Matrix metalloproteinases are associated with increased blood-brain barrier opening in vascular cognitive impairment
Open accessAbstract
Background and Purpose—: Subcortical ischemic vascular disease (SIVD) is a major form of vascular cognitive impairment (VCI) due to small vessel disease. Matrix metalloproteinases (MMPs) are neutral proteases that disrupt the blood–brain barrier and degrade myelin basic protein under conditions of neuroinflammation. Brain tissues and cerebrospinal fluid (CSF) of patients with VCI have increased levels of MMPs. We hypothesized that patients with SIVD have increased MMPs in the CSF, which are associated with increased CSF albumin. Methods—: We studied 60 patients with suspected VCI. Twenty-five were classified as SIVD, whereas other groups included mixed Alzheimer disease and VCI, multiple strokes, and leukoaraiosis when white matter lesions were present and the diagnosis of VCI was uncertain. MMP-2 and MMP-9 in CSF and plasma were measured by gel zymography and indexed to CSF and plasma albumin. MMP-3 activity was measured by fluorescent assay. Results—: We found reduced MMP-2 index ( P <0.001) in the CSF for the full group of patients (SIVD, multiple strokes, mixed Alzheimer disease and VCI, and leukoaraiosis) compared with control subjects, whose CSF was obtained during spinal anesthesia. MMP-3 activity was increased in VCI compared with control subjects ( P <0.01). In SIVD, MMP-2 index showed a negative correlation with albumin index, which was absent with the MMP-9 index. Combining MMP-2 index and MMP-3 activity separated the patients with SIVD from the control subjects with high specificity ( P <0.0005). Conclusions—: Our results support the hypothesis that MMPs are associated with increased CSF albumin and suggest that they may contribute to the pathophysiology of SIVD.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Plasma albumin is increased in the cerebrospinal fluid of patients with vascular cognitive impairment, reflecting blood-brain barrier breakdown.
“First, the plasma protein albumin is increased in the CSF of patient with VCI, reflecting BBB breakdown (Candelario-Jalil et al., 2011).”
From The Pathobiology of Vascular Dementia (2013) · cites this paper as Candelario-Jalil et al., 2011
In a similar model, blood-brain barrier alteration was due to MMP9 production by oligodendrocyte precursors, which are increased in ischemic white matter injury in rodents and in patients with vascular cognitive impairment.
“In a similar model, the BBB alteration was found to be due to MMP9 production by oligodendrocyte precursors, which are increased in ischemic white matter injury in rodent models (Seo et al., 2013) and in patients with VCI (Candelario-Jalil et al., 2011).”
From The Pathobiology of Vascular Dementia (2013) · cites this paper as Candelario-Jalil et al., 2011
Pathological studies show markers of oxidative stress and inflammation in damaged white matter associated with vascular cognitive impairment.
“Pathological studies have shown markers of oxidative stress (isoprostanes) and inflammation (cytokines and adhesion molecules) in the damaged white matter associated with VCI (Back et al., 2011; Candelario-Jalil et al., 2011; Fernando et al., 2006).”
From The Pathobiology of Vascular Dementia (2013) · cites this paper as Candelario-Jalil et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Hachinski, V., Iadecola, C., Petersen, R. C., Breteler, M. M., Nyenhuis, D. L., Black, S. E., Powers, W. J., DeCarli, C., Merino, J. G., Kalaria, R. N., et al. (2006) · Stroke · doi:10.1161/01.str.0000237236.88823.47 · Cited by 1,722 · see citing works
Self-citationSubcortical ischaemic vascular dementia
Román, G. C., Erkinjuntti, T., Wallin, A., Pantoni, L., & Chui, H. C. (2002) · The Lancet Neurology · doi:10.1016/s1474-4422(02)00190-4 · Cited by 1,067 · see citing works
Yang, Y., Estrada, E. Y., Thompson, J. F., Liu, W., & Rosenberg, G. A. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600375 · Cited by 1,060 · see citing works
Self-citationIs Breakdown of the Blood-Brain Barrier Responsible for Lacunar Stroke, Leukoaraiosis, and Dementia?
Wardlaw, J. M., Sandercock, P. A. G., Dennis, M. S., & Starr, J. (2003) · Stroke · doi:10.1161/01.str.0000058480.77236.b3 · Cited by 628 · see citing works
Matrix metalloproteinases and their multiple roles in neurodegenerative diseases
Rosenberg, G. A. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70016-x · Cited by 594 · see citing works
Self-citationCandelario‐Jalil, E., Yang, Y., & Rosenberg, G. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.025 · Cited by 524 · see citing works
Self-citationLacunar stroke is associated with diffuse blood-brain barrier dysfunction
Wardlaw, J. M., Doubal, F., Armitage, P., Chappell, F., Carpenter, T., Muñoz Maniega, S., Farrall, A., Sudlow, C., Dennis, M., & Dhillon, B. (2009) · Annals of Neurology · doi:10.1002/ana.21549 · Cited by 364 · see citing works
Clark, A. W., Krekoski, C. A., Bou, S.-S., Chapman, K. R., & Edwards, D. R. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00859-8 · Cited by 328 · see citing works
Matrix metalloproteinases degrade myelin basic protein
Chandler, S., Coates, R. E., Gearing, A. J. H., Lury, J., Wells, G., & Bone, E. A. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)12173-0 · Cited by 294 · see citing works
Maeda, A., & Sobel, R. A. (1996) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199603000-00005 · Cited by 293 · see citing works
Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke
Anthony, D. C., Ferguson, B., Matyzak, M. K., Miller, K., Esiri, M. M., & Perry, V. H. (1997) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1997.tb01315.x · Cited by 268 · see citing works
Nagase, H., Fields, C. G., & Fields, G. B. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31914-2 · Cited by 249 · see citing works
Binswanger's disease--revisited
Caplan, L. R. (1995) · Neurology · doi:10.1212/wnl.45.4.626 · Cited by 227 · see citing works
White matter damage is associated with matrix metalloproteinases in vascular dementia
Rosenberg, G. A., Sullivan, N., & Esiri, M. M. (2001) · Stroke · doi:10.1161/01.str.32.5.1162 · Cited by 207 · see citing works
Self-citationClinical diagnosis of Binswanger's disease.
Bennett, D. A., Wilson, R. S., Gilley, D. W., & Fox, J. H. (1990) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.53.11.961 · Cited by 195 · see citing works
Binswanger's encephalopathy: a review
Fisher, C. M. (1989) · Journal of Neurology · doi:10.1007/bf00314400 · Cited by 188 · see citing works
White matter lesion progression
Schmidt, R., Scheltens, P., Erkinjuntti, T., Pantoni, L., Markus, H. S., Wallin, A., Barkhof, F., & Fazekas, F. (2004) · Neurology · doi:10.1212/01.wnl.0000132635.75819.e5 · Cited by 176 · see citing works
OLSZEWSKI, J. (1962) · PubMed · Cited by 163 · see citing works
Modern concept of vascular cognitive impairment
Bowler, J. V. (2007) · British Medical Bulletin · doi:10.1093/bmb/ldm021 · Cited by 139 · see citing works
Adair, J. C., Charlie, J., Dencoff, J. E., Kaye, J. A., Quinn, J. F., Camicioli, R. M., Stetler‐Stevenson, W. G., & Rosenberg, G. A. (2004) · Stroke · doi:10.1161/01.str.0000127420.10990.76 · Cited by 138 · see citing works
Self-citationFeigin, I., & Popoff, N. A. (1963) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-196307000-00011 · Cited by 138 · see citing works
Blood-brain barrier dysfunction in Binswanger’s disease; an immunohistochemical study
Akiguchi, I., Tomimoto, H., Suenaga, T., Wakita, H., & Budka, H. (1998) · Acta Neuropathologica · doi:10.1007/s004010050768 · Cited by 104 · see citing works
Liuzzi, G. M., Trojano, M., Fanelli, M., Avolio, C., Fasano, A., Livrea, P., & Riccio, P. (2002) · Multiple Sclerosis Journal · doi:10.1191/1352458502ms800oa · Cited by 102 · see citing works
Subcortical Arteriosclerotic Encephalopathy
Valk, J., & van der Knaap, M. S. (1989) · Springer eBooks · doi:10.1007/978-3-662-02568-0_45 · Cited by 79 · see citing works
Mandler, R. N., Dencoff, J. D., Midani, F., Ford, C. C., Ahmed, W., & Rosenberg, G. A. (2001) · Brain · doi:10.1093/brain/124.3.493 · Cited by 77 · see citing works
Self-citationSchalin‐Jäntti, C., Laine, T., Valli‐Jaakola, K., Lönnqvist, T. R. I., Kontula, K., & Välimäki, M. J. (2005) · Hormone Research in Paediatrics · doi:10.1159/000084689 · Cited by 61 · see citing works
Hanyu, H., Asano, T., Tanaka, Y., Iwamoto, T., Takasaki, M., & Abe, K. (2002) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000058326 · Cited by 51 · see citing works
Zhang, W. W., & Olsson, Y. (1997) · Acta Neuropathologica · doi:10.1007/s004010050607 · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Pathobiology of Vascular Dementia
Iadecola, C. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.008 · Cited by 1,857 · see citing works
“First, the plasma protein albumin is increased in the CSF of patient with VCI, reflecting BBB breakdown (Candelario-Jalil et al., 2011).”
Apolipoprotein E controls cerebrovascular integrity via cyclophilin A
Bell, R. D., Winkler, E. A., Singh, I., Sagare, A. P., Deane, R., Wu, Z., Holtzman, D. M., Betsholtz, C., Armulik, A., Sallstrom, J., et al. (2012) · Nature · doi:10.1038/nature11087 · Cited by 1,293 · see citing works
Post-stroke dementia – a comprehensive review
Mijajlovic, M. D., Pavlovic, A. M., Brainin, M., Heiss, W., Quinn, T. J., Ihle‐Hansen, H., Hermann, D. M., Assayag, E. B., Richard, E., Thiel, A., et al. (2017) · BMC Medicine · doi:10.1186/s12916-017-0779-7 · Cited by 710 · see citing works
Models and Mechanisms of Vascular Dementia
Venkat, P., Chopp, M., & Chen, J.-L. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.05.006 · Cited by 323 · see citing works
Rajeev, V., Fann, D. Y., Dinh, Q. N., Kim, H. A., Silva, T. M. D., Lai, M. K. P., Chen, C., Drummond, G. R., Sobey, C. G., & Arumugam, T. V. (2022) · Theranostics · doi:10.7150/thno.68304 · Cited by 314 · see citing works
Oxidative stress and β-amyloid protein in Alzheimer’s disease
Cai, Z., Zhao, B., & Ratka, A. (2011) · NeuroMolecular Medicine · doi:10.1007/s12017-011-8155-9 · Cited by 279 · see citing works
Hussain, B., Fang, C., & Chang, J. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.688090 · Cited by 251 · see citing works
Rajeev, V., Chai, Y. L., Poh, L., Selvaraji, S., Fann, D. Y., Jo, D., Silva, T. M. D., Drummond, G. R., Sobey, C. G., Arumugam, T. V., et al. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01590-1 · Cited by 237 · see citing works
Consensus statement for diagnosis of subcortical small vessel disease
Rosenberg, G. A., Wallin, A., Wardlaw, J. M., Markus, H. S., Montaner, J., WOLFSON, L. I., Iadecola, C., Zloković, B. V., Joutel, A., Dichgans, M., et al. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.172 · Cited by 224 · see citing works
Self-citationBlood–Brain Barrier Breakdown in Alzheimer’s Disease: Mechanisms and Targeted Strategies
Alkhalifa, A. E., Al-Ghraiybah, N. F., Odum, J., Shunnarah, J. G., Austin, N., & Kaddoumi, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216288 · Cited by 212 · see citing works
Tian, Z., Ji, X., & Liu, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116224 · Cited by 210 · see citing works
Extracellular matrix inflammation in vascular cognitive impairment and dementia
Rosenberg, G. A. (2017) · Clinical Science · doi:10.1042/cs20160604 · Cited by 210 · see citing works
Self-citationMolecular biomarkers for vascular cognitive impairment and dementia
Hosoki, S., Hansra, G. K., Jayasena, T., Poljak, A., Mather, K. A., Catts, V. S., Rust, R., Sagare, A. P., Kovacic, J. C., Brodtmann, A. G., et al. (2023) · Nature Reviews Neurology · doi:10.1038/s41582-023-00884-1 · Cited by 166 · see citing works
Iadecola, C., Smith, E. E., Anrather, J., Gu, C., Mishra, A., Misra, S., Pérez‐Pinzón, M. A., Shih, A. Y., Sorond, F. A., van Veluw, S. J., et al. (2023) · Stroke · doi:10.1161/str.0000000000000431 · Cited by 156 · see citing works
Myelin Loss Associated With Neuroinflammation in Hypertensive Rats
Jalal, F. Y., Yang, Y. R., Thompson, J., Lopez, A. C., & Rosenberg, G. A. (2012) · Stroke · doi:10.1161/strokeaha.111.643080 · Cited by 146 · see citing works
Self-citationSudduth, T. L., Powell, D. K., Smith, C. D., Greenstein, A. W., & Wilcock, D. M. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.1 · Cited by 142 · see citing works
96 perfusable blood vessels to study vascular permeability in vitro
van Duinen, V., van den Heuvel, A., Trietsch, S. J., Lanz, H. L., van Gils, J. M., van Zonneveld, A. J., Vulto, P., & Hankemeier, T. (2017) · Scientific Reports · doi:10.1038/s41598-017-14716-y · Cited by 130 · see citing works
Price, B. R., Wilcock, D. M., & Weekman, E. M. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00350 · Cited by 128 · see citing works
Chou, S. H.-Y., Feske, S. K., Simmons, S. L., Konigsberg, R. G., Orzell, S. C., Marckmann, A., Bourget, G., Bauer, D. J., Jager, P. L. D., Du, R., et al. (2011) · Translational Stroke Research · doi:10.1007/s12975-011-0117-x · Cited by 120 · see citing works
Recent advances in the mechanisms of neuroinflammation and their roles in neurodegeneration
Niranjan, R. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.07.003 · Cited by 112 · see citing works
Matrix metalloproteinase‐3 in the central nervous system: a look on the bright side
Hove, I. V., Lemmens, K., de Velde, S. V., Verslegers, M., & Moons, L. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07900.x · Cited by 112 · see citing works
Matrix Metalloproteinase in Blood-Brain Barrier Breakdown in Dementia
Weekman, E. M., & Wilcock, D. M. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150759 · Cited by 103 · see citing works
Endothelial Dysfunction in Neurodegenerative Diseases
Fang, Y., Hsieh, Y., Hu, C., & Tu, Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032909 · Cited by 101 · see citing works
Cipollini, V., Troili, F., & Giubilei, F. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112812 · Cited by 98 · see citing works
Acupuncture and neuroregeneration in ischemic stroke
Hsieh, C., Chang, Q.-Y., & Lin, Y. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.230272 · Cited by 97 · see citing works
Rosenberg, G. A., Bjerke, M., & Wallin, A. (2014) · Stroke · doi:10.1161/strokeaha.113.004534 · Cited by 96 · see citing works
Self-citationYang, Y. R., Kimura‐Ohba, S., Thompson, J. F., Salayandia, V. M., Cossé, M., Raz, L., Jalal, F. Y., & Rosenberg, G. A. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.02.012 · Cited by 97 · see citing works
Self-citationToyama, K., Spin, J. M., Deng, A. C., Huang, T., Wei, K., Wagenhäuser, M. U., Yoshino, T., Nguyen, H., Mulorz, J. U., Kundu, S., et al. (2018) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.118.310822 · Cited by 92 · see citing works
Wallin, A., Kapaki, E., Boban, M., Engelborghs, S., Hermann, D. M., Huisa, B. N., Jonsson, M. A. G., Kramberger, M. G., Lossi, L., Malojčić, B., et al. (2017) · BMC Neurology · doi:10.1186/s12883-017-0877-3 · Cited by 87 · see citing works
Self-citationNyúl‐Tóth, Á., Patai, R., Csiszár, A., Ungvari, A., Gulej, R., Mukli, P., Yabluchanskiy, A., Benyó, Z., Sótonyi, P., Prodan, C. I., et al. (2024) · GeroScience · doi:10.1007/s11357-024-01194-0 · Cited by 91 · see citing works
Cerebrovascular disorders: molecular insights and therapeutic opportunities
Storkebaum, E., Quaegebeur, A., Vikkula, M., & Carmeliet, P. (2011) · Nature Neuroscience · doi:10.1038/nn.2947 · Cited by 86 · see citing works
Sarvari, S., Moakedi, F., Hone, E., Simpkins, J. W., & Ren, X. S. (2020) · Metabolic Brain Disease · doi:10.1007/s11011-020-00573-8 · Cited by 83 · see citing works
Emerging Role of Immunity in Cerebral Small Vessel Disease
Fu, Y., & Yan, Y. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00067 · Cited by 79 · see citing works
Myelin Injury and Degraded Myelin Vesicles in Alzheimer’s Disease
Zhan, X., Jickling, G. C., Ander, B. P., Liu, D., Stamova, B. S., Cox, C. D., Jin, L. W., DeCarli, C. S., & Sharp, F. R. (2014) · Current Alzheimer Research · doi:10.2174/1567205011666140131120922 · Cited by 79 · see citing works
Patwa, J., & Flora, S. J. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113862 · Cited by 80 · see citing works
Hill, J. W., Poddar, R., Thompson, J. F., Rosenberg, G. A., & Yang, Y. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.06.019 · Cited by 78 · see citing works
Self-citationRost, N. S., Cougo, P., Lorenzano, S., Li, H., Cloonan, L. K., Bouts, M. J. R. J., Lauer, A., Etherton, M. R., Karadeli, H. H., Musolino, P. L., et al. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17706449 · Cited by 77 · see citing works
Neurovascular Alterations in Vascular Dementia: Emphasis on Risk Factors
Lecordier, S., Manrique‐Castano, D., Moghrabi, Y. E., & ElAli, A. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.727590 · Cited by 76 · see citing works
A brief overview of a mouse model of cerebral hypoperfusion by bilateral carotid artery stenosis
Ishikawa, H., Shindo, A., Mizutani, A., Tomimoto, H., Lo, E. H., & Arai, K. (2023) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x231154597 · Cited by 73 · see citing works
Update on the Neurobiology of Vascular Cognitive Impairment: From Lab to Clinic
Vinciguerra, L., Lanza, G., Puglisi, V., Fisicaro, F., Pennisi, M., Bella, R., & Cantone, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082977 · Cited by 69 · see citing works
Sudduth, T. L., Greenstein, A. W., & Wilcock, D. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1220-13.2013 · Cited by 67 · see citing works
ApoE Influences the Blood-Brain Barrier Through the NF-κB/MMP-9 Pathway After Traumatic Brain Injury
Teng, Z., Guo, Z., Zhong, J., Cheng, C., Huang, Z., Wu, Y., Tang, S., Luo, C., Peng, X., Wu, H., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-06932-3 · Cited by 68 · see citing works
Frankowski, J. C., DeMars, K. M., Ahmad, A. S., Hawkins, K. E., Yang, C., Leclerc, J. L., Doré, S., & Candelario‐Jalil, E. (2015) · Scientific Reports · doi:10.1038/srep17956 · Cited by 65 · see citing works
Self-citationMatrix metalloproteinases and ADAMs in stroke
Montaner, J., Ramiro, L., Simats, A., Hernández‐Guillamón, M., Delgado, P., Bustamante, A., & Rosell, A. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03175-5 · Cited by 66 · see citing works
Ponce-Lopez, T. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26094209 · Cited by 75 · see citing works
DeMars, K. M., Yang, C., & Candelario‐Jalil, E. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.03.004 · Cited by 63 · see citing works
Self-citationHafez, S. S., Abdelsaid, M. A., Elshafey, S., Johnson, M. H., Fagan, S. C., & Ergul, A. (2016) · Stroke · doi:10.1161/strokeaha.115.011258 · Cited by 61 · see citing works
Blood-based biomarkers of cerebral small vessel disease
Wu, L., Chai, Y. L., Cheah, I. K.-M., Chia, R. S. L., Hilal, S., Arumugam, T. V., Chen, C., & Lai, M. K. P. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102247 · Cited by 62 · see citing works
Vilar‐Bergua, A., Llena, I. R., Nafría, C., Bustamante, A., Llombart, V., Delgado, P., & Montaner, J. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.68 · Cited by 60 · see citing works
Serum Matrix Metalloproteinase‐9 and Cognitive Impairment After Acute Ischemic Stroke
Zhong, C., Bu, X., Xu, T., Guo, L., Wang, X., Zhang, J., Cui, Y., Li, D., Zhang, J., Ju, Z., et al. (2018) · Journal of the American Heart Association · doi:10.1161/jaha.117.007776 · Cited by 60 · see citing works
Feng, T., Fu, W., Cheng, N., MENG, D., & Gu, Y. (2015) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2015.2365 · Cited by 59 · see citing works
Vascular pathology and pathogenesis of cognitive impairment and dementia in older adults
Agrawal, S., & Schneider, J. A. (2022) · Cerebral Circulation - Cognition and Behavior · doi:10.1016/j.cccb.2022.100148 · Cited by 60 · see citing works
Shindo, A., Liang, A. C., Maki, T., Miyamoto, N., Tomimoto, H., Lo, E. H., & Arai, K. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.80 · Cited by 58 · see citing works
Post-stroke Neurogenesis: Friend or Foe?
Cuartero, M. I., García‐Culebras, A., Torres‐López, C., Medina, V., Fraga, E., Vázquez‐Reyes, S., Jareño-Flores, T., García-Segura, J. M., Lizasoaín, I., & Moro, M. Á. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657846 · Cited by 59 · see citing works
Sudduth, T. L., Weekman, E. M., Brothers, H. M., Braun, K. J., & Wilcock, D. M. (2014) · Alzheimer s Research & Therapy · doi:10.1186/alzrt262 · Cited by 55 · see citing works
Shibasaki, C., Takebayashi, M., Itagaki, K., Abe, H., Kajitani, N., Okada‐Tsuchioka, M., & Yamawaki, S. (2016) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw019 · Cited by 56 · see citing works
Hawkins, K. E., DeMars, K. M., Singh, J., Yang, C., Cho, H. S., Frankowski, J. C., Doré, S., & Candelario‐Jalil, E. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12607 · Cited by 52 · see citing works
Self-citationAcupuncture Therapy for Stroke Patients
Li, X., & Wang, Q. (2013) · International review of neurobiology · doi:10.1016/b978-0-12-411545-3.00008-0 · Cited by 50 · see citing works
Lee, E., Yoon, J., Choi, J., Andika, F. R., Lee, T., & Jeong, Y. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17736963 · Cited by 49 · see citing works
Wallin, A., Nordlund, A., Jonsson, M. A. G., Blennow, K., Zetterberg, H., Öhrfelt, A., Stålhammar, J., Eckerström, M., Carlsson, M., Olsson, E., et al. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.148 · Cited by 48 · see citing works
French, S. R., Meyer, B. P., Arias, J. C., Levendovszky, S. R., & Weinkauf, C. C. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70104 · Cited by 45 · see citing works
Minocycline Reduces Spontaneous Hemorrhage in Mouse Models of Cerebral Amyloid Angiopathy
Yan, P., Zhu, A., Liao, F., Xiao, Q.-L., Kraft, A. W., Gonzales, E., Perez, R., Greenberg, S., Holtzman, D., & Lee, J.-M. (2015) · Stroke · doi:10.1161/strokeaha.115.008582 · Cited by 35 · see citing works
Rosenberg, G. A. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14218 · Cited by 45 · see citing works
Self-citationInjury-Induced Inhibition of Bystander Neurons Requires dSarm and Signaling from Glia
Hsu, J.-M., Kang, Y., Corty, M. M., Mathieson, D., Peters, O. M., & Freeman, M. R. (2020) · Neuron · doi:10.1016/j.neuron.2020.11.012 · Cited by 44 · see citing works
Oxidative stress and chronic cerebral hypoperfusion: An overview from preclinical rodent models
Kimura, S., Iwata, M., Takase, H., Lo, E. H., & Arai, K. (2024) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x241305899 · Cited by 44 · see citing works
Neurovascular Unit: Basic and Clinical Imaging with Emphasis on Advantages of Ferumoxytol
Netto, J. P., Iliff, J. J., Stanimirovic, D. B., Krohn, K. A., Hamilton, B. E., Várallyay, C. G., Gahramanov, S., Daldrup-Link, H. E., d’Esterre, C. D., Zloković, B. V., et al. (2017) · Neurosurgery · doi:10.1093/neuros/nyx357 · Cited by 41 · see citing works
Self-citationRoot, J. C., Pryor, K. O., Downey, R. J., Alici, Y., Davis, M. L., Holodny, A. I., Korc‐Grodzicki, B., & Ahles, T. A. (2013) · Psycho-Oncology · doi:10.1002/pon.3262 · Cited by 40 · see citing works
Li, X., Luo, P., Wang, Q., & Xiong, L. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/195397 · Cited by 38 · see citing works
Cerebrovascular inflammation: A critical trigger for neurovascular injury?
Naveed, M., Zhou, Q., & Han, F. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.03.011 · Cited by 36 · see citing works
Han, Q., Zhang, H., Zhang, X., He, D., Wang, S., Cao, X., Dai, Y., Xu, Y., & Han, L. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13189 · Cited by 39 · see citing works
Rosenberg, G. A., Prestopnik, J., Adair, J. C., Huisa, B. N., Knoefel, J. E., Caprihan, A., Gasparovic, C., Thompson, J. F., Erhardt, E. B., & Schrader, R. (2015) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2014-309421 · Cited by 39 · see citing works
Self-citationBinswanger’s disease: toward a diagnosis agreement and therapeutic approach
Huisa, B. N., & Rosenberg, G. A. (2014) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2014.956726 · Cited by 37 · see citing works
Self-citationThe role of MMP genes in recurrent depressive disorders and cognitive functions
Bobińska, K., Szemraj, J., Gałecki, P., & Talarowska, M. E. (2016) · Acta Neuropsychiatrica · doi:10.1017/neu.2015.72 · Cited by 36 · see citing works
The emerging role of nitric oxide in the synaptic dysfunction of vascular dementia
Zhang, X., Chen, Z., Xiong, Y., Zhou, Q., Zhu, L., & Liu, D. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-23-01353 · Cited by 39 · see citing works
Gao, Y., Li, W., Liu, Y., Wang, Y., Zhang, J., Li, M., & Bu, M. (2017) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2017.01.025 · Cited by 35 · see citing works
Novak, V. (2012) · Current Cardiovascular Risk Reports · doi:10.1007/s12170-012-0260-2 · Cited by 35 · see citing works
DeMars, K. M., McCrea, A. O., Siwarski, D. M., Sanz, B. D., Yang, C., & Candelario‐Jalil, E. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00089 · Cited by 34 · see citing works
Self-citationFischer, M., Dietmann, A., Beer, R., Broessner, G., Helbok, R., Pfausler, B., Schmutzhard, E., & Lackner, P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059952 · Cited by 33 · see citing works
Garcia, G., Fernandes, A., Stein, F., & Brites, D. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.833066 · Cited by 32 · see citing works
Regulatory mechanisms of tetramethylpyrazine on central nervous system diseases: A review
Liu, Y., Yang, G., Cui, W., Zhang, Y., & Liang, X. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.948600 · Cited by 32 · see citing works
Hawkins, K. E., DeMars, K. M., Yang, C., Rosenberg, G. A., & Candelario‐Jalil, E. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-14 · Cited by 31 · see citing works
Self-citationSamat, H. N. A., Razali, N. N., Mahadzir, H., Muhammad, T. S. T., Ling, K., Mansor, N. I., & Abidin, S. Z. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26188905 · Cited by 31 · see citing works
Al-Thani, M., Goodwin-Trotman, M., Bell, S., Patel, K., Fleming, L., Vilain, C. N., Abramowicz, M. J., Allan, S. M., Wang, T., Cader, M. Z., et al. (2023) · Stem Cell Reports · doi:10.1016/j.stemcr.2023.10.014 · Cited by 28 · see citing works
Omori, W., Hattori, K., Kajitani, N., Okada‐Tsuchioka, M., Boku, S., Kunugi, H., Okamoto, Y., & Takebayashi, M. (2020) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaa049 · Cited by 29 · see citing works
Corbin, Z. A., Rost, N. S., Lorenzano, S., Kernan, W. N., Parides, M. K., Blumberg, J. B., Milbury, P. E., Arai, K., Hartdegen, S. N., Lo, E. H., et al. (2014) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2013.11.002 · Cited by 27 · see citing works
Rosenberg, G. A. (2016) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-015-0277-4 · Cited by 27 · see citing works
Self-citationDebrah, L. B., Albers, A., Debrah, A. Y., Brockschmidt, F. F., Becker, T., Herold, C., Hofmann, A., Osei-Mensah, J., Mubarik, Y., Fröhlich, H., et al. (2017) · Human Genomics · doi:10.1186/s40246-017-0121-7 · Cited by 25 · see citing works
Small Vessel Disease: Ancient Description, Novel Biomarkers
Moretti, R., & Caruso, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073508 · Cited by 25 · see citing works
Biomarkers identify the Binswanger type of vascular cognitive impairment
Erhardt, E. B., Pesko, J. C., Prestopnik, J., Thompson, J., Caprihan, A., & Rosenberg, G. A. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x18762655 · Cited by 25 · see citing works
Self-citationUngvari, A., Nyúl‐Tóth, Á., Patai, R., Csík, B., Gulej, R., Nagy, D., Shanmugarama, S., Benyó, Z., Kiss, T., Ungvari, Z. I., et al. (2025) · GeroScience · doi:10.1007/s11357-025-01621-w · Cited by 24 · see citing works
Guo, S., Xu, J., Wei, N., Han, J., Xue, R., Xu, P., & Gao, C. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190324 · Cited by 24 · see citing works
Ahmadpour, D., & Grange‐Messent, V. (2020) · Neuroendocrinology · doi:10.1159/000509218 · Cited by 22 · see citing works
Hypercholesterolemia and the Increased Risk of Vascular Dementia: a Cholesterol Perspective
Shang, G., Shao, Q., Lv, K., Xu, W., Ji, J., Fan, S., Kang, X., Cheng, F., Wang, X., & Wang, Q. (2024) · Current Atherosclerosis Reports · doi:10.1007/s11883-024-01217-3 · Cited by 24 · see citing works
Hafez, S. S., Abdelsaid, M. A., Fagan, S. C., & Ergul, A. (2017) · Neurochemical Research · doi:10.1007/s11064-017-2411-9 · Cited by 23 · see citing works
Substances of abuse and the blood brain barrier: Interactions with physical exercise
Małkiewicz, M. A., Małecki, A., Toborek, M. J., Szarmach, A., & Winklewski, P. J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.026 · Cited by 20 · see citing works
Metalloproteinases and neurodegenerative diseases: pathophysiological and therapeutic perspectives
Rosenberg, G. A. (2015) · Metalloproteinases In Medicine · doi:10.2147/mnm.s68849 · Cited by 21 · see citing works
Self-citationGong, M., & Jia, J. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.949129 · Cited by 20 · see citing works
Vascular Dementia and Crosstalk Between the Complement and Coagulation Systems
Parsi, M. M., Duval, C., & Ariëns, R. A. S. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.803169 · Cited by 21 · see citing works
Zhang, Y., Wang, Y., Zuo, Z., Wang, Z., Roy, J., Hou, Q., Tong, E., Hoffmann, A., Sperberg, E., Bredno, J., et al. (2014) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2014.09.036 · Cited by 19 · see citing works
Ljubisavljević, S., Stojanović, I. R., Bašić, J., Vojinović, S., Stojanov, D. A., Djordjević, G., & Pavlovic, D. D. (2015) · Journal of Molecular Neuroscience · doi:10.1007/s12031-015-0521-x · Cited by 19 · see citing works
- Authors
- Candelario-Jalil, E., Thompson, J., Taheri, S., Grossetete, M., Adair, J. C., Edmonds, E., Prestopnik, J., Wills, J., & Rosenberg, G. A.
- Affiliations
- From the Departments of Neurology (E.C.-J., J.T., S.T., M.G., J.A., E.E., J.P., G.A.R.), Neurosciences (G.A.R.), Cell Biology and Physiology (G.A.R.), and Anesthesiology (J.W.), University of New Mexico Health Sciences Center, Albuquerque, NM.
- University of New Mexico (US)
- Venue
- Stroke
- Published
- 2011-05
- Volume
- 42
- Issue
- 5
- Pages
- 1345-1350
- ISSN
- 0039-2499 (ISSN-L)
- 1524-4628
- PMC
- PMC3119779
- OpenAlex
- W1966214665
- Cited by
- 173
- References
- 28
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 11 · 2023: 14 · 2022: 14 · 2021: 7 · 2020: 11 · 2019: 11 · 2018: 12 · 2017: 12 · 2016: 9 · 2015: 13 · 2014: 15 · 2013: 11 · 2012: 8
- FWCI
- 6.71
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Stroke (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (UL1TR000041, UL1TR001449)
- National Institute of Neurological Disorders and Stroke (R01NS052305)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- matrix metalloproteinases, vascular cognitive impairment, subcortical ischemic vascular disease, blood-brain barrier permeability, cerebrospinal fluid albumin, MMP-2, MMP-3, MMP-9, cerebral small vessel disease, white matter hyperintensities, neuroinflammation, Alzheimer's disease
- MeSH terms
- Albumins, Alzheimer Disease, Blood-Brain Barrier, Cognition Disorders, Female, Humans, Male, Vascular Diseases, Case-Control Studies, Matrix Metalloproteinase 3, Stroke, Matrix Metalloproteinase 2, Matrix Metalloproteinase 9, Leukoaraiosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
