Diverse Microglial Motility Behaviors during Clearance of Dead Cells in Hippocampal Slices

GLIA

Volumn 46, Issue 2, 2004, Pages 195-206

  Petersen, Mark A ^a   Dailey, Michael E ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Brain slice; Cell death; Cell motility; Microglia; Phagocytosis; Time lapse imaging

Indexed keywords

FLUORESCENT DYE; LECTIN; SYTOX ORANGE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN SLICE; CELL MOTILITY; HIPPOCAMPUS; MICROGLIA; NERVE CELL NECROSIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TISSUE INJURY;

ANIMALS; CELL COMMUNICATION; CELL DEATH; CELL MOVEMENT; CELL NUCLEUS; HIPPOCAMPUS; MICROGLIA; MICROSCOPY, CONFOCAL; NEURONS; PHAGOCYTOSIS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 2342647947     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/glia.10362     Document Type: Article

References (58)

1. Abd-el-Basset EM, Fedoroff S. 1994. Dynamics of actin filaments in microglia during Fc receptor-mediated phagocytosis. Acta Neuropathol 88:527-537.
2. Amat JA, Ishiguro H, Nakamura K, Norton WT. 1996. Phenotypic diversity and kinetics of proliferating microglia and astrocytes following cortical stab wounds. Glia 16:368-382.
3. Bechmann I, Nitsch R. 1997. Astrocytes and microglial cells incorporate degenerating fibers following entorhinal lesion: a light, confocal, and electron microscopical study using a phagocytosis-dependent labeling technique. Glia 20:145-154.
4. Behl C, Skutella T, Lezoualc HF, Post A, Widmann M, Newton CJ, Holsboer F. 1997. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharm 51:535-541.
5. Bohatschek M, Kloss CU, Kalla R, Raivich G. 2001. In vitro model of microglial deramification: ramified microglia transform into amoeboid phagocytes following addition of brain cell membranes to microglia-astrocyte cocultures. J Neurosci Res 64:508-522.
6. Booth PL, Thomas WE. 1991. Dynamic features of cells expressing macrophage properties in tissue cultures of dissociated cerebral cortex from the rat. Cell Tissue Res 266:541-551.
7. Brockhaus J, Moller T, Kettenmann H. 1996. Phagocytozing ameboid microglial cells studied in a mouse corpus callosum slice preparation. Glia 16:81-90.
8. Calvo CF, Yoshimura T, Gelman M, Mallat M. 1996. Production of monocyte chemotactic protein1 by rat brain macrophages. Eur J Neurosci 8:1725-1734.
9. Chan A, Magnus T, Gold R. 2001. Phagocytosis of apoptotic inflammatory cells by microglia and modulation by different cytokines: mechanism for removal of apoptotic cells in the inflamed nervous system. Glia 33:87-95.
10. Coltman BW, Ide CF. 1996. Temporal characterization of microglia, IL-1B-like immunoreactivity and astrocytes in the dentate gyrus of hippocampal organotypic slice cultures. Int J Devl Neurosci 14:707-719.
11. Cross AK, Woodroofe MN. 1999. Chemokines induce migration and changes in actin polymerization in adult rat brain microglia and a human fetal microglial cell line in vitro. J Neurosci Res 55:17-23.
12. Czapiga M, Colton CA. 1999. Function of microglia in organotypic slice cultures. J Neurosci Res 56:644-651.
13. Dailey ME, Waite M. 1999. Confocal imaging of microglial cell dynamics in hippocampal slice cultures. Methods 18:222-230.
14. Davis EJ, Foster TD, Thomas WE. 1994. Cellular forms and functions of brain microglia. Brain Res Bull 34:73-78.
15. DeWitt DA, Perry G, Cohen M, Doller C, Silver J. 1998. Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease. Exper Neurol 149:329-340.
16. Gähwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM. 1997. Organotypic slice cultures: a technique has come of age. Trends Neurosci 20:471-477.
17. Gonzalez-Scarano F, Baltuch G. 1999. Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219-240.
18. Grossmann R, Stence N, Carr J, Fuller L, Waite M, Dailey ME. 2002. Juxtavascular microglia migrate along brain microvessels following activation during early postnatal development. Glia 37:229-240.
19. Haapaniemi H, Tomita M, Tanahashi N, Takeda H, Yokoyama M, Fukuuchi Y. 1995. Non-amoeboid locomotion of cultured microglia obtained from newborn rat brain. Neurosci Lett 193:121-124.
20. Hailer NP, Jarhult JD, Nitsch R. 1996. Resting microglial cells in vitro: analysis of morphology and adhesion molecule expression in organotypic hippocampal slice cultures. Glia 18:319-331.
21. Hailer NP, Bechmann I, Heizmann S, Nitsch R. 1997. Adhesion molecule expression on phagocytic microglial cells following anterograde degeneration of perforant path axons. Hippocampus 7:341-349.
22. Hailer NP, Wirjatijasa F, Roser N, Hischebeth GT, Korf HW, Dehghani F. 2001. Astrocytic factors protect neuronal integrity and reduce microglial activation in an in vitro model of N-methyl-D-aspartate-induced excitotoxic injury in organotypic hippocampal slice cultures. Euro J Neurosci 14:315-326.
23. Hartlage-Rubsamen M, Schliebs R. 2001. Sequential upregulation of cell adhesion molecules in degenerating rat basal forebrain cholinergic neurons and in phagocytotic microglial cells. Brain Res 897: 20-26.
24. Heppner FL, Skutella T, Hailer NP, Haas D, Nitsch R. 1998. Activated microglial cells migrate towards sites of excitotoxic neuronal injury inside organotypic hippocampal slice cultures. Eur J Neurosci 10:3284-3290.
25. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka A. 2001. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 21:1975-1982.
26. Koshinaga M, Katayama Y, Fukushima M, Oshima H, Suma T, Takahata T. 2000. Rapid and widespread microglial activation induced by traumatic brain injury in rat brain slices. J Neurotrauma 17:185-192.
27. Kreutzberg GW. 1996. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
28. Laake JH, Haug FM, Wieloch T, Ottersen OP. 1999. A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Res Protocols 4:173-184.
29. Liu W, Liu R, Chun JT, Bi R, Hoe W, Schreiber SS, Baudry M. 2001. Kainate excitotoxicity in organotypic hippocampal slice cultures: evidence for multiple apoptotic pathways. Brain Res 916:239-248.
30. Macklis JD, Madison RD. 1990. Progressive incorporation of propidium iodide in cultured mouse neurons correlates with declining electrophysiological status: a fluorescence scale of membrane integrity. J Neurosci Meth 31:43-46.
31. Majno G, Joris I. 1995. Apoptosis, oncosis, and necrosis: an overview of cell death. Am J Pathol 146:3-15.
32. McGlade-McCulloh E, Morrissey AM, Norona F, Muller KJ. 1989. Individual microglia move rapidly and directly to nerve lesions in the leech central nervous system. Proc Natl Acad Sci USA 86:1093-1097.
33. Milner R, Campbell IL. 2002. Cytokines regulate microglial adhesion to laminin and astrocyte extracellular matrix via protein kinase C-dependent activation of the α6β1 integrin. J Neurosci 22:1562-1572.
34. i signaling in mouse microglia. J Neurosci 17:615-624.
35. Neary JT, Rathbone MP, Cattabeni F, Abbracchio MP, Burnstock G. 1996. Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci 19:13-18.
36. Nolte C, Möller T, Walter T, Kettenmann H. 1996. Complement 5a controls motility of murine microglial cells in vitro via activation of an inhibitory G-protein and the rearrangement of the actin cytoskeleton. Neuroscience 73:1091-1107.
37. 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.
38. Ohsawa K, Imai Y, Kanazawa H, Sasaki Y, Kohsaka S. 2000. Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J Cell Sci 113:3073-3084.
39. Pozzo Miller, LD, Mahanty NK, Connor JA, Landis DMD. 1994. Spontaneous pyramidal cell death in organotypic slice cultures from rat hippocampus is prevented by glutamate receptor antagonists. Neuroscience 63:471-487.
40. Raivich G, Gehrmann J, Kreutzberg GW. 1991. Increase of macrophage colony-stimulating factor and granulocyte-macrophage colony-stimulating factor receptors in the regenerating rat facial nucleus. J Neurosci Res 30:682-686.
41. Raivich G, Moreno Flores, MT, Moller JC, Kreutzberg GW. 1994. Inhibition of posttraumatic microglial proliferation in a genetic model of macrophage colony-stimulating factor deficiency in the mouse. Eur J Neurosci 6:1615-1618.
42. Raivich G, Bohatschek M, Kloss CUA, Werner A, Jones LL, Kreutzberg GW. 1999. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Rev 30:77-105.
43. Sastry PS, Rao KS. 2000. Apoptosis and the nervous system. J Neurochem 74:1-20.
44. Schiefer JH, Kampe K, Dodt HU, Zieglgansberger W, Kreutzberg GW. 1999. Microglial motility in the rat facial nucleus following peripheral axotomy. J Neurocytol 28:439-453.
45. Schmidtmayerova H, Nottet HS, Nuovo G, Raabe T, Flanagan CR, Dubrovsky L, Gendelman HE, Cerami A, Bukrinsky M, Sherry B. 1996. Human immunodeficiency virus type 1 infection alters chemokine beta peptide expression in human monocytes: implications for recruitment of leukocytes into brain and lymph nodes. Proc Natl Acad Sci USA 93:700-704.
46. Sievers J, Parwaresch R, Wottge HU. 1994. Blood monocytes and spleen macrophages differentiate into microglia-like cells on monolayers of astrocytes: morphology. Glia 12:245-258.
47. Skibo GG, Nikonenko IR, Savchenko VL, McKanna JA. 2000. Microglia in organotypic hippocampal slice culture and effects of hypoxia: ultrastructure and lipocortin-1 immunoreactivity. Neuroscience 96: 427-438.
48. Smith ME, Hoerner MT. 2000. Astrocytes modulate macrophage phagocytosis of myelin in vitro. J Neuroimmunol 102:154-162.
49. Smith SJ, Cooper M, Waxman A. 1990. Laser microscopy of subcellular structure in living neocortex: can one see dendritic spines twitch? In: Squire LR, Lindenlaub E, editors. XXIII Symposia Medica Hoechst: the biology of memory. Stuttgart: Schattauer. p 49-71.
50. Stence NS, Waite M, Dailey ME. 2001. Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 33:256-266.
51. Streit WJ. 1990. An improved staining method for rat microglial cells using the lectin from Griffonia simplicifolia (GSA I-B4). J Histochem Cytochem 38:1683-1686.
52. Takeda H, Tomita M, Tanahashi N, Kobari M, Yokoyama M, Takao M, Ito D, Fukuuchi Y. 1998. Hydrogen peroxide enhances phagocytic activity of ameboid microglia. Neurosci Lett 240:5-8.
53. Thomas WE. 1992. Brain macrophages: evaluation of microglia and their functions. Brain Res Rev 17:61-74.
54. Tomita M, Fukuuchi Y, Tanahashi N, Kobari M, Takeda H, Yokoyama M, Ito D, Terakawa S. 1996. Swift transformation and locomotion of polymorphonuclear leukocytes and microglia as observed by VEC-DIC microscopy (video microscopy). Keio J Med 45:213-224.
55. von Zahn J, Moller T, Kettenmann H, Nolte C. 1997. Microglial phagocytosis is modulated by pro- and anti-inflammatory cytokines. Neuroreport 8:3851-3856.
56. Ward SA, Ransom PA, Booth PL, Thomas WE. 1991. Characterization of ramified microglia in tissue culture: pinocytosis and motility. J Neurosci Res 29:13-28.
57. Witting A, Muller P, Herrmann A, Kettenmann H, Nolte C. 2000. Phagocytic clearance of apoptotic neurons by microglia/brain macrophages in vitro: involvement of lectin-, integrin-, and phosphatidyl-serine-mediated recognition. J Neurochem 75:1060-1070.
58. Yao J, Harvath L, Gilbert DL, Colton CA. 1990. Chemotaxis by a CNS macrophage, the microglia. J Neurosci Res 27:36-42.