Characterization of sheep (Ovis aries) palatine tonsil innervation

Neuroscience

Volumn 161, Issue 3, 2009, Pages 813-826

  Russo, D ^a   Fantaguzzi, C Mongardi ^a   Di Guardo, G ^b   Clavenzani, P ^a   Lalatta Costerbosa, G ^a   Ligios, C ^c   Chiocchetti, R ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF TERAMO   (Italy)

^c ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA SARDEGNA   (Italy)

Author keywords

fluorescent tracers; immunohistochemistry; prion diseases; sympathetic innervation

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; DOPAMINE BETA MONOOXYGENASE; NEURONAL NITRIC OXIDE SYNTHASE; PROTEIN S 100; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLOSSOPHARYNGEAL NERVE; NONHUMAN; PALATINE TONSIL; PRIORITY JOURNAL; SHEEP; SYMPATHETIC INNERVATION; TRIGEMINAL NERVE; VAGUS NERVE;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; CALCITONIN GENE-RELATED PEPTIDE; CELL SIZE; DOPAMINE BETA-HYDROXYLASE; FEMALE; GANGLIA, SENSORY; GANGLIA, SYMPATHETIC; LYMPH NODES; NEURAL PATHWAYS; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; PALATINE TONSIL; S100 PROTEINS; SHEEP; SPINAL CORD; SUBSTANCE P; TYROSINE 3-MONOOXYGENASE;

EID: 65749112210     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.04.015     Document Type: Article

References (58)

1. Aguzzi A., and Polymenidou M. Mammalian prion biology: one century of evolving concepts. Cell 116 (2004) 313-327
2. Aguzzi A., and Heikenwalder M. Pathogenesis of prion diseases: current status and future outlook. Nat Rev Microbiol 4 (2006) 765-775
3. Albanese V., Lawson V.A., Hill A., Cappai R., Di Guardo G., Staikopoulos V., Thacker M., Furness J.B., and Chiocchetti R. Evidence for prion protein expression in enteroglial cells of the myenteric plexus of mouse intestine. Auton Neurosci Basic Clin 140 (2008) 17-23
4. Andréoletti O., Berthon P., Marc D., Sarradin P., Grosclaude J., van Keulen L., Schelcher F., Elsen J.M., and Lantier F. Early accumulation of PrP(Sc) in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J Gen Virol 81 (2000) 3115-3126
5. Arey L.B. Developmental anatomy: a textbook and laboratory manual of embryology (1974), W. B. Saunders Company, Philadelphia
6. Barone R. Anatomia comparata dei mammiferi domestici. Volume 3: splancnologia: apparecchio digerente e respiratorio (1981), Edagricole, Bologna p 234
7. Beekes M., and McBride P.A. The spread of prions through the body in naturally acquired transmissible spongiform encephalopathies. FEBS J 274 (2007) 588-605
8. Bellinger D.L., Millar B.A., Perez S., Carter J., Wood C., Thyagarajan S., Molinaro C., Lubahn C., and Lorton D. Sympathetic modulation of immunity: relevance to disease. Cell Immunol 252 (2008) 27-56
9. Berg R. Anatomia topografica e applicata degli animali domestici veterinaria (1982), UTET, Torino
10. Besedovsky H.O., del Rey A., Sorkin E., Da Prada M., and Keller H.H. Immunoregulation mediated by the sympathetic nervous system. Cell Immunol 48 (1979) 346-355
11. Brandner S. CNS pathogenesis of prion diseases. Br Med Bull 66 (2003) 131-139
12. Brodal. Neurological anatomy (1981), Oxford University Press, New York
13. Cesta M.F. Normal structure, function, and histology of mucosa-associated lymphoid tissue. Toxicol Pathol 34 (2006) 599-608
14. Chiocchetti R., Grandis A., Bombardi C., Lucchi M.L., Tadini Dal Lago D., Bortolami R., and Furness J.B. Extrinsic and intrinsic sources of calcitonin gene-related peptide immunoreactivity in the lamb ileum. A morphometric and neurochemical investigation. Cell Tissue Res 323 (2006) 183-196
15. Chiocchetti R., Mazzuoli G., Albanese V., Mazzoni M., Clavenzani P., Lalatta-Costerbosa G., Lucchi M.L., Di Guardo G., Marruchella G., and Furness J.B. Anatomical evidence for ileal Peyer's patches innervation by enteric nervous system: a potential route for prion neuroinvasion?. Cell Tissue Res 332 (2008) 185-194
16. Defaweux V., Dorban G., Antoine N., Piret J., Gabriel A., Jacqmot O., Falisse-Poirier N., Flandroy S., Zorzi D., and Heinen E. Neuroimmune connections in jejunal and ileal Peyer's patches at various bovine ages: potential sites for prion neuroinvasion. Cell Tissue Res 329 (2007) 35-44
17. DeVane C.L. Substance P: a new era, a new role. Pharmacotherapy 21 (2001) 1061-1069
18. Diedrich J.F., Bendheim P.E., Kim Y.S., Carp R.I., and Haase A.T. Scrapie-associated prion protein accumulates in astrocytes during scrapie infection. Proc Natl Acad Sci U S A 88 (1991) 375-379
19. Ducsay C.A., Hyatt K., Mlynarczyk M., Root B.K., Kaushal K.M., and Myers D.A. Long-term hypoxia modulates expression of key genes regulating adrenomedullary function in the late gestation ovine fetus. Am J Physiol Regul Integr Comp Physiol 293 (2007) R1997-R2005
20. Effat K.G., and Milad M. Comparative study of palatine tonsil histology in mammals, with special reference to tonsillar salivary glands. J Laryngol Otol 121 (2007) 468-471
21. Felten D.L., Livnat S., Felten S.Y., Carlson S.L., Bellinger D.L., and Yeh P. Sympathetic innervation of lymph nodes in mice. Brain Res Bull 13 (1984) 693-699
22. Felten D.L., Felten S.Y., Carlson S.L., Olschowaka J.A., and Livnat S. Noradrenergic and peptidergic innervation of lymphoid tissue. J Immunol 135 (1985) 755S-765S
23. Felten D.L., Felten S.Y., Bellinger D.L., Carlson S.L., Ackerman K.D., Madden K.S., Olschowki J.A., and Livnat S. Noradrenergic sympathetic neural interactions with the immune system. Structure and function. Immunol Rev 100 (1987) 225-260
24. Felten S.Y., Felten D.L., Bellinger D.L., Carlson S.L., Ackerman K.D., Madden K.S., Olschowka J.A., and Livnat S. Noradrenergic sympathetic innervation of lymphoid organs. Prog Allerg 43 (1988) 14-36
25. Follet J., Lemaire-Vieille C., Blanquet-Grossard F., Podevin-Dimster V., Lehmann S., Chauvin J.P., Decavel J.P., Varea R., Grassi J., Fontès M., and Cesbron J.Y. PrP expression and replication by Schwann cells: implications in prion spreading. J Virol 76 (2002) 2434-2439
26. Fraeyman N.H., Van de Velde E.J., and De Smet F.H. Molecular forms of dopamine beta-hydroxylase in rat superior cervical ganglion and adrenal gland. Experientia 44 (1988) 746-749
27. Gibbins I.L. Target-related patterns of co-existence of neuropeptide Y, vasoactive intestinal peptide, enkephalin and substance P in cranial parasympathetic neurons innervating the facial skin and exocrine glands of guinea-pigs. Neuroscience 38 (1990) 541-560
28. Glatzel M., Heppner F.L., Albers K.M., and Aguzzi A. Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 31 (2001) 25-34
29. Goetzl E.J. Neuropetide mediators of neuro-immune communications. In: Aminoff M.J., and Daroff R.B. (Eds). Encyclopedia of the neurological sciences (2003), Elsevier Science Ltd, San Diego, CA
30. Habel R.E. Ruminant digestive system: pharynx. In: Getty R. (Ed). Sisson and Grossman's the anatomy of the domestic animals. 5th ed (1975), W. B. Saunders, Philadelphia 874
31. Hatanaka Y., Hobara N., Honghua J., Akiyama S., Nawa H., Kobayashi Y., Takayama F., Gomita Y., and Kawasaki H. Neuronal nitric-oxide synthase inhibition facilitates adrenergic neurotransmission in rat mesenteric resistance arteries. J Pharmacol Exp Ther 316 (2006) 490-497
32. Jeffrey M., Ryder S., Martin S., Hawkins S.A., Terry L., Berthelin-Baker C., and Bellworthy S.J. Oral inoculation of sheep with the agent of bovine spongiform encephalopathy (BSE). 1. Onset and distribution of disease-specific PrP accumulation in brain and viscera. J Comp Pathol 124 (2001) 280-289
33. Jenkins T.W. Functional mammalian neuroanatomy (1983), Lea & Febiger, Philadelphia
34. Mabbott N.A., and MacPherson G.G. Prions and their lethal journey to the brain. Nat Rev Microbiol 4 (2006) 201-211
35. Marruchella G., Ligios C., Albanese V., Cancedda M.G., Madau L., Lalatta-Costerbosa G., Mazzoni M., Clavenzani P., Chiocchetti R., Sarli G., De Grossi L., Agrimi U., Aguzzi A., and Di Guardo G. Enteroglia and neuron involvement without apparent neuronal loss in ileal enteric nervous system plexi from scrapie-affected sheep. J Gen Virol 88 (2007) 2899-2904
36. Massmann G.A., Zhang J., Sallah J., and Figuero J.P. Developmental and regional expression patterns of type I nitric oxide synthase mRNA and protein in fetal sheep brain during the last 1 third of gestation. Dev Brain Res 124 (2000) 141-152
37. McCorry L.K. Physiology of the autonomic nervous system. Am J Pharm Educ 71 (2007) 1-11
38. Nagahama M., Kairada K., and Ohno S. Distribution of preganglionic cells of superior cervical ganglion in the spinal cord in the cat. Nippon Ganka Gakkai Zasshi 94 (1990) 359-366
39. Nickel R., Schummer A., and Seiferle E. Lehrbuch der anatomize der Haustiere, Band IV (1975), Parey, Berlin 278
40. Oku R., Satoh M., Fujii N., Otaka A., Yajima H., and Takagi H. Calcitonin gene-related peptide promotes mechanical nociception by potentiating release of substance P from the spinal dorsal horn in rats. Brain Res 403 (1987) 350-354
41. Palmer M.V., Thacker T.C., and Waters W.R. Histology, immunohistochemistry and ultrastructure of the bovine palatine tonsil with special emphasis on reticular epithelium. Vet Immunol Immunopathol 127 (2009) 277-285
42. Payan D.G., McGillis J.P., Renold F.K., Mitsuhashi M., and Goetzl E.J. Neuropeptide modulation of leukocyte function. Ann N Y Acad Sci 496 (1987) 182-191
43. Pfannkuche H., Schemann M., and Gäbel G. Ruminal muscle of sheep is innervated by non-polarized pathways of cholinergic and nitrergic myenteric neurones. Cell Tissue Res 309 (2002) 347-354
44. Pilowsky P., Llewellyn-Smith I.J., Minson J., and Chalmers J. Sympathetic preganglionic neurons in rabbit spinal cord that project to the stellate or the superior cervical ganglion. Brain Res 577 (1992) 181-188
45. Press C.M.L., Heggeb R., and Espenes A. Involvement of gut-associated lymphoid tissue of ruminants in the spread of transmissible spongiform encephalopathies. Adv Drug Deliv Rev 56 (2004) 885-899
46. Rando T.A., Bowers C.W., and Zigmond R.E. Localization of neurons in the rat spinal cord which project to the superior cervical ganglion. J Comp Neurol 196 (1981) 73-83
47. Sadler T.W. Langman's medical embryology. 7th ed. (1995), Williams & Wilkins, Baltimore
48. Shankland II W.E. The trigeminal nerve. Part III: the maxillary division. Cranio 19 (2001) 78-83
49. Testut, and Latarjet. Trattato di anatomia umana Vol. 3 (1971), UTET, Torino
50. Thornbury K.D., McHale N.G., Allen J.M., and Huges G. Nerve-mediated contractions of sheep mesenteric lymph node capsules. J Physiol 422 (1990) 513-522
51. Ueyama T., Kozuki K., Houtani T., Ikeda M., Kitajiri M., Yamashita T., Kumazawa T., Nagatsu I., and Sugimoto T. Immunolocalization of tyrosine hydroxylase and vasoactive intestinal polypeptide in nerve fibers innervating human palatine tonsil and paratonsillar glands. Neurosci Lett 116 (1990) 70-74
52. van Keulen L.J., Schreuder B.E., Vromans M.E., Langeveld J.P., and Smits M.A. Pathogenesis of natural scrapie in sheep. Arch Virol Suppl 16 (2000) 57-71
53. van Keulen L.J.M., Vromans M.E.W., and Van Zijderveld F.G. Early and late pathogenesis of natural scrapie infection in sheep. APMIS 110 (2002) 23-32
54. vonWaldeyer-Hartz W. Ueber den lymphatischen Apparat des Pharynx. Dtsch Med Wochenschr 10 (1884) 313
55. Wang H.W., Chen H.L., and Wang J.Y. A histofluorescent study of sympathetic innervation of human palatine tonsils. Eur Arch Otorhinolaryngol 249 (1992) 340-343
56. Williams P.L., Bannister L., Berry M.M., Collins P., Dyson M., Dussek J.E., Ferguson M.W.J., Amprino R., and Marotti G. ANATOMIA DEL GRAY. fourth edition Vol. 2 (2001), Zanichelli, Bologna
57. Wood C.E., Chen G.F., and Keller-Wood M. Expression of nitric oxide synthase isoforms is reduced in late-gestation ovine fetal brainstem. Am J Physiol Regul Integr Comp Physiol 289 (2005) R613-R619
58. Zubrzycka M., and Janecka A. Substance P: transmitter of nociception (Minireview). Endocr Regul 34 (2000) 195-201