Rapid manifestation of reactive astrogliosis in acute hippocampal brain slices

GLIA

Volumn 62, Issue 1, 2014, Pages 78-95

  Takano, Takahiro ^a   He, Wei ^a   Han, Xiaoning ^a   Wang, Fushun ^a   Xu, Qiwu ^a   Wang, Xiaohai ^a   Oberheim Bush, Nancy Ann ^a   Cruz, Nancy ^b   Dienel, Gerald A ^b   Nedergaard, Maiken ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Astrohcytes; Electron microscopy; Interstitial space; Mitochondria; NADH; Purinergic receptors; Two photon microscopy

Indexed keywords

CALCIUM; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE RECEPTOR 5; GREEN FLUORESCENT PROTEIN; NESTIN; PURINERGIC RECEPTOR; STRUCTURAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN SLICE; CALCIUM SIGNALING; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GLYCOGEN ANALYSIS; HIPPOCAMPUS; IMMUNOELECTRON MICROSCOPY; IN VIVO STUDY; MITOCHONDRIAL VOLUME; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ASTROHCYTES; ELECTRON MICROSCOPY; INTERSTITIAL SPACE; MITOCHONDRIA; NADH; PURINERGIC RECEPTORS; TWO-PHOTON MICROSCOPY;

ANIMALS; ANIMALS, NEWBORN; AQUAPORIN 4; ASTROCYTES; CALCIUM; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; GLYCOGEN; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; LACTIC ACID; MALE; MICE; NAD; QUATERNARY AMMONIUM COMPOUNDS;

EID: 84888138943     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22588     Document Type: Article

References (75)

1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H. 2009. Purinergic signalling in the nervous system: An overview. Trends Neurosci 32:19-29.
2. Agulhon C, Petravicz J, McMullen AB, Sweger EJ, Minton SK, Taves SR, Casper KB, Fiacco TA, McCarthy KD. 2008. What is the role of astrocyte calcium in neurophysiology? Neuron 59:932-946.
3. Aitken PG, Breese GR, Dudek FF, Edwards F, Espanol MT, Larkman PM, Lipton P, Newman GC, Nowak TS Jr, Panizzon KL, Raley-Susman KM, Reid KH, Rice ME, Sarvey JM, Schoepp DD, Segal M, Taylor CP, Teyler TJ, Voulalas PJ. 1995. Preparative methods for brain slices: A discussion. J Neurosci Methods 59:139-149.
4. Allen NJ, Barres BA. 2009. Neuroscience: Glia-More than just brain glue. Nature 457:675-677.
5. Ball KK, Gandhi GK, Thrash J, Cruz NF, Dienel GA. 2007. Astrocytic connexin distributions and rapid, extensive dye transfer via gap junctions in the inferior colliculus: Implications for [(14)C]glucose metabolite trafficking. J Neurosci Res 85:3267-3283.
6. Bekar L, Libionka W, Tian GF, Xu Q, Torres A, Wang X, Lovatt D, Williams E, Takano T, Schnermann J, Bakos R, Nedergaard M. 2008. Adenosine is crucial for deep brain stimulation-mediated attenuation of tremor. Nat Med 14:75-80.
7. Booth RF, Patel TB, Clark JB. 1980. The development of enzymes of energy metabolism in the brain of a precocial (guinea pig) and non-precocial (rat) species. J Neurochem 34:17-25.
8. Brown TH, Chapman PF, Kairiss EW, Keenan CL. 1988. Long-term synaptic potentiation. Science 242:724-728.
9. Clarke SR, Shetty AK, Bradley JL, Turner DA. 1994. Reactive astrocytes express the embryonic intermediate neurofilament nestin. Neuroreport 5:1885-1888.
10. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M. 1998. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci U S A 95:15735-15740.
11. Cruz NF, Dienel GA. 2002. High glycogen levels in brains of rats with minimal environmental stimuli: Implications for metabolic contributions of working astrocytes. J Cereb Blood Flow Metab 22:1476-1489.
12. Dermietzel R, Traub O, Hwang TK, Beyer E, Bennett MV, Spray DC, Willecke K. 1989. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc Natl Acad Sci U S A 86:10148-10152.
13. Dienel GA. 2012. Fueling and imaging brain activation. ASN Neuro 4:e00093.
14. Dienel GA, Wang RY, Cruz NF. 2002. Generalized sensory stimulation of conscious rats increases labeling of oxidative pathways of glucose metabolism when the brain glucose-oxygen uptake ratio rises. J Cereb Blood Flow Metab 22:1490-1502.
15. Dodt HU, Zieglgansberger W. 1990. Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy. Brain Res 537:333-336.
16. Duchen MR, Szabadkai G. 2010. Roles of mitochondria in human disease. Essays Biochem 47:115-137.
17. Edwards FA, Konnerth A, Sakmann B, Takahashi T. 1989. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch 414:600-612.
18. Fiala JC, Kirov SA, Feinberg MD, Petrak LJ, George P, Goddard CA, Harris KM. 2003. Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro. J Comp Neurol 465:90-103.
19. Franke H, Verkhratsky A, Burnstock G, Illes P. 2012. Pathophysiology of astroglial purinergic signalling. Purinergic Signal 8:629-657.
20. Galic MA, Riazi K, Pittman QJ. 2012. Cytokines and brain excitability. Front Neuroendocrinol 33:116-125.
21. Gibbs ME, Anderson DG, Hertz L. 2006. Inhibition of glycogenolysis in astrocytes interrupts memory consolidation in young chickens. Glia 54:214-222.
22. Guthrie PB, Knappenberger J, Segal M, Bennett MV, Charles AC, Kater SB. 1999. ATP released from astrocytes mediates glial calcium waves. J Neurosci 19:520-528.
23. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D. 2006. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9:1512-1519.
24. Hertz L, Peng L, Dienel GA. 2007. Energy metabolism in astrocytes: High rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27:219-249.
25. Hom JR, Gewandter JS, Michael L, Sheu SS, Yoon Y. 2007. Thapsigargin induces biphasic fragmentation of mitochondria through calcium-mediated mitochondrial fission and apoptosis. J Cell Physiol 212:498-508.
26. Huang C, Han X, Li X, Lam E, Peng W, Lou N, Torres A, Yang M, Garre JM, Tian GF Bennett MV, Nedergaard M, Takano T. 2012. Critical role of connexin 43 in secondary expansion of traumatic spinal cord injury. J Neurosci 32:3333-3338.
27. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M. 2012. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 4:147ra111.
28. Kaneko Y, Tajiri N, Yu S, Hayashi T, Stahl CE, Bae E, Mestre H, Franzese N, Rodrigues A Jr, Rodrigues MC, Ishikawa H, Shinozuka K, Hethorn W, Weinbren N, Glover LE, Tan J, Achyuta AH, van Loveren H, Sanberg PR, Shivsankar S, Borlongan CV. 2012. Nestin overexpression precedes caspase-3 upregulation in rats exposed to controlled cortical impact traumatic brain injury. Cell Med 4:55-63.
29. Kang J, Jiang L, Goldman SA, Nedergaard M. 1998. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683-692.
30. Kasischke KA, Lambert EM, Panepento B, Sun A, Gelbard HA, Burgess RW, Foster TH, Nedergaard M. 2011. Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions. J Cereb Blood Flow Metab 31:68-81.
31. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW. 2004. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103.
32. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. 2011. Physiology of microglia. Physiol Rev 91:461-553.
33. Kimelberg HK. 2007. Supportive or information-processing functions of the mature protoplasmic astrocyte in the mammalian CNS? A critical appraisal. Neuron Glia Biol 3:181-189.
34. Knull HR, Khandelwal RL. 1982. Glycogen metabolizing enzymes in brain. Neurochem Res 7:1307-1317.
35. Koizumi S, Ohsawa K, Inoue K, Kohsaka S. 2013. Purinergic receptors in microglia: Functional modal shifts of microglia mediated by P2 and P1 receptors. Glia 61:47-54.
36. Langmoen I, Anderson P. 1981. The hippocampal slice in vitro. A description of the technique and some examples of the opportunities it offers. In: Kerkut GA, Wheal HV, editors. Electrophysiology of Isolated Mammalian CNS Preparations. New York: Academic Press. pp 51-105.
37. Li Y, Chopp M. 1999. Temporal profile of nestin expression after focal cerebral ischemia in adult rat. Brain Res 838:1-10.
38. Liem RK, Messing A. 2009. Dysfunctions of neuronal and glial intermediate filaments in disease. J Clin Invest 119:1814-1824.
39. Lin JH, Lou N, Kang N, Takano T, Hu F, Han X, Xu Q, Lovatt D, Torres A, Willecke K, Yang J, Kang J, Nedergaard M. 2008. A central role of connexin 43 in hypoxic preconditioning. J Neurosci 28:681-695.
40. Lipton P. 1989. Regulation of glycogen in the dentate gyrus of the in vitro guinea pig hippocampus; effect of combined deprivation of glucose and oxygen. J Neurosci Methods 28:147-154.
41. Lipton, P, Aitken PG, Dudek FE, Eskessen K, Espanol MT, Ferchmin PA, Kelly JB, Kreisman NR, Landfield PW, Larkman PM, Leybaert L, Newman GC, Panizzon KL, Payne RS, Phillips P, Raley-Susman KM, Rice ME, Santamaria R, Sarvey JM, Schurr A, Segal M, Sejer V, Taylor CP, Teyler TJ, Vasilenko VY, Veregge S, Wu SH, Wallis R. 1995. Making the best of brain slices: comparing preparative methods. J Neurosci Methods 59:151-156.
42. Llano I, Marty A, Johnson JW, Ascher P, Gahwiler BH. 1988. Patch-clamp recording of amino acid-activated responses in organotypic slice cultures. Proc Natl Acad Sci U S A 85:3221-3225.
43. Lovatt D, Sonnewald U, Waagepetersen HS, Schousboe A, He W, Lin JH, Han X, Takano T, Wang S, Sim FJ, Goldman SA, Nedergaard M. 2007. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 27:12255-12266.
44. Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP. 2010. The perivascular astroglial sheath provides a complete covering of the brain microvessels: An electron microscopic 3D reconstruction. Glia 58:1094-1103.
45. Nakase T, Yoshida Y, Nagata K. 2006. Enhanced connexin 43 immunoreactivity in penumbral areas in the human brain following ischemia. Glia 54:369-375.
46. Nedergaard M, Verkhratsky A. 2012. Artifact versus reality-How astrocytes contribute to synaptic events. Glia 60:1013-1023.
47. Neher E, Sakmann B. 1976. Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260:799-802.
48. Nicholson C. 1992. Quantitative analysis of extracellular space using the method of TMA+ iontophoresis and the issue of TMA+ uptake. Can J Physiol Pharmacol 70(Suppl S3):14-22.
49. Nicholson C, Kamali-Zare P, Tao L. 2011. Brain extracellular space as a diffusion barrier. Comput Visual Sci 14:309-325.
50. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. 1997. Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171-180.
51. Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M. 2009. Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276-3287.
52. Oberheim NA, Tian GF, Han X, Peng W, Takano T, Ransom B, Nedergaard M. 2008. Loss of astrocytic domain organization in the epileptic brain. J Neurosci 28:3264-3276.
53. Peters A, Palay SL, Webster HD. 1991. The fine structure of the nervous system: Neurons and their supporting cells. New York: Oxford University Press.
54. Pfeiffer B, Buse E, Meyermann R, Rocha MJ, Hamprecht B. 1993. Glycogen phosphorylase activity and immunoreactivity during pre- and postnatal development of rat brain. Histochemistry 100:265-270.
55. Ransohoff RM, Engelhardt B. 2012. The anatomical and cellular basis of immune surveillance in the central nervous system. Nat Rev Immunol 12:623-635.
56. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, Rothstein JD. 2007. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci 27:6607-6619.
57. Richard CD. 1981. The preparation of brain tissue slices for electrophysiological studies. In: Kerkut GA, Wheal HV, editors. Electrophysiology of isolated mammalian CNS preparations. New York: Academic Press. pp 107-132.
58. Sarvey JM, Burgard EC, Decker G. 1989. Long-term potentiation: Studies in the hippocampal slice. J Neurosci Methods 28:109-124.
59. Schwartzkroin PA, Wester K. 1975. Long-lasting facilitation of a synaptic potential following tetanization in the in vitro hippocampal slice. Brain Res 89:107-119.
60. Sigworth FJ, Neher E. 1980. Single Na+ channel currents observed in cultured rat muscle cells. Nature 287:447-449.
61. Skrede K, Westgaard R. 1971. The transverse hippocampal slice: A well-defined cortical structure maintained in vitro. Brain Res Bull 5:391-403.
62. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
63. Sun W, McConnell E, Pare JF, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M. 2013. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339:197-200.
64. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, Alberini CM. 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810-823.
65. Sykova E, Nicholson C. 2008. Diffusion in brain extracellular space. Physiol Rev 88:1277-1340.
66. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M. 2007. Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754-762.
67. Torres A, Wang F, Xu Q, Fujita T, Dobrowolski R, Willecke K, Takano T, Nedergaard M. 2012. Extracellular Ca(2)(+) acts as a mediator of communication from neurons to glia. Sci Signal 5:ra8.
68. Tulapurkar ME, Zundorf G, Reiser G. 2006. Internalization and desensitization of a green fluorescent protein-tagged P2Y nucleotide receptor are differently controlled by inhibition of calmodulin-dependent protein kinase II. J Neurochem 96:624-634.
69. VanSlyke JK, Musil LS. 2005. Cytosolic stress reduces degradation of connexin43 internalized from the cell surface and enhances gap junction formation and function. Mol Biol Cell 16:5247-5257.
70. Verkhratsky A, Sofroniew MV, Messing A, deLanerolle NC, Rempe D, Rodriguez JJ, Nedergaard M. 2012. Neurological diseases as primary gliopathies: A reassessment of neurocentrism. ASN Neuro 5:e00082.
71. Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P, Li P, Xu Q, Liu QS, Goldman SA, Nedergaard M. 2004. P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med 10:821-827.
72. Whittingham TS, Lust WD, Christakis DA, Passonneau JV. 1984. Metabolic stability of hippocampal slice preparations during prolonged incubation. J Neurochem 43:689-696.
73. Yamamoto C, McIlwain H. 1966. Electrical activities in thin sections from the mammalian brain maintained in chemically defined media in vitro. J Neurochem 13:1333-1343.
74. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A. 1997. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187:36-42.
75. 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.