Age-related frontal periventricular white matter hyperintensities and miR-92a-3p are associated with early-onset post-stroke depression

Frontiers in Aging Neuroscience

Volumn 9, Issue OCT, 2017, Pages

  He, Ji Rong ^a   Zhang, Yu ^a   Lu, Wen Jing ^a   Liang, Huai Bin ^a   Tu, Xuan Qiang ^a   Ma, Fei Yue ^a   Yang, Guo Yuan ^a   Zeng, Li Li ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Depression; Frontal caps; microRNA; Stroke; White matter hyperintensities

Indexed keywords

MICRORNA; MICRORNA 92A 3P; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BRAIN INFARCTION; BRAIN VENTRICLE; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; FRONTAL CORTEX; GENETIC ASSOCIATION; HUMAN; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PERIVENTRICULAR WHITE MATTER HYPERINTENSITY; POST-STROKE DEPRESSION; PREDICTION; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; WHITE MATTER;

EID: 85031111471     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2017.00328     Document Type: Article

References (60)

1. Becker, K. J. (2016). Inflammation and the silent sequelae of stroke. Neurotherapeutics 13, 801-810. doi: 10.1007/s13311-016-0451-5
2. Berg, A., Palomaki, H., Lehtihalmes, M., Lonnqvist, J., and Kaste, M. (2003). Poststroke depression: an 18-month follow-up. Stroke 34, 138-143. doi: 10.1161/01.STR.0000048149.84268.07
3. Chemerinski, E., Robinson, R. G., and Kosier, J. T. (2001). Improved recovery in activities of daily living associated with remission of poststroke depression. Stroke 32, 113-117. doi: 10.1161/01.STR.32.1.113
4. Daniel, J. M., Penzkofer, D., Teske, R., Dutzmann, J., Koch, A., Bielenberg, W., et al. (2014). Inhibition of miR-92a improves re-endothelialization and prevents neointima formation following vascular injury. Cardiovasc. Res. 103, 564-572. doi: 10.1093/cvr/cvu162
5. de Groot, J. C., De Leeuw, F. E., Oudkerk, M., Van Gijn, J., Hofman, A., Jolles, J., et al. (2000). Cerebral white matter lesions and cognitive function: the rotterdam scan study. Ann. Neurol. 47, 145-151. doi: 10.1002/1531-8249(200002)47:2<145::AID-ANA3>3.0.CO;2-P
6. de Leeuw, F. E., De Groot, J. C., Achten, E., Oudkerk, M., Ramos, L. M., Heijboer, R., et al. (2001). Prevalence of cerebral white matter lesions in elderly people: a population based magnetic resonance imaging study. The Rotterdam Scan Study. J. Neurol. Neurosurg. Psychiatry 70, 9-14. doi: 10.1136/jnnp.70.1.9
7. Di Napoli, M., Godoy, D. A., Campi, V., Masotti, L., Smith, C. J., Parry Jones, A. R., et al. (2012). C-reactive protein in intracerebral hemorrhage: time course, tissue localization, and prognosis. Neurology 79, 690-699. doi: 10.1212/WNL.0b013e318264e3be
8. Esparrago Llorca, G., Castilla-Guerra, L., Fernandez Moreno, M. C., Ruiz Doblado, S., and Jimenez Hernandez, M. D. (2015). Post-stroke depression: an update. Neurologia 30, 23-31. doi: 10.1016/j.nrl.2012.06.008
9. Fazekas, F., Chawluk, J. B., Alavi, A., Hurtig, H. I., and Zimmerman, R. A. (1987). MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am. J. Roentgenol. 149, 351-356. doi: 10.2214/ajr.149.2.351
10. Fazekas, F., Kleinert, R., Offenbacher, H., Schmidt, R., Kleinert, G., Payer, F., et al. (1993). Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 43, 1683-1689. doi: 10.1212/WNL.43.9.1683
11. Gunning-Dixon, F. M., and Raz, N. (2000). The cognitive correlates of white matter abnormalities in normal aging: a quantitative review. Neuropsychology 14, 224-232. doi: 10.1037/0894-4105.14.2.224
12. Herrmann, N., Black, S. E., Lawrence, J., Szekely, C., and Szalai, J. P. (1998). The sunnybrook stroke study: a prospective study of depressive symptoms and functional outcome. Stroke 29, 618-624. doi: 10.1161/01.STR.29.3.618
13. House, A., Knapp, P., Bamford, J., and Vail, A. (2001). Mortality at 12 and 24 months after stroke may be associated with depressive symptoms at 1 month. Stroke 32, 696-701. doi: 10.1161/01.STR.32.3.696
14. Jiang, X. G., Lin, Y., and Li, Y. S. (2014). Correlative study on risk factors of depression among acute stroke patients. Eur. Rev. Med. Pharmacol. Sci. 18, 1315-1323.
15. Kang, H. J., Stewart, R., Park, M. S., Bae, K. Y., Kim, S. W., Kim, J. M., et al. (2013). White matter hyperintensities and functional outcomes at 2 weeks and 1 year after stroke. Cerebrovasc. Dis. 35, 138-145. doi: 10.1159/000346604
16. Kapeller, P., Barber, R., Vermeulen, R. J., Ader, H., Scheltens, P., Freidl, W., et al. (2003). Visual rating of age-related white matter changes on magnetic resonance imaging: scale comparison, interrater agreement, and correlations with quantitative measurements. Stroke 34, 441-445. doi: 10.1161/01.STR.0000049766.26453.E9
17. Kawano, M., Kanazawa, T., Kikuyama, H., Tsutsumi, A., Kinoshita, S., Kawabata, Y., et al. (2016). Correlation between frontal lobe oxy-hemoglobin and severity of depression assessed using near-infrared spectroscopy. J. Affect. Disord. 205, 154-158. doi: 10.1016/j.jad.2016.07.013
18. Kynast, J., Lampe, L., Luck, T., Frisch, S., Arelin, K., Hoffmann, K. T., et al. (2017). White matter hyperintensities associated with small vessel disease impair social cognition beside attention and memory. J. Cereb. Blood Flow Metab. doi: 10.1177/0271678X17719380 [Epub ahead of print].
19. Larson, S. L., Owens, P. L., Ford, D., and Eaton, W. (2001). Depressive disorder, dysthymia, and risk of stroke: thirteen-year follow-up from the Baltimore epidemiologic catchment area study. Stroke 32, 1979-1983. doi: 10.1161/hs0901.094623
20. Leentjens, A. F., Aben, I., Lodder, J., and Verhey, F. R. (2006). General and disease-specific risk factors for depression after ischemic stroke: a two-step Cox regression analysis. Int. Psychogeriatr. 18, 739-748. doi: 10.1017/S1041610206003486
21. Leys, D., Soetaert, G., Petit, H., Fauquette, A., Pruvo, J. P., and Steinling, M. (1990). Periventricular and white matter magnetic resonance imaging hyperintensities do not differ between Alzheimer's disease and normal aging. Arch. Neurol. 47, 524-527. doi: 10.1001/archneur.1990.00530050040010
22. Li, Y., Li, M., Zhang, X., Shi, Q., Yang, S., Fan, H., et al. (2017). Higher blood-brain barrier permeability is associated with higher white matter hyperintensities burden. J. Neurol. 264, 1474-1481. doi: 10.1007/s00415-017-8550-8
23. Lin, J., Wang, D., Lan, L., and Fan, Y. (2017). Multiple factors involved in the pathogenesis of white matter lesions. Biomed. Res. Int. 2017:9372050. doi: 10.1155/2017/9372050
24. Loubinoux, I., Kronenberg, G., Endres, M., Schumann-Bard, P., Freret, T., Filipkowski, R. K., et al. (2012). Post-stroke depression: mechanisms, translation and therapy. J. Cell Mol. Med. 16, 1961-1969. doi: 10.1111/j.1582-4934.2012.01555.x
25. Loyer, X., Potteaux, S., Vion, A. C., Guerin, C. L., Boulkroun, S., Rautou, P. E., et al. (2014). Inhibition of microRNA-92a prevents endothelial dysfunction and atherosclerosis in mice. Circ. Res. 114, 434-443. doi: 10.1161/CIRCRESAHA.114.302213
26. May, M., Mccarron, P., Stansfeld, S., Ben-Shlomo, Y., Gallacher, J., Yarnell, J., et al. (2002). Does psychological distress predict the risk of ischemic stroke and transient ischemic attack? The Caerphilly Study. Stroke 33, 7-12. doi: 10.1161/hs0102.100529
27. Meader, N., Moe-Byrne, T., Llewellyn, A., and Mitchell, A. J. (2014). Screening for poststroke major depression: a meta-analysis of diagnostic validity studies. J. Neurol. Neurosurg. Psychiatry 85, 198-206. doi: 10.1136/jnnp-2012-304194
28. Miyamoto, N., Pham, L. D., Seo, J. H., Kim, K. W., Lo, E. H., and Arai, K. (2014). Crosstalk between cerebral endothelium and oligodendrocyte. Cell Mol. Life. Sci. 71, 1055-1066. doi: 10.1007/s00018-013-1488-9
29. Morris, P. L., Robinson, R. G., Andrzejewski, P., Samuels, J., and Price, T. R. (1993). Association of depression with 10-year poststroke mortality. Am. J. Psychiatry 150, 124-129. doi: 10.1176/ajp.150.1.124
30. Nys, G. M., Van Zandvoort, M. J., Van Der Worp, H. B., De Haan, E. H., De Kort, P. L., and Kappelle, L. J. (2005). Early depressive symptoms after stroke: neuropsychological correlates and lesion characteristics. J. Neurol. Sci. 228, 27-33. doi: 10.1016/j.jns.2004.09.031
31. Parikh, R. M., Robinson, R. G., Lipsey, J. R., Starkstein, S. E., Fedoroff, J. P., and Price, T. R. (1990). The impact of poststroke depression on recovery in activities of daily living over a 2-year follow-up. Arch. Neurol. 47, 785-789. doi: 10.1001/archneur.1990.00530070083014
32. Perez, J., and Tardito, D. (2002). The interface between depression and cerebrovascular disease-some hope but no hype. Clin. Exp. Hypertens 24, 639-646. doi: 10.1081/CEH-120015340
33. Popa-Wagner, A., Buga, A. M., Tica, A. A., and Albu, C. V. (2014). Perfusion deficits, inflammation and aging precipitate depressive behaviour. Biogerontology 15, 439-448. doi: 10.1007/s10522-014-9516-1
34. Richter, N., Michel, A., Onur, O. A., Kracht, L., Dietlein, M., Tittgemeyer, M., et al. (2017). White matter lesions and the cholinergic deficit in aging and mild cognitive impairment. Neurobiol. Aging 53, 27-35. doi: 10.1016/j.neurobiolaging.2017.01.012
35. Rincon, F., and Wright, C. B. (2014). Current pathophysiological concepts in cerebral small vessel disease. Front. Aging Neurosci. 6:24. doi: 10.3389/fnagi.2014.00024
36. Robinson, R. G., and Jorge, R. E. (2016). Post-stroke depression: a review. Am. J. Psychiatry 173, 221-231. doi: 10.1176/appi.ajp.2015.15030363
37. Sandu, R. E., Buga, A. M., Uzoni, A., Petcu, E. B., and Popa-Wagner, A. (2015). Neuroinflammation and comorbidities are frequently ignored factors in CNS pathology. Neural Regen. Res. 10, 1349-1355. doi: 10.4103/1673-5374.165208
38. Santos, A., Resmini, E., Gomez-Anson, B., Crespo, I., Granell, E., Valassi, E., et al. (2015). Cardiovascular risk and white matter lesions after endocrine control of Cushing's syndrome. Eur. J. Endocrinol. 173, 765-775. doi: 10.1530/EJE-15-0600
39. Scheltens, P., Barkhof, F., Leys, D., Pruvo, J. P., Nauta, J. J., Vermersch, P., et al. (1993). A semiquantative rating scale for the assessment of signal hyperintensities on magnetic resonance imaging. J. Neurol. Sci. 114, 7-12. doi: 10.1016/0022-510X(93)90041-V
40. Scheltens, P., Erkinjunti, T., Leys, D., Wahlund, L. O., Inzitari, D., Del Ser, T., et al. (1998). White matter changes on CT and MRI: an overview of visual rating scales. European task force on age-related white matter changes. Eur. Neurol. 39, 80-89. doi: 10.1159/000007921
41. Schulte, C., and Zeller, T. (2015). microRNA-based diagnostics and therapy in cardiovascular disease-Summing up the facts. Cardiovasc. Diagn. Ther. 5, 17-36. doi: 10.3978/j.issn.2223-3652.2014.12.03
42. Serafini, G., Pompili, M., Hansen, K. F., Obrietan, K., Dwivedi, Y., Shomron, N., et al. (2014). The involvement of microRNAs in major depression, suicidal behavior, and related disorders: a focus on miR-185 and miR-491-3p. Cell. Mol. Neurobiol. 34, 17-30. doi: 10.1007/s10571-013-9997-5
43. Shi, Y. Z., Xiang, Y. T., Wu, S. L., Zhang, N., Zhou, J., Bai, Y., et al. (2014). The relationship between frontal lobe lesions, course of post-stroke depression, and 1-year prognosis in patients with first-ever ischemic stroke. PLOS ONE 9:e100456. doi: 10.1371/journal.pone.0100456
44. Shibata, K., Nishimura, Y., Otsuka, K., and Sakura, H. (2016). Influence of cerebral white matter hyperintensities on cognitive impairment in elderly medical patients. Geriatr. Gerontol. Int. doi: 10.1111/ggi.12900 [Epub ahead of print].
45. Slevin, M., Matou, S., Zeinolabediny, Y., Corpas, R., Weston, R., Liu, D., et al. (2015). Monomeric C-reactive protein-a key molecule driving development of Alzheimer's disease associated with brain ischaemia? Sci. Rep. 5:13281. doi: 10.1038/srep13281
46. Sun, A. X., Crabtree, G. R., and Yoo, A. S. (2013). MicroRNAs: regulators of neuronal fate. Curr. Opin. Cell Biol. 25, 215-221. doi: 10.1016/j.ceb.2012.12.007
47. Szolnoki, Z. (2007). Pathomechanism of leukoaraiosis: a molecular bridge between the genetic, biochemical, and clinical processes (a mitochondrial hypothesis). Neuromolecular Med. 9, 21-33. doi: 10.1385/NMM:9:1:21
48. Tanaka, T., Shimizu, T., and Fukuhara, T. (2009). The relationship between leukoaraiosis volume and parameters of carotid artery duplex ultrasonographic scanning in asymptomatic diabetic patients. Comput. Med. Imaging Graph. 33, 489-493. doi: 10.1016/j.compmedimag.2009.04.007
49. Tang, W. K., Chen, Y. K., Lu, J. Y., Chu, W. C., Mok, V. C., Ungvari, G. S., et al. (2010). White matter hyperintensities in post-stroke depression: a case control study. J. Neurol. Neurosurg. Psychiatry 81, 1312-1315. doi: 10.1136/jnnp.2009.203141
50. Turner-Stokes, L., and Hassan, N. (2002). Depression after stroke: a review of the evidence base to inform the development of an integrated care pathway. Part 2: treatment alternatives. Clin. Rehabil. 16, 248-260. doi: 10.1191/0269215502cr488oa
51. Vataja, R., Pohjasvaara, T., Leppavuori, A., Mantyla, R., Aronen, H. J., Salonen, O., et al. (2001). Magnetic resonance imaging correlates of depression after ischemic stroke. Arch. Gen. Psychiatry 58, 925-931. doi: 10.1001/archpsyc.58.10.925
52. Williams, L. S., Ghose, S. S., and Swindle, R. W. (2004). Depression and other mental health diagnoses increase mortality risk after ischemic stroke. Am. J. Psychiatry 161, 1090-1095. doi: 10.1176/appi.ajp.161.6.1090
53. Wiszniewska, M., Devuyst, G., Bogousslavsky, J., Ghika, J., and Van Melle, G. (2000). What is the significance of leukoaraiosis in patients with acute ischemic stroke? Arch. Neurol. 57, 967-973.
54. Witwer, K. W. (2015). Circulating microRNA biomarker studies: pitfalls and potential solutions. Clin. Chem. 61, 56-63. doi: 10.1373/clinchem.2014.221341
55. Yang, S., Hua, P., Shang, X., Cui, Z., Zhong, S., Gong, G., et al. (2015). A significant risk factor for poststroke depression: the depression-related subnetwork. J. Psychiatry Neurosci. 40, 259-268. doi: 10.1503/jpn.140086
56. Zeng, L., He, X., Liu, J., Wang, L., Weng, S., Wang, Y., et al. (2013a). Differences of circulating inflammatory markers between large- and small vessel disease in patients with acute ischemic stroke. Int. J. Med. Sci. 10, 1399-1405. doi: 10.7150/ijms.6652
57. Zeng, L., Wang, Y., Liu, J., Wang, L., Weng, S., Chen, K., et al. (2013b). Pro-inflammatory cytokine network in peripheral inflammation response to cerebral ischemia. Neurosci. Lett. 548, 4-9. doi: 10.1016/j.neulet.2013.04.037
58. Zhang, T., Wang, C., Liu, L., Zhao, X., Xue, J., Zhou, Y., et al. (2010). A prospective cohort study of the incidence and determinants of post-stroke depression among the mainland Chinese patients. Neurol. Res. 32, 347-352. doi: 10.1179/016164110X12656393665125
59. Zhang, Y., Cheng, L., Chen, Y., Yang, G. Y., Liu, J., and Zeng, L. (2016). Clinical predictor and circulating microRNA profile expression in patients with early onset post-stroke depression. J. Affect. Disord. 193, 51-58. doi: 10.1016/j.jad.2015.12.061
60. Zheng, J. J., Delbaere, K., Close, J. C., Sachdev, P. S., and Lord, S. R. (2011). Impact of white matter lesions on physical functioning and fall risk in older people: a systematic review. Stroke 42, 2086-2090. doi: 10.1161/STROKEAHA.110.610360