Dynamic motility of microglia: Purinergic modulation of microglial movement in the normal and pathological brain

GLIA

Volumn 59, Issue 12, 2011, Pages 1793-1799

  Ohsawa, Keiko ^a   Kohsaka, Shinichi ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

Adenosine; ATP; Chemotaxis; Microglia; Migration; Process extension

Indexed keywords

ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE; BETA1 INTEGRIN; CALCIUM; CD11 ANTIGEN; CD172A PROTEIN; CD18 ANTIGEN; CD200 ANTIGEN; CD200 RECEPTOR; CD22 ANTIGEN; CD45 ANTIGEN; CD47 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FRACTALKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; NERVE PROTEIN; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROSTAGLANDIN SYNTHASE; PURINERGIC P2X RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC P2Y12 RECEPTOR; PURINERGIC P2Y6 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CALCIUM CELL LEVEL; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CELL SWELLING; CENTRAL NERVOUS SYSTEM; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; MICROENVIRONMENT; MICROGLIA; NERVE INJURY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; POTASSIUM CURRENT; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SYNAPSE; UPREGULATION;

ANIMALS; BRAIN; BRAIN DISEASES; CELL MOVEMENT; HUMANS; MICROGLIA; PURINES;

EID: 80053575339     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21238     Document Type: Article

References (72)

1. Barclay AN, Wright GJ, Brooke G, Brown MH. 2002. CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol 23: 285-290.
2. Bayer TA, Buslei R, Havas L, Falkai P. 1999. Evidence for activation of microglia in patients with psychiatric illnesses. Neurosci Lett 271: 126-128.
3. Block ML, Zecca L, Hong JS. 2007. Microglia-mediated neurotoxicity: Uncovering the molecular mechanisms. Nat Rev Neurosci 8: 57-69.
4. Braun N, Lenz C, Gillardon F, Zimmermann M, Zimmermann H. 1997. Focal cerebral ischemia enhances glial expression of ecto-5'-nucleotidase. Brain Res 766: 213-226.
5. Calvo M, Zhu N, Tsantoulas C, Ma Z, Grist J, Loeb JA, Bennett DL. 2010. Neuregulin-ErbB signaling promotes microglial proliferation and chemotaxis contributing to microgliosis and pain after peripheral nerve injury. J Neurosci 30: 5437-5450.
6. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM. 2006. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9: 917-924.
7. Cavaliere F, Florenzano F, Amadio S, Fusco FR, Viscomi MT, D'Ambrosi N, Vacca F, Sancesario G, Bernardi G, Molinari M, Volonte C. 2003. Up-regulation of P2X2, P2X4 receptor and ischemic cell death: Prevention by P2 antagonists. Neuroscience 120: 85-98.
8. Chan WY, Kohsaka S, Rezaie P. 2007. The origin and cell lineage of microglia: New concepts. Brain Res Rev 53: 344-354.
9. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752-758.
10. Dibaj P, Nadrigny F, Steffens H, Scheller A, Hirrlinger J, Schomburg ED, Neusch C, Kirchhoff F. 2010. NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia 58: 1133-1144.
11. Du Yan S, Zhu H, Fu J, Yan SF, Roher A, Tourtellotte WW, Rajavashisth T, Chen X, Godman GC, Stern D, Schmidt AM. 1997. Amyloid-beta peptide-receptor for advanced glycation endproduct interaction elicits neuronal expression of macrophage-colony stimulating factor: A proinflammatory pathway in Alzheimer disease. Proc Natl Acad Sci USA 94: 5296-5301.
12. Ducharme G, Newell EW, Pinto C, Schlichter LC. 2007. Small-conductance Cl-channels contribute to volume regulation and phagocytosis in microglia. Eur J Neurosci 26: 2119-2130.
13. Farber K, Markworth S, Pannasch U, Nolte C, Prinz V, Kronenberg G, Gertz K, Endres M, Bechmann I, Enjyoji K, Robson SC, Kettenmann H. 2008. The ectonucleotidase cd39/ENTPDase1 modulates purinergic-mediated microglial migration. Glia 56: 331-341.
14. Fiebich BL, Biber K, Lieb K, van Calker D, Berger M, Bauer J, Gebicke-Haerter PJ. 1996. Cyclooxygenase-2 expression in rat microglia is induced by adenosine A2a-receptors. Glia 18: 152-160.
15. Fontainhas AM, Wang M, Liang KJ, Chen S, Mettu P, Damani M, Fariss RN, Li W, Wong WT. 2011. Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One 6: e15973
16. Franklin A, Parmentier-Batteur S, Walter L, Greenberg DA, Stella N. 2003. Palmitoylethanolamide increases after focal cerebral ischemia and potentiates microglial cell motility. J Neurosci 23: 7767-7775.
17. Gahmberg CG, Tian L, Ning L, Nyman-Huttunen H. 2008. ICAM-5-A novel two-facetted adhesion molecule in the mammalian brain. Immunol Lett 117: 131-135.
18. Gamo K, Kiryu-Seo S, Konishi H, Aoki S, Matsushima K, Wada K, Kiyama H. 2008. G-protein-coupled receptor screen reveals a role for chemokine receptor CCR5 in suppressing microglial neurotoxicity. J Neurosci 28: 11980-11988.
19. Gilad GM, Gilad VH. 1995. Chemotaxis and accumulation of nerve growth factor by microglia and macrophages. J Neurosci Res 41: 594-602.
20. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330: 841-845.
21. Hanisch UK, Kettenmann H. 2007. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
22. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, Botti P, Bacon KB, Fen L. 1998. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci USA 95: 10896-10901.
23. Hayashi M, Luo Y, Laning J, Strieter RM, Dorf ME. 1995. Production and function of monocyte chemoattractant protein-1 and other beta-chemokines in murine glial cells. J Neuroimmunol 60: 143-150.
24. 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.
25. Hines DJ, Hines RM, Mulligan SJ, Macvicar BA. 2009. Microglia processes block the spread of damage in the brain and require functional chloride channels. Glia 57: 1610-1618.
26. Hoek RM, Ruuls SR, Murphy CA, Wright GJ, Goddard R, Zurawski SM, Blom B, Homola ME, Streit WJ, Brown MH, Barclay AN, Sedgwick JD. 2000. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 290: 1768-1771.
27. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. 2001. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 21: 1975-1982.
28. Hundhausen C, Misztela D, Berkhout TA, Broadway N, Saftig P, Reiss K, Hartmann D, Fahrenholz F, Postina R, Matthews V, Kallen KJ, Rose-John S, Ludwig A. 2003. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102: 1186-1195.
29. Hynes RO. 2002. Integrins: Bidirectional, allosteric signaling machines. Cell 110: 673-687.
30. 2+ exchanger. J Neurosci 27: 13065-13073.
31. Inoue K. 2002. Microglial activation by purines and pyrimidines. Glia 40: 156-163.
32. 2+-dependent plasminogen release from cultured microglia. Br J Pharmacol 123: 1304-1310.
33. Irino Y, Nakamura Y, Inoue K, Kohsaka S, Ohsawa K. 2008. Akt activation is involved in P2Y12 receptor-mediated chemotaxis of microglia. J Neurosci Res 86: 1511-1519.
34. James G, Butt AM. 2002. P2Y and P2X purinoceptor mediated Ca2+ signalling in glial cell pathology in the central nervous system. Eur J Pharmacol 447: 247-260.
35. Junker A, Krumbholz M, Eisele S, Mohan H, Augstein F, Bittner R, Lassmann H, Wekerle H, Hohlfeld R, Meinl E. 2009. MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47. Brain 132: 3342-3352.
36. Kawamata T, Akiyama H, Yamada T, McGeer PL. 1992. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Pathol 140: 691-707.
37. Kreutzberg GW. 1996. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19: 312-318.
38. Lauro C, Catalano M, Trettel F, Mainiero F, Ciotti MT, Eusebi F, Limatola C. 2006. The chemokine CX3CL1 reduces migration and increases adhesion of neurons with mechanisms dependent on the beta1 integrin subunit. J Immunol 177: 7599-7606.
39. Liang KJ, Lee JE, Wang YD, Ma W, Fontainhas AM, Fariss RN, Wong WT. 2009. Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest Ophthalmol Vis Sci 50: 4444-4451.
40. 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.
41. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M. 2007. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10: 1544-1553.
42. Milner R, Crocker SJ, Hung S, Wang X, Frausto RF, del Zoppo GJ. 2007. Fibronectin- and vitronectin-induced microglial activation and matrix metalloproteinase-9 expression is mediated by integrins alpha5beta1 and alphavbeta5. J Immunol 178: 8158-8167.
43. Morgan JT, Chana G, Pardo CA, Achim C, Semendeferi K, Buckwalter J, Courchesne E, Everall IP. 2010. Microglial activation and increased microglial density observed in the dorsolateral prefrontal cortex in autism. Biol Psychiatry 68: 368-376.
44. Mott RT, Ait-Ghezala G, Town T, Mori T, Vendrame M, Zeng J, Ehrhart J, Mullan M, Tan J. 2004. Neuronal expression of CD22: Novel mechanism for inhibiting microglial proinflammatory cytokine production. Glia 46: 369-379.
45. Nakajima K, Kohsaka S. 2005. Response of microglia to brain injury. In: Kettenmann H, Ransom B, editors. Neuroglia. New York: Oxford University Press. pp 443-453.
46. Nasu-Tada K, Koizumi S, Inoue K. 2005. Involvement of beta1 integrin in microglial chemotaxis and proliferation on fibronectin: different regulations by ADP through PKA. Glia 52: 98-107.
47. Nasu-Tada K, Koizumi S, Tsuda M, Kunifusa E, Inoue K. 2006. Possible involvement of increase in spinal fibronectin following peripheral nerve injury in upregulation of microglial P2X4, a key molecule for mechanical allodynia. Glia 53: 769-775.
48. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
49. Nolte C, Kirchhoff F, Kettenmann H. 1997. Epidermal growth factor is a motility factor for microglial cells in vitro: Evidence for EGF receptor expression. Eur J Neurosci 9: 1690-1698.
50. Ohsawa K, Irino Y, Nakamura Y, Akazawa C, Inoue K, Kohsaka S. 2007. Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 55: 604-616.
51. Ohsawa K, Irino Y, Sanagi T, Nakamura Y, Suzuki E, Inoue K, Kohsaka S. 2010. P2Y12 receptor-mediated integrin-beta1 activation regulates microglial process extension induced by ATP. Glia 58: 790-801.
52. Orr AG, Orr AL, Li XJ, Gross RE, Traynelis SF. 2009. Adenosine A(2A) receptor mediates microglial process retraction. Nat Neurosci 12: 872-878.
53. Pedata F, Corsi C, Melani A, Bordoni F, Latini S. 2001. Adenosine extracellular brain concentrations and role of A2A receptors in ischemia. Ann NY Acad Sci 939: 74-84.
54. Prinz M, Mildner A. 2011. Microglia in the CNS: Immigrants from another world. Glia 59: 177-187.
55. Ralevic V, Burnstock G. 1998. Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492.
56. Robson SC, Sevigny J, Zimmermann H. 2006. The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance. Purinergic Signal 2: 409-430.
57. Sasaki Y, Hoshi M, Akazawa C, Nakamura Y, Tsuzuki H, Inoue K, Kohsaka S. 2003. Selective expression of Gi/o-coupled ATP receptor P2Y12 in microglia in rat brain. Glia 44: 242-250.
58. Saura J, Angulo E, Ejarque A, Casado V, Tusell JM, Moratalla R, Chen JF, Schwarzschild MA, Lluis C, Franco R, Serratosa J. 2005. Adenosine A2A receptor stimulation potentiates nitric oxide release by activated microglia. J Neurochem 95: 919-929.
59. Schwab JM, Guo L, Schluesener HJ. 2005. Spinal cord injury induces early and persistent lesional P2X4 receptor expression. J Neuroimmunol 163: 185-189.
60. Schwarzschild MA, Agnati L, Fuxe K, Chen JF, Morelli M. 2006. Targeting adenosine A2A receptors in Parkinson's disease. Trends Neurosci 29: 647-654.
61. Sperlagh B, Illes P. 2007. Purinergic modulation of microglial cell activation. Purinergic Signal 3: 117-127.
62. Stence N, Waite M, Dailey ME. 2001. Dynamics of microglial activation: A confocal time-lapse analysis in hippocampal slices. Glia 33: 256-266.
63. Streit WJ. 2004. Microglia and Alzheimer's disease pathogenesis. J Neurosci Res 77: 1-8.
64. Tiffany HL, Lavigne MC, Cui YH, Wang JM, Leto TL, Gao JL, Murphy PM. 2001. Amyloid-beta induces chemotaxis and oxidant stress by acting at formylpeptide receptor 2, a G protein-coupled receptor expressed in phagocytes and brain. J Biol Chem 276: 23645-23652.
65. Tozaki-Saitoh H, Tsuda M, Miyata H, Ueda K, Kohsaka S, Inoue K. 2008. P2Y12 receptors in spinal microglia are required for neuropathic pain after peripheral nerve injury. J Neurosci 28: 4949-4956.
66. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K. 2004. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45: 89-95.
67. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K. 2003. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424: 778-783.
68. van der Putten C, Zuiderwijk-Sick EA, van Straalen L, de Geus ED, Boven LA, Kondova I, AP IJ, Bajramovic JJ. 2009. Differential expression of adenosine A3 receptors controls adenosine A2A receptor-mediated inhibition of TLR responses in microglia. J Immunol 182: 7603-7612.
69. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J. 2009. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 29: 3974-3980.
70. Wu LJ, Vadakkan KI, Zhuo M. 2007. ATP-induced chemotaxis of microglial processes requires P2Y receptor-activated initiation of outward potassium currents. Glia 55: 810-821.
71. Yao J, Harvath L, Gilbert DL, Colton CA. 1990. Chemotaxis by a CNS macrophage, the microglia. J Neurosci Res 27: 36-42.
72. Zhang Z, Artelt M, Burnet M, Trautmann K, Schluesener HJ. 2006. Lesional accumulation of P2X4 receptor+ monocytes following experimental traumatic brain injury. Exp Neurol 197: 252-257.