Limited intravascular coupling in the rodent brainstem and retina supports a role for glia in regional blood flow

Journal of Comparative Neurology

Volumn 511, Issue 6, 2008, Pages 773-787

  Kuo, Ivana Y ^a   Chan Ling, Tailoi ^b   Wojcikiewicz, Richard J ^c   Hill, Caryl E ^a  

^a Biology and Environment   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Astrocytes; Calcium stores; Connexins; Immunohistochemistry; IP3R

Indexed keywords

CONNEXIN 37; CONNEXIN 40; CONNEXIN 43; GLIAL FIBRILLARY ACIDIC PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; GAP JUNCTION PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; ASTROCYTE; AUDITORY BRAINSTEM; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; BRAIN CIRCULATION; BRAIN STEM; CALCIUM CELL LEVEL; CONTROLLED STUDY; ENDOTHELIUM; GLIA CELL; IMMUNOREACTIVITY; NONHUMAN; PIA ARTERY; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA; SIGNAL TRANSDUCTION; WISTAR RAT; ANIMAL; BASILAR ARTERY; CALCIUM SIGNALING; CBA MOUSE; CELL JUNCTION; CYTOLOGY; FEMALE; MALE; METABOLISM; MICROCIRCULATION; MOUSE; PHYSIOLOGY; PIA MATER; RETINA ARTERY; SPECIES DIFFERENCE; SYNAPTIC TRANSMISSION; ULTRASTRUCTURE; VASCULARIZATION; VASODILATATION;

ANIMALS; ARTERIOLES; ASTROCYTES; BASILAR ARTERY; BRAIN STEM; CALCIUM SIGNALING; CEREBROVASCULAR CIRCULATION; CONNEXINS; FEMALE; GAP JUNCTIONS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MALE; MICE; MICE, INBRED CBA; MICROCIRCULATION; PIA MATER; RATS; RATS, WISTAR; RETINAL ARTERY; SPECIES SPECIFICITY; SYNAPTIC TRANSMISSION; VASODILATION;

EID: 58749105837     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21873     Document Type: Article

References (56)

1. Armstrong ML, Dua AK, Murrant CL. 2007. Potassium initiates vasodilatation induced by a single skeletal muscle contraction in hamster cremaster muscle. J Physiol 581:841-852.
2. Bushong EA, Martone ME, Jones YZ, Ellisman MH. 2002. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192.
3. Ceelen PW, Lockridge A, Newman EA. 2001. Electrical coupling between glial cells in the rat retina. Glia 35:1-13.
4. Chan-Ling T. 1997. Glial, vascular, and neuronal cytogenesis in whole-mounted cat retina. Microsc Res Tech 36:1-16.
5. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ. 1990. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247:470-473.
6. Cotrina ML, Nedergaard M. 2005. Intracellular calcium control mechanisms in glia. In: Kettenmann H, Ransom B, editors. Neuroglia, 2nd ed. Oxford: Oxford University Press. p 229-239.
7. de Wit C, Roos F, Bolz SS, Kirchhoff S, Kruger O, Willecke K, Pohl U. 2000. Impaired conduction of vasodilation along arterioles in connexin40-deficient mice. Circ Res 86:649-655.
8. Diep HK, Vigmond EJ, Segal SS, Welsh DG. 2005. Defining electrical communication in skeletal muscle resistance arteries: a computational approach. J Physiol 568:267-281.
9. Dietrich HH, Kajita Y, Dacey RG, Jr. 1996. Local and conducted vasomotor responses in isolated rat cerebral arterioles. Am J Physiol 271:H1109-1116.
10. Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, Dong X, Chen J, McCarthy KD. 2007. Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54:611-626.
11. Figueroa XF, Paul DL, Simon AM, Goodenough DA, Day KH, Damon DN, Duling BR. 2003. Central role of connexin40 in the propagation of electrically activated vasodilation in mouse cremasteric arterioles in vivo. Circ Res 92:793-800.
12. Filosa JA, Bonev AD, Nelson MT. 2004. Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ Res 95: e73-81.
13. Foskett JK, White C, Cheung KH, Mak DO. 2007. Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87:593-658.
14. Girouard H, Iadecola C. 2006. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100:328-335.
15. Grayson TH, Haddock RE, Murray TP, Wojcikiewicz RJ, Hill CE. 2004. Inositol 1,4,5-trisphosphate receptor subtypes are differentially distributed between smooth muscle and endothelial layers of rat arteries. Cell Calcium 36:447-458.
16. Harder DR, Alkayed NJ, Lange AR, Gebremedhin D, Roman RJ. 1998. Functional hyperemia in the brain: hypothesis for astrocyte-derived vasodilator metabolites. Stroke 29:229-234.
17. Hill CE, Phillips JK, Sandow SL. 2001. Heterogeneous control of blood flow among different vascular beds. Med Res Rev 21:1-60.
18. Hollander H, Makarov F, Dreher Z, van Driel D, Chan-Ling TL, Stone J. 1991. Structure of the macroglia of the retina: sharing and division of labour between astrocytes and Muller cells. J Comp Neurol 313:587-603.
19. Holtzclaw LA, Pandhit S, Bare DJ, Mignery GA, Russell JT. 2002. Astrocytes in adult rat brain express type 2 inositol 1,4,5-trisphosphate receptors. Glia 39:69-84.
20. Horiuchi T, Dietrich HH, Hongo K, Dacey RG, Jr. 2002. Mechanism of extracellular K+-induced local and conducted responses in cerebral penetrating arterioles. Stroke 33:2692-2699.
21. Houades V, Koulakoff A, Ezan P, Seif I, Giaume C. 2008. Gap junction-mediated astrocytic networks in the mouse barrel cortex. J Neurosci 28:5207-5217.
22. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, Nedergaard M. 2008. Connexin 43 hemichannels are permeable to ATP. J Neurosci 28:4702-4711.
23. Kruger O, Plum A, Kim JS, Winterhager E, Maxeiner S, Hallas G, Kirchhoff S, Traub O, Lamers WH, Willecke K. 2000. Defective vascular development in connexin 45-deficient mice. Development (Cambridge Eng) 127:4179-4193.
24. Li X, Simard JM. 2001. Connexin45 gap junction channels in rat cerebral vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 281: H1890-1898.
25. Metea MR, Newman EA. 2006. Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26: 2862-2870.
26. Morel JL, Fritz N, Lavie JL, Mironneau J. 2003. Crucial role of type 2 inositol 1,4,5-trisphosphate receptors for acetylcholine-induced. Ca2+ oscillations in vascular myocytes. Arterioscler Thromb Vasc Biol 23: 1567-1575.
27. Mulligan SJ, MacVicar BA. 2004. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431:195-199.
28. Nagy JI, Patel D, Ochalski PA, Stelmack GL. 1999. Connexin30 in rodent, cat and human brain: selective expression in gray matter astrocytes, co-localization with connexin43 at gap junctions and late developmental appearance. Neuroscience 88:447-468.
29. Nagy JI, Li X, Rempel J, Stelmack G, Patel D, Staines WA, Yasumura T, Rash JE. 2001. Connexin26 in adult rodent central nervous system: demonstration at astrocytic gap junctions and colocalization with connexin30 and connexin43. J Comp Neurol 441:302-323.
30. Newman EA. 2001. Propagation of intercellular calcium waves in retinal astrocytes and Muller cells. J Neurosci 21:2215-2223.
31. Newman EA. 2003. Glial cell inhibition of neurons by release of ATP. J Neurosci 23:1659-1666.
32. Newman EA. 2005. Calcium increases in retinal glial cells evoked by light-induced neuronal activity. J Neurosci 25:5502-5510.
33. Ngai AC, Winn HR. 2002. Pial arteriole dilation during somatosensory stimulation is not mediated by an increase in CSF metabolites. Am J Physiol Heart Circ Physiol 282:H902-907.
34. Paul ER, Christian AL, Franke R, Groschel-Stewart U. 1994. Embryonic chicken gizzard: smooth muscle and non-muscle myosin isoforms. Cell Tissue Res 276:381-386.
35. Peppiatt CM, Howarth C, Mobbs P, Attwell D. 2006. Bidirectional control of CNS capillary diameter by pericytes. Nature 443:700-704.
36. Rummery NM, Hill CE. 2004. Vascular gap junctions and implications for hypertension. Clin Exp Pharmacol Physiol 31:659-667.
37. Rummery NM, Hickey H, McGurk G, Hill CE. 2002. Connexin37 is the major connexin expressed in the media of caudal artery. Arterioscler Thromb Vasc Biol 22:1427-1432.
38. Rummery NM, Grayson TH, Hill CE. 2005. Angiotensin-converting enzyme inhibition restores endothelial but not medial connexin expression in hypertensive rats. J Hypertens 23:317-328.
39. Satzler K, Sohl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B, Lubke JH. 2002. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22:10567-10579.
40. Scemes E. 2000. Components of astrocytic intercellular calcium signaling. Mol Neurobiol 22:167-179.
41. Segal SS. 2005. Regulation of blood flow in the microcirculation. Microcirculation 12:33-45.
42. Segal SS, Welsh DG, Kurjiaka DT. 1999. Spread of vasodilatation and vasoconstriction along feed arteries and arterioles of hamster skeletal muscle. J Physiol 516:283-291.
43. Sharp AH, Nucifora FC, Jr., Blondel O, Sheppard CA, Zhang C, Snyder SH, Russell JT, Ryugo DK, Ross CA. 1999. Differential cellular expression of isoforms of inositol 1,4,5-triphosphate receptors in neurons and glia in brain. J Comp Neurol 406:207-220.
44. Soulsby MD, Wojcikiewicz RJ. 2007. Calcium mobilization via type III inositol 1,4,5-trisphosphate receptors is not altered by PKA-mediated phosphorylation of serines 916, 934, and 1832. Cell Calcium 42:261-270.
45. Spray DC, Ye ZC, Ransom BR. 2006. Functional connexin "hemichannels": a critical appraisal. Glia 54:758-773.
46. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M. 2006. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9:260-267.
47. Taylor CW, Laude AJ. 2002. IP3 receptors and their regulation by calmodulin and cytosolic Ca2+. Cell Calcium 32:321-334.
48. Wagner AJ, Holstein-Rathlou NH, Marsh DJ. 1997. Internephron coupling by conducted vasomotor responses in normotensive and spontaneously hypertensive rats. Am J Physiol 272:F372-379.
49. Wojcikiewicz RJ. 1995. Type I, II, and III inositol 1,4,5-trisphosphate receptors are unequally susceptible to down-regulation and are expressed in markedly different proportions in different cell types. J Biol Chem 270:11678-11683.
50. Wojcikiewicz RJ, Luo SG. 1998. Differences among type I, II, and III inositol-1,4,5-trisphosphate receptors in ligand-binding affinity influence the sensitivity of calcium stores to inositol-1,4,5-trisphosphate. Mol Pharmacol 53:656-662.
51. Wolfle SE, Schmidt VJ, Hoepfl B, Gebert A, Alcolea S, Gros D, de Wit C. 2007. Connexin45 cannot replace the function of connexin40 in conducting endothelium-dependent dilations along arterioles. Circ Res 101:1292-1299.
52. Xu HL, Mao L, Ye S, Paisansathan C, Vetri F, Pelligrino DA. 2008. Astrocytes are a key conduit for upstream signaling of vasodilation during cerebral cortical neuronal activation in vivo. Am J Physiol Heart Circ Physiol 294:H622-632.
53. Yamamoto-Hino M, Miyawaki A, Kawano H, Sugiyama T, Furuichi T, Hasegawa M, Mikoshiba K. 1995. Immunohistochemical study of inositol 1,4,5-trisphosphate receptor type 3 in rat central nervous system. Neuroreport 6:273-276.
54. Yamamoto Y, Klemm MF, Edwards FR, Suzuki H. 2001. Intercellular electrical communication among smooth muscle and endothelial cells in guinea-pig mesenteric arterioles. J Physiol 535:181-195.
55. Zahs KR, Kofuji P, Meier C, Dermietzel R. 2003. Connexin immunoreactivity in glial cells of the rat retina. J Comp Neurol 455:531-546.
56. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G. 2003. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50.