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Hints of a functional connection between the neuropeptidergic innervation of arteriovenous anastomoses and the appearance of epithelioid cells in the rabbit ear

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Abstract

Peripheral blood flow can be regulated by specialized vessel segments, the arteriovenous anastomoses. Their wall consists of a relatively thick layer of smooth muscle cells and so-called epithelioid cells. The epithelioid cell is a specialized myogenic cell phenotype expressing nitric oxide synthase. We studied the innervation of the different segments of arteriovenous anastomoses in the rabbit ear using antisera against neuropeptide Y, tyrosine hydroxylase, calcitonin gene-related peptide and substance P, as well as neuron-specific enolase, calbindin D and neurotubulin. The participation was especially examined of neuropeptidergic innervation and a possible morphological connection to the occurrence of epithelioid cells and a paracrine function. The NADPH diaphorase reaction and α-smooth muscle actin immunoelectron microscopy served to distinguish epithelioid cells from smooth muscle cells. Using conventional fluorescence microscopy and confocal laser scanning microscopy, we found the most dense innervation pattern of pan-neuronal markers (neurotubulin, neuron-specific enolase), tyrosine hydroxylase-immunor eactive nerve fibres and neuro-peptidergic nerve fibres (neuropeptide Y, calcitonin gene-related peptide, substance P) around the intermediate segment in arteriovenous anastomoses, whereas the venous segment was barely marked. Single nerve fibres penetrated into the medial layer and reached the epithelioid cells. Using immunoelectron microscopy, we found intercellular contacts between epithelioid cells, but not the gap junction protein connexin 43. Here, we report for the first time a correlation of the innervation pattern with epithelioid cell type in arteriovenous anastomoses. Our findings suggest that epithelioid cells of the arteriovenous anastomoses are controlled by a dense network of neuropeptidergic nerve fibres in functional connection to their paracrine role as a nitric oxide producer. © 1998 Chapman & Hall

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References

  • Akester, A. R. (1971) Nervous control of blood flow patterns in the avian kidney. J. Anat. 108, 606-7.

    Google Scholar 

  • Anderson, C. R. & Mclachlan, E. M. (1991) The time course of the development of the sympathetic innervation of the vasculature of the rat tail. J. Auton. Nerv Syst. 35, 117-32.

    Google Scholar 

  • Beny, J. L. & Connat, J. L. (1991) An electron-microscopic study of smooth muscle cell dye coupling in the pig coronary arteries. Circulation Res. 70, 49-55

    Google Scholar 

  • Brain, S. D. & Williams, T. J. (1985) Inflammatory edema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability. Br. J. Pharmacol. 86, 855-60.

    Google Scholar 

  • Brain, S. D., Cambridge, H., Hughes S. R. & Wilson-croft, P. (1992) Evidence that calcitonin gene-related peptide contributes to inflammation in the skin and joint. Ann. NY Acad. Sci. 657, 412-19.

    Google Scholar 

  • Cambridge, H. & Brain, S. D. (1992) Calcitonin gene-related peptide increases blood flow and potentiates plasma protein extravasation in the rat knee joint. Br. J. Pharmacol. 106, 746-50.

    Google Scholar 

  • Clara, M. (1956) Die arterio-venösen Anastomosen. Anato-mie. Biologie. Pathologie. Vienna: Springer.

    Google Scholar 

  • Clark, E. R. (1934) Observation on living performed blood vessels as seen in a transparent chamber insert in the rabbits ear. Am. J. Anat. 54, 229-86.

    Google Scholar 

  • Dixon, J. S. & Gosling, J. A. (1973) The fine structure of pacemaker cells in the pig renal calices. Anat Rec. 175, 139-54.

    Google Scholar 

  • Dun, N. J. & Jiang, Z. (1982) Non-cholinergic excitatory transmission in inferior mesenteric ganglia of the guinea-pig: possible mediation by substance P. J. Physiol. 325, 145-59.

    Google Scholar 

  • Funk, R. H. W., MAYER, B. & WÖRL, J. (1994) Nitrergic innervation and nitrergic cells in arteriovenous anastomoses. Cell Tissue Res. 277, 477-84.

    Google Scholar 

  • Haegerstrand, A., Dalsgaard, C. J., Jonzon, B., Larsson, O. & Nilsson, J. (1990) Calcitonin gene-related peptide stimulates proliferation of human endothelial cells. Proc. Natl. Acad. Sci. USA 87, 3299-303.

    Google Scholar 

  • Hale, A. R. & Burch, G. E. (1960) The arteriovenous anastomoses and blood vessels of the human finger. Medicine 39, 191-240.

    Google Scholar 

  • Hammersen, F. (1971) The fine structure of epitheloid vascular cells. A comparative electron microscopic study. In Sixth European Conference on the Microcirculation (edited by Ditzel, J. & Lewis, D. H.), pp. 45-56, Basle: Karger.

    Google Scholar 

  • Hammersen, F. (1976) On the fine structure of the arteriovenous anastomoses of the rabbit ear. In Microcirculation (edited by Grayson, Z. & Zingg, W.), pp. 155-57, New York: Plenum Press.

    Google Scholar 

  • Hofer, A., Saez, J. C., Chang, C. C. Trosko, J. E. Spray, D. C. & Dermietzel, R. (1996) C-erbB2/neu transfection induces gap junctional communication incompetence in glial cells. J. Neurosci. 16, 4311-21.

    Google Scholar 

  • Iij ima, T., Kondo, T. & Hasegawa, K. (1987) Autonomic innervation of the arteriovenous anastomoses in the dog tongue. A histochemical and ultrastructural study. Cell Tissue Res. 247, 167-77.

    Google Scholar 

  • Iij ima, T., Hasegawa, T. & Hirose, H. (1988) Wall structure of arteriovenous anastomoses in the rabbit ear. Combined light-, scanning-and transmission electron-microscopic studies. Cell Tissue Res. 252, 1-8.

    Google Scholar 

  • Iijima, T. Kondo, T., Nishijima, K. & Tanaka, T. (1989) Innervation of the arteriovenous anastomoses in the dog tongue. Cell Tissue Res. 258, 425-28.

    Google Scholar 

  • Jiang, Z., Dun, N. J. & Karczmar, A. G. (1982) Substance P: a putative sensory transmitter in mammalian autonomic ganglia. Science 217, 739-41.

    Google Scholar 

  • Kameda, Y. (1996) Immunoelectron microscopic localization of vimentin in sustentacular cells of the carotid body and the adrenal medulla of guinea pigs. J. Histochem. Cytochem. 44, 1439-49.

    Google Scholar 

  • Kasper, M., GÖlfert, F. & Funk, R. H. W. (1997) Immunoelectron microscopical characterization of the epithelioid type of smooth muscle cells in human glomus organs. Ultrastruct. Pathol. 21, 425-30.

    Google Scholar 

  • Komuro, T. & Seki, K. (1995) Fine structural study of interstitial cells associated with the deep muscular plexus of the rat small intestine, with special reference to the intestinal pacemaker cells. Cell Tissue Res 282, 129-34.

    Google Scholar 

  • Kresse, A., Jacobowitz, D. M. & SKOFITSCH, G. (1995) Detailed mapping of CGRP mRNA expression in the rat central nervous system: comparison with previous immunocytochemical findings. Brain Res. Bull. 36, 261-74.

    Google Scholar 

  • KrÖnert, H., Wurster, R. D., Pierau, F. & Pleschka, K. (1980) Vasodilatory response of arteriovenous anasto-moses to local cold stimuli in the dog's tongue. Pflügers Arch. 388, 17-19.

    Google Scholar 

  • Lam, F. Y. & Ferrell, W. R. (1990) Mediators of substance P-induced inflammation in the rat knee joint. Agents Actions 31, 298-307.

    Google Scholar 

  • Lam, F. Y. & Ferrell, W. R. (1991) Specific neurokinin receptors mediate plasma extravasation in the rat knee joint. Br. J. Pharmacol. 103, 1263-7.

    Google Scholar 

  • Luckner, H. & Staubesand, J. (1951) Die inkretorische Funktion des Glomus coccygeum. Z. Ges. Exp. Med. 117, 96-102.

    Google Scholar 

  • Messenger, J. P. (1993) Immunohistochemical analysis of neurons and their projections in the proximal colon of the guinea-pig. Arch. Histol. Cytol. 56, 459-74.

    Google Scholar 

  • Midtgard, U. (1988) Innervation of arteriovenous anasto-moses in the brood patch of the domestic fowl. Cell Tissue Res. 252, 207-10.

    Google Scholar 

  • Molyneux, G. S. (1977) The role of arteriovenous anasto-moses in the peripheral circulation. Proc. R. Soc. Lond. [Biol] 88, 1-9.

    Google Scholar 

  • Molyneux, G. S. (1981) Neural control of cutaneous arteriovenous anastomoses. In Progress in Microcirculation Research (edited by GARLICK, D. ), pp. 296-315, Sydney: University Press.

    Google Scholar 

  • Morris, J. L. & Bevan, R. D. (1986) Proliferation of arteriovenous anastomoses in the developing rabbit ear is enhanced after denervation. Am. J. Anat. 176, 497-509.

    Google Scholar 

  • Nebert, H. (1964) Histochemische Untersuchungen an den epitheloidzelligen Gefäß strecken der Glomerula caudalia. I. Mitt. Cholinesterasen. Z. Zellforschung 62, 363-70.

    Google Scholar 

  • Ozaka, T., Doi, Y., Kayashima, K. & Fujimoto, S. (1997) Weibel-Palade bodies as a storage site of calcitonin gene related peptide and endothelin-1 in blood vessels of the rat carotid body. Anat. Rec. 388-94.

  • Palestini, M., Guegan, M., Saavedra, H., Thomasset, M. & Batini, C. (1993) Glutamate, GABA, calbindin-D28k and parvalbumin immunoreactivity in the pulvinar-lateralis posterior complex of the cat: rela-tion to the projection to the Clare-Bishop area. Neurosci. Lett. 160, 89-92.

    Google Scholar 

  • Parton, R. G. (1996) Caveolae and caveolins. Curr. Opin. Cell Biol. 8, 542-8.

    Google Scholar 

  • Scherer-Singler, U., Vincent, S. R., Kimura, H. & Mcgeer, E. G. (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Methods 9, 229-34.

    Google Scholar 

  • Stelzner, F., Staubesand, J & Machleidt, H. (1962) Das Corpus cavernosum rectidie Grundlage der inneren Hämorrhoiden. Langenbecks Arch. Klin. 299, 302-12.

    Google Scholar 

  • Suzuki, N., Hardebo, J. E. & Owman, C. (1989) Origins and pathways of cerebrovascular nerves storing substance P and calcitonin gene-related peptide in rat. Neuroscience 31, 427-38.

    Google Scholar 

  • Thomson, E. M. & Pleschka, K. (1980) Vasodilatory mechanisms in the tongue and nose of the dog under heat load. Pflügers Arch. 387, 161-6.

    Google Scholar 

  • Villablanca, A. C., Murphy, C. J. & Reid, T. W. (1994) Growth-promoting effects of substance P on endothe-lial cells in vitro. Synergism with calcitonin gene-related peptide, insulin, and plasma factors. Circ. Res. 75, 1113-20.

    Google Scholar 

  • Weintraub, A. S., Giachelli, C. M., Krauss, R. S., Almei-da, M. & Taubman, M. B. (1996) Autocrine secretion of osteopontin by vascular smooth muscle cells regulates their adhesion to collagen gels. Am. J. Pathol. 149, 259-72.

    Google Scholar 

  • White, S. R., Garland, A., Gitter, B., Rodger, I., Al-ger, L. E., Necheles, J., Nawrocki, A. R. & Solway, J. (1995) Proliferation of guinea pig tracheal epithelial cells in coculture with rat dorsal root ganglion neural cells. Am. J. Physiol. 268, 957-65.

    Google Scholar 

  • Ziche, M. L., Morbidelli, L., Masini, E., Amerini, S., Granger, H. J., Maggi, C. A., Geppetti, P. & Ledda, F. (1994) Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest. 94, 2036-44.

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Technical University Dresden, Fetscherstrasse 74, D-01307, Dresden, Germany

    F GÖLFERT, M Witt, K Scheele, A Hofer, M Kasper & R H W Funk

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  1. F GÖLFERT
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  2. M Witt
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  3. K Scheele
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  4. A Hofer
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  5. M Kasper
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  6. R H W Funk
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GÖLFERT, F., Witt, M., Scheele, K. et al. Hints of a functional connection between the neuropeptidergic innervation of arteriovenous anastomoses and the appearance of epithelioid cells in the rabbit ear. Histochem J 30, 435–445 (1998). https://doi.org/10.1023/A:1003276310649

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