Neurotrophins and neurotransmitters in human palatine tonsils: An immunohistochemical and RT-PCR analysis

International Journal of Molecular Medicine

Volumn 18, Issue 1, 2006, Pages 49-58

  Bronzetti, Elena ^a   Artico, Marco ^a   Pompili, Elena ^a   Felici, Laura M ^a   Stringaro, Annarita ^b   Bosco, Sandro ^a   Magliulo, Giuseppe ^a   Colone, Marisa ^b   Arancia, Giuseppe ^b   Vitale, Marco ^c,d   Fumagalli, Lorenzo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c UNIVERSITY OF PARMA   (Italy)

^d CNR   (Italy)

Author keywords

CGRP; Cholinacetyltransferase; Electron microscopy; Human tonsil; Immunohistochemistry; Neurotrophins; nNOS; SP; VIP

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; NERVE GROWTH FACTOR; NEUROTROPHIN 3; NEUROTROPHIN 3 RECEPTOR; PROTEIN TYROSINE KINASE A;

ARTICLE; BLOOD VESSEL; CHEMISTRY; CRYOELECTRON MICROSCOPY; HUMAN; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE; MACROPHAGE; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TONSIL; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

BLOOD VESSELS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CRYOELECTRON MICROSCOPY; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES; MACROPHAGES; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE GROWTH FACTOR; NERVE GROWTH FACTORS; NEUROTRANSMITTER AGENTS; NEUROTROPHIN 3; RECEPTOR, TRKA; RECEPTOR, TRKB; RECEPTOR, TRKC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TONSIL;

EID: 33748162738     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.18.1.49     Document Type: Article

References (70)

1. Felten SY, Felten DL, Bellinger DL and Olschowka JA: Noradrenergic and peptidergic innervation of lymphoid organs. Chem Immunol 52: 25-48, 1992.
2. Lewin GR and Barde YA: Physiology of neurotrophins. Ann Rev Neurosci 9: 289-217, 1996.
3. Barbacid M: The Trk family of neurotrophin receptors. J Neuroimmunol 25: 1386-1403, 1994.
4. Kaplan DR and Miller FD: Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol 9: 213-221, 1997.
5. Lomen HC and Shooter EM: Widespread neurotrophin receptor expression in the immune system and other non-neuronal rat tissue. J Neurochem 64: 1780-1789, 1995.
6. Lommatzsch M, Braun A, Mannsfeldt A, Botchkarev VA, Botchkareva NV, Paus R, Fischer A, Lewin GR and Renz H: Abundant production of brain-derived neurotrophic factor by adult visceral epithelia implications for paracrine and targetderived neurotrophic functions Am J Pathol 155: 1183-1193, 1999.
7. Snider WD: Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77: 627-638, 1994.
8. Canning BJ, Reynolds SM, Anukwu LU, Kajekar R and Myers AC: Endogenous neurokinins facilitate synaptic transmission in guinea pig airway parasympathetic ganglia. Am J Physiol Regul Integr Comp Physiol 283: R320-R330, 2002. (Pubitemid 34863878)
9. Djakiew D, Delsite R, Pflug B, Wrathall J, Lynch JH and Onoda M: Regulation of growth by a nerve growth factor-like protein which modulates paracrine interactions between a neoplastic epithelial cell line and stromal cells of the human prostate. Cancer Res 51: 3304-3310, 1991.
10. Varvella F, Colella G and Scala G: Innervation of the bronchial tree in cattle. Boll Soc Ital Biol Sper 57: 304-309, 1981.
11. Mutoh T, Bonham AC and Joad JP: Substance P in the nucleus of the solitary tract augments bronchopulmonary C fiber reflex output. Am J Physiol Regul Integr Comp Physiol 279: R1215-R1223, 2000.
12. Schlosser RJ, Czaja JM, Yang B and McCaffrey TV: Signal transduction mechanisms in substance P-mediated ciliostimulation. Otolaryngol Head Neck Surg 113: 582-588, 1995.
13. Otten U and Gadient RA: Neurotrophins and cytokines-intermediaries between the immune and nervous systems. Int J Dev Neurosci 13: 147-151, 1995.
14. Tessarollo L: Pleiotropic functions of neurotrophins in development. Cytokine Growth Factor Rev 9: 125-137, 1998.
15. Aloe L, Simone MD and Properzi F: Nerve growth factor: a neurotrophin with activity on cells of the immune system. Microsc Res Tech 45: 285-291, 1999. (Pubitemid 29264992)
16. Aloe L: Nerve growth factor and neuroimmune responses: basic and clinical observations. Arch Physiol Biochem 109: 354-356, 2001. (Pubitemid 35216882)
17. Sariola H: The neurotrophic factors in non-neuronal tissues. Cell Mol Life Sci 58: 1061-1066, 2001.
18. Kannan Y, Stead RH, Goldsmith CH and Bienenstock J: Lymphoid tissues induce NGF-dependent and NGF-independent neurite outgrowth from rat superior cervical ganglia explants in culture. J Neurosci Res 37: 374-383, 1994. (Pubitemid 24072923)
19. Kannan Y, Bienenstock J, Ohta M, Stanisz AM and Stead RH: Nerve growth factor and cytokines mediate lymphoid tissue-induced neurite outgrowth from mouse superior cervical ganglia in vitro. J Immunol 157: 313-320, 1996. (Pubitemid 26190563)
20. Carlson SL, Albers KM, Beiting DJ, Parish M, Conner JM and Davis BM: NGF modulates sympathetic innervation of lymphoid tissues. J Neurosci 15: 5892-5899, 1995.
21. Carlson SL, Johnson S, Parrish ME and Cass WA: Development of immune hyperinnervation in NGF-transgenic mice. Exp Neurol 149: 209-220, 1998. (Pubitemid 28091030)
22. Tokuyasu KT: A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57: 551-565, 1973.
23. Yaeger MJ, Koestner A, Marushige K and Marushige Y: The reverse transforming effects of nerve growth factor on five human neurogenic tumor cell lines: in vitro results. Acta Neuropathol 83: 72-80, 1991.
24. Oelmann E, Sreter L, Schuller I, Serve H, Koenigsmann M, Wiedenmann B, Oberberg D, Reufi B, Thiel E and Berdel WE: Nerve growth factor stimulates clonal growth of human lung cancer cell lines and a human glioblastoma cell line expressing high-affinity nerve growth factor binding sites involving tyrosine kinase signaling. Cancer Res 55: 2212-2219, 1995.
25. Pahlman S and Hoenher JC: Neurotrophin receptors, tumor progression and tumor maturation. Mol Med Today 2: 432-438, 1996. (Pubitemid 126376942)
26. Sala R, Viegi A, Rossi FM, Pizzorusso T, Bonanno G, Raiteri M and Maffei L: Nerve growth factor and brain derived neurotrophic factor increase neurotransmitter release in the rat visual cortex. Eur J Neurosci 10: 2185-2191, 1998. (Pubitemid 28327365)
27. Inoue N, Magari S and Sakanaka M: Distribution of peptidergic nerve fibers in rat bronchus-associated lymphoid tissue: light microscopic observations. Lymphology 23: 155-160, 1990. (Pubitemid 20370640)
28. Dean DH, Hiramoto RN and Ghanta VK: Modulation of immune response. A possible role for murine salivary epidermal and nerve growth factors. J Periodontol 58: 498-500, 1987.
29. Vega JA, Garcia-Suarez O, Hannestad J, Perez-Perez M and Germana A: Neurotrophins and the immune system. J Anat 203: 1-19, 2003.
30. Kerschensteiner M, Gallmeier E, Behrens L, Leal VV, Misgeld T, Klinkert WE, Kolbeck R, Hoppe E, Oropeza-Wekerle RL, Bartke I, Stadelmann C, Lassmann H, Wekerle H and Hohlfeld R: Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: a neuroprotective role of inflammation? J Exp Med 189: 865-870, 1999.
31. Moalem G, Gdalyahu A, Shani Y, Otten U, Lazarovici P, Cohen IR and Schwartz M: Production of neurotrophins by activated T cells: implications for neuroprotective autoimmunity. J Autoimmun 15: 331-345, 2000.
32. Ehrhard PB, Erb P, Graumann U and Otten U: Expression of nerve growth factor and nerve growth factor receptor tyrosine kinase Trk in activated CD4-positive T-cell clones. Proc Natl Acad Sci USA 90: 10984-10988, 1993. (Pubitemid 23354353)
33. Santambrogio L, Benedetti M, Chao MV, Muzaffar R, Kulig K, Gabellini N and Hochwald G: Nerve growth factor production by lymphocytes. J Immunol 153: 4488-4495, 1994.
34. + T cell clones produce and release nerve growth factor and express high-affinity nerve growth factor receptors. J Allergy Clin Immunol 100: 408-414, 1997.
35. Besser M and Wank R: Cutting edge: clonally restricted production of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3 mRNA by human immune cells and Th1/Th2-polarized expression of their receptors. J Immunol 162: 6303-6306, 1999. (Pubitemid 29309346)
36. Braun A, Lommatzsch M, Mannsfeldt A, Neuhaus-Steinmetz U, Fischer A, Schnoy N, Lewin GR and Renz H: Cellular sources of enhanced brain-derived neurotrophic factor production in a mouse model of allergic inflammation. Am J Respir Cell Mol Biol 21: 537-546, 1999.
37. Kittur SD, Song L, Endo H and Adler WH: Nerve growth factor receptor gene expression in human peripheral blood lymphocytes in aging. J Neurosci Res 32: 444-448, 1992.
38. Melamed I, Kelleher CA, Franklin RA, Brodie C, Hempstead B, Kaplan D and Gelfand EW: Nerve growth factor signal transduction in human B lymphocytes is mediated by gp140Trk. Eur J Immunol 26: 1985-1992, 1996.
39. Torcia M, Bracci-Laudiero L, Lucibello M, Nencioni L, Labardi D, Rubartelli A, Cozzolino F, Aloe L and Garaci E: Nerve growth factor is an autocrine survival factor for memory B lymphocytes. Cell 85: 345-356, 1996. (Pubitemid 26160706)
40. D'Onofrio M, de Grazia U, Morrone S, Cuomo L, Spinsanti P, Frati L, Gulino A and Ragona G: Expression of neurotrophin receptors in normal and malignant B lymphocytes. Eur Cytokine Netw 11: 283-291, 2000.
41. Brodie C, Oshiba A, Renz H, Bradley K and Gelfand EW: Nerve growth-factor and anti-CD40 provide opposite signals for the production of IgE in interleukin-4-treated lymphocytes. Eur J Immunol 26: 171-178, 1996. (Pubitemid 26028430)
42. Schenone A, Gill JS, Zacharias DA and Windebank AJ: Expression of high- and low-affinity neurotrophin receptors on human transformed B lymphocytes. J Neuroimmunol 64: 141-149, 1996. (Pubitemid 26094631)
43. Pezzati P, Stanisz AM, Marshall JS, Bienenstock J and Stead RH: Expression of nerve growth factor receptor immunoreactivity on follicular dendritic cells from human mucosa associated lymphoid tissues. Immunology 76: 485-490, 1992.
44. Hannestad J, Levanti MB and Vega JA: Distribution of neurotrophin receptors in human palatine tonsils: an immunohistochemical study. J Neuroimmunol 58: 131-137, 1995.
45. Garcia-Suarez O, Hannestad J, Esteban I, Martinez del Valle M, Naves FJ and Vega JA: Neurotrophin receptor-like protein immunoreactivity in human lymph nodes. Anat Rec 249: 226-232, 1997. (Pubitemid 27426326)
46. Labouyrie E, Parrens M, de Mascarel A, Bloch B and Merlio JP: Distribution of NGF receptors in normal and pathologic human lymphoid tissues. J Neuroimmunol 77: 161-173, 1997. (Pubitemid 27312353)
47. Levanti B, Hannestad J, Esteban I, Ciriaco E, Germana G and Vega JA: Neurotrophin receptor-like proteins in Peyer's patches. Anat Rec 249: 365-372, 1997. (Pubitemid 27469288)
48. Levanti MB, Germana A, Catania S, Germana GP, Gauna-Anasco L, Vega JA and Ciriaco E: Neurotrophin receptor-like proteins in the bovine (Bos taurus) lymphoid organs, with special reference to thymus and spleen. Anat Histol Embryol 30: 193-198, 2001.
49. Ricci A, Greco S, Amenta F, Bronzetti E, Felici L, Rossodivita I, Sabbatini M and Mariotta S: Neurotrophins and neurotrophin receptors in human pulmonary arteries. J Vasc Res 37: 355-363, 2000.
50. Bronzetti E, Artico M, Lo Vasco VR, Felici LM, Bosco S, Magliulo G, Pompili E and Fumagalli L: Expression of neurotransmitters and neurotrophins in human adenoid tissue. Int J Mol Med 15: 921-928, 2005.
51. Martling CR, Matran R, Alving K, Hokfelt T and Lundberg JM: Innervation of lower airways and neuropeptide effects on bronchial and vascular tone in the pig. Cell Tissue Res 260: 223-233, 1990. (Pubitemid 20138431)
52. Reinheimer T, Bernedo P, Klapproth H, Oelert H, Zeiske B, Racke K and Wessler I: Acetylcholine in isolated airways of the rat, guinea pig, and human: species differences in role of airway mucosa. Am J Physiol 270: L722-728, 1996.
53. Nohr D and Weihe E: The neuroimmune link in the bronchus-associated lymphoid tissue (BALT) of cat and rat: peptides and neural markers. Brain Behav Immun 5: 84-101, 1991.
54. Sonea IM, Bowker RM, Robinson NE and Broadstone RV: Substance P and calcitonin gene-related peptide-like immunoreactive nerve fibers in lungs from adult equids. Am J Vet Res 55: 1066-1074, 1994.
55. Busse W, Elias J, Sheppard D and Banks-Schlegel S: Airway remodelling and repair. Am J Respir Crit Care Med 160: 1035-1042, 1999.
56. Schober A, Huber K, Fey J and Unsicker K: Distinct populations of macrophages in the adult rat adrenal gland: a subpopulation with neurotrophin-4-like immunoreactivity. Cell Tissue Res 291: 365-373, 1998. (Pubitemid 28104985)
57. Boven LA, Middel J, Portegies P, Verhoef J, Jansen GH and Nottet HS: Overexpression of nerve growth factor and basic fibroblast growth factor in AIDS dementia complex. J Neuroimmunol 97: 154-162, 1999. (Pubitemid 29301425)
58. Caroleo MC, Costa N, Bracci-Laudiero L and Aloe L: Human monocyte/macrophages activate by exposure to LPS overexpress NGF and NGF receptors. J Neuroimmunol 113: 193-201, 2001. (Pubitemid 32112745)
59. Bayas A, Kruse N, Moriabadi NF, Weber F, Hummel V, Wohleben G, Gold R, Toyka KV and Rieckmann P: Modulation of cytokine mRNA expression by brain-derived neurotrophic factor and nerve growth factor in human immune cells. Neurosci Lett 335: 155-158, 2003.
60. Stanisz AM and Stanisz JA: Nerve growth factor and neuroimmune interactions in inflammatory diseases. Ann NY Acad Sci 917: 268-272, 2000.
61. Bonini S, Lambiase A, Bonini S, Angelucci F, Magrini L, Manni L and Aloe L: Circulating nerve growth factor levels are increased in humans with allergic diseases and asthma. Proc Natl Acad Sci USA 93: 10955-10960, 1996.
62. Sanico AM, Koliatsos VE, Stanisz AM, Bienenstock J and Togias A: Neural hyperresponsiveness and nerve growth factor in allergic rhinitis. Int Arch Allergy Immunol 118: 154-158, 1999. (Pubitemid 29195492)
63. Renz H: The role of neurotrophins in bronchial asthma. Eur J Pharmacol 429: 231-237, 2001.
64. de Vries A, Engels F, Henricks PA, Leusink-Muis T, Fischer A and Nijkamp FP: Antibodies directed against nerve growth factor inhibit the acute bronchoconstriction due to allergen challenge in guinea-pigs. Clin Exp Allergy 32: 325-328, 2002. (Pubitemid 34429614)
65. de Vries A, Dessing MC, Engels F, Henricks PA and Nijkamp FP: Nerve growth factor induces a neurokinin-1 receptor-mediated airway hyperresponsiveness in guinea pigs. Am J Respir Crit Care Med 159: 1541-1544, 1999. (Pubitemid 29227866)
66. Rubin JB and Segal RA: Growth, survival and migration: the Trk to cancer. Cancer Treat Res 115: 1-18, 2003.
67. Miknyoczki SJ, Lang D, Huang L, Klein-Szanto AJ, Dionne CA and Ruggeri BA: Neurotrophins and Trk receptors in human pancreatic ductal adenocarcinoma: expression patterns and effects on in vitro invasive behavior. Int J Cancer 81: 417-427, 1999. (Pubitemid 29165201)
68. Innominato PF, Libbrecht L and van den Oord JJ: Expression of neurotrophins and their receptors in pigment cell lesions of the skin. J Pathol 194: 95-100, 2001. (Pubitemid 32390454)
69. Satoh F, Mimata H, Nomura T, Fujita Y, Shin T, Sakamoto S, Hamada Y and Nomura Y: Autocrine expression of neurotrophins and their receptors in prostate cancer. Int J Urol 8: S28-34, 2001. (Pubitemid 34225134)
70. Ricci A, Greco S, Mariotta S, Felici L, Bronzetti E, Cavazzana A, Cardillo G, Amenta F, Bisetti A and Barbolini G: Neurotrophins and neurotrophin receptors in human lung cancer. Am J Respir Cell Mol Biol 25: 439-446, 2001. (Pubitemid 33037676)