Reversal of the Detrimental Effects of Post-Stroke Social Isolation by Pair-Housing is Mediated by Activation of BDNF-MAPK/ERK in Aged Mice

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Verma, Rajkumar ^a   Harris, Nia M ^a   Friedler, Brett D ^a   Crapser, Joshua ^a   Patel, Anita R ^a   Venna, Venugopal ^a   McCullough, Louise D ^a,b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; INTERLEUKIN 6; INTERLEUKIN-6, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL; BLOOD; CEREBROVASCULAR ACCIDENT; COMPLICATION; GENE EXPRESSION PROFILING; MALE; METABOLISM; MOUSE; NERVE CELL PLASTICITY; PATHOLOGY; SOCIAL ISOLATION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION PROFILING; INTERLEUKIN-6; MALE; MICE; NEURONAL PLASTICITY; SOCIAL ISOLATION; STROKE;

EID: 84964897040     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep25176     Document Type: Article

References (60)

1. Mozafarian, D. et al. Executive Summary: Heart Disease and Stroke Statistics-2016 Update: A Report From the American Heart Association. Circulation 133, 447-454, doi: 10.1161/CIR.0000000000000366 (2016).
2. Go, A. S. et al. Heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 129, e28-e292, doi: 10.1161/01.cir.0000441139.02102.80 (2014).
3. Popa-Wagner, A., Buga, A. M. & Kokaia, Z. Perturbed cellular response to brain injury during aging. Ageing research reviews 10, 71-79, doi: 10.1016/j.arr.2009.10.008 (2011).
4. Liu, F. et al. Age-related changes in AMP-activated protein kinase afer stroke. Age 34, 157-168, doi: 10.1007/s11357-011-9214-8 (2012).
5. Manwani, B. et al. Functional recovery in aging mice afer experimental stroke. Brain, behavior, and immunity 25, 1689-1700, doi: 10.1016/j.bbi.2011.06.015 (2011).
6. Buga, A. M., Di Napoli, M. & Popa-Wagner, A. Preclinical models of stroke in aged animals with or without comorbidities: role of neuroinfammation. Biogerontology 14, 651-662, doi: 10.1007/s10522-013-9465-0 (2013).
7. Burke, S. N. & Barnes, C. A. Neural plasticity in the ageing brain. Nature reviews. Neuroscience 7, 30-40, doi: 10.1038/nrn1809 (2006).
8. Ritzel, R. M. et al. Age-and location-related changes in microglial function. Neurobiology of aging, doi: 10.1016/j. neurobiolaging.2015.02.016 (2015).
9. Campuzano, O., Castillo-Ruiz, M. M., Acarin, L., Castellano, B. & Gonzalez, B. Increased levels of proinfammatory cytokines in the aged rat brain attenuate injury-induced cytokine response afer excitotoxic damage. Journal of neuroscience research 87, 2484-2497, doi: 10.1002/jnr.22074 (2009).
10. Petcu, E. B. et al. Cellular and molecular events underlying the dysregulated response of the aged brain to stroke: a mini-review. Gerontology 54, 6-17, doi: 10.1159/000112845 (2008).
11. Steptoe, A., Shankar, A., Demakakos, P. & Wardle, J. Social isolation, loneliness, and all-cause mortality in older men and women. Proceedings of the National Academy of Sciences of the United States of America 110, 5797-5801, doi: 10.1073/pnas.1219686110 (2013).
12. Cacioppo, J. T., Hawkley, L. C. & Tisted, R. A. Perceived social isolation makes me sad: 5-year cross-lagged analyses of loneliness and depressive symptomatology in the Chicago Health, Aging, and Social Relations Study. Psychology and aging 25, 453-463, doi: 10.1037/a0017216 (2010).
13. Cornwell, E. Y. & Waite, L. J. Social disconnectedness, perceived isolation, and health among older adults. Journal of health and social behavior 50, 31-48 (2009).
14. Henderson, K. M. et al. Psychosocial distress and stroke risk in older adults. Stroke; a journal of cerebral circulation 44, 367-372, doi: 10.1161/STROKEAHA.112.679159 (2013).
15. Perissinotto, C. M., Stijacic Cenzer, I. & Covinsky, K. E. Loneliness in older persons: a predictor of functional decline and death. Archives of internal medicine 172, 1078-1083, doi: 10.1001/archinternmed.2012.1993 (2012).
16. Tomaka, J., Tompson, S. & Palacios, R. The relation of social isolation, loneliness, and social support to disease outcomes among the elderly. Journal of aging and health 18, 359-384, doi: 10.1177/0898264305280993 (2006).
17. Boden-Albala, B., Litwak, E., Elkind, M. S., Rundek, T. & Sacco, R. L. Social isolation and outcomes post stroke. Neurology 64, 1888-1892, doi: 10.1212/01.WNL.0000163510.79351.AF (2005).
18. Friedler, B., Crapser, J. & McCullough, L. One is the deadliest number: the detrimental efects of social isolation on cerebrovascular diseases and cognition. Acta neuropathologica 129, 493-509, doi: 10.1007/s00401-014-1377-9 (2015).
19. Liu, J. et al. Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nature neuroscience 15, 1621-1623, doi: 10.1038/nn.3263 (2012).
20. Pereda-Perez, I. et al. Long-term social isolation in the adulthood results in CA1 shrinkage and cognitive impairment. Neurobiology of learning and memory 106, 31-39, doi: 10.1016/j.nlm.2013.07.004 (2013).
21. McKenzie, I. A. et al. Motor skill learning requires active central myelination. Science 346, 318-322, doi: 10.1126/science.1254960 (2014).
22. Fields, R. D. White matter in learning, cognition and psychiatric disorders. Trends in neurosciences 31, 361-370, doi: 10.1016/j. tins.2008.04.001 (2008).
23. O'Keefe, L. M. et al. Social isolation afer stroke leads to depressive-like behavior and decreased BDNF levels in mice. Behavioural brain research 260, 162-170, doi: 10.1016/j.bbr.2013.10.047 (2014).
24. Chourbaji, S. et al. The impact of environmental enrichment on sex-specifc neurochemical circuitries-efects on brain-derived neurotrophic factor and the serotonergic system. Neuroscience 220, 267-276, doi: 10.1016/j.neuroscience.2012.06.016 (2012).
25. Endres, T. & Lessmann, V. Age-dependent defcits in fear learning in heterozygous BDNF knock-out mice. Learning & memory 19, 561-570, doi: 10.1101/lm.028068.112 (2012).
26. Karelina, K. et al. Oxytocin mediates social neuroprotection afer cerebral ischemia. Stroke; a journal of cerebral circulation 42, 3606-3611, doi: 10.1161/STROKEAHA.111.628008 (2011).
27. Verma, R., Friedler, B. D., Harris, N. M. & McCullough, L. D. Pair housing reverses post-stroke depressive behavior in mice. Behavioural brain research 269, 155-163, doi: 10.1016/j.bbr.2014.04.044 (2014).
28. Karelina, K. et al. Social isolation alters neuroinfammatory response to stroke. Proceedings of the National Academy of Sciences of the United States of America 106, 5895-5900, doi: 10.1073/pnas.0810737106 (2009).
29. Venna, V. R. et al. NF-kappaB contributes to the detrimental effects of social isolation after experimental stroke. Acta neuropathologica 124, 425-438, doi: 10.1007/s00401-012-0990-8 (2012).
30. Cojocaru, G. R., Popa-Wagner, A., Stanciulescu, E. C., Babadan, L. & Buga, A. M. Post-stroke depression and the aging brain. Journal of molecular psychiatry 1, 14, doi: 10.1186/2049-9256-1-14 (2013).
31. Ostwald, S. K., Wasserman, J. & Davis, S. Medications, comorbidities, and medical complications in stroke survivors: the CAReS study. Rehabilitation nursing: the ofcial journal of the Association of Rehabilitation Nurses 31, 10-14 (2006).
32. Barth, J., Schneider, S. & von Kanel, R. Lack of social support in the etiology and the prognosis of coronary heart disease: a systematic review and meta-analysis. Psychosomatic medicine 72, 229-238, doi: 10.1097/PSY.0b013e3181d01611 (2010).
33. Cohen, S., Doyle, W. J., Skoner, D. P., Rabin, B. S. & Gwaltney, J. M., Jr. Social ties and susceptibility to the common cold. Jama 277, 1940-1944 (1997).
34. Bassuk, S. S., Glass, T. A. & Berkman, L. F. Social disengagement and incident cognitive decline in community-dwelling elderly persons. Annals of internal medicine 131, 165-173 (1999).
35. Beadle, J. N., Yoon, C. & Gutchess, A. H. Age-related neural diferences in afliation and isolation. Cognitive, afective & behavioral neuroscience 12, 269-279, doi: 10.3758/s13415-012-0085-y (2012).
36. Buchhold, B. et al. Environmental enrichment improves functional and neuropathological indices following stroke in young and aged rats. Restorative neurology and neuroscience 25, 467-484 (2007).
37. Suenaga, J. et al. White matter injury and microglia/macrophage polarization are strongly linked with age-related long-term defcits in neurological function afer stroke. Experimental neurology 272, 109-119, doi: 10.1016/j.expneurol.2015.03.021 (2015).
38. Ceulemans, A. G. et al. The dual role of the neuroinfammatory response afer ischemic stroke: modulatory efects of hypothermia. Journal of neuroinfammation 7, 74, doi: 10.1186/1742-2094-7-74 (2010).
39. Clarkson, A. N., Parker, K., Nilsson, M., Walker, F. R. & Gowing, E. K. Combined ampakine and BDNF treatments enhance poststroke functional recovery in aged mice via AKT-CREB signaling. Journal of cerebral blood fow and metabolism: ofcial journal of the International Society of Cerebral Blood Flow and Metabolism, doi: 10.1038/jcbfm.2015.33 (2015).
40. Markus, T. M. et al. Recovery and brain reorganization afer stroke in adult and aged rats. Annals of neurology 58, 950-953, doi: 10.1002/ana.20676 (2005).
41. Martino, G., Pluchino, S., Bonfanti, L. & Schwartz, M. Brain regeneration in physiology and pathology: the immune signature driving therapeutic plasticity of neural stem cells. Physiological reviews 91, 1281-1304, doi: 10.1152/physrev.00032.2010 (2011).
42. Silver, J. & Miller, J. H. Regeneration beyond the glial scar. Nature reviews. Neuroscience 5, 146-156, doi: 10.1038/nrn1326 (2004).
43. Fawcett, J. W. & Asher, R. A. The glial scar and central nervous system repair. Brain research bulletin 49, 377-391 (1999).
44. Li, H. et al. Histological, cellular and behavioral assessments of stroke outcomes afer photothrombosis-induced ischemia in adult mice. BMC neuroscience 15, 58, doi: 10.1186/1471-2202-15-58 (2014).
45. Lu, B., Nagappan, G., Guan, X., Nathan, P. J. & Wren, P. BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nature reviews. Neuroscience 14, 401-416, doi: 10.1038/nrn3505 (2013).
46. Barrientos, R. M. et al. Brain-derived neurotrophic factor mRNA downregulation produced by social isolation is blocked by intrahippocampal interleukin-1 receptor antagonist. Neuroscience 121, 847-853 (2003).
47. Lommatzsch, M. et al. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiology of aging 26, 115-123, doi: 10.1016/j.neurobiolaging.2004.03.002 (2005).
48. Jovanovic, J. N., Czernik, A. J., Fienberg, A. A., Greengard, P. & Sihra, T. S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nature neuroscience 3, 323-329, doi: 10.1038/73888 (2000).
49. Clarkson, A. N., Huang, B. S., Macisaac, S. E., Mody, I. & Carmichael, S. T. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery afer stroke. Nature 468, 305-309, doi: 10.1038/nature09511 (2010).
50. Collinson, N. et al. Enhanced learning and memory and altered GABAergic synaptic transmission in mice lacking the alpha 5 subunit of the GABAA receptor. The Journal of neuroscience: the ofcial journal of the Society for Neuroscience 22, 5572-5580, doi: 20026436 (2002).
51. Carmichael, S. T. Brain excitability in stroke: the yin and yang of stroke progression. Archives of neurology 69, 161-167, doi: 10.1001/archneurol.2011.1175 (2012).
52. Mattson, M. P. & Mefert, M. K. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell death and diferentiation 13, 852-860, doi: 10.1038/sj.cdd.4401837 (2006).
53. Ramos-Cejudo, J. et al. Spatial and temporal gene expression diferences in core and periinfarct areas in experimental stroke: a microarray analysis. Plos one 7, e52121, doi: 10.1371/journal.pone.0052121 (2012).
54. Vondran, M. W., Clinton-Luke, P., Honeywell, J. Z. & Dreyfus, C. F. BDNF+/-mice exhibit defcits in oligodendrocyte lineage cells of the basal forebrain. Glia 58, 848-856, doi: 10.1002/glia.20969 (2010).
55. Xiao, J. et al. Brain-derived neurotrophic factor promotes central nervous system myelination via a direct effect upon oligodendrocytes. Neuro-Signals 18, 186-202, doi: 10.1159/000323170 (2010).
56. Aggleton, J. P., Albasser, M. M., Aggleton, D. J., Poirier, G. L. & Pearce, J. M. Lesions of the rat perirhinal cortex spare the acquisition of a complex confgural visual discrimination yet impair object recognition. Behavioral neuroscience 124, 55-68, doi: 10.1037/a0018320 (2010).
57. Venna, V. R., Xu, Y., Doran, S. J., Patrizz, A. & McCullough, L. D. Social interaction plays a critical role in neurogenesis and recovery afer stroke. Translational psychiatry 4, e351, doi: 10.1038/tp.2013.128 (2014).
58. Li, J., Zeng, Z., Viollet, B., Ronnett, G. V. & McCullough, L. D. Neuroprotective efects of adenosine monophosphate-activated protein kinase inhibition and gene deletion in stroke. Stroke; a journal of cerebral circulation 38, 2992-2999, doi: 10.1161/STROKEAHA.107.490904 (2007).
59. Ennaceur, A. & Delacour, J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioural brain research 31, 47-59 (1988).
60. Leger, M. et al. Object recognition test in mice. Nature protocols 8, 2531-2537, doi: 10.1038/nprot.2013.155 (2013).