Functional recovery in aging mice after experimental stroke

Brain, Behavior, and Immunity

Volumn 25, Issue 8, 2011, Pages 1689-1700

  Manwani, Bharti ^a   Liu, Fudong ^a   Xu, Yan ^a   Persky, Rebecca ^a   Li, Jun ^a   McCullough, Louise D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Aging; Astrocytes; Cerebral atrophy; Cerebral blood flow (CBF); Cerebral ischemia; Functional recovery; GFAP (glial fibrillary acid protein); Glial scar; Iba1; Microglia

Indexed keywords

AGE; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BEHAVIOR DISORDER; BRAIN ATROPHY; BRAIN INFARCTION SIZE; CONTROLLED STUDY; GLIOSIS; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; STROKE;

AGING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; BRAIN CHEMISTRY; CALCIUM-BINDING PROTEINS; FUNCTIONAL LATERALITY; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; ISCHEMIC ATTACK, TRANSIENT; MALE; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; MOTOR ACTIVITY; MUSCLE STRENGTH; POSTURAL BALANCE; PSYCHOMOTOR PERFORMANCE; RECOVERY OF FUNCTION; STROKE;

EID: 80053893066     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.06.015     Document Type: Article

References (53)

1. Abe T., Kunz A., Shimamura M., Zhou P., Anrather J., Iadecola C. The neuroprotective effect of prostaglandin E2 EP1 receptor inhibition has a wide therapeutic window, is sustained in time and is not sexually dimorphic. J. Cereb. Blood Flow Metab. 2009, 29:66-72.
2. Anderson M.F., Blomstrand F., Blomstrand C., Eriksson P.S., Nilsson M. Astrocytes and stroke: networking for survival?. Neurochem. Res. 2003, 28:293-305.
3. Badan I., Buchhold B., Hamm A., Gratz M., Walker L.C., Platt D., Kessler C., Popa-Wagner A. Accelerated glial reactivity to stroke in aged rats correlates with reduced functional recovery. J. Cereb. Blood Flow Metab. 2003, 23:845-854.
4. Boche D., Cunningham C., Gauldie J., Perry V.H. Transforming growth factor-beta 1-mediated neuroprotection against excitotoxic injury in vivo. J. Cereb. Blood Flow Metab. 2003, 23:1174-1182.
5. Bouet V., Freret T., Toutain J., Divoux D., Boulouard M., Schumann-Bard P. Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp. Neurol. 2007, 203:555-567.
6. Colbourne F., Corbett D. Delayed postischemic hypothermia: a six month survival study using behavioral and histological assessments of neuroprotection. J. Neurosci. 1995, 15:7250-7260.
7. De Martinis M., Franceschi C., Monti D., Ginaldi L. Inflammation markers predicting frailty and mortality in the elderly. Exp. Mol. Pathol. 2006, 80:219-227.
8. Dickson D.W., Crystal H.A., Mattiace L.A., Masur D.M., Blau A.D., Davies P., Yen S.H., Aronson M.K. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol. Aging 1992, 13:179-189.
9. DiNapoli V.A., Huber J.D., Houser K., Li X., Rosen C.L. Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats. Neurobiol. Aging. 2008, 29:753-764.
10. Endres M., Engelhardt B., Koistinaho J., Lindvall O., Meairs S., Mohr J.P., Planas A., Rothwell N., Schwaninger M., Schwab M.E., Vivien D., Wieloch T., Dirnagl U. Improving outcome after stroke: overcoming the translational roadblock. Cerebrovasc. Dis. 2008, 25:268-278.
11. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res. Bull. 1999, 49:377-391.
12. Feigin V.L., Lawes C.M., Bennett D.A., Anderson C.S. Stroke epidemiology: a review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol. 2003, 2:43-53.
13. Flurkey, K., Currer, J.M., Harrison, D.E., 2007. The mouse in aging research. In: Fox, J.G. et al. (Eds.), The Mouse in Biomedical Research, 2nd ed. American College Laboratory Animal Medicine (Elsevier), Burlington, MA, 2007, pp. 637-672.
14. Frank M.G., Baratta M.V., Sprunger D.B., Watkins L.R., Maier S.F. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav. Immun. 2007, 21:47-59.
15. Godbout J.P., Johnson R.W. Age and neuroinflammation: a lifetime of psychoneuroimmune consequences. Immunol. Allergy Clin. North Am. 2009, 29:321-337.
16. Harrison, D.E., 2008. http://research.jax.org/faculty/harrison/ger1vi_LifeStudy1.html.
17. Hattori K., Lee H., Hurn P.D., Crain B.J., Traystman R.J., DeVries A.C. Cognitive deficits after focal cerebral ischemia in mice. Stroke 2000, 31:1939-1944.
18. Howard G., Toole J.F., Frye-Pierson J., Hinshelwood L.C. Factors influencing the survival of 451 transient ischemic attack patients. Stroke 1987, 18:552-557.
19. 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.
20. 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.
21. Katz R.J., Roth K.A., Carroll B.J. Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci. Biobehav. Rev. 1981, 5:247-251.
22. Lambertsen K.L., Clausen B.H., Babcock A.A., Gregersen R., Fenger C., Nielsen H.H., Haugaard L.S., Wirenfeldt M., Nielsen M., Dagnaes-Hansen F., Bluethmann H., Faergeman N.J., Meldgaard M., Deierborg T., Finsen B. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J. Neurosci. 2009, 29:1319-1330.
23. Li X., Blizzard K.K., Zeng Z., DeVries A.C., Hurn P.D., McCullough L.D. Chronic behavioral testing after focal ischemia in the mouse: functional recovery and the effects of gender. Exp. Neurol. 2004, 187:94-104.
24. Little A.R., O'Callagha J.P. Astrogliosis in the adult and developing CNS: is there a role for proinflammatory cytokines?. Neurotoxicology 2001, 22:607-618.
25. Liu F., McCullough L.D. Middle cerebral artery occlusion model in rodents: methods and potential pitfalls. J. Biomed. Biotechnol. 2011, 464701.
26. Liu F., Yuan R., Benashski S.E., McCullough L.D. Changes in experimental stroke outcome across the life span. J. Cereb. Blood Flow Metab. 2009, 29:792-802.
27. Liu F., Akella P., Benashski S.E., Xu Y., McCullough L.D. Expression of Na-K-Cl cotransporter and edema formation are age dependent after ischemic stroke. Exp. Neurol. 2010, 224:356-361.
28. Lucin K.M., Wyss-Coray T. Immune activation in brain aging and neurodegeneration: too much or too little?. Neuron 2009, 64:110-122.
29. Mckay, J., Mensah, G., 2004. The Atlas of Heart Disease and Stroke, WHO, 2004.
30. McCullough L.D., Zeng Z., Li H., Landree L.E., McFadden J., Ronnett G.V. Pharmacological inhibition of AMP-activated protein kinase provides neuroprotection in stroke. J. Biol. Chem. 2005, 280:20493-20502.
31. McGraw J., Hiebert G.W., Steeves J.D. Modulating astrogliosis after neurotrauma. J. Neurosci. Res. 2001, 63:109-115.
32. Miller R.A., Nadon N.L. Principles of animal use for gerontological research. J. Gerontol. A: Biol. Sci. Med. Sci. 2000, 55:B117-123.
33. Milot M.R., Plamondon H. Time-dependent effects of global cerebral ischemia on anxiety, locomotion, and habituation in rats. Behav. Brain Res. 2009, 200:173-180.
34. Nakayama H., Jorgensen H.S., Raaschou H.O., Olsen T.S. The influence of age on stroke outcome. The Copenhagen Stroke Study. Stroke 1994, 25:808-813.
35. Ogura K., Ogawa M., Yoshida M. Effects of ageing on microglia in the normal rat brain: immunohistochemical observations. Neuroreport 1994, 5:1224-1226.
36. Paylor R., Nguyen M., Crawley J.N., Patrick J., Beaudet A., Orr-Urtreger A. Alpha7 nicotinic receptor subunits are not necessary for hippocampal-dependent learning or sensorimotor gating: a behavioral characterization of Acra7-deficient mice. Learn Mem. 1998, 5:302-316.
37. Perry V.H., Newman T.A., Cunningham C. The impact of systemic infection on the progression of neurodegenerative disease. Nat. Rev. Neurosci. 2003, 4:103-112.
38. Peters A., Josephson K., Vincent S.L. Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex. Anat. Rec. 1991, 229:384-398.
39. Plamondon H., Khan S. Characterization of anxiety and habituation profile following global ischemia in rats. Physiol. Behav. 2005, 84:543-552.
40. Ridet J.L., Malhotra S.K., Privat A., Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 1997, 20:570-577.
41. Robinson R.G., Coyle J.T. The differential effect of right versus left hemispheric cerebral infarction on catecholamines and behavior in the rat. Brain Res. 1980, 188:63-78.
42. Roth K.A., Katz R.J. Stress, behavioral arousal, and open field activity-a reexamination of emotionality in the rat. Neurosci. Biobehav. Rev. 1979, 3:247-263.
43. Rudge J.S., Silver J. Inhibition of neurite outgrowth on astroglial scars in vitro. J. Neurosci. 1990, 10:3594-3603.
44. Shapira S., Sapir M., Wengier A., Grauer E., Kadar T. Aging has a complex effect on a rat model of ischemic stroke. Brain Res. 2002, 925:148-158.
45. Sheffield L.G., Berman N.E. Microglial expression of MHC class II increases in normal aging of nonhuman primates. Neurobiol. Aging. 1998, 19:47-55.
46. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
47. Smith C.J., Emsley H.C., Gavin C.M., Georgiou R.F., Vail A., Barberan E.M., del Zoppo G.J., Hallenbeck J.M., Rothwell N.J., Hopkins S.J., Tyrrell P.J. Peak plasma interleukin-6 and other peripheral markers of inflammation in the first week of ischaemic stroke correlate with brain infarct volume, stroke severity and long-term outcome. BMC Neurol. 2004, 4:2.
48. Sparkman N.L., Johnson R.W. Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. Neuroimmunomodulation 2008, 15:323-330.
49. Stroemer R.P., Kent T.A., Hulsebosch C.E. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 1995, 26:2135-2144.
50. Wahl F., Allix M., Plotkine M., Boulu R.G. Neurological and behavioral outcomes of focal cerebral ischemia in rats. Stroke 1992, 23:267-272.
51. Wang R.Y., Wang P.S., Yang Y.R. Effect of age in rats following middle cerebral artery occlusion. Gerontology 2003, 49:27-32.
52. Wang S.H., Zhang Z.J., Guo Y.J., Zhou H., Teng G.J., Chen B.A. Anhedonia and activity deficits in rats: impact of post-stroke depression. J. Psychopharmacol. 2009, 23:295-304.
53. Zhang L., Chen J., Li Y., Zhang Z.G., Chopp M. Quantitative measurement of motor and somatosensory impairments after mild (30min) and severe (2h) transient middle cerebral artery occlusion in rats. J. Neurol. Sci. 2000, 174:141-146.