Maturation and long-term hypoxia alters Ca2+-induced Ca 2+ release in sheep cerebrovascular sympathetic neurons

Journal of Applied Physiology

Volumn 107, Issue 4, 2009, Pages 1223-1234

  Behringer, Erik J ^a   Leite, Laura D ^b   Buchholz, Nickolaus E ^a   Keeney, Michael G ^a   Pearce, William J ^a   Vanterpool, Conwin K ^c   Wilson, Sean M ^a   Buchholz, John N ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^c ALABAMA A AND M UNIVERSITY   (United States)

Author keywords

Electric field stimulation evoked calcium transients; Function of superior cervical ganglia; Intracellular calcium release; Intracellular calcium stores; Sympathetic development

Indexed keywords

CAFFEINE; CALCIUM ION; NITRIC OXIDE SYNTHASE; RYANODINE RECEPTOR 2; RYANODINE RECEPTOR 3; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ARTICLE; BRAIN BLOOD VESSEL; BRAIN MATURATION; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROSTIMULATION; FETUS; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHEEP; SMOOTH ENDOPLASMIC RETICULUM; SUPERIOR CERVICAL GANGLION; SYMPATHETIC NERVE CELL;

AGE FACTORS; AGING; ANIMALS; ANOXIA; CAFFEINE; CALCIUM; CALCIUM SIGNALING; CEREBRAL ARTERIES; CYCLIC ADP-RIBOSE; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ENZYME INHIBITORS; FETAL HYPOXIA; INDOLES; NITRIC OXIDE SYNTHASE TYPE I; RYANODINE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SHEEP; SUPERIOR CERVICAL GANGLION; SYMPATHETIC FIBERS, POSTGANGLIONIC; TIME FACTORS;

EID: 70350111329     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00363.2009     Document Type: Article

References (57)

1. Behringer EJ, Vanterpool CK, Pearce WJ, Wilson SM, Buchholz JN. Advancing age alters the contribution of calcium release from smooth endoplasmic reticulum stores in superior cervical ganglion. J Gerontol Biol Sci Med Sci 64A: 34-44, 2009.
2. Blood AB, Tiso M, Verma ST, Lo J, Joshi MS, Azarov I, Longo LD, Gladwin MT, Kim-Shapiro DB, Power GG. Increased nitrite reductase activity of fetal versus adult ovine hemoglobin. Am J Physiol Heart Circ Physiol 296: H237-H246, 2009.
3. Bowers CW, Zigmond RE. Localization of neurons in the rat superior cervical ganglion that project into different postganglionic trunks. J Comp Neurol 185: 381-391, 1979.
4. 2+ entry in vascular smooth muscle cells. J Pharmacol Exp Ther 317: 488-499, 2006.
5. Buchholz J, Teunissen KE, Duckles SP. Impact of development and chronic hypoxia on NE release from adrenergic nerves in sheep arteries. Am J Physiol Regul Integr Comp Physiol 276: R799-R808, 1999. (Pubitemid 29157510)
6. 2-adrenoceptor function in vascular adrenergic nerves of adult and fetal sheep. Am J Physiol Regul Integr Comp Physiol 281: R926-R934, 2001.
7. 2+ homeostasis in peripheral neurones: Implications for changes in function. Aging Cell 6: 285-296, 2007.
8. Cardinali DP, Vacas MI, Gejman PV, Pisarev MA, Barontini M, Boado RJ, Juvenal GJ. The sympathetic superior ganglia as "little neuroendocrine brains". Acta Physiol Latinoam 33: 205-221, 1983.
9. Cassaglia PA, Griffiths RI, Walker AM. Sympathetic nerve acitivity in the superior cervical ganglia increases in response to imposed increases in arterial pressure. Am J Physiol Regul Integr Comp Physiol 294: R1255-R1261, 2008.
10. 2+ current inhibition in rat sympathetic neurons. J Physiol 482: 521-531, 1995.
11. Choi S, Weisenberg SN, Kellogg CK. Control of endogenous norepinephrine release in the hypothalamus of male rats changes over adolescent development. Brain Res Dev Brain Res 98: 134-141, 1997. (Pubitemid 27033661)
12. Clementi E, Riccio M, Sciorati C, Nistico G, Meldolesi J. The type 2 ryanodine receptor of neurosecretory PC12 cells is activated by cyclic ADP-ribose. J Biol Chem 271: 17739-17745, 1996.
13. Faure AV, Grunwald D, Moutin MJ, Hilly M, Mauger JP, Marty I, De WM, Villaz M, Albrieux M. Developmental expression of the calcium release channels during early neurogenesis of the mouse cerebral cortex. Eur J Neurosci 14: 1613-1622, 2001. (Pubitemid 35478030)
14. Fill M, Copello JA. Ryanodine receptor calcium release channels. Physiol Rev 82: 893-922, 2002.
15. 2+ regulatory network in intact cells. Trends Neurosci 31: 8-19, 2008.
16. i. J Physiol 450: 217-246, 1992.
17. Furuichi S, Endo S, Haji A, Takeda R, Nisijima M, Takaku A. Related changes in sympathetic nerve activity, cerebral blood flow and intracranial pressure, and effect of an α-blocker in experimental subarachnoid hemmorhage. Acta Neurochir (Wien) 141: 415-424, 1999. (Pubitemid 29192191)
18. Galante M, Marty A. Presynaptic ryanodine-sensitive calcium stores contribute to evoked neurotransmitter release at the basket cell purkinje cell synapse. J Neurosci 23: 11229-11234, 2003. (Pubitemid 37548959)
19. Gleed RD, Poore ER, Figueroa JP, Nathanielsz PW. Modification of maternal and fetal oxygenation with the use of tracheal gas infusion. Am J Obstet Gynecol 155: 429-435, 1986.
20. Graeff R, Lee HC. A novel cycling assay for cellular cADP-ribose with nanomolar sensitivity. Biochem J 361: 379-1284, 2002. (Pubitemid 34174505)
21. Grunwald R, Meissner G. Lumenal sites and C terminus accessibility of the skeletal muscle calcium release channel (ryanodine receptor). J Biol Chem 270: 11338-111247, 1995.
22. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
23. Hainsworth R, Drinkhill MJ, Rivera-Chira M. The autonomic nervous system at high altitude. Clin Auton Res 17: 13-19, 2007. (Pubitemid 46255148)
24. Hamel E. Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100: 1059-1064, 2006. (Pubitemid 43671565)
25. Kamitomo M, Longo LD, Gilbert RD. Right and left ventricular function in fetal sheep exposed to long-term high-altitude hypoxemia. Am J Physiol Heart Circ Physiol 262: H399-H405, 1992.
26. Lee HC. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol Rev 37: 1133-1164, 1997. (Pubitemid 27459581)
27. Longo LD, Hull AD, Long DM, Pearce WJ. Cerebrovascular adaptations to high-altitude hypoxemia in fetal and adult sheep. Am J Physiol Regul Integr Comp Physiol 264: R65-R72, 1993.
28. Longo LD, Pearce WJ. Fetal cerebrovascular acclimitization responses to high-altitude, long-term hypoxia: a model for prenatal programming of adult disease? Am J Physiol Regul Integr Comp Physiol 288: R16-R24, 2005.
29. Lu S, Gu X, Hoestje S, Epner DE. Identification of an additional hypoxia responsive element in the glyceraldehyde-3-phosphate dehydrogenase gene promoter. Biochim Biophys Acta 1574: 152-156, 2002. (Pubitemid 34304326)
30. Marks AR. Ryanodine receptors/calcium release channels in heart failure and sudden cardiac death. J Mol Cell Cardiol 33: 615-624, 2001. (Pubitemid 32538975)
31. Mbaku EN, Zhang L, Duckles SP, Buchholz JN. Nitric oxide synthase-containing nerves facilitate adrenergic transmitter release in sheep middle cerebral arteries. J Pharmacol Exp Ther 293: 397-402, 2000. (Pubitemid 30244087)
32. Mbaku EN, Zhang L, Pearce WJ, Duckles SP, 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. (Pubitemid 36158252)
33. Messutat S, Heine M, Wicher D. Calcium-induced calcium release in neurosecretory insect neurons: fast and slow responses. Cell Calcium 30: 199-211, 2001. (Pubitemid 32785533)
34. Mori F, Fukaya M, Abe H, Wakabayashi K, Watanabe M. Developmental changes in expression of the three ryanodine receptor mRNAs in the mouse brain. Neurosci Lett 285: 57-60, 2000. (Pubitemid 30224623)
35. Murchison D, Griffith WH. Increased calcium buffering in basal forebrain neurons during aging. J Neurophysiol 80: 350-364, 1998. (Pubitemid 28326268)
36. 2+ channels to ryanodine receptors at presynaptic terminals. Amplification of exocytosis and plasticity. J Gen Physiol 115: 519-532, 2000.
37. Negulescu PA, Machen TE. Intracellular ion activities and membrane transport in parietal cells measured with fluorescent dyes. Methods Enzymol 192: 38-81, 1990.
38. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20: 389-399, 1998.
39. Pearce WJ, Duckles SP, Buchholz J. Effects of maturation on adrenergic neurotransmission in ovine cerebral arteries. Am J Physiol Regul Integr Comp Physiol 277: R931-R937, 1999. (Pubitemid 29525944)
40. Pei JM, Kravtsov GM, Wu S, Das R, Fung ML, Wong TM. Calcium homeostasis in rat cardiomyocytes during chronic hypoxia: a time course study. Am J Physiol Cell Physiol 285: C1420-C1428, 2003. (Pubitemid 37429616)
41. Pottorf WJ, Duckles SP, Buchholz JN. Adrenergic nerves compensate for a decline in calcium buffering during ageing. J Auton Pharmacol 20: 1-13, 2000.
42. Rittenhouse AR, Zigmond RE. Role of N- and L-type calcium channels in depolarization-induced activation of tyrosine hydroxylase and release of norepinephrine by sympathetic cell bodies and nerve terminals. J Neurobiol 40: 137-148, 1999.
43. Said HM, Hagemann C, Stojic J, Schoemig B, Vince GH, Flentje M, Roosen K, Vordermark D. GAPDH is not regulated in human glioblastoma under hypoxic conditions. BMC Mol Biol 8: 55, 2007. (Pubitemid 47074149)
44. Scheerlinck JP, Snibson KJ, Bowles VM, Sutton P. Biomedical applications of sheep models: from asthma to vaccines. Trends Biotechnol 26: 259-266, 2008.
45. Smith AB, Cunnane TC. Ryanodine-sensitive calcium stores involved in neurotransmitter release from sympathetic nerve terminals of the guineapig. J Physiol 497: 657-664, 1996.
46. Smith PK, Krohn RI, Harmanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk D. Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85, 1985.
47. Teschemacher AG. Real-time measurements of noradrenaline release in periphery and central nervous system. Autonom Neurosci Basic Clin 117: 1-8, 2005. (Pubitemid 40037855)
48. Tsai H, Pottorf WJ, Buchholz JN, Duckles SP. Adrenergic nerve smooth endoplasmic reticulum calcium buffering declines with age. Neurobiol Aging 19: 89-96, 1998. (Pubitemid 28167801)
49. 2+ release. J Neurophysiol 92: 135-143, 2004.
50. 2+ channels in rat sensory neurons. J Neurosci 17: 7404-7414, 1997.
51. 2+ release in neurons. Bioessays 21: 743-750, 1999.
52. Vanterpool CK, Pearce WJ, 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.
53. Vanterpool CK, Vanterpool EA, Pearce WJ, Buchholz JN. Advancing age alters the expression of ryanodine receptor 3 isoform in adult rat superior cervical ganglia. J Appl Physiol 101: 392-400, 2006.
54. Wagerle LC, Heffernan TM, Sacks LM, Delivoria-Papadopoulos M. Sympathetic effect on cerebral blood flow regulation in hypoxic newborn lambs. Am J Physiol Heart Circ Physiol 245: H487-H494, 1983.
55. Wagerle LC, Kurth CD, Roth RA. Sympathetic reactivity of cerebral arteries in the developing fetal lamb and adult sheep. Am J Physiol Heart Circ Physiol 258: H1432-H1438, 1990.
56. Wilfinger WW, Mackey K, Chomcynski P. Effect of pH and ionic strength on the spectrophotometric assessment of nucleic acid purity. Biotechniques 22: 474-481, 1997. (Pubitemid 27131043)
57. 2+ signaling in mediating endothelial nitric oxide production in bovine coronary arteries. Am J Physiol Heart Circ Physiol 290: H1172-H1181, 2006.