Ageing alters perivascular nerve function of mouse mesenteric arteries in vivo

Journal of Physiology

Volumn 591, Issue 5, 2013, Pages 1251-1263

  Westcott, Erika B ^a   Segal, Steven S ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENERGIC RECEPTOR; BRIMONIDINE; CAPSAICIN; CONNEXIN 40; CYCLIC AMP; PHENYLEPHRINE; PRAZOSIN; PROPRANOLOL; RAUWOLSCINE; TETRODOTOXIN;

AGE DISTRIBUTION; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY BLOOD FLOW; ARTERY CONSTRICTION; ARTERY DIAMETER; ARTICLE; BLOOD VESSEL INNERVATION; BLOOD VESSEL REACTIVITY; CONCENTRATION RESPONSE; DRUG EFFICACY; ENZYME ACTIVATION; FEMALE; IN VIVO STUDY; JEJUNUM; MALE; MESENTERIC ARTERY; MOTOR CONTROL; MOUSE; NERVE FUNCTION; NERVE STIMULATION; NONHUMAN; PERIVASCULAR NERVE; PERIVASCULAR NERVE STIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLANCHNIC BLOOD FLOW; VASOCONSTRICTION; VASOMOTOR REFLEX;

ADRENERGIC ALPHA-1 RECEPTOR AGONISTS; ADRENERGIC ALPHA-1 RECEPTOR ANTAGONISTS; AGE FACTORS; AGING; ANIMALS; CONNEXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; ENDOTHELIAL CELLS; FEMALE; GREEN FLUORESCENT PROTEINS; JEJUNUM; MALE; MESENTERIC ARTERIES; MICE; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC; RECEPTORS, ADRENERGIC, ALPHA-1; SENSORY RECEPTOR CELLS; SPLANCHNIC CIRCULATION; SPLANCHNIC NERVES; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASOMOTOR SYSTEM;

EID: 84874410739     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.244483     Document Type: Article

References (73)

1. Arenas IA, Xu Y & Davidge ST (2006). Age-associated impairment in vasorelaxation to fluid shear stress in the female vasculature is improved by TNF-α antagonism. Am J Physiol Heart Circ Physiol 290, H1259-1263.
2. Aukes AM, Bishop N, Godfrey J & Cipolla MJ (2008). The influence of pregnancy and gender on perivascular innervation of rat posterior cerebral arteries. Reprod Sci 15, 411-419.
3. Azemin MZ, Kumar DK, Wong TY, Wang JJ, Mitchell P, Kawasaki R & Wu H (2012). Age-related rarefaction in the fractal dimension of retinal vessel. Neurobiol Aging 33, 194.e191-194.
4. BAC-GCaMP2 transgenic mice. Microcirculation 18, 331-338.
5. BAC-GCaMP2 transgenic mice. Am J Physiol Heart Circ Physiol 301, H794-802.
6. Barodka VM, Joshi BL, Berkowitz DE, Hogue CW & Nyhan D (2011). Review article: implications of vascular aging. Anesth Analg 112, 1048-1060.
7. Bearden SE (2006). Effect of aging on the structure and function of skeletal muscle microvascular networks. Microcirculation 13, 279-288.
8. Behnke BJ, Prisby RD, Lesniewski LA, Donato AJ, Olin HM & Delp MD (2006). Influence of ageing and physical activity on vascular morphology in rat skeletal muscle. J Physiol 575, 617-626.
9. Bergaya S, Matrougui K, Meneton P, Henrion D & Boulanger CM (2004). Role of tissue kallikrein in response to flow in mouse resistance arteries. J Hypertens 22, 745-750.
10. Bevan JA & Brayden JE (1987). Nonadrenergic neural vasodilator mechanisms. Circ Res 60, 309-326.
11. Bleys RL, Cowen T, Groen GJ & Hillen B (1996). Perivascular nerves of the human basal cerebral arteries: II. Changes in aging and Alzheimer's disease. J Cereb Blood Flow Metab 16, 1048-1057.
12. Brain SD & Grant AD (2004). Vascular actions of calcitonin gene-related peptide and adrenomedullin. Physiol Rev 84, 903-934.
13. Chilian WM, Harrison DG, Haws CW, Snyder WD & Marcus ML (1986). Adrenergic coronary tone during submaximal exercise in the dog is produced by circulating catecholamines. Evidence for adrenergic denervation supersensitivity in the myocardium but not in coronary vessels. Circ Res 58, 68-82.
14. Dhall U, Cowen T, Haven AJ & Burnstock G (1986). Perivascular noradrenergic and peptide-containing nerves show different patterns of changes during development and ageing in the guinea-pig. J Auton Nerv Syst 16, 109-126.
15. Dinenno FA, Jones PP, Seals DR & Tanaka H (2000). Age-associated arterial wall thickening is related to elevations in sympathetic activity in healthy humans. Am J Physiol Heart Circ Physiol 278, H1205-1210.
16. Dinenno FA & Joyner MJ (2006). α-Adrenergic control of skeletal muscle circulation at rest and during exercise in aging humans. Microcirculation 13, 329-341.
17. Drake WM, Lowe SR, Mirtella A, Bartlett TJ & Clark AJ (2000). Desensitisation of calcitonin gene-related peptide responsiveness but not adrenomedullin responsiveness in vascular smooth muscle cells. J Endocrinol 165, 133-138.
18. Dubroca C, Loyer X, Retailleau K, Loirand G, Pacaud P, Feron O, Balligand JL, Lévy BI, Heymes C & Henrion D (2007). RhoA activation and interaction with Caveolin-1 are critical for pressure-induced myogenic tone in rat mesenteric resistance arteries. Cardiovasc Res 73, 190-197.
19. Dumont O, Pinaud F, Guihot AL, Baufreton C, Loufrani L & Henrion D (2008). Alteration in flow (shear stress)-induced remodelling in rat resistance arteries with aging: improvement by a treatment with hydralazine. Cardiovasc Res 77, 600-608.
20. Edvinsson L (2002). Calcitonin gene-related peptide (CGRP) in cerebrovascular disease. ScientificWorldJournal 2, 1484-1490.
21. Faber JE, Zhang H, Lassance-Soares RM, Prabhakar P, Najafi AH, Burnett MS & Epstein SE (2011). Aging causes collateral rarefaction and increased severity of ischemic injury in multi-ple tissues. Arterioscler Thromb Vasc Biol 31, 1748-1756.
22. Flamm SD, Taki J, Moore R, Lewis SF, Keech F, Maltais F, Ahmad M, Callahan R, Dragotakes S & Alpert N (1990). Redistribution of regional and organ blood volume and effect on cardiac function in relation to upright exercise intensity in healthy human subjects. Circulation 81, 1550-1559.
23. Fleming BP, Barron KW, Howes TW & Smith JK (1987). Response of the microcirculation in rat cremaster muscle to peripheral and central sympathetic stimulation. Circ Res 61, II26-31.
24. Franchini K & Cowley A (2004). Neurogenic control of blood vessels. In Primer on the Autonomic Nervous System, ed. Robertson D, pp. 139-143. Elsevier, Amsterdam.
25. Furness JB & Marshall JM (1974). Correlation of the directly observed responses of mesenteric vessels of the rat to nerve stimulation and noradrenaline with the distribution of adrenergic nerves. J Physiol 239, 75-88.
26. Gros R, Van Wert R, You X, Thorin E & Husain M (2002). Effects of age, gender, and blood pressure on myogenic responses of mesenteric arteries from C57BL/6 mice. Am J Physiol Heart Circ Physiol 282, H380-388.
27. Haddock RE, Grayson TH, Morris MJ, Howitt L, Chadha PS & Sandow SL (2011). Diet-induced obesity impairs endothelium-derived hyperpolarization via altered potassium channel signaling mechanisms. PLoS One 6, e16423.
28. Haddock RE & Hill CE (2011). Sympathetic overdrive in obesity involves purinergic hyperactivity in the resistance vasculature. J Physiol 589, 3289-3307.
29. Hausman N, Martin J, Taggart MJ & Austin C (2012). Age-related changes in the contractile and passive arterial properties of murine mesenteric small arteries are altered by caveolin-1 knockout. J Cell Mol Med 16, 1720-1730.
30. Heckman GA & McKelvie RS (2008). Cardiovascular aging and exercise in healthy older adults. Clin J Sport Med 18, 479-485.
31. Heistad DD, Marcus ML & Gross PM (1978). Effects of sympathetic nerves on cerebral vessels in dog, cat, and monkey. Am J Physiol Heart Circ Physiol 235, H544-552.
32. Hobara N, Goda M, Hashikawa N, Jin X, Zamami Y, Takatori S & Kawasaki H (2010). [Role of angiontensin receptors in remodeling perivascular nerves]. Yakugaku Zasshi 130, 1421-1425.
33. Izzo JL & Mitchell GF (2007). Aging and arterial structure-function relations. Adv Cardiol 44, 19-34.
34. 2+-activated potassium channels. Circ Res 108, 1439-1447.
35. Kawasaki H (2002). Regulation of vascular function by perivascular calcitonin gene-related peptide-containing nerves. Jpn J Pharmacol 88, 39-43.
36. Kawasaki H, Nuki C, Saito A & Takasaki K (1990a). Adrenergic modulation of calcitonin gene-related peptide (CGRP)-containing nerve-mediated vasodilation in the rat mesenteric resistance vessel. Brain Res 506, 287-290.
37. Kawasaki H, Nuki C, Saito A & Takasaki K (1990b). Role of calcitonin gene-related peptide-containing nerves in the vascular adrenergic neurotransmission. J Pharmacol Exp Ther 252, 403-409.
38. Kawasaki H, Saito A & Takasaki K (1990c). Age-related decrease of calcitonin gene-related peptide-containing vasodilator innervation in the mesenteric resistance vessel of the spontaneously hypertensive rat. Circ Res 67, 733-743.
39. Kawasaki H & Takasaki K (1992). Age-related decrease of neurogenic release of calcitonin gene-related peptide from perivascular nerves in spontaneously hypertensive rats. Clin Exp Hypertens A 14, 989-1001.
40. Kawasaki H, Takasaki K, Saito A & Goto K (1988). Calcitonin gene-related peptide acts as a novel vasodilator neurotransmitter in mesenteric resistance vessels of the rat. Nature 335, 164-167.
41. Khurana S, Raina H, Pappas V, Raufman JP & Pallone TL (2012). Effects of deoxycholylglycine, a conjugated secondary bile acid, on myogenic tone and agonist-induced contraction in rat resistance arteries. PLoS One 7, e32006.
42. Koch DW, Newcomer SC & Proctor DN (2005). Blood flow to exercising limbs varies with age, gender, and training status. Can J Appl Physiol 30, 554-575.
43. - cotransport-dependent signaling. Purinergic Signal 5, 343-349.
44. Kreulen DL (2003). Properties of the venous and arterial innervation in the mesentery. J Smooth Muscle Res 39, 269-279.
45. Lakatta EG & Levy D (2003). Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part I: aging arteries: a "set up" for vascular disease. Circulation 107, 139-146.
46. Laurant P, Adrian M & Berthelot A (2004). Effect of age on mechanical properties of rat mesenteric small arteries. Can J Physiol Pharmacol 82, 269-275.
47. Ledoux J, Taylor MS, Bonev AD, Hannah RM, Solodushko V, Shui B, Tallini Y, Kotlikoff MI & Nelson MT (2008). Functional architecture of inositol 1, 4, 5-trisphosphate signaling in restricted spaces of myoendothelial projections. Proc Natl Acad Sci U S A 105, 9627-9632.
48. Li YJ, Song QJ & Xiao J (2000). Calcitonin gene-related peptide: an endogenous mediator of preconditioning. Acta Pharmacol Sin 21, 865-869.
49. Li Z & Duckles SP (1994). Influence of gender on vascular reactivity in the rat. J Pharmacol Exp Ther 268, 1426-1431.
50. 2+ stores enhances flow-induced vascular dilatation in rat small mesenteric artery. Br J Pharmacol 147, 506-515.
51. Long JB & Segal SS (2009). Quantifying perivascular sympathetic innervation: regional differences in male C57BL/6 mice at 3 and 20 months. J Neurosci Methods 184, 124-128.
52. Marshall JM (1982). The influence of the sympathetic nervous system on individual vessels of the microcirculation of skeletal muscle of the rat. J Physiol 332, 169-186.
53. Moore AW, Jackson WF & Segal SS (2010). Regional heterogeneity of α-adrenoreceptor subtypes in arteriolar networks of mouse skeletal muscle. J Physiol 588, 4261-4274.
54. Muller-Delp JM (2006). Aging-induced adaptations of microvascular reactivity. Microcirculation 13, 301-314.
55. Muller-Delp JM, Spier SA, Ramsey MW & Delp MD (2002). Aging impairs endothelium-dependent vasodilation in rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 283, H1662-1672.
56. 2+ signals to oppose vasoconstriction of mouse mesenteric arteries. Am J Physiol Heart Circ Physiol 302, H594-602.
57. Newman AB, Gottdiener JS, Mcburnie MA, Hirsch CH, Kop WJ, Tracy R, Walston JD, Fried LP & Group CHSR (2001). Associations of subclinical cardiovascular disease with frailty. J Gerontol A Biol Sci Med Sci 56, M158-166.
58. Ng AV, Callister R, Johnson DG & Seals DR (1993). Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension 21, 498-503.
59. Osol G, Laher I & Cipolla M (1991). Protein kinase C modulates basal myogenic tone in resistance arteries from the cerebral circulation. Circ Res 68, 359-367.
60. Rowell LB (1974). Human cardiovascular adjustments to exercise and thermal stress. Physiol Rev 54, 75-159.
61. Seals DR & Dinenno FA (2004). Collateral damage: cardiovascular consequences of chronic sympathetic activation with human aging. Am J Physiol Heart Circ Physiol 287, H1895-1905.
62. Seals DR, Jablonski KL & Donato AJ (2011). Aging and vascular endothelial function in humans. Clin Sci (Lond) 120, 357-375.
63. 2+ signals through endothelial TRPV4 channels regulate vascular function. Science 336, 597-601.
64. Sonntag WE, Lynch CD, Cooney PT & Hutchins PM (1997). Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1. Endocrinology 138, 3515-3520.
65. Sweazea KL & Walker BR (2012). Impaired myogenic tone in mesenteric arteries from overweight rats. Nutr Metab (Lond) 9, 18.
66. Takenaga M & Kawasaki H (1999). Endogenous calcitonin gene-related peptide suppresses vasoconstriction mediated by adrenergic nerves in rat mesenteric resistance blood vessels. Eur J Pharmacol 367, 239-245.
67. BAC-GCaMP2 transgenic mice. Circ Res 101, 1300-1309.
68. + channel blockers and herbimycin of acetylcholine- and flow-evoked vasodilatation in rat mesenteric small arteries. Br J Pharmacol 138, 1562-1570.
69. Urbieta-Caceres VH, Syed FA, Lin J, Zhu XY, Jordan KL, Bell CC, Bentley MD, Lerman A, Khosla S & Lerman LO (2012). Age-dependent renal cortical microvascular loss in female mice. Am J Physiol Endocrinol Metab 302, E979-986.
70. Welsh DG & Segal SS (1996). Muscle length directs sympathetic nerve activity and vasomotor tone in resistance vessels of hamster retractor. Circ Res 79, 551-559.
71. Xu KM, Tang F & Han C (1997). Alterations of mRNA levels of alpha 1-adrenoceptor subtypes with maturation and ageing in different rat blood vessels. Clin Exp Pharmacol Physiol 24, 415-417.
72. +. Am J Physiol Heart Circ Physiol 293, H152-159.
73. 2+ channel current and lowers blood pressure. Am J Physiol Heart Circ Physiol 298, H1472-1483.