Ontogeny of intrinsic innervation in the human thymus and spleen

Journal of Histochemistry and Cytochemistry

Volumn 55, Issue 8, 2007, Pages 813-820

  Anagnostou, Valsamo K ^a   Doussis Anagnostopoulou, Ipatia ^a   Tiniakos, Dina G ^a   Karandrea, Despina ^a   Agapitos, Emmanouil ^a   Karakitsos, Petros ^b   Kittas, Christos ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b KAT HOSPITAL   (Greece)

Author keywords

Fetal; Human; Image analysis; Immunohistochemistry; Innervation; Spleen; Thymus

Indexed keywords

GENE PRODUCT; NEURON SPECIFIC ENOLASE; PROTEIN PGP9.5; PROTEIN S 100; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ARTICLE; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INNERVATION; LYMPHOID ORGAN; NERVE ENDING; NERVE FIBER; ONTOGENY; PRIORITY JOURNAL; SPLEEN; THYMUS;

FETUS; GESTATIONAL AGE; HUMANS; IMMUNOHISTOCHEMISTRY; NERVE FIBERS; SPLEEN; THYMUS GLAND;

EID: 34447544573     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/jhc.6A7168.2007     Document Type: Article

References (52)

1. Ackerman KD, Felten SY, Bellinger DL, Felten DL (1987a) Noradrenergic sympathetic innervation of spleen and lymph nodes in relation to specific cellular compartments. Prog Immunol 6:588-600
2. Ackerman KD, Felten SY, Bellinger DL, Felten DL (1987b) Noradrenergic sympathetic innervation of the spleen. III. Development of innervation in the rat spleen. J Neurosci Res 18:49-54
3. Ackerman KD, Felten SY, Bellinger DL, Felten DL (1991) Ontogeny and senescence of noradrenergic innervation of the rodent thymus and spleen. In Ader R, Felten DL, and Cohen N, eds. Psychoneuroimmunology. San Diego, Academic Press, 72-115
4. Akagi T, Nose S, Takahashi K, Yoshito T, Horie Y, Motoi M, Sonobe H, et al. (1989) Ontogeny of S100 protein-positive histiocytes and lymphocytes in the human fetal lymphoreticular system. Acta Med Okayama 43:203-210
5. Bellinger DL, Ackerman KD, Felten SY, Felten DL (1992) A longitudinal study of age-related loss of noradrenergic nerves and lymphoid cells in the rat spleen. Exp Neurol 116:295-311
6. Bellinger DL, Felten SY, Collier TJ, Felten DL (1987) Noradrenergic sympathetic innervation of the spleen: IV. Morphometric analysis in adult and aged F344 rats. J Neurosci Res 18:55-63, 126-129
7. Blennerhassett MG, Bienenstock J (1998) Sympathetic nerve contact causes maturation of mast cells in vitro. J Neurobiol 35:173-182
8. Brelinska R, Ostalska D, Zabel M (2000) Subtypes of thymic epithelial cells defined by neuroendocrine markers. Histochem Cell Biol 114:239-244
9. Brelinska R, Seidel HJ, Kreja L (1991) Thymic nurse cells: differentiation of thymocytes within complexes. Cell Tissue Res 264:175-183
10. Buckley PJ (1991) Phenotypic subpopulations of macrophages and dendritic cells in human spleen. Scanning Microsc 5:147-157
11. Bulloch K, Cullen MR, Schwartz RH, Longo DL (1987) Development of innervation within syngeneic thymus tissue transplanted under the kidney capsule of the nude mouse: a light and ultrastructural microscope study. J Neurosci Res 18:16-27
12. Bulloch K, Pomerantz W (1984) Autonomic nervous system innervation of thymic-related lymphoid tissue in wild type and nude mice. J Comp Neurol 228:57-68
13. Cavallotti C, Artico M, Cavallotti D (1999) Occurrence of adrenergic nerve fibers and of noradrenaline in thymus gland of juvenile and aged rats. Immunol Lett 70:53-62
14. de Leeuw FE, Jansen GH, Batanero E, van Wichen DF, Huber J, Schuurman HJ (1992) The neural and neuro-endocrine component of the human thymus. I. Nerve-like structures. Brain Behav Immun 6:234-248
15. De Waal EJ, Rademakers LH (1997) Heterogeneity of epithelial cells in the rat thymus. Microsc Res Tech 38:227-236
16. Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES (2000) The sympathetic nerve - an integrative interface between supersystems: the brain and the immune system. Pharmacol Rev 52:595-638
17. Felten DL (1993) Direct innervation of lymphoid organs: substrate for neurotransmitter signaling of cells of the immune system. Neuropsychobiology 28:110-112
18. Felten DL, Felten SY, Carlson SL, Olschowka JA, Livnat S (1985) Noradrenergic and peptidergic innervation of lymphoid tissue. J Immunol 135:755s-765s
19. Felten SY, Felten DL, Bellinger DL, Olschowka JA (1992) Noradrenergic and peptidergic innervation of lymphoid organs. Chem Immunol 52:25-48
20. Friedman EM, Irwin MR (1997) Modulation of immune cell function by the autonomic nervous system. Pharmacol Ther 74:27-38
21. Ghali WM, Abdel-Rahman S, Nagib M, Mahran ZY (1980) Intrinsic innervation and vasculature of pre- and post-natal human thymus. Acta Anat (Basel) 108:115-123
22. Giron LT Jr, Crutcher KA, Davis JN (1980) Lymph nodes - a possible site for sympathetic neuronal regulation of immune responses. Ann Neurol 8:520-525
23. Hammar JA (1935) Konstitutionsanatomische Studien über die Neurotisierung des Menschenembryos. Zeitschrift für mikroskopischanatomie Forschumg. 38:253-293
24. Hasko G, Szabo C, Nemeth ZH, Salzman AL, Vizi ES (1998) Stimulation of beta-adrenoreceptors inhibits endotoxin-induced IL-12 production in normal and IL-10 deficient mice. J Neuroimmunol 88:57-61
25. Heusermann U (1988) Morphology and function of the human spleen. Enzyme histochemical and electron microscopy studies of the splenic lymphatic vessels, nerves and connective tissue structures. Veroff Pathol 129:1-165
26. Heusermann U, Stutte HJ (1977) Electron microscopic studies of the innervation of the human spleen. Cell Tissue Res 184: 225-236
27. Hiramine C, Nakagawa T, Hojo K (1995) Murine nursing thymic epithelial cell lines capable of inducing thymocyte apoptosis express the self-superantigen Mls-1a. Cell Immunol 160: 157-162
28. Kendall MD (1989) The morphology of perivascular spaces in the thymus. Thymus 13:157-164
29. Kendall MD, al-Shawaf AA (1991) Innervation of the rat thymus gland. Brain Behav Immun 5:9-28
30. Kendall MD, al-Shawaf A, Zaidi SA (1988) The cholinergic and adrenergic innervation of the rat thymus. Adv Exp Med Biol 237:255-261
31. Klein RL, Wilson SP, Dzielak DJ, Yang WH, Viveros OH (1982) Opioid peptides and noradrenaline co-exist in large dense-cored vesicles from sympathetic nerve. Neuroscience 7:2255-2261
32. Kranz A, Kendall MD, von Gaudecker B (1997) Studies on rat and human thymus to demonstrate immunoreactivity of calcitonin gene-related peptide, tyrosine hydroxylase and neuropeptide Y. J Anat 191:441-450
33. Kudoh G, Hoshi K, Murakami T (1979) Fluorescence microscopic and enzyme histochemical studies of the innervation of the human spleen. Arch Histol Jpn 42:169-180
34. Kurz B, Feindt J, von Gaudecker B, Kranz A, Loppnow H, Mentlein R (1997) Beta-adrenoreceptor-mediated effects in rat cultured thymic epithelial cells. Br J Pharmacol 120:1401-1408
35. Madden KS, Ackerman KD, Livnat S, Felten S, Felten DL (1993) Neonatal sympathetic denervation alters the development of natural killer (NK) cell activity in F344 rats. Brain Behav Immun 7: 334-351
36. Mignini F, Streccioni V, Amenta F (2003) Autonomic innervation of immune organs and neuroimmune modulation. Auton Autacoid Pharmacol 23:1-25
37. Pavlov VA, Wang H, Czura CJ, Friedman SG, Tracey KJ (2003) The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation. Mol Med 9:125-134
38. Qiu YH, Peng YP, Jiang JM, Wang JJ (2004) Expression of tyrosine hydroxylase in lymphocytes and effect of endogenous catecholamines on lymphocyte function. Neuroimmunomodulation 11:75-83
39. Reilly FD, McCuskey RS, Meineke HA (1976) Studies of the hemopoietic microenvironment. VIII. Adrenergic and cholinergic innervation of the murine spleen. Anat Rec 185:109-117
40. Rinner I, Felsner P, Falus A, Skreiner E, Kukulansky T, Globerson A, Hirokawa K, et al. (1995) Cholinergic signals to and from the immune system. Immunol Lett 44:217-220
41. Rogausch H, Bock T, Voigt KH, Besedovsky H (2004) The sympathetic control of blood supply is different in the spleen and lymph nodes. Neuroimmunomodulation 11:58-64
42. Saeed RW, Varma S, Peng-Nemeroff T, Sherry B, Balakhaneh D, Huston J, Tracey KJ, et al. (2005) Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation. J Exp Med 201:1113-1123
43. Savchenko AS, Hasegawa G, Naito M (2006) Development and maturation of thymic dendritic cells during human ontogeny. Cell Tissue Res 325:455-460
44. Stevens-Felten SY, Bellinger DL (1997) Noradenergic and peptidergic innervation of lymphoid organs. Chem Immunol 69:99-131
45. Tonkoff W (1899) Zur Kenntnis der Nerven der Lymphdrusen. Anat Anz 16:456-459
46. Tracey KJ (2002) The inflammatory reflex. Nature 420:853-859
47. Uccini S, Vitolo D, Stoppacciaro A, Paliotta D, Cassano AM, Barsotti P, Ruco LP, et al. (1986) Immunoreactivity for S-100 protein in dendritic and in lymphocyte-like cells in human lymphoid tissues. Virchows Arch B Cell Pathol Incl Mol Pathol 52:129-141
48. Vizi ES, Orso E, Osipenko ON, Hasko G, Elenkov IJ (1995) Neurochemical, electrophysiological and immunocytochemical evidence for a noradrenergic link between the sympathetic nervous system and thymocytes. Neuroscience 68:1263-1276
49. Williams JM, Felten DL (1981) Sympathetic innervation of murine thymus and spleen: a comparative histofluorescence study. Anat Rec 199:531-542
50. Wrona D (2006) Neural-immune interactions: an integrative view of the bidirectional relationship between the brain and immune systems. J Neuroimmunol 172:38-58
51. Zetterstrom BE, Hokfelt T, Norberg KA, Olsson P (1973) Possibilities of a direct adrenergic influence on blood elements in the dog spleen. Acta Chir Scand 139:117-122
52. Zimring JC, Kapp LM, Yamada M, Wess J, Kapp JA (2005) Regulation of CD8+ cytolytic T lymphocyte differentiation by a cholinergic pathway. J Neuroimmunol 164:66-75