The spleen contributes to stroke-induced neurodegeneration

Journal of Neuroscience Research

Volumn 86, Issue 10, 2008, Pages 2227-2234

  Ajmo Jr , Craig T ^a   Vernon, Dionne O L ^a   Collier, Lisa ^a   Hall, Aaron A ^a   Garbuzova Davis, Svitlana ^a,b   Willing, Alison ^a,b   Pennypacker, Keith R ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Inflammation; Ischemia; Neurodegeneration; Spleen; Stroke

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL ACTIVATION; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE DEGENERATION; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RAT; SPLEEN; SPLENECTOMY; STROKE; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

ANIMALS; BRAIN; IMMUNOHISTOCHEMISTRY; LASER-DOPPLER FLOWMETRY; MALE; NERVE DEGENERATION; RATS; RATS, SPRAGUE-DAWLEY; SPLEEN; SPLENECTOMY; STROKE;

EID: 48249100117     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21661     Document Type: Article

References (45)

1. Abbott NJ. 2000. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell Mol Neurobiol 20:131-147.
2. Abraham CS, Harada N, Deli MA, Niwa M. 2002. Transient forebrain ischemia increases the blood-brain barrier permeability for albumin in stroke-prone spontaneously hypertensive rats. Cell Mol Neurobiol 22:455-462.
3. Akopov SE, Simonian NA, Grigorian GS. 1996. Dynamics of polymorphonuclear leukocyte accumulation in acute cerebral infarction and their correlation with brain tissue damage. Stroke 27:1739-1743.
4. Allan SM, Rothwell NJ. 2003. Inflammation in central nervous system injury. Phil Trans R Soc Lond B Biol Sci 358:1669-1677.
5. Barone FC, Feuerstein GZ. 1999. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19:819-834.
6. Barone FC, Hillegass LM, Tzimas MN, Schmidt DB, Foley JJ, White RF, Price WJ, Feuerstein GZ, Clark RK, Griswold DE, Sarau HM. 1995. Time-related changes in myeloperoxidase activity and leukotriene B4 receptor binding reflect leukocyte influx in cerebral focal stroke. Mol Chem Neuropathol 24:13-30.
7. Benner EJ, Mosley RL, Destache CJ, Lewis TB, Jackson-Lewis V, Gorantla S, Nemachek C, Green SR, Przedborski S, Gendelman HE. 2004. Therapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease. Proc Natl Acad Sci U S A 101:9435-9440.
8. Chen H, Chopp M, Zhang RL, Bodzin G, Chen Q, Rusche JR, Todd RF, 3rd. 1994. Anti-CD11b monoclonal antibody reduces ischemic cell damage after ttansient focal cerebral ischemia in rat. Ann Neurol 35:458-463.
9. Chopp M, Zhang RL, Chen H, Li Y, Jiang N, Rusche JR. 1994. Postischemic administration of an anti-Mac-1 antibody reduces ischemic cell damage after transient middle cerebral artery occlusion in rats. Stroke 25:869-875.
10. Dirnagl U, Iadecola C, Moskowitz MA. 1999. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397.
11. Duckworth EA, Butler TL, De Mesquita D, Collier SN, Collier L, Pennypacker KR. 2005. Temporary focal ischemia in the mouse: technical aspects and patterns of Fluoro-Jade evident neurodegeneration. Brain Res 1042:29-36.
12. Emerich DF, Dean RL, 3rd, Bartus RT. 2002. The role of leukocytes following cerebral ischemia: pathogenic variable or bystander reaction to emerging infarct? Exp Neurol 173:168-181.
13. Emsley HC, Smith CJ, Gavin CM, Georgiou RF, Vail A, Barberan EM, Hallenbeck JM, del Zoppo GJ, Rothwell NJ, Tyrrell PJ, Hopkins SJ. 2003. An early and sustained peripheral inflammatory response in acute ischaemic stroke: relationships with infection and atherosclerosis. J Neuroimmunol 139:93-101.
14. Feuerstein GZ, Wang X, Barone FC. 1998. The role of cytokines in the neuropathology of stroke and neurotrauma. Neuroimmunomodulation 5:143-159.
15. Gendron A, Teitelbaum J, Cossette C, Nuara S, Dumont M, Geadah D, du Souich P, Kouassi E. 2002. Temporal effects of left versus right middle cerebral artery occlusion on spleen lymphocyte subsets and mitogenic response in Wistar rats. Brain Res 955:85-97.
16. Hausmann EH, Berman NE, Wang YY, Meara JB, Wood GW, Klein RM. 1998. Selective chemokine mRNA expression following brain injury. Brain Res 788:49-59.
17. Iadecola C, Alexander M. 2001. Cerebral ischemia and inflammation. Curr Opin Neurol 14:89-94.
18. Kim JH, Kim JH, Park JA, Lee SW, Kim WJ, Yu YS, Kim KW. 2006. Blood-neural barrier: intercellular communication at glio-vascular interface. J Biochem Mol Biol 39:339-345.
19. Kirino T, Nakagomi T, Kanemitsu H, Tamura A. 1996. Ischemic tolerance. Adv Neurol 71:505-511.
20. Liu B, Hong JS. 2003. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther 304:1-7.
21. Longa EZ, Weinstein PR, Carlson S, Cummins R. 1989. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84-91.
22. Lucas SM, Rothwell NJ, Gibson RM. 2006. The role of inflammation in CNS injury and disease. Br J Pharmacol 147(Suppl 1):S232-S240.
23. Lyons SA, Pastor A, Ohlemeyer C, Kann O, Wiegand F, Prass K, Knapp F, Kettenmann H, Dirnagl U. 2000. Distinct physiologic properties of microglia and blood-borne cells in rat brain slices after permanent middle cerebral artery occlusion. J Cereb Blood Flow Metab 20:1537-1549.
24. Marler JR, Goldstein LB. 2003. Medicine. Stroke - tPA and the clinic. Science 301:1677.
25. Matsuo Y, Kihara T, Ikeda M, Ninomiya M, Onodera H, Kogure K. 1995. Role of neutrophils in radical production during ischemia and reperfusion of the rat brain: effect of neutrophil depletion on extracellular ascorbyl radical formation. J Cereb Blood Flow Metab 15:941-947.
26. Matsuo Y, Kihara T, Ikeda M, Ninomiya M, Onodera H, Kogure K. 1996. Role of platelet-activating factor and thromboxane A2 in radical production during ischemia and reperrusion of the rat brain. Brain Res 709:296-302.
27. Nauseef WM. 1998. Insights into myeloperoxidase biosynthesis from its inherited deficiency. J Mol Med 76:661-668.
28. Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD. 2006a. Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 26:654-665.
29. Offner H, Subramanian S, Parker SM, Wang C, Afentoulis ME, Lewis A, Vandenbark AA, Hurn PD. 2006b. Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J Immunol 176:6523-6531.
30. Prass K, Meisel C, Hoflich C, Braun J, Halle E, Wolf T, Ruscher K, Victorov IV, Priller J, Dirnagl U, Volk HD, Meisel A. 2003. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med 198:725-736.
31. Raivich G, Bohatschek M, Kloss CU, 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 Brain Res Rev 30:77-105.
32. Schaller B, Graf R. 2002. Cerebral ischemic preconditioning. An experimental phenomenon or a clinical important entity of stroke prevention? J Neurol 249:1503-1511.
33. Schilling M, Besselmann M, Leonhard C, Mueller M, Ringelstein EB, Kiefer R. 2003. Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: a study in green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 183:25-33.
34. Shi J, Gilbert GE, Kokubo Y, Ohashi T. 2001. Role of the liver in regulating numbers of circulating neutrophils. Blood 98:1226-1230.
35. Schmued LC, Albertson C, Slikker W Jr. 1997. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 751:37-46.
36. Stewart IB, McKenzie DC. 2002. The human spleen during physiological stress. Sports Med 32:361-369.
37. Stoll G, Jander S, Schroeter M. 1998. Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56:149-171.
38. Stoll G, Jander S, Schroeter M. 2000. Cytokines in CNS disorders: neurotoxicity versus neuroprotection. J Neural Transm Suppl 59:81-89.
39. Stoll G, Jander S, Schroeter M. 2002. Detrimental and beneficial effects of injury-induced inflammation and cytokine expression in the nervous system. Adv Exp Med Biol 513:87-113.
40. Vendrame M, Cassady J, Newcomb J, Butler T, Pennypacker KR, Zigova T, Sanberg CD, Sanberg PR, Willing AE. 2004. Infusion of human umbilical cord blood cells in a rat model of stroke dose-dependendy rescues behavioral deficits and reduces infarct volume. Stroke 35:2390-2395.
41. Vendrame M, Gemma C, de Mesquita D, Collier L, Bickford PC, Sanberg CD, Sanberg PR, Pennypacker KR, Willing AE. 2005. Anti-inflammatory effects of human cord blood cells in a rat model of stroke. Stem Cells Dev 14:595-604.
42. Vendrame M, Gemma C, Pennypacker KR, Bickford PC, Davis Sanberg C, Sanberg PR, Willing AE. 2006. Cord blood rescues stroke-induced changes in splenocyte phenotype and function. Exp Neurol 199:191-200.
43. Weston RM, Jones NM, Jarrott B, Callaway JK. 2007. Inflammatory cell infiltration after endothelin-1-induced cerebral ischemia: histochemical and myeloperoxidase correlation with temporal changes in brain injury. J Cereb Blood Flow Metab 27:100-114.
44. Zhang RL, Chopp M, Chen H, Garcia JH. 1994. Temporal profile of ischemic tissue damage, neutrophil response, and vascular plugging following permanent and transient (2H) middle cerebral artery occlusion in the rat. J Neurol Sci 125:3-10.
45. Zhang ZG, Chopp M, Tang WX, Jiang N, Zhang RL. 1995. Postishemic treatment (2-4 h) with anti-CD11b and anti-CD18 monoclonal antibodies are neuroprotective after transient (2 h) focal cerebral ischemia in the rat. Brain Res 698:79-85.