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. 1995 Sep 15;487(Pt 3):773–786. doi: 10.1113/jphysiol.1995.sp020917

Effects of vitamin E deficiency on autonomic neuroeffector mechanisms in the rat caecum, vas deferens and urinary bladder.

C H Hoyle 1, V Ralevic 1, J Lincoln 1, G E Knight 1, M A Goss-Sampson 1, P J Milla 1, G Burnstock 1
PMCID: PMC1156662  PMID: 8544138

Abstract

1. Modified sucrose-gap, standard organ-bath techniques and transmitter release studies were used to examine neuromuscular transmission in the caecum, vas deferens and urinary bladder in normal rats and in rats maintained for 12 months on a diet free of vitamin E. 2. In the caecum circular muscle, non-adrenergic, non-cholinergic inhibitory junction potentials were absent from 48 and 15% of preparations from vitamin E-deficient and control animals, respectively. Cholinergic excitatory junction potentials were absent from 83 and 8% of vitamin E-deficient and control preparations, respectively. Responses to applied noradrenaline (0.1-30 microM), alpha,beta-methylene ATP (3-100 microM) and acetylcholine (0.1-30 microM) were attenuated or absent in vitamin E-deficient tissues. Responses to applied KCl were similar in both groups. Release of [3H]noradrenaline or endogenous acetylcholine could not be evoked from vitamin E-deficient tissues. 3. In contrast, in isolated preparations of the vas deferens and urinary bladder, neuromuscular transmission by adrenergic, cholinergic and purinergic components were unaffected by long-term vitamin E deficiency. 4. In conclusion, vitamin E deficiency causes dysfunction of autonomic neuroeffector mechanisms in the smooth muscle of the rat caecum, at both a pre- and postjunctional level. The lesions in autonomic transmission mechanisms brought about by long-term vitamin E deficiency were found only in the caecum; no changes in sympathetic neuromuscular transmission were observed in the vas deferens, or in parasympathetic neuromuscular transmission in the urinary bladder.

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Selected References

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  1. Balasubramanian K. A., Nalini S., Cheeseman K. H., Slater T. F. Nonesterified fatty acids inhibit iron-dependent lipid peroxidation. Biochim Biophys Acta. 1989 Jun 28;1003(3):232–237. doi: 10.1016/0005-2760(89)90227-0. [DOI] [PubMed] [Google Scholar]
  2. Banks B. E., Brown C., Burgess G. M., Burnstock G., Claret M., Cocks T. M., Jenkinson D. H. Apamin blocks certain neurotransmitter-induced increases in potassium permeability. Nature. 1979 Nov 22;282(5737):415–417. doi: 10.1038/282415a0. [DOI] [PubMed] [Google Scholar]
  3. Belai A., Lincoln J., Burnstock G. Lack of release of vasoactive intestinal polypeptide and calcitonin gene-related peptide during electrical stimulation of enteric nerves in streptozotocin-diabetic rats. Gastroenterology. 1987 Nov;93(5):1034–1040. doi: 10.1016/0016-5085(87)90567-1. [DOI] [PubMed] [Google Scholar]
  4. Belai A., Lincoln J., Milner P., Crowe R., Loesch A., Burnstock G. Enteric nerves in diabetic rats: increase in vasoactive intestinal polypeptide but not substance P. Gastroenterology. 1985 Nov;89(5):967–976. doi: 10.1016/0016-5085(85)90195-7. [DOI] [PubMed] [Google Scholar]
  5. Doelman C. J., Kramer K., Timmerman H., Bast A. Vitamin E and selenium regulate balance between beta-adrenergic and muscarinic responses in rat lungs. FEBS Lett. 1988 Jun 20;233(2):427–431. doi: 10.1016/0014-5793(88)80476-9. [DOI] [PubMed] [Google Scholar]
  6. Goss-Sampson M. A., Kriss A., Muller D. P. A longitudinal study of somatosensory, brainstem auditory and peripheral sensory-motor conduction during vitamin E deficiency in the rat. J Neurol Sci. 1990 Dec;100(1-2):79–84. doi: 10.1016/0022-510x(90)90016-g. [DOI] [PubMed] [Google Scholar]
  7. Harding A. E. Vitamin E and the nervous system. Crit Rev Neurobiol. 1987;3(1):89–103. [PubMed] [Google Scholar]
  8. Hassall C. J., Burnstock G. Intrinsic neurones and associated cells of the guinea-pig heart in culture. Brain Res. 1986 Jan 29;364(1):102–113. doi: 10.1016/0006-8993(86)90991-1. [DOI] [PubMed] [Google Scholar]
  9. Hoyle C. H. A modified single sucrose gap. Junction potentials and electrotonic potentials in gastrointestinal smooth muscles. J Pharmacol Methods. 1987 Nov;18(3):219–226. doi: 10.1016/0160-5402(87)90072-6. [DOI] [PubMed] [Google Scholar]
  10. Hoyle C. H., Reilly W. M., Lincoln J., Burnstock G. Adrenergic, but not cholinergic or purinergic, responses are potentiated in the cecum of diabetic rats. Gastroenterology. 1988 Jun;94(6):1357–1367. doi: 10.1016/0016-5085(88)90674-9. [DOI] [PubMed] [Google Scholar]
  11. Hubel C. A., Griggs K. C., McLaughlin M. K. Lipid peroxidation and altered vascular function in vitamin E-deficient rats. Am J Physiol. 1989 Jun;256(6 Pt 2):H1539–H1545. doi: 10.1152/ajpheart.1989.256.6.H1539. [DOI] [PubMed] [Google Scholar]
  12. Israël M., Lesbats B. Application to mammalian tissues of the chemiluminescent method for detecting acetylcholine. J Neurochem. 1982 Jul;39(1):248–250. doi: 10.1111/j.1471-4159.1982.tb04727.x. [DOI] [PubMed] [Google Scholar]
  13. Keller R., Oke A., Mefford I., Adams R. N. Liquid chromatographic analysis of catecholamines routine assay for regional brain mapping. Life Sci. 1976 Oct 1;19(7):995–1003. doi: 10.1016/0024-3205(76)90290-3. [DOI] [PubMed] [Google Scholar]
  14. Kirkpatrick K., Burnstock G. Sympathetic nerve-mediated release of ATP from the guinea-pig vas deferens is unaffected by reserpine. Eur J Pharmacol. 1987 Jun 19;138(2):207–214. doi: 10.1016/0014-2999(87)90434-1. [DOI] [PubMed] [Google Scholar]
  15. Landrieu P., Selva J., Alvarez F., Ropert A., Métral S. Peripheral nerve involvement in children with chronic cholestasis and vitamin E deficiency. A clinical, electrophysiological and morphological study. Neuropediatrics. 1985 Nov;16(4):194–201. doi: 10.1055/s-2008-1059536. [DOI] [PubMed] [Google Scholar]
  16. Loesch A., Belai A., Lincoln J., Burnstock G. Enteric nerves in diabetic rats: electron microscopic evidence for neuropathy of vasoactive intestinal polypeptide-containing fibres. Acta Neuropathol. 1986;70(2):161–168. doi: 10.1007/BF00691434. [DOI] [PubMed] [Google Scholar]
  17. Machlin L. J., Filipski R., Nelson J., Horn L. R., Brin M. Effects of a prolonged vitamin E deficiency in the rat. J Nutr. 1977 Jul;107(7):1200–1208. doi: 10.1093/jn/107.7.1200. [DOI] [PubMed] [Google Scholar]
  18. Manzini S., Hoyle C. H., Burnstock G. An electrophysiological analysis of the effect of reactive blue 2, a putative P2-purinoceptor antagonist, on inhibitory junction potentials of rat caecum. Eur J Pharmacol. 1986 Aug 15;127(3):197–204. doi: 10.1016/0014-2999(86)90364-x. [DOI] [PubMed] [Google Scholar]
  19. McCay P. B. Vitamin E: interactions with free radicals and ascorbate. Annu Rev Nutr. 1985;5:323–340. doi: 10.1146/annurev.nu.05.070185.001543. [DOI] [PubMed] [Google Scholar]
  20. Milner P., Ralevic V., Hopwood A. M., Fehér E., Lincoln J., Kirkpatrick K. A., Burnstock G. Ultrastructural localisation of substance P and choline acetyltransferase in endothelial cells of rat coronary artery and release of substance P and acetylcholine during hypoxia. Experientia. 1989 Feb 15;45(2):121–125. doi: 10.1007/BF01954843. [DOI] [PubMed] [Google Scholar]
  21. Muakkassah-Kelly S. F., Andresen J. W., Shih J. C., Hochstein P. Dual effects of ascorbate on serotonin and spiperone binding in rat cortical membranes. J Neurochem. 1983 Nov;41(5):1429–1439. doi: 10.1111/j.1471-4159.1983.tb00842.x. [DOI] [PubMed] [Google Scholar]
  22. Muller D. P., Goss-Sampson M. A. Neurochemical, neurophysiological, and neuropathological studies in vitamin E deficiency. Crit Rev Neurobiol. 1990;5(3):239–263. [PubMed] [Google Scholar]
  23. Nakashima Y., Esashi T. Age-related changes in sympathetic nervous activity of rats receiving vitamin E-deficient diet. J Nutr Sci Vitaminol (Tokyo) 1986 Dec;32(6):569–579. doi: 10.3177/jnsv.32.569. [DOI] [PubMed] [Google Scholar]
  24. Nelson J. S., Fitch C. D., Fischer V. W., Broun G. O., Jr, Chou A. C. Progressive neuropathologic lesions in vitamin E-deficient rhesus monkeys. J Neuropathol Exp Neurol. 1981 Mar;40(2):166–186. doi: 10.1097/00005072-198103000-00008. [DOI] [PubMed] [Google Scholar]
  25. Nielsen K. C., Owman C. Difference in cardiac adrenergic innervation between hibernators and non-hibernating mammals. Acta Physiol Scand Suppl. 1968;316:1–30. doi: 10.1111/j.1748-1716.1968.tb04316.x. [DOI] [PubMed] [Google Scholar]
  26. Ralevic V., Burnstock G. Actions mediated by P2-purinoceptor subtypes in the isolated perfused mesenteric bed of the rat. Br J Pharmacol. 1988 Oct;95(2):637–645. doi: 10.1111/j.1476-5381.1988.tb11686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ringsted A. A preliminary note on the appearance of paresis in adult rats suffering from chronic avitaminosis E. Biochem J. 1935 Mar;29(3):788–795. doi: 10.1042/bj0290788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schmidt R. E., Coleman B. D., Nelson J. S. Differential effect of chronic vitamin E deficiency on the development of neuroaxonal dystrophy in rat gracile/cuneate nuclei and prevertebral sympathetic ganglia. Neurosci Lett. 1991 Feb 11;123(1):102–106. doi: 10.1016/0304-3940(91)90168-s. [DOI] [PubMed] [Google Scholar]
  29. Shuba M. F., Vladimirova I. A. Effect of apamin on the electrical responses of smooth muscle to adenosine 5'-triphosphate and to non-adrenergic, non-cholinergic nerve stimulation. Neuroscience. 1980;5(5):853–859. doi: 10.1016/0306-4522(80)90154-2. [DOI] [PubMed] [Google Scholar]
  30. Slater T. F. Free-radical mechanisms in tissue injury. Biochem J. 1984 Aug 15;222(1):1–15. doi: 10.1042/bj2220001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sokol R. J., Guggenheim M. A., Iannaccone S. T., Barkhaus P. E., Miller C., Silverman A., Balistreri W. F., Heubi J. E. Improved neurologic function after long-term correction of vitamin E deficiency in children with chronic cholestasis. N Engl J Med. 1985 Dec 19;313(25):1580–1586. doi: 10.1056/NEJM198512193132505. [DOI] [PubMed] [Google Scholar]
  32. Sokol R. J. Vitamin E and neurologic deficits. Adv Pediatr. 1990;37:119–148. [PubMed] [Google Scholar]
  33. Towfighi J. Effects of chronic vitamin E deficiency on the nervous system of the rat. Acta Neuropathol. 1981;54(4):261–267. doi: 10.1007/BF00696998. [DOI] [PubMed] [Google Scholar]
  34. Welford L. A., Cusack N. J., Hourani S. M. The structure-activity relationships of ectonucleotidases and of excitatory P2-purinoceptors: evidence that dephosphorylation of ATP analogues reduces pharmacological potency. Eur J Pharmacol. 1987 Sep 2;141(1):123–130. doi: 10.1016/0014-2999(87)90418-3. [DOI] [PubMed] [Google Scholar]

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