Phenotypic Changes in Immune Cell Subsets Reflect Increased Infarct Volume in Male vs. Female Mice

Translational Stroke Research

Volumn 4, Issue 5, 2013, Pages 554-563

  Banerjee, Anirban ^a,b   Wang, Jianming ^b   Bodhankar, Sheetal ^a,b   Vandenbark, Arthur A ^a,b   Murphy, Stephanie J ^b   Offner, Halina ^a,b  

^a PORTLAND VA MEDICAL CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Activated T cells; Experimental stroke; Gender bias; Immune markers; Ischemia; Suppressor T cells

Indexed keywords

CD69 ANTIGEN; HERMES ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR BETA; VERY LATE ACTIVATION ANTIGEN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN TISSUE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; IMMUNOPATHOGENESIS; MACROPHAGE ACTIVATION; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REPERFUSION INJURY; SEX DIFFERENCE; SPLEEN; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD44; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CEREBRAL INFARCTION; DISEASE MODELS, ANIMAL; FEMALE; INFARCTION, MIDDLE CEREBRAL ARTERY; INTEGRIN ALPHA4BETA1; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR BETA SUBUNIT; LECTINS, C-TYPE; MALE; MICE; REPERFUSION INJURY; SEX FACTORS; SPLEEN;

EID: 84884844820     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-013-0268-z     Document Type: Article

References (46)

1. Brait VH, Jackman KA, Walduck AK, Selemidis S, Diep H, Mast AE, et al. Mechanisms contributing to cerebral infarct size after stroke: gender, reperfusion, T lymphocytes, and Nox2-derived superoxide. Journal of Cerebral Blood Flow and Metabolism. 2010;30: 1306-17.
2. Alkayed NJ, Harukuni I, Kimes AS, London ED, Traystman RJ, Hurn PD. Gender-linked brain injury in experimental stroke. Stroke. 1998;29: 159-66.
3. Di Carlo A, Lamass M, Baldereschi M, et al. Sex differences in the clinical presentation, resource use, and 3-month outcome of acute stroke in Europe: data from a multicenter multinational hospital-based registry. Stroke. 2003;34: 1114-9.
4. Seshadri S, Beiser A, Kelly-Hayes M, Kase CS, Au R, Kannel WB, et al. The lifetime risk of stroke: estimates from the Framingham Study. Stroke. 2006;37: 345-50.
5. Sudlow CLM, Warlow CP. Comparable studies of the incidence of stroke and its pathological types. Stroke. 1997;28: 491-9.
6. Sacco RL, Boden-Albala B, Gan R, Chen X, Kargman DE, Shea S, et al. Stroke incidence among White, Black, and Hispanic residents of an urban community: the Northern Manhattan Stroke Study. American Journal of Epidemiology. 1998;147: 259-68.
7. Koerner I, Murphy SJ, Hurn PD. Gender, sex steroids, and cerebral ischemic pathobiology. In: Chan P, editor. Acute ischemic injury and repair in the nervous system. New York: Kluwer Academic/Plenum Publishers; 2007. p. 186-207.
8. Hurn PD, Vannucci SJ, Hagberg H. Adult or perinatal brain injury: does sex matter? Stroke. 2005;36: 193-5.
9. Murphy SJ, McCullough LD, Smith JM. Stroke in the female: role of biological sex and estrogen. ILAR Journal. 2004;45: 147-59.
10. Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD. Experimental stroke induces massive, rapid activation of the peripheral immune system. Journal of Cerebral Blood Flow and Metabolism. 2006;26: 654-65.
11. Allan SM, Rothwell NJ. Inflammation in central nervous system injury. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences. 2003;358: 1669-77.
12. Haast RA, Gustafson DR, Kiliaan AJ. Sex differences in stroke. Journal of Cerebral Blood Flow and Metabolism. 2012;32: 2100-7.
13. Appelros P, Stegmayr B, Terént A. A review on sex differences in stroke treatment and outcome. Acta Neurologica Scandinavica. 2010;121: 359-69.
14. Hurn PD, Subramanian S, Parker SM, Afentoulis ME, Kaler LJ, Vandenbark AA, et al. T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation. Journal of Cerebral Blood Flow and Metabolism. 2007;27: 1798-805.
15. Offner H, Subramanian S, Parker SM, Wang C, Afentoulis ME, Lewis A, et al. Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. The Journal of Immunology. 2006;176: 6523-31.
16. + phenotype controls T cell-dependent inflammatory responses. Immunity. 2008;28: 639-50.
17. 3 protection in EAE. Metabolic Brain Disease. 2012;27: 29-35.
18. Ajmo CT, Vernon DO, Collier L, Hall AA, Garbuzova-Davis S, Willing A, et al. The spleen contributes to stroke-induced neurodegeneration. Journal of Neuroscience Research. 2008;86: 2227-34.
19. Yilmaz G, Arumugam TV, Stokes KY, Granger DN. Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation. 2006;113: 2105-12.
20. Seifert HA, Hall AA, Chapman CB, Collier LA, Willing AE, Pennypacker KR. A transient decrease in spleen size following stroke corresponds to splenocytes release into systemic circulation. Journal of Neuroimmune Pharmacology. 2012;7: 1017-24.
21. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. Journal of Leukocyte Biology. 2010;87: 779-89.
22. Yilmaz G, Granger DN. Leukocyte recruitment and ischemic brain injury. Neuromolecular Medicine. 2010;12: 193-04.
23. Arumugam TV, Granger DN, Mattson MP. Stroke and T-cells. Neuromolecular Medicine. 2005;7: 229-42.
24. Jackman KA, Miller AA, De Silva TM, Crack PJ, Drummond GR, Sobey CG. Reduction of cerebral infarct volume by apocynin requires pretreatment and is absent in Nox2-deficient mice. British Journal of Pharmacology. 2009;156: 680-8.
25. Kahles T, Luedike P, Endres M, Galla HJ, Steinmetz H, Busse R, et al. NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke. 2007;38: 3000-6.
26. Becker K, Kindrick D, Relton J, Harlan J, Winn R. Antibody to the alpha4 integrin decreases infarct size in transient focal cerebral ischemia in rats. Stroke. 2001;32: 206-11.
27. Liesz A, Suri-Payer E, Veltkamp C, Doerr H, Sommer C, Rivest S, et al. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nature Medicine. 2009;15: 192-9.
28. Relton JK, Sloan KE, Frew EM, Whalley ET, Adams SP, Lobb RR. Inhibition of alpha4 integrin protects against transient focal cerebral ischemia in normotensive and hypertensive rats. Stroke. 2001;32: 199-205.
29. Angele MK, Schwacha MG, Ayala A, Chaudry IH. Effect of gender and sex hormones on immune responses following shock. Shock. 2000;14: 81-90.
30. Pelfrey CM, Cotleur AC, Lee JC, Rudick RA. Sex differences in cytokine responses to myelin peptides in multiple sclerosis. Journal of Neuroimmunology. 2002;130: 211-23.
31. Voskuhl RR, Palaszynski K. Sex hormones in EAE: implications for multiple sclerosis. The Neuroscientist. 2001;7: 258-70.
32. Walder CE, Green SP, Darbonne WC, Mathias J, Rae J, Dinauer MC, et al. Ischemic stroke injury is reduced in mice lacking a functional NADPH oxidase. Stroke. 1997;28: 2252-8.
33. + T suppressor cells. Expert Opinion on Biological Therapy. 2009;9: 951-65.
34. + T cells. The Journal of Immunology. 2005;175: 7093-7.
35. Noble A, Giorgini A, Jamie AL. Distinct suppressor T-cell lineage cytokine-induced IL-10-secreting CD8 T cells represent a phenotypically distinct suppressor T-cell lineage. Blood. 2006;107: 4475-83.
36. + T cells fine-tune the myelin basic protein-reactive T cell receptor Vβ repertoire during experimental autoimmune encephalomyelitis. PNAS. 2003;100: 8378-83.
37. Ishimaru N, Saegusa K, Yanagi K, Haneji N, Saito I, Hayashi Y. Estrogen deficiency accelerates autoimmune exocrinopathy in murine Sjögren's syndrome through fas-mediated apoptosis. The American Journal of Pathology. 1999;155: 173-81.
38. Marks MA, Gravitt PE, Burk RD, Studentsov Y, Farzadegan H, Klein SL. Progesterone and 17beta-estradiol enhance regulatory responses to human papillomavirus type 16 virus-like particles in peripheral blood mononuclear cells from healthy women. Clinical and Vaccine Immunology. 2010;17: 609-17.
39. Roof RL, Edward DH. Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. Journal of Neurotrauma. 2000;17: 367-88.
40. Zhang B, Subramanian S, Dziennis S, Jia J, Uchida M, Akiyoshi K, et al. Estradiol and G1 reduce infarct size and improve immunosuppression after experimental stroke. The Journal of Immunology. 2010;184: 4087-94.
41. Planas AM, Gómez-Choco M, Urra X, Gorina R, Caballero M, Chamorro Á. Brain-derived antigens in lymphoid tissue of patients with acute stroke. The Journal of Immunology. 2012;188: 2156-63.
42. Yilmaz G, Vital S, Yilmaz CE, Stokes KY, Alexander JS, Granger DN. Selectin-mediated recruitment of bone marrow stromal cells in the postischemic cerebral microvasculature. Stroke. 2011;42: 806-11.
43. Baron JL, Madri JA, Ruddle NH, Hashim G, Janeway Jr CA. Surface expression of alpha 4 integrin by CD4 T cells is required for their entry into brain parenchyma. The Journal of Experimental Medicine. 1993;177: 57-68.
44. Marques CP, Cheeran MC, Palmquist JM, Hu S, Urban SL, Lokensgard JR. Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. The Journal of Immunology. 2008;181: 6417-26.
45. Campanella M, Sciorati C, Tarozzo G, Beltramo M. Flow cytometric analysis of inflammatory cells in ischemic rat brain. Stroke. 2002;33: 586-92.
46. Ponomarev ED, Veremeyko T, Barteneva N, Krichevsky AM, Weiner HL. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU. 1 pathway. Nature Medicine. 2011;17: 64-70.