Advancing age alters the expression of the ryanodine receptor 3 isoform in adult rat superior cervical ganglia

Journal of Applied Physiology

Volumn 101, Issue 2, 2006, Pages 392-400

  Vanterpool, Conwin K ^a   Vanterpool, Elaine A ^a   Pearce, William J ^a   Buchholz, John N ^a  

^a LOMA LINDA UNIVERSITY   (United States)

Author keywords

Aging; Cerebrovasculature

Indexed keywords

CALCIUM; ION CHANNEL; MESSENGER RNA; NITRIC OXIDE SYNTHASE; RYANODINE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CIRCULATION; CERVICAL SPINE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GROUPS BY AGE; HOMEOSTASIS; HYPERTENSION; MALE; MOLECULAR MECHANICS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL GANGLION; SYMPATHETIC NERVE;

AGING; ANIMALS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; MALE; NITRIC OXIDE SYNTHASE TYPE I; PROTEIN ISOFORMS; RATS; RATS, INBRED F344; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SENSITIVITY AND SPECIFICITY; SUPERIOR CERVICAL GANGLION;

EID: 33746733014     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00167.2006     Document Type: Article

References (69)

1. Abbott RD, Curb JD, Rodriguez BL, Masaki KH, Popper JS, Ross GW, and Petrovitch H. Age-related changes in risk factor effects on the incidence of thromboembolic and hemorrhagic stroke. J Clin Epidemiol 56: 479-486, 2003.
2. Anzai K, Ogawa K, Ozawa T, and Yamamoto H. Oxidative modification of ion channel activity of ryanodine receptor. Antioxid Redox Signal 2: 35-40, 2000.
3. Balshaw DM, Yamaguchi N, and Meissner G. Modulation of intracellular calcium-release channels by calmodulin. J Membr Biol 185: 1-8, 2002.
4. Brewer GJ. Neuronal plasticity and stressor toxicity during aging. Exp Gerontol 35: 1165-1183, 2000.
5. Buchholz J, Tsai H, Foucart S, and Duckles SP. Advancing age alters intracellular calcium buffering in rat adrenergic nerves. Neurobiol Aging 17: 885-892, 1996.
6. Busija DW and Heistad DD. Factors involved in the physiological regulation of the cerebral circulation. Rev Physiol Biochem Pharmacol 101: 161-211, 1984.
7. Cardinali DP and Stern JE. Peripheral neuroendocrinology of the cervical autonomic nervous system. Braz J Med Biol Res 27: 573-599, 1994.
8. Cardinali DP, Vacas MI, and Gejman PV. The sympathetic superior cervical ganglia as peripheral neuroendocrine centers. J Neural Transm 52: 1-21, 1981.
9. Cardinali DP, Vacas MI, Gejman PV, Pisarev MA, Barontini M, Boado RJ, and Juvenal GJ. The sympathetic superior cervical ganglia as "little neuroendocrine brains." Acta Physiol Lat Am 33: 205-221, 1983.
10. Chiba T and Tanaka K. A target specific pathway from nitric oxide synthase immunoreactive preganglionic sympathetic to superior cervical ganglion neurons innervating the submandibular salivary gland. J Auton Nerv Syst 71: 139-147, 1998.
11. Danila CI and Hamilton SL. Phosphorylation of ryanodine receptors. Biol Res 37: 521-525, 2004.
12. Dun NJ, Dun SL, Chiba T, and Forstermann U. Nitric oxide synthase-immunoreactive vagal afferent fibers in rat superior cervical ganglia. Neuroscience 65: 231-239, 1995.
13. Eu JP, Xu L, Stamler JS, and Meissner G. Regulation of ryanodine receptors by reactive nitrogen species. Biochem Pharmacol 57: 1079-1084, 1999.
14. Faraci FM and Heistad DD. Regulation of the cerebral circulation: role of endothelium and potassium channels. Physiol Rev 78: 53-97, 1998.
15. Faure AV, Grunwald D, Moutin MJ, Hilly M, Mauger JP, Marty I, De Waard M, Villaz M, and Albrieux M. Developmental expression of the calcium release channels during early neurogenesis of the mouse cerebral cortex. Eur J Neurosci 14: 1613-1622, 2001.
16. Ferrington DA, Krainev AG, and Bigelow DJ. Altered turnover of calcium regulatory proteins of the sarcoplasmic reticulum in aged skeletal muscle. J Biol Chem 273: 5885-5891, 1998.
17. Fill M and Copello JA. Ryanodine receptor calcium release channels. Physiol Rev 82: 893-922, 2002.
18. Fill M and Coronado R. Ryanodine receptor channel of sarcoplasmic reticulum. Trends Neurosci 11: 453-457, 1988.
19. Furuichi S, Endo S, Haji A, Takeda R, Nisijima M, and Takaku A. Related changes in sympathetic activity, cerebral blood flow and intracranial pressure, and effect of an alpha-blocker in experimental subarachnoid haemorrhage. Acta Neurochir (Wien) 141: 415-423, 1999.
20. Galione A. Cyclic ADP-ribose: a new way to control calcium. Science 259: 325-326, 1993.
21. Grunwald R and Meissner G. Lumenal sites and C terminus accessibility of the skeletal muscle calcium release channel (ryanodine receptor). J Biol Chem 270: 11338-11347, 1995.
22. Hamilton SL and Reid MB. RyR1 modulation by oxidation and calmodulin. Antioxid Redox Signal 2: 41-45, 2000.
23. Hill CE and Vidovic M. The role of competition in the refinement of the projections of sympathetic neurons to the rat eye during development. Int J Dev Neurosci 7: 539-551, 1989.
24. 2+ entry in bullfrog sympathetic neurons. Neuron 12: 1073-1079, 1994.
25. Insel PA. Adrenergic receptors, G proteins, and cell regulation: implications for aging research. Exp Gerontol 28: 341-348, 1993.
26. Jallageas M, Mas N, Saboureau M, Roussel JP, and Lacroix A. Effects of bilateral superior cervical ganglionectomy on thyroid and gonadal functions in the edible dormouse Glis glis. Comp Biochem Physiol Comp Physiol 104: 299-304, 1993.
27. 2+ cycling. Curr Opin Drug Discov Devel 6: 658-666, 2003.
28. Kihira T, Utunomiya H, and Kondo T. Expression of FKBP12 and ryanodine receptors (RyRs) in the spinal cord of MND patients. Amyotroph Lateral Scler Other Motor Neuron Disord 6: 94-99, 2005.
29. Korsching S and Thoenen H. Developmental changes of nerve growth factor levels in sympathetic ganglia and their target organs. Dev Biol 126: 40-46, 1988.
30. Larsen PJ. Tracing autonomic innervation of the rat pineal gland using viral transneuronal tracing. Microsc Res Tech 46: 296-304, 1999.
31. Larsen PJ, Enquist LW, and Card JP. Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing. Eur J Neurosci 10: 128-145, 1998.
32. Lawes CM, Bennett DA, Feigin VL, and Rodgers A. Blood pressure and stroke: an overview of published reviews. Stroke 35: 776-785, 2004.
33. 2- adrenoceptors mediate nicotine-induced NOergic neurogenic dilation in porcine basilar arteries. Am J Physiol Heart Circ Physiol 279: H808-H816, 2000.
34. Marrion NV and Adams PR. Release of intracellular calcium and modulation of membrane currents by caffeine in bull-frog sympathetic neurones. J Physiol 445: 515-535, 1992.
35. Marx SO and Marks AR. Regulation of the ryanodine receptor in heart failure. Basic Res Cardiol 97, Suppl 1: I49 -I51, 2002.
36. Mathison R, Carter L, Mowat C, Bissonnette E, Davison JS, and Befus AD. Temporal analysis of the anti-inflammatory effects of decentralization of the rat superior cervical ganglia. Am J Physiol Regul Integr Comp Physiol 266: R1537-R1543, 1994.
37. Mbaku EM, Zhang L, Pearce WJ, Duckles SP, and Buchholz J. Chronic hypoxia alters the function of NOS nerves in cerebral arteries of near-term fetal and adult sheep. J Appl Physiol 94: 724-732, 2003.
38. Mbaku EN, Zhang L, Duckles SP, and Buchholz J. Nitric-oxide synthase-containing nerves facilitate adrenergic transmitter release in sheep middle cerebral arteries. J Pharmacol Exp Ther 293: 397-402, 2000.
39. 2+ release channel. J Biol Chem 268: 13765-13768, 1993.
40. Meissner G. Regulation of mammalian ryanodine receptors. Front Biosci 7: d2072-d2080, 2002.
41. Miura M and Okada J. Cardiac and non-cardiac preganglionic neurones of the thoracic vagus nerve: an HRP study in the cat. Jpn J Physiol 31: 53-66, 1981.
42. Mori F, Fukaya M, Abe H, Wakabayashi K, and Watanabe M. Developmental changes in expression of the three ryanodine receptor mRNAs in the mouse brain. Neurosci Lett 285: 57-60, 2000.
43. Mouton J, Marty I, Villaz M, Feltz A, and Maulet Y. Molecular interaction of dihydropyridine receptors with type-1 ryanodine receptors in rat brain. Biochem J 354: 597-603, 2001.
44. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20: 389-399, 1998.
45. Ogawa Y, Kurebayashi N, and Murayama T. Putative roles of type 3 ryanodine receptor isoforms (RyR3). Trends Cardiovasc Med 10: 65-70, 2000.
46. Pessah IN and Feng W. Functional role of hyperreactive sulfhydryl moieties within the ryanodine receptor complex. Antioxid Redox Signal 2: 17-25, 2000.
47. Pottorf WJ, Duckles SP, and Buchholz JN. SERCA function declines with age in adrenergic nerves from the superior cervical ganglion. J Auton Pharmacol 20: 281-290, 2000.
48. Ramaswamy K, Mathison R, Carter L, Kirk D, Green F, Davison JS, and Befus D. Marked antiinflammatory effects of decentralization of the superior cervical ganglia. J Exp Med 172: 1819-1830, 1990.
49. Romeo HE, Gonzalez SC, Vacas MI, Rosenstein RE, Barontini M, and Cardinali DP. Origins of the sympathetic projections to rat thyroid and parathyroid glands. J Auton Nerv Syst 17: 63-70, 1986.
50. 2+-release channels. Cell Calcium 32: 307-319, 2002.
51. Sorrentino V. The ryanodine receptor family of intracellular calcium release channels. Adv Pharmacol 33: 67-90, 1995.
52. Stern JE and Cardinali DP. Influence of the autonomic nervous system on calcium homeostasis in the rat. Biol Signals 3: 15-25, 1994.
53. Stevens LM and Landis SC. Target influences on transmitter choice by sympathetic neurons developing in the anterior chamber of the eye. Dev Biol 137: 109-124, 1990.
54. Tavernarakis N and Driscoll M. Caloric restriction and lifespan: a role for protein turnover? Mech Ageing Dev 123: 215-229, 2002.
55. Toda N. Age-related changes in responses to nerve stimulation and catecholamines in isolated monkey cerebral arteries. Am J Physiol Heart Circ Physiol 260: H1443-H1448, 1991.
56. 2+ channels in rat sensory neurons. J Neurosci 17: 7404-7414, 1997.
57. 2+ stores. J Physiol 519: 115-130, 1999.
58. 2+ release in neurons. Bioessays 21: 743-750, 1999.
59. Van den Bosch L, Verhoeven K, De Smedt H, Wuytack F, Missiaen L, and Robberecht W. Calcium handling proteins in isolated spinal motoneurons. Life Sci 65: 1597-1606, 1999.
60. Vanterpool CK, Pearce WJ, and Buchholz JN. Advancing age alters rapid and spontaneous refilling of caffeine-sensitive calcium stores in sympathetic superior cervical ganglion cells. J Appl Physiol 99: 963-971, 2005.
61. Verberne ME, Gittenberger-De Groot AC, Van Iperen L, and Poelmann RE. Contribution of the cervical sympathetic ganglia to the innervation of the pharyngeal arch arteries and the heart in the chick embryo. Anat Rec 255: 407-419, 1999.
62. Vidovic M and Hill CE. Withdrawal of collaterals of sympathetic axons to the rat eye during postnatal development: the role of function. J Auton Nerv Syst 22: 57-65, 1988.
63. Waddell SC, Davison JS, Befus AD, and Mathison RD. Role for the cervical sympathetic trunk in regulating anaphylactic and endotoxic shock. J Manipulative Physiol Ther 15: 10-15, 1992.
64. Wiley LA, Rupp GR, and Steinle JJ. Sympathetic innervation regulates basement membrane thickening and pericyte number in rat retina. Invest Ophthalmol Vis Sci 46: 744-748, 2005.
65. Wingerd KL, Goodman NL, Leu ST, and Clegg DO. Expression and function of integrin alpha4beta1 and vascular cell adhesion molecule-1 (VCAM-1) during sympathetic innervation of the heart. Dev Dyn 231: 359-369, 2004.
66. Wingerd KL, Goodman NL, Tresser JW, Smail MM, Leu ST, Rohan SJ, Pring JL, Jackson DY, and Clegg DO. Alpha 4 integrins and vascular cell adhesion molecule-1 play a role in sympathetic innervation of the heart. J Neurosci 22: 10772-10780, 2002.
67. Wu SY and Dun NJ. Potentiation of IPSCs by nitric oxide in immature rat sympathetic preganglionic neurones in vitro. J Physiol 495: 479-490, 1996.
68. Yu BP, Masoro EJ, and McMahan CA. Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. J Gerontol 40: 657-670, 1985.
69. Zhang B, Fugleholm K, Day LB, Ye S, Weller RO, and Day IN. Molecular pathogenesis of subarachnoid haemorrhage. Int J Biochem Cell Biol 35: 1341-1360, 2003.