A new role for matrix metalloproteinase-3 in the NGF metabolic pathway: Proteolysis of mature NGF and sex-specific differences in the continuum of Alzheimer's pathology
Open accessAbstract
Matrix metalloproteinase-3 (MMP-3) has been associated with risk of Alzheimer's disease (AD). In this study we introduce a novel role for MMP-3 in degrading nerve growth factor (NGF) in vivo and examine its mRNA and protein expression across the continuum of AD pathology. We provide evidence that MMP-3 participates in the degradation of mature NGF in vitro and in vivo and that it is secreted from the rat cerebral cortex in an activity-dependent manner. We show that cortical MMP-3 is upregulated in the McGill-R-Thy1-APP transgenic rat model of AD-like amyloidosis. A similar upregulation was found in AD and MCI brains as well as in cognitively normal individuals with elevated amyloid deposition. We also observed that frontal cortex MMP-3 protein levels are higher in males. MMP-3 protein correlated with more AD neuropathology, markers of NGF metabolism, and lower cognitive scores in males but not in females. These results suggest that MMP-3 upregulation in AD might contribute to NGF dysmetabolism, and therefore to cholinergic atrophy and cognitive deficits, in a sex-specific manner. MMP-3 should be further investigated as a biomarker candidate or as a therapeutic target in AD.
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Among the most upregulated DEGs, higher amounts of MMP3, IBSP, or TAGLN in the brain have been linked to increased risk of AD.
“Among the most upregulated DEGs, higher amounts of MMP3 (52), IBSP (53), or TAGLN (54) in the brain have been linked to increased risk of AD.”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [52]
The Results section, “Alterations of MMP-3 levels in the human cerebral cortex through the continuum of AD pathology” (page not supplied), reports higher brain MMP-3 in AD, MCI, and cognitively normal people with AD-like pathology. It also links higher MMP-3 to greater amyloid burden. These findings support an association with AD pathology, but the paper does not show that higher brain MMP-3 predicts an increased risk of developing AD. Citation (52) is attached to MMP3, not IBSP or TAGLN. (LLM, conf=0.84)
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1 retracted
RETRACTED AND REPLACED: Nerve growth factor metabolic dysfunction in Down’s syndrome brains
Iulita, M. F., Carmo, S. D., Ower, A. K., Fortress, A. M., Aguilar, L. F., Hanna, M., Wısnıewskı, T., Granholm, A., Buhusi, M. C., Busciglio, J. A., et al. (2014) · Brain · doi:10.1093/brain/awt372 · Cited by 88 · see citing works
Self-citationRetractedMcKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984) · Neurology · doi:10.1212/wnl.34.7.939 · Cited by 27,915 · see citing works
The cholinergic hypothesis of geriatric memory dysfunction
Bartus, R. T., Dean, R. L., Beer, B., & Lippa, A. S. (1982) · Science · doi:10.1126/science.7046051 · Cited by 5,545 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Alzheimer's Disease and Senile Dementia: Loss of Neurons in the Basal Forebrain
Whitehouse, P., Price, D., Struble, R., Clark, A., Coyle, J., & DeLong, M. R. (1982) · Science · doi:10.1126/science.7058341 · Cited by 3,627 · see citing works
Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections
Hefti, F. F. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-08-02155.1986 · Cited by 1,455 · see citing works
Human Memory and the Cholinergic System
Drachman, D. A. (1974) · Archives of Neurology · doi:10.1001/archneur.1974.00490320001001 · Cited by 1,398 · see citing works
CENTRAL CHOLINERGIC SYSTEMS AND COGNITION
Everitt, B. J., & Robbins, T. W. (1997) · Annual Review of Psychology · doi:10.1146/annurev.psych.48.1.649 · Cited by 1,348 · see citing works
Neuropathology of older persons without cognitive impairment from two community-based studies
Bennett, D. A., Schneider, J. A., Arvanitakis, Z., Kelly, J. F., Aggarwal, N. T., Shah, R. C., & Wilson, R. S. (2006) · Neurology · doi:10.1212/01.wnl.0000219668.47116.e6 · Cited by 1,336 · see citing works
Self-citationSex differences in Alzheimer disease — the gateway to precision medicine
for the Women’s Brain Project and the Alzheimer Precision Medicine Initiative, Ferretti, M. T., Iulita, M. F., Cavedo, E., Chiesa, P. A., Schumacher Dimech, A., Santuccione Chadha, A., Baracchi, F., Girouard, H., Misoch, S., et al. (2018) · Nature Reviews Neurology · doi:10.1038/s41582-018-0032-9 · Cited by 1,009 · see citing works
Self-citationModes and models of forebrain cholinergic neuromodulation of cognition
Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733 · see citing works
Schönbeck, U., Mach, F., & Libby, P. (1998) · PubMed · Cited by 681 · see citing works
Overview and Findings from the Religious Orders Study
Bennett, D. A., Schneider, J. A., Arvanitakis, Z., & Wilson, R. S. (2012) · Current Alzheimer Research · doi:10.2174/156720512801322573 · Cited by 647 · see citing works
Self-citationOgata, Y., Enghild, J. J., & Nagase, H. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)50563-4 · Cited by 633 · see citing works
Schönbeck, U., Mach, F., & Libby, P. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.7.3340 · Cited by 605 · see citing works
Fahnestock, M., Michalski, B., Xu, B., & Coughlin, M. (2001) · Molecular and cellular neurosciences · doi:10.1006/mcne.2001.1016 · Cited by 482 · see citing works
The Cholinergic Lesion of Alzheimer's Disease: Pivotal Factor or Side Show?
Mesulam, M. (2004) · Learning & Memory · doi:10.1101/lm.69204 · Cited by 467 · see citing works
Gasche, Y., Copin, J., Sugawara, T., Fujimura, M., & Chan, P. H. (2001) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200112000-00003 · Cited by 388 · see citing works
Dementia in Down syndrome: unique insights for Alzheimer disease research
Lott, I. T., & Head, E. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-018-0132-6 · Cited by 383 · see citing works
Bruno, M. A., & Cuello, A. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510645103 · Cited by 344 · see citing works
Self-citationPearson, R. C. A., Sofroniew, M. V., Cuello, A. C., Powell, T. P. S., Eckenstein, F. P., Esiri, M. M., & Wilcock, G. K. (1983) · Brain Research · doi:10.1016/0006-8993(83)90046-x · Cited by 334 · see citing works
Self-citationWhite, A. R., Du, T., Laughton, K. M., Volitakis, I., Sharples, R. A., Xilinas, M. E., Hoke, D. E., Holsinger, R. M. D., Evin, G., Cherny, R. A., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602487200 · Cited by 284 · see citing works
Meighan, S. E., Meighan, P. C., Choudhury, P., Davis, C. J., Olson, M. L., Zornes, P. A., Wright, J. W., & Harding, J. W. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03565.x · Cited by 281 · see citing works
Lee, E.-J., Woo, M.-S., Moon, P., Baek, M., Choi, I.-Y., Kim, W.-K., Junn, E., & Kim, H.-S. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903480 · Cited by 267 · see citing works
Kim, Y. S., Kim, S. S., Cho, J. J., Choi, D. H., Hwang, O., Shin, D. H., Chun, H. S., Beal, M. F., & Joh, T. H. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4346-04.2005 · Cited by 256 · see citing works
Gurney, K., Estrada, E. Y., & Rosenberg, G. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.02.006 · Cited by 243 · see citing works
Matrix metalloproteinases and free radicals in cerebral ischemia
JIANLIU, K., & Rosenberg, G. A. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.03.033 · Cited by 230 · see citing works
Ribbens, C., Porras, M., Franchimont, N., Kaiser, M.-J., Jaspar, J.-M., Damas, P., Houssiau, F. A., & Malaise, M. (2002) · Annals of the Rheumatic Diseases · doi:10.1136/ard.61.2.161 · Cited by 222 · see citing works
León, W., Canneva, F., Partridge, V., Allard, S., Ferretti, M. T., DeWilde, A., Vercauteren, F., Atifeh, R., Ducatenzeiler, A., Klein, W. L., et al. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-1349 · Cited by 221 · see citing works
Self-citationEckhard, U., Huesgen, P. F., Schilling, O., Bellac, C. L., Butler, G. S., Cox, J. H., Dufour, A., Goebeler, V., Kappelhoff, R., Keller, U. A. D., et al. (2015) · Matrix Biology · doi:10.1016/j.matbio.2015.09.003 · Cited by 208 · see citing works
Cytokine-regulated proteases in autoimmune diseases
Opdenakker, G., & Damme, J. V. (1994) · Immunology Today · doi:10.1016/0167-5699(94)90151-1 · Cited by 208 · 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
Kim, Y. S., Choi, D. H., Block, M. L., Lorenzl, S., Yang, L., Kim, Y., Sugama, S., Cho, B. P., Hwang, O., Browne, S. E., et al. (2006) · The FASEB Journal · doi:10.1096/fj.06-5865com · Cited by 199 · see citing works
Amyloid β Oligomers Disrupt Blood–CSF Barrier Integrity by Activating Matrix Metalloproteinases
Brkić, M., Balusu, S., Wonterghem, E. V., Gorlé, N., Benilova, I., Kremer, A., Hove, I. V., Moons, L., Strooper, B. D., Kanazir, S., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0006-15.2015 · Cited by 179 · see citing works
Deb, S., & Gottschall, P. E. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.66041641.x · Cited by 163 · see citing works
Increased Matrix Metalloproteinase 9 Activity in Mild Cognitive Impairment
Bruno, M. A., Mufson, E. J., Wuu, J., & Cuello, A. C. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181c22569 · Cited by 163 · see citing works
Self-citationNerve growth factor-induced synaptogenesis and hypertrophy of cortical cholinergic terminals.
Garofalo, L., Ribeiro‐da‐Silva, A., & Cuello, A. C. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.7.2639 · Cited by 163 · see citing works
Self-citationWoo, M., Park, J., Choi, I., Kim, W., & Kim, H. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05430.x · Cited by 160 · see citing works
Ferretti, M. T., Martínková, J., Biskup, E. M., Benke, T., Gialdini, G., Nedelská, Z., Rauen, K., Mantua, V., Religa, D., Hort, J., et al. (2020) · European Journal of Neurology · doi:10.1111/ene.14174 · Cited by 150 · see citing works
Amyloid β-Induced Nerve Growth Factor Dysmetabolism in Alzheimer Disease
Bruno, M. A., León, W., Fragoso, G., Mushynski, W. E., Almazán, G., & Cuello, A. C. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181aed9e6 · Cited by 148 · see citing works
Self-citationNerve growth factor metabolic dysfunction in Alzheimer's disease and Down syndrome
Iulita, M. F., & Cuello, A. C. (2014) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2014.04.010 · Cited by 135 · see citing works
Self-citationSelective distribution of matrix metalloproteinase-3 (MMP-3) in Alzheimer’s disease brain
Yoshiyama, Y., Asahina, M., & Hattori, T. (2000) · Acta Neuropathologica · doi:10.1007/pl00007428 · Cited by 128 · see citing works
Wang, X., Wang, H., Yang, H., Li, J., Cai, Q., Shapiro, I. M., & Risbud, M. V. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2014.06.006 · Cited by 126 · see citing works
A novel intracellular role of matrix metalloproteinase‐3 during apoptosis of dopaminergic cells
Choi, D. H., Kim, E., Son, H. J., JOH, T. H., Kim, Y. S., Kim, D., Beal, M. F., & Hwang, O. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05399.x · Cited by 124 · see citing works
Cholinergic Involvement in Alzheimer’s Disease. A Link with NGF Maturation and Degradation
Cuello, A. C., Bruno, M. A., Allard, S., León, W., & Iulita, M. F. (2009) · Journal of Molecular Neuroscience · doi:10.1007/s12031-009-9238-z · Cited by 119 · see citing works
Self-citationHorstmann, S., Budig, L., Gardner, H., Koziol, J. A., Deuschle, M., Schilling, C., & Wagner, S. (2010) · International Psychogeriatrics · doi:10.1017/s1041610210000827 · Cited by 111 · see citing works
The Brain NGF Metabolic Pathway in Health and in Alzheimer’s Pathology
Cuello, A. C., Pentz, R., & Hall, H. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00062 · Cited by 108 · see citing works
Self-citationStomrud, E., Björkqvist, M., Janciauskiene, S. M., Minthon, L., & Hansson, O. (2010) · Alzheimer s Research & Therapy · doi:10.1186/alzrt44 · Cited by 105 · see citing works
Iulita, M. F., Allard, S. T. M., Richter, L., Munter, L. M., Ducatenzeiler, A., Weise, C., Carmo, S. D., Klein, W. L., Multhaup, G., & Cuello, A. C. (2014) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-2-61 · Cited by 102 · see citing works
Self-citationIulita, M. F., Ower, A., Barone, C., Pentz, R., Gubert, P., Romano, C., Cantarella, R. A., Elia, F., Buono, S., Recupero, M., et al. (2016) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.05.001 · Cited by 99 · see citing works
Self-citationOvercoming neurite‐inhibitory chondroitin sulfate proteoglycans in the astrocyte matrix
Cua, R. C., Lau, L. W., Keough, M. B., Midha, R., Apte, S., & Yong, V. W. (2013) · Glia · doi:10.1002/glia.22489 · Cited by 87 · see citing works
Iulita, M. F., Millón, M. B. B., Pentz, R., Aguilar, L. F., Carmo, S. D., Allard, S. T. M., Michalski, B., Wilson, E. N., Ducatenzeiler, A., Bruno, M. A., et al. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2017.08.019 · Cited by 84 · see citing works
Self-citationOkada, Y., Nagase, H., & Harris, E. D. (1987) · PubMed · Cited by 78 · see citing works
Giacobini, E., & Pepeu, G. (2018) · Current Alzheimer Research · doi:10.2174/1567205015666180613111504 · Cited by 77 · see citing works
Kim, E., Shin, E.-J., Choi, J. H., Son, H. J., Park, I., JOH, T. H., & Hwang, O. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.093799 · Cited by 72 · see citing works
Tamai, K., Ishikawa, H., Mauviel, A., & Uitto, J. (1995) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12665857 · Cited by 72 · see citing works
NF-κB binds to a polymorphic repressor element in the MMP-3 promoter
Borghaei, R. C., Rawlings, P. L., Javadi, M., & Woloshin, J. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.02.030 · Cited by 69 · see citing works
Pentz, R., Iulita, M. F., Ducatenzeiler, A., Bennett, D. A., & Cuello, A. C. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-0797-2 · Cited by 68 · see citing works
Self-citationWalker, E. J., & Rosenberg, G. A. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.11.022 · Cited by 67 · see citing works
Hanzel, C. E., Iulita, M. F., Eyjolfsdottir, H., Hjorth, E., Schultzberg, M., Eriksdotter, M., & Cuello, A. C. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-132282 · Cited by 64 · see citing works
Self-citationD’Souza, C. A., & Moscarello, M. A. (2006) · Neurochemical Research · doi:10.1007/s11064-006-9116-9 · Cited by 61 · see citing works
Nübling, G., Levin, J., Bader, B., Israel, L., Bötzel, K., Lorenzl, S., & Giese, A. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.07.018 · Cited by 59 · see citing works
Artham, S., Gao, F., Verma, A., Alwhaibi, A. M., Sabbineni, H., Hafez, S. S., Ergul, A., & Somanath, P. R. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.01.006 · Cited by 58 · see citing works
Wiera, G., Nowak, D., Hove, I. V., Dzięgiel, P., Moons, L., & Mozrzymas, J. W. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2170-16.2016 · Cited by 53 · see citing works
p38 MAPK alpha mediates cytokine-induced IL-6 and MMP-3 expression in human cardiac fibroblasts
Sinfield, J. K., Das, A., O'Regan, D. J., Ball, S. G., Porter, K. E., & Turner, N. A. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.11.071 · Cited by 53 · see citing works
Heggland, I., Storkaas, I. S., Soligard, H., Kobro‐Flatmoen, A., & Witter, M. P. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12876 · Cited by 51 · see citing works
Gonthier, B., Nasarre, C., Roth, L., Perraut, M., Thomasset, N., Roussel, G., Aunis, D., & Bagnard, D. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl082 · Cited by 50 · see citing works
Effects of cerebrospinal fluid proteins on brain atrophy rates in cognitively healthy older adults
Mattsson, N., Insel, P. S., Nosheny, R. L., Trojanowski, J. Q., Shaw, L. M. J., Jack, C. R., Tosun, D., & Weiner, M. W. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.08.027 · Cited by 49 · see citing works
Mlekusch, R., & Humpel, C. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.09.043 · Cited by 49 · see citing works
Arends, S., van der Veer, E., Groen, H., Houtman, P. M., Jansen, T., Leijsma, M. K., Bijzet, J., Limburg, P. C., Kallenberg, C. G. M., Spoorenberg, A. J. P. L., et al. (2011) · The Journal of Rheumatology · doi:10.3899/jrheum.101128 · Cited by 46 · see citing works
Cerebrospinal Fluid proNGF: A Putative Biomarker for Early Alzheimer's Disease
Counts, S., He, B., Prout, J. G., Michalski, B., Farotti, L., Fahnestock, M. L., & Mufson, E. J. (2016) · Current Alzheimer Research · doi:10.2174/1567205013666160129095649 · Cited by 45 · see citing works
Iulita, M. F., Ganesh, A., Pentz, R., Aguilar, L. F., Gubert, P., Ducatenzeiler, A., Christie, S., Wilcock, G. K., & Cuello, A. C. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-180970 · Cited by 45 · see citing works
Self-citationBaig, S., Kehoe, P. G., & Love, S. (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00897.x · Cited by 40 · see citing works
D’Souza, C. A., Mak, B. C., & Moscarello, M. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m108817200 · Cited by 39 · see citing works
Chapter 32: Trophic responses of forebrain cholinergic neurons: a discussion
Cuello, A. C. (1993) · Progress in brain research · doi:10.1016/s0079-6123(08)62408-5 · Cited by 38 · see citing works
Self-citationBrzdąk, P., Wójcicka, O., Zaręba-Kozioł, M., Minge, D., Henneberger, C., Włodarczyk, J., Mozrzymas, J. W., & Wójtowicz, T. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx324 · Cited by 34 · see citing works
Plasma gelsolin and matrix metalloproteinase 3 as potential biomarkers for Alzheimer disease
Mao, P., Jia, J., & Qin, W. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.04.014 · Cited by 33 · see citing works
Glial Cells in Health and Disease of the CNS
Rommy von Bernhardi, M. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-40764-7 · Cited by 28 · see citing works
Trabjerg, E., Kartberg, F., Christensen, S., & Rand, K. D. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.803320 · Cited by 26 · see citing works
Pizzi, M. A., & Crowe, M. J. (2006) · Journal of Neurotrauma · doi:10.1089/neu.2006.23.1750 · Cited by 24 · see citing works
Saarela, M., Lehtimäki, T. J., Rinne, J. O., Hervonen, A., Jylhä, M. K., Röyttä, M., Ahonen, J.-P., & Mattila, K. M. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.06.027 · Cited by 23 · see citing works
Impact of the matrix metalloproteinase MMP-3 on dementia
Helbecque, N., Cottel, D., Hermant, X., & Amouyel, P. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.05.030 · Cited by 23 · see citing works
Reina, S., Sterin‐Borda, L., Passafaro, D., & Borda, E. (2011) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2010.08.017 · Cited by 23 · see citing works
Almodóvar, R., Rios, V., Ocaña, S., Gobbo, M., Casas, M. L., Zarco, P., & Juanola, X. (2013) · Clinical Rheumatology · doi:10.1007/s10067-013-2349-5 · Cited by 21 · see citing works
The Structure of the Pro-domain of Mouse proNGF in Contact with the NGF Domain
Yan, R., Yalinca, H., Paoletti, F., Gobbo, F., Marchetti, L., Kuzmanic, A., Lamba, D., Gervasio, F. L., Konarev, P. V., Cattaneo, A., et al. (2018) · Structure · doi:10.1016/j.str.2018.09.013 · Cited by 20 · see citing works
Peripheral and central nervous system alterations in a rat model of inflammatory arthritis
Locke, S., Yousefpour, N., Mannarino, M., Xing, S., Yashmin, F., Bourassa, V., & Ribeiro‐da‐Silva, A. (2020) · Pain · doi:10.1097/j.pain.0000000000001837 · Cited by 20 · see citing works
Brzdąk, P., Włodarczyk, J., Mozrzymas, J. W., & Wójtowicz, T. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-9970-7 · Cited by 19 · see citing works
Hoyos, H. C., Marder, M., Ulrich, R., Gudi, V., Stangel, M., Rabinovich, G. A., Pasquini, L. A., & Pasquini, J. M. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-40764-7_15 · Cited by 19 · see citing works
Debeir, T., Saragovi, H. U., & Cuello, A. C. (1998) · Journal of Physiology-Paris · doi:10.1016/s0928-4257(98)80011-9 · Cited by 12 · see citing works
Self-citationPita, A. D. C., Borda, E., Ganzinelli, S., Passafaro, D., & Sterin‐Borda, L. (2009) · Journal of Endodontics · doi:10.1016/j.joen.2009.01.004 · Cited by 12 · see citing works
Matrix metalloproteinase 3 haplotypes and dementia and Alzheimer's disease
Reitz, C., van Rooij, F. J. A., de Maat, M. P. M., den Heijer, T., Albert Hofman, D., Witteman, J. C. M., & Breteler, M. M. B. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.01.001 · Cited by 11 · see citing works
Romas (2000) · Pure Amsterdam UMC · doi:10.1002/1529-0131(200004)43:4
Flagged first, then by citations
1 of the 93 references couldn’t be matched to a known paper.
Research works printed but not linked: 6
- Cuello AC, 1993 Trophic responses of forebrain cholinergic neurons. Progress in brain research. 98, 265– 265. 8248516
- Iulita MF,, 2014b Intracellular Aβ pathology and early cognitive impairments in a transgenic rat overexpressing human amyloid precursor protein: a multidimensional study. Acta neuropathologica communications. 2, 61. 24903713 PMC4229908
- Iulita MF,, 2014c Nerve growth factor metabolic dysfunction in Down’s syndrome brains. Brain. 137, 860– 872. 24519975 PMC3927704
- Paxinos G, Watson C, 2006 The rat brain in stereotaxic coordinates: hard cover edition. Elsevier. 6110810
- Stomrud E,, 2010b Alterations of matrix metalloproteinases in the healthy elderly with increased risk of prodromal Alzheimer’s disease. 2, 20. PMC2919700 20576109
- Yamanaka H,, 2000 Serum matrix metalloproteinase 3 as a predictor of the degree of joint destruction during the six months after measurement, in patients with early rheumatoid arthritis. Arthritis. 43, 852– 858. 10765930
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- Authors
- Pentz, R., Iulita, M. F., Mikutra-Cencora, M., Ducatenzeiler, A., Bennett, D. A., & Cuello, A. C.
- Affiliations
- McGill University (CA)
- Universitat Autònoma de Barcelona (ES)
- Rush University Medical Center (US)
- Corresponding author
- Cuello, A. Claudio
- Venue
- Neurobiology of Disease
- Publisher
- Elsevier BV
- Published
- 2021-01
- Volume
- 148
- Pages
- 105150
- ISSN
- 0969-9961 (ISSN-L)
- PMC
- PMC7856186
- OpenAlex
- W3097891564
- Cited by
- 31
- References
- 93
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 5 · 2023: 6 · 2022: 6 · 2021: 5 · 2020: 1
- FWCI
- 2.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Neurobiology of Disease (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- matrix metalloproteinase-3, nerve growth factor, Alzheimer's disease, sex differences, amyloidosis, cognitive impairment, frontal cortex, biomarkers, therapeutic target, mild cognitive impairment
- MeSH terms
- Alzheimer Disease, Animals, Brain, Cerebral Cortex, Female, Male, RNA, Messenger, Sex Factors, Matrix Metalloproteinase 3, Nerve Growth Factor, Rats, Rats, Transgenic, Proteolysis, Cognitive Dysfunction
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