinergic neurons of exocrine glands: Functional significance of coexisting transmitters for vasodilation and secretion. Proc Natl Acad Sci USA 77:1651-1655.
77. Lundberg JM, Terenis L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Blooms S, Goldstein M. 1982. Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand 116:477-480.
78. Malvin GM, Dail WG. 1986. Adrenergic innervation of the gills, pulmonary arterial plexus, and dorsal aorta in the neotenic salamander, Ambystoma tigrinum. J Morphol 189:67-70.
79. McGregor KH, Gil J, Lahiri S. 1984. A morphometric study of the carotid body in chronically hypoxic rats. J Appl Physiol 57:1430-1438.
80. Meyer F. 1927. Versuvhe über blutdruckzügler beim forsch. Pflüger Arch Ges Physiol 215:545-552.
81. Mishima D. 1944a. On the development of the carotid gland of anurans. I. In Rhacophprous arborea schlegelli. Kaibougaku Zasshi 22:399-408.
82. Mishima D. 1944b. On the development of the carotid gland of anurans. II. In Bufo formosus. Kaibougaku Zasshi 22:399-408.
83. Murakami T. 1971. Application of the scanning electron microscope to the study of the fine distribution of the blood vessels. Arch Histol Jpn 32:445-454.
84. Neil E, Ström L, Zotterman Y. 1950. Action potential studies of afferent fibres in the IXth and Xth cranial nerves of the frog. Acta Physiol Scand 20:338-350.
85. Nicander L. 1964. Fine structure and cytochemistry of nuclear inclusions in the dog epididymis. Exp Cell Res 35:533-541.
86. Noguchi R, Kobayashi S. 1977. On the vascular architecture of the carotid labyrinth in Cynops pyrrhogaster and Onychodactylus japonicus. Arch Histol Jpn 40:347-360.
87. Ookawara S, Suzuki K, Yoshida Y, Ooneda G. 1974. Monoaminestoring cells in the media of the thoracic aorta of Gullus domesticus. Cell Tissue Res 151:309-316.
88. Palade GE. 1953. Fine structure of blood capillaries. J Appl Physics 24:1424.
89. Palme F. 1934. Die paraganglein über dem herzen und im endingungsgebiet des nervus depressor. Z Mikrosk Anat Forsch 36:391-420.
90. Pequignot JM, Hellström S. 1983. Intact and sympathectomized study of the carotid bodies of long-term hypoxic rats: A morphometric light microscopical study. Virchows Arch Pathol Anat 400:235-243.
91. Pfeiffer CJ, Marry MJ, Legends L. 1987. The equine colonial mucosal granular cell: Identification and x-ray microanalysis of apical granules and nuclear bodies. Anat Rec 219:258-267.
92. Pischinger A. 1934. Uber die entwicklung und des wesen des carotislabyrinths bei anuren. Z Anat Entwicjlungsgesch 103:45-52.
93. Poullet-Krieger M. 1973. Innervation du labyrinthe carotidien du crapaud Bufo bufo: Etude ultrastructurale et histochimique. J Microsc (Paris) 18:55-64.
94. 2. Brain Res 481:205-214.
95. Rogers DC. 1963. Distinct cell types in the carotid labyrinth. Nature 200:492-493.
96. Rogers DC. 1966. A histological and histochemical study of the carotid labyrinth in the anuran amphibians, Bufo marinus, Hyla aurea and Neobatrachus pictus. Acta Anat 63:249-280.
97. Scheibner T, Read DJC, Sullivan CE. 1988. Distribution of substance P-immunoreactive structures in the developing cat carotid body. Brain Res 453:72-78.
98. Simionescu N, Simionescu M, Palade GE. 1975. Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J Cell Biol 64:586-607.
99. Smith P, Gosney J, Heath D, Burnett H. 1990. The occurrence and distribution of certain polypeptides within the human carotid body. Cell Tissue Res 261:565-571.
100. Taylor AC, Kollros JJ. 1946. Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7-23.
101. Toews D, Shelton G, Boutilier R. 1982. The amphibian carotid labyrinth: Some anatomical and physiological relationships. Can J Zool 60:1153-1160.
102. Verna A. 1979. Ultrastructure of the carotid body in the mammals. Int Rev Cytol 60:271-330.
103. Wang ZZ, Stensaas LJ, Dinger B, Fidone SJ. 1992. The co-existence of biogenic amines and neuropeptides in the type I cells of the cat carotid body. Neuroscience 47:473-480.
104. West NH, Topor ZL, Van Vliet BN. 1987. Hypoxemic threshold for lung ventilation in the toad. Respir Physiol 70:377-390.
105. Wharton J, Polak JM, Pearse AGE, McGregor GP, Bryant MG, Bloom SR, Emson PC, Bisgard GE, Will JA. 1980. Enkephalin-, VIP- and substance P-like immunoreactivity in the carotid body. Nature 284:269-271.
106. Wilson DA, O'Neill JT, Saido SI, Traystman RJ. 1981. Vasoactive intestinal polypeptide and canine cerebral circulation. Circ Res 48:138-148.
107. Yamauchi A. 1977. On the recepto-endocrine property of granulecontaining (GC) cells in the autonomic nervous system. Arch Histol Jpn 40(Suppl):147-161.
108. Yates RD, Chen I. 1987. Substance P in the carotid body. Exp Brain Res Ser 16:78-83.
109. Yates RD, Chen I, Duncan D. 1970. Effects of sinus nerve stimulation on the carotid body glomus cells. J Cell Biol 46:544-552.