Sympathetic nervous system and lymphocyte proliferation in the Fischer 344 rat spleen: A longitudinal study

NeuroImmunoModulation

Volumn 15, Issue 4-6, 2008, Pages 260-271

  Bellinger, Denise L ^a   Silva, Dorian ^a   Millar, Ashley Brooke ^a   Molinaro, Christine ^a   Ghamsary, Mark ^a   Carter, Jeff ^a   Perez, Sam ^a   Lorton, Dianne ^b   Lubahn, Cheri ^b   Araujoa, Gerson ^a   Thyagarajan, Srinivasan ^a  

^a LOMA LINDA UNIVERSITY   (United States)

^b SUN HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Aging; Immune function; Norepinephrine turnover; Plasma; Spleen

Indexed keywords

ADRENALIN; BETA ADRENERGIC RECEPTOR; CONCANAVALIN A; CYCLIC AMP; NORADRENALIN;

ADRENALIN BLOOD LEVEL; ADRENERGIC SYSTEM; ADRENERGIC TRANSMISSION; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FISCHER 344 RAT; LONGITUDINAL STUDY; LYMPHOCYTE PROLIFERATION; MALE; NONHUMAN; NORADRENALIN BLOOD LEVEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; RAT; SPLEEN; SPLEEN CELL;

1-METHYL-3-ISOBUTYLXANTHINE; AGING; ALPHA-METHYLTYROSINE; ANIMALS; CONCANAVALIN A; CYCLIC AMP; CYTOKINES; EPINEPHRINE; ISOPROTERENOL; LYMPHOCYTE ACTIVATION; MALE; NEUROIMMUNOMODULATION; NOREPINEPHRINE; RATS; RATS, INBRED F344; RECEPTORS, ADRENERGIC, BETA; SPLEEN; SYMPATHETIC NERVOUS SYSTEM; T-LYMPHOCYTE SUBSETS; TYROSINE 3-MONOOXYGENASE;

EID: 57149120117     PISSN: 10217401     EISSN: None     Source Type: Journal    
DOI: 10.1159/000156469     Document Type: Article

References (75)

1. Bellinger DL, Lorton D, Lubahn C, Felten DL: Innervation of lymphoid organs: association of nerves with cells of the immune system and their implications in disease; in Ader R, Felten DL, Cohen N (eds): Psychoneuroimmunology, ed 3. New York, Academic Press, 2001, vol 1, pp 55-113.
2. Nance DM, Sanders VM: Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav Immun 2007;21:736-745.
3. Bellinger DL, Millar BA, Perez S, Carter J, Wood C, Thyagarajan S, Molinaro C, Lubahn C, Lorton D: Sympathetic modulation of immunity: relevance to disease. Cell Immunol 2008;252:27-56.
4. Cohen S, Miller GE, Rabin BS: Psychological stress and antibody response to immunization: a critical review of human literature. Psychosom Med 2001;63:7-18.
5. Hoeldtke RD Cilmi KM: Effects of aging on catecholamine metabolism. J Clin Endocrinol Metab 1985;60:479-484.
6. MacGilchrist AJ, Hawksby C, Howes LG, Reid JL: Rise in plasma noradrenaline with age results from an increase in spillover rate. Gerontology 1989;35:7-13.
7. Ziegler MG, Lake CR, Kopin IJ: Plasma noradrenaline increases with age. Nature 1976;261:333-335.
8. Jones PP, Shapiro LF, Keisling GA, Jordan J, Shannon JR, Quaife RA, Seals DR: Altered autonomic support of arterial blood pressure with age in healthy men. Circulation 2001;104:2424-2429.
9. Ward KD, Sparrow D, Landsberg L, Young JB, Vokonas PS, Weiss ST: Influence of insulin, sympathetic nervous system activity, and obesity on blood pressure: the Normative Aging Study. J Hypertens 1996;14:301-308.
10. Webb GD, Toth MJ, Poehlman ET: Influence of physiological factors on the age-related increase in blood pressure in healthy men. Exp Gerontol 1996;31:341-350.
11. White M, Leenen FH: Aging and cardiovascular responsiveness to β-agonist in humans: role of changes in beta-receptor responses versus baroreflex activity. Clin Pharmacol Ther 1994;56:543-553.
12. Young JB, Rowe JW, Pallotta JA, Sparrow D, Landsberg L: Enhanced plasma norepinephrine response to upright posture and oral glucose administration in elderly human subjects. Metabolism 1980;29:532-539.
13. McCarty R: Cardiovascular responses to acute footshock stress in adult and aged Fischer 344 male rats. Neurobiol Aging 1985;6:47-50.
14. Mabry TR, Gold PE, McCarty R: Age-related changes in plasma catecholamine responses to chronic intermittent stress. Physiol Behav 1995;58:49-56.
15. Barnet SR, Morin RJ, Kiely DK, Ganon M, Azhar G, Knight EL, Nelson JC, Lipsitz LA: Effects of age and gender on autonomic control of blood pressure dynamics. Hypertension 1999;33:1195-1200.
16. Galarza CR, Alfie J, Waisman GD, Mayorga LM, Camera LA, del Rio M, Vasvari F, Limansky R, Farias J, Tessler J, Camera MI: Diastolic pressure underestimates age-related hemodynamic impairment. Hypertension 1997;30:809-816.
17. Pears E, Hannaford PC, Taylor MW: Gender, age and deprivation differences in the primary care management of hypertension in Scotland: a cross-sectional database study. Fam Pract 2003;20:22-31.
18. Kaye D, Esler M: Sympathetic neuronal regulation of the heart in aging and heart failure. Cardiovasc Res 2005;66:256-264.
19. Dinenno FA, Jones PP, Seals DR, Tanaka H: Limb blood flow and vascular conductance are reduced with age in healthy humans: relation to elevations in sympathetic nerve activity and declines in oxygen demand. Circulation 1999;100:164-170.
20. Grassi G, Colombo M, Seravalle G, Spaziani D, Mancia G: Dissociation between muscle and skin sympathetic nerve activity in essential hypertension, obesity, and congestive heart failure. Hypertension 1998;31:64-67.
21. Seals DR, Esler MD: Topical review: human ageing and the sympathoadrenal system. J Physiol 2000;528:407-417.
22. Esler M, Kaye D, Thompson J, Jennings G, Cox H, Turner A, Lambert G, Seals D: Effects of aging on epinephrine secretion, and on regional release of epinephrine from the human heart. J Clin Endocrinol Metab 1995;80:435-442.
23. Esler M, Hastings J, Lambert G, Kaye D, Jennings G, Seals DR: The influence of aging on the human sympathetic nervous system and brain norepinephrine turnover. Am J Physiol Reg Integr Comp Physiol 2002;282:R909-R916.
24. Bellinger DL, Stevens SY, Thyaga Rajan S, Lorton D, Madden KS: Aging and sympathetic modulation of immune function in Fischer 344 rats: effects of chemical sympathectomy on primary antibody response. J Neuroimmunol 2005;165:21-32.
25. Ackerman KD, Bellinger DL, Felten SY, Felten DL: Ontogeny and senescence of noradrenergic innervation of the rodent thymus and spleen; in Ader R, Felten DL, Cohen N (eds): Psychoneuroimmunology, ed 2. New York, Academic Press, 1991, pp 71-125.
26. Bellinger DL, Ackerman KD, Felten SY, Felten DL: A longitudinal study of age-related loss of noradrenergic nerves and lymphoid cells in the rat spleen. Exp Neurol 1992;116:295-311.
27. Bellinger DL, Felten SY, Collier TJ, Felten DL: Noradrenergic sympathetic innervation of the spleen. IV. Morphometric analysis in adult and aged F344 rats. J Neurosci Res 1987;18:55-63 and 126-129.
28. Bellinger D, Tran L, Kang JI, Lubahn C, Felten DL, Lorton D: Age-related changes in noradrenergic sympathetic innervation of the rat spleen are strain dependent. Brain Behav Immun 2002;16:247-261.
29. Felten SY, Bellinger DL, Collier TJ, Coleman PD, Felten DL: Decreased sympathetic innervation of spleen in aged Fischer 344 rats. Neurobiol Aging 1987;8:159-165.
30. Bellinger DL, Lorton D, Felten SY, Felten DL: Innervation of lymphoid organs and implications in development, aging, and autoimmunity. Int J Immunopharmacol 1992;14:329-344.
31. Bellinger DL Felten DL: Sympathetic nervous system and aging; in Mobbs CV, Hof PR (eds): Functional Endocrinology of Aging. Basel, Karger, 1998, vol 29, pp 166-203.
32. Grubeck-Loebenstein B: Changes in the aging immune system. Biologicals 1997;25:205-208.
33. Yung RL: Changes in immune function with age. Rheum Dis Clin North Am 2000;26:455-473.
34. Linton P, Thoman ML: T cell senescence. Front Biosci 2001;6:D248-D261.
35. Holmes DJ: Naturally long-lived animal models for the study of slow aging and longevity. Ann NY Acad Sci 2004;1019:483-485.
36. Weindruch R, Masoro EJ: Concerns about rodent models for aging research. J Gerontol 1991;46:B87-B88.
37. Moore KE, Dominic JA: Tyrosine hydroxylase inhibitors. Fed Proc 1971;30:859-870.
38. Trayhurn P, Wusteman MC: Sympathetic activity in brown adipose tissue in lactating mice. Am J Physiol 1987;253:E515-E520.
39. Landsberg L, Young JB: The role of the sympathoadrenal system in modulating energy expenditure. Clin Endocrinol Metab 1984;13:475-499.
40. Jones SB Musacchia XJ: Norepinephrine turnover in heart and spleen of 7-, 22-, and 34 degree C-acclimated hamsters. Am J Physiol 1976;230:564-568.
41. Bishop YMM, Fienberg SE, Holland PW: Discrete Mutivariate Analyses: Theory and Practice. Cambridge, MIT Press, 1975.
42. Avakian EV, Horvath SM: Influence of aging and tyrosine hydroxylase inhibition on tissue levels of norepinephrine during stress. J Gerontol 1982;37:257-261.
43. Jones SB, Kovarik MF, Romano FD: Cardiac and splenic norepinephrine turnover during septic peritonitis. Am J Physiol 1986;250:R892-R897.
44. Alexandre JM, Chevillard C: Influence of β-adrenoceptor blocking agents on the turnover rate of cardiac and splenic noradrenaline in rats. Br J Pharmacol 1980;69:35-40.
45. Albino Teixeira A, Azevedo I, Branco D, Rodrigues-Pereira E, Osswald W: Sympathetic denervation caused by long-term noradrenaline infusions; prevention by desipramine and superoxide dismutase. Br J Pharmacol 1989;97:95-102.
46. Haavik J, Almås B, Flatmark T: Generation of reactive oxygen species by tyrosine hydroxylase: a possible contribution to the degeneration of dopaminergic neuron? J Neurochem 1997;68:328-332.
47. Sullivan KA, Feldman EL: New developments in diabetic neuropathy. Curr Opin Neurol 2005;18:586-590.
48. Gatzinsky KP, Thrasivoulou C, Campioni-Noack M, Underwood C, Cowen T: The role of NGF uptake in selective vulnerability to cell death in ageing sympathetic neurons. Eur J Neurosci 2004;20:2848-2856.
49. Vyas S, Molinaro CA, Perez SD, Millar B, Cater J, Wood C, Bellinger DL: Effects of ageing antihypertensive drug rilmenidine on nerve growth factor expression in the spleen of male F344 rats. 13th Annual Meeting of the Psychoneuroimmunology Research Society, 2006, p 61.
50. Glebova NO, Ginty DD: Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J Neurosci 2004;24:743-751.
51. Esler M, Jennings G, Lambert G, Meredith I, Horne M, Eisenhofer G: Overflow of catecholamine neurotransmitters to the circulation: source, fate, and functions. Physiol Rev 1990;70:963-985.
52. Morrow LA, Linares OA, Hill TJ, Sanfield JA, Supiano MA, Rosen SG, Halter JB: Age differences in the plasma clearance mechanisms for epinephrine and norepinephrine in humans. J Clin Endocrinol Metab 1987;65:508-511.
53. Rubin PC, Scott PJW, McLean K, Reid JL: Noradrenaline release and clearance in relation to age blood pressure in man. Eur J Clin Invest 1982;12:121-125.
54. Veith RC, Featherstone JA, Linares OA, Halter JB: Age differences in plasma norepinephrine kinetics in humans. J Gerontol 1986;41:319-324.
55. Barnes RF, Raskind M, Gumbrecht G, Halter JB: The effects of age on the plasma catecholamine response to mental stress in man. J Clin Endocrinol Metab 1982;54:64-69.
56. Raskind MA, Peskind ER, Veith RC, Beard JC, Gumbrecht G, Halter JB: Increased plasma and cerebrospinal fluid norepinephrine in older men: differential suppression by clonidine. J Clin Endocrinol Metab 1988;66:438-443.
57. Wilkie FL, Halter JB, Prinz PN, Benedetti C, Eisdorfer C, Atwood B, Yamasaki D: Age-related changes in venous catecholamines basally and during epinephrine infusion in man. J Gerontol 1985;40:133-140.
58. McCarty R: Aged rats: diminished sympathetic-adrenal medullary responses to acute stress. Behav Neural Biol 1981;33:204-212.
59. McCarty R: Sympathetic-adrenal medullary and cardiovascular responses to acute cold stress in adult and aged rats. J Auton Nerv Syst 1985;12:15-22.
60. Milakofsky L, Harris N, Vogel WH: Effect of repeated stress on plasma catecholamines and taurine in young and old rats. Neurobiol Aging 1993;14:359-366.
61. Bishopric NH, Cohen HJ, Lefkowitz RJ: β adrenergic receptors in lymphocyte subpopulations. J Allergy Clin Immunol 1980;65:29-33.
62. Hadden JW, Hadden EM, Middleton E Jr: Lymphocyte blast transformation. I. Demonstration of adrenergic receptors in human peripheral lymphocytes. Cell Immunol 1970;1:583-595.
63. Landmann R, Burgisser E, West M, Buhler FR: β adrenergic receptors are different in subpopulations of human circulating lymphocytes. J Recept Res 1985;4:37-50.
64. Abello J, Damien C, De Neef P, Tastenoy M, Googhe R, Robberecht P, Christophe J: Properties of vasoactive intestinal peptide receptors and β-adrenoceptors in the murine radiation leukemia virus-induced lymphoma cell line BL/VL3. Eur J Biochem 1989;183:263-267.
65. O'Dorisio MS, Compolito LB: Comparison of vasoactive intestinal peptide-mediated protein phosphorylation in human lymphoblasts and colonic epithelial cells. Mol Immunol 1989;26:583-590.
66. Madden KS, Felten DL: Experimental basis for neural-immune interactions. Physiol Rev 1995;75:77-106.
67. Madden KS, Stevens SY, Felten DL, Bellinger DL: Alterations in T lymphocyte activity following chemical sympathectomy in young and old Fischer 344 rats. J Neuroimmunol 2000;103:131-145.
68. Hausdorff WP, Caron MG, Lefkowitz RJ: Turning off the signal: desensitization of beta-adrenergic receptor function. FASEB J 1990;4:2881-2889.
69. 2-adrenoceptor. Life Sci 1993;52:2083-2091.
70. Kazanietz MG, Enero MA: Decreased β-adrenoceptor-mediated vasodilation in aorta from aged rats: possible involvement of a stimulatory GTP-binding protein. Eur J Pharmacol 1991;198:177-181.
71. Tsujimoto G, Lee C, Hoffman BB: Age-related decrease in β adrenergic receptor-mediated vascular smooth muscle relaxation. J Pharmacol Exp Ther 1986;239:411-415.
72. Madden KS, Stevens SY, Felten DL, Bellinger DL: Sympathetic nervous system-immune system interactions in young and old Fischer 344 rats. Ann NY Acad Sci 1995;771:523-534.
73. Chakravarti B, Abraham GN: Aging and T-cell-mediated immunity. Mech Ageing Dev 1999;108:183-206.
74. Shearer GM: Th1/Th2 changes in aging. Mech Aging Dev 1997;94:1-6.
75. Sanders VM, Kasprowicz DJ, Kohm AP, Swanson MA: Neurotransmitter receptors on lymphocytes and other lymphoid cells; in Ader R, Cohen N, Felten DL (eds): Psychoneuroimmunology, ed 3. San Diego, Academic Press, 2001, pp 161-196.