Microglial depletion using intrahippocampal injection of liposome-encapsulated clodronate in prolonged hypothermic cardiac arrest in rats

Resuscitation

Volumn 83, Issue 4, 2012, Pages 517-526

  Drabek, Tomas ^a,b   Janata, Andreas ^a,b   Jackson, Edwin K ^a,c   End, Brad ^a   Stezoski, Jason ^a   Vagni, Vincent A ^a   Janesko Feldman, Keri ^a   Wilson, Caleb D ^a   van Rooijen, Nico ^d   Tisherman, Samuel A ^a,b,e   Kochanek, Patrick M ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Brain ischemia; Cardiac arrest; Emergency preservation; Hypothermia; Iba 1; Inflammation; Resuscitation

Indexed keywords

CLODRONIC ACID; LIPOSOME; PHOSPHATE BUFFERED SALINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANNULATION; CARDIOPULMONARY BYPASS; CELL ACTIVATION; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; CRYOPRESERVATION; DEEP HYPOTHERMIC CIRCULATORY ARREST; DISEASE DURATION; ENCAPSULATION; EXSANGUINATION; HEART ARREST; HIPPOCAMPUS; MACROPHAGE; MALE; MICROGLIA; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; RESUSCITATION; ROOM TEMPERATURE; SHAM PROCEDURE;

ANIMALS; CARDIOPULMONARY RESUSCITATION; CELL PROLIFERATION; CLODRONIC ACID; DISEASE MODELS, ANIMAL; HEART ARREST; HIPPOCAMPUS; HYPOTHERMIA, INDUCED; INJECTIONS, INTRALESIONAL; LIPOSOMES; MALE; MICROGLIA; NERVE DEGENERATION; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REFERENCE VALUES; RISK ASSESSMENT; SURVIVAL RATE;

EID: 84858076186     PISSN: 03009572     EISSN: 18731570     Source Type: Journal    
DOI: 10.1016/j.resuscitation.2011.09.016     Document Type: Article

References (50)

1. Safar P., Tisherman S.A., Behringer W., et al. Suspended animation for delayed resuscitation from prolonged cardiac arrest that is unresuscitable by standard cardiopulmonary-cerebral resuscitation. Crit Care Med 2000, 28:N214-N218.
2. Gehrmann J., Banati R.B., Wiessner C., Hossmann K.A., Kreutzberg G.W. Reactive microglia in cerebral ischaemia: an early mediator of tissue damage?. Neuropathol Appl Neurobiol 1995, 21:277-289.
3. Lalancette-Hebert M., Gowing G., Simard A., Weng Y.C., Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 2007, 27:2596-2605.
4. Liu J., Bartels M., Lu A., Sharp F.R. Microglia/macrophages proliferate in striatum and neocortex but not in hippocampus after brief global ischemia that produces ischemic tolerance in gerbil brain. J Cereb Blood Flow Metab 2001, 21:361-373.
5. Stirling D.P., Koochesfahani K.M., Steeves J.D., Tetzlaff W. Minocycline as a neuroprotective agent. Neuroscientist 2005, 11:308-322.
6. Tang M., Alexander H., Clark R.S., Kochanek P.M., Kagan V.E., Bayir H. Minocycline reduces neuronal death and attenuates microglial response after pediatric asphyxial cardiac arrest. J Cereb Blood Flow Metab 2010, 30:119-129.
7. van Rooijen N. The liposome-mediated macrophage 'suicide' technique. J Immunol Methods 1989, 124:1-6.
8. Marin-Teva J.L., Dusart I., Colin C., Gervais A., van Rooijen N., Mallat M. Microglia promote the death of developing Purkinje cells. Neuron 2004, 41:535-547.
9. Schilling M., Besselmann M., Muller M., Strecker J.K., Ringelstein E.B., Kiefer R. Predominant phagocytic activity of resident microglia over hematogenous macrophages following transient focal cerebral ischemia: an investigation using green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 2005, 196:290-297.
10. Drabek T., Tisherman S.A., Beuke L., et al. Deep hypothermia attenuates microglial proliferation independent of neuronal death after prolonged cardiac arrest in rats. Anesth Analg 2009, 109:914-923.
11. Van Rooijen N., Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 1994, 174:83-93.
12. Neumar R.W., Bircher N.G., Sim K.M., et al. Epinephrine and sodium bicarbonate during CPR following asphyxial cardiac arrest in rats. Resuscitation 1995, 29:249-263.
13. Schmued L.C., Hopkins K.J., Fluoro-Jade B. A high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000, 874:123-130.
14. Ito D., Imai Y., Ohsawa K., Nakajima K., Fukuuchi Y., Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 1998, 57:1-9.
15. Ito D., Tanaka K., Suzuki S., Dembo T., Fukuuchi Y. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 2001, 32:1208-1215.
16. Koshinaga M., Suma T., Fukushima M., Tsuboi I., Aizawa S., Katayama Y. Rapid microglial activation induced by traumatic brain injury is independent of blood brain barrier disruption. Histol Histopathol 2007, 22:129-135.
17. Lai A.Y., Todd K.G. Microglia in cerebral ischemia: molecular actions and interactions. Can J Physiol Pharmacol 2006, 84:49-59.
18. Nakajima K., Kohsaka S. Microglia: neuroprotective and neurotrophic cells in the central nervous system. Curr Drug Targets Cardiovasc Haematol Disord 2004, 4:65-84.
19. Imai F., Suzuki H., Oda J., et al. Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab 2007, 27:488-500.
20. Kitamura Y., Takata K., Inden M., et al. Intracerebroventricular injection of microglia protects against focal brain ischemia. J Pharmacol Sci 2004, 94:203-206.
21. Hanisch U.K. Microglia as a source and target of cytokines. Glia 2002, 40:140-155.
22. Lai A.Y., Todd K.G. Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 2008, 56:259-270.
23. Stoll G., Jander S., Schroeter M. Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 1998, 56:149-171.
24. Wang J., Wei Q., Wang C.Y., Hill W.D., Hess D.C., Dong Z. Minocycline up-regulates Bcl-2 and protects against cell death in mitochondria. J Biol Chem 2004, 279:19948-19954.
25. Frediani B., Cavalieri L., Cremonesi G. Clodronic acid formulations available in Europe and their use in osteoporosis: a review. Clin Drug Investig 2009, 29:359-379.
26. Pavlakis N., Schmidt R., Stockler M. Bisphosphonates for breast cancer. Cochrane Database Syst Rev 2005, CD003474.
27. van Rooijen N., Sanders A., van den Berg T.K. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J Immunol Methods 1996, 193:93-99.
28. Fleisch H. Bisphosphonates: a new class of drugs in diseases of bone and calcium metabolism. Recent Results Cancer Res 1989, 116:1-28.
29. Van Rooijen N., Kors N., vd Ende M., Dijkstra C.D. Depletion and repopulation of macrophages in spleen and liver of rat after intravenous treatment with liposome-encapsulated dichloromethylene diphosphonate. Cell Tissue Res 1990, 260:215-222.
30. Barbe E., Huitinga I., Dopp E.A., Bauer J., Dijkstra C.D. A novel bone marrow frozen section assay for studying hematopoietic interactions in situ: the role of stromal bone marrow macrophages in erythroblast binding. J Cell Sci 1996, 109:2937-2945.
31. Micklus M.J., Greig N.H., Tung J., Rapoport S.I. Organ distribution of liposomal formulations following intracarotid infusion in rats. Biochim Biophys Acta 1992, 1124:7-12.
32. Lahoud-Rahme M.S., Stezoski J., Kochanek P.M., Melick J., Tisherman S.A., Drabek T. Blood-brain barrier integrity in a rat model of emergency preservation and resuscitation. Resuscitation 2009, 80:484-488.
33. Polfliet M.M., Goede P.H., van Kesteren-Hendrikx E.M., van Rooijen N., Dijkstra C.D., van den Berg T.K. A method for the selective depletion of perivascular and meningeal macrophages in the central nervous system. J Neuroimmunol 2001, 116:188-195.
34. Lehenkari P.P., Kellinsalmi M., Napankangas J.P., et al. Further insight into mechanism of action of clodronate: inhibition of mitochondrial ADP/ATP translocase by a nonhydrolyzable, adenine-containing metabolite. Mol Pharmacol 2002, 61:1255-1262.
35. Bergh A., Damber J.E., van Rooijen N. Liposome-mediated macrophage depletion: an experimental approach to study the role of testicular macrophages in the rat. J Endocrinol 1993, 136:407-413.
36. Dehghani F., Conrad A., Kohl A., Korf H.W., Hailer N.P. Clodronate inhibits the secretion of proinflammatory cytokines and NO by isolated microglial cells and reduces the number of proliferating glial cells in excitotoxically injured organotypic hippocampal slice cultures. Exp Neurol 2004, 189:241-251.
37. Gowing G., Vallieres L., Julien J.P. Mouse model for ablation of proliferating microglia in acute CNS injuries. Glia 2006, 53:331-337.
38. Fan L.W., Lin S., Pang Y., Rhodes P.G., Cai Z. Minocycline attenuates hypoxia-ischemia-induced neurological dysfunction and brain injury in the juvenile rat. Eur J Neurosci 2006, 24:341-350.
39. Xu L., Fagan S.C., Waller J.L., et al. Low dose intravenous minocycline is neuroprotective after middle cerebral artery occlusion-reperfusion in rats. BMC Neurol 2004, 4:7.
40. Lampl Y., Boaz M., Gilad R., et al. Minocycline treatment in acute stroke: an open-label, evaluator-blinded study. Neurology 2007, 69:1404-1410.
41. Stirling D.P., Khodarahmi K., Liu J., et al. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J Neurosci 2004, 24:2182-2190.
42. Fox C., Dingman A., Derugin N., et al. Minocycline confers early but transient protection in the immature brain following focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 2005, 25:1138-1149.
43. Hewlett K.A., Corbett D. Delayed minocycline treatment reduces long-term functional deficits and histological injury in a rodent model of focal ischemia. Neuroscience 2006, 141:27-33.
44. Drabek T., Fisk J.A., Dixon C.E., et al. Prolonged deep hypothermic circulatory arrest in rats can be achieved without cognitive deficits. Life Sci 2007, 81:543-552.
45. Neumann J., Sauerzweig S., Ronicke R., et al. Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: a new mechanism of CNS immune privilege. J Neurosci 2008, 28:5965-5975.
46. Sanchez Mejia R.O., Ona V.O., Li M., Friedlander R.M. Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 2001, 48:1393-1399. [discussion 1399-401].
47. Liu Z., Fan Y., Won S.J., et al. Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 2007, 38:146-152.
48. Bendel O., Bueters T., von Euler M., Ove Ogren S., Sandin J., von Euler G. Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory. J Cereb Blood Flow Metab 2005, 25:1586-1595.
49. Scheff S.W., Price D.A., Hicks R.R., Baldwin S.A., Robinson S., Brackney C. Synaptogenesis in the hippocampal CA1 field following traumatic brain injury. J Neurotrauma 2005, 22:719-732.
50. Yamashima T., Tonchev A.B., Borlongan C.V. Differential response to ischemia in adjacent hippocampalsectors: neuronal death in CA1 versus neurogenesis in dentate gyrus. Biotechnol J 2007, 2:596-607.