Poly(ADP-ribose)polymerase-1 modulates microglial responses to amyloid β

Kauppinen, Tiina M; Suh, Sang; Higashi, Youichirou; Berman, Ari E; Escartin, Carole; Won, Seok; Wang, Chao; Cho, Seo-Hyun; Gan, Li; Swanson, Raymond A

doi:10.1186/1742-2094-8-152

Cited by 113Neuroinflammation and Neurodegeneration MechanismsAlzheimer's disease research and treatmentsNeurological Disease Mechanisms and Treatments

Poly(ADP-ribose)polymerase-1 modulates microglial responses to amyloid β

Open access

Kauppinen, Tiina M, Suh, Sang, Higashi, Youichirou, Berman, Ari E, Escartin, Carole, Won, Seok, Wang, Chao, Cho, Seo-Hyun +2 more·2011·Journal of Neuroinflammation

DOI 10.1186/1742-2094-8-152PMC PMC3247192

Open this paper in CoChat — free account Open PDF

Abstract

BACKGROUND: Amyloid β (Aβ) accumulates in Alzheimer's disease (AD) brain. Microglial activation also occurs in AD, and this inflammatory response may contribute to disease progression. Microglial activation can be induced by Aβ, but the mechanisms by which this occurs have not been defined. The nuclear enzyme poly(ADP-ribose) polymerase-1 (PARP-1) regulates microglial activation in response to several stimuli through its interactions with the transcription factor, NF-κB. The purpose of this study was to evaluate whether PARP-1 activation is involved in Aβ-induced microglial activation, and whether PARP-1 inhibition can modify microglial responses to Aβ. METHODS: hAPP(J20) mice, which accumulate Aβ with ageing, were crossed with PARP-1(-/-) mice to assess the effects of PARP-1 depletion on microglial activation, hippocampal synaptic integrity, and cognitive function. Aβ peptide was also injected into brain of wt and PARP-1(-/-) mice to directly determine the effects of PARP-1 on Aβ-induced microglial activation. The effect of PARP-1 on Aβ-induced microglial cytokine production and neurotoxicity was evaluated in primary microglia cultures and in microglia-neuron co-cultures, utilizing PARP-1(-/-) cells and a PARP-1 inhibitor. NF-κB activation was evaluated in microglia infected with a lentivirus reporter gene. RESULTS: The hAPP(J20) mice developed microglial activation, reduced hippocampal CA1 calbindin expression, and impaired novel object recognition by age 6 months. All of these features were attenuated in hAPP(J20)/PARP-1(-/-) mice. Similarly, Aβ(1-42) injected into mouse brain produced a robust microglial response in wild-type mice, and this was blocked in mice lacking PARP-1 expression or activity. Studies using microglial cultures showed that PARP-1 activity was required for Aβ-induced NF-κB activation, morphological transformation, NO release, TNFα release, and neurotoxicity. Conversely, PARP-1 inhibition increased release of the neurotrophic factors TGFβ and VEGF, and did not impair microglial phagocytosis of Aβ peptide. CONCLUSIONS: These results identify PARP-1 as a requisite and previously unrecognized factor in Aβ-induced microglial activation, and suggest that the effects of PARP-1 are mediated, at least in part, by its interactions with NF-κB. The suppression of Aβ-induced microglial activation and neurotoxicity by PARP-1 inhibition suggests this approach could be useful in AD and other disorders in which microglial neurotoxicity may contribute.

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

Crossref · 10.1186/1742-2094-8-152

Cites

69 of 69 references verified0 citation errors · 0 not checkable

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?

In vivo studies using various Alzheimer disease and Parkinson disease models have shown that loss of PARP1 protects from brain dysfunctions and cognitive decline.
“In vivo studies using various Alzheimer disease and Parkinson disease models have shown that loss of PARP1 protects from brain dysfunctions and cognitive decline170–174.”
From NAD+ metabolism and its roles in cellular processes during ageing (2021) · cites this paper as [170]
PARP1 activation is associated with Alzheimer disease and Parkinson disease pathogenesis.
“PARP1 activation is also associated with Alzheimer disease170,171 and Parkinson disease172,173 pathogenesis.”
From NAD+ metabolism and its roles in cellular processes during ageing (2021) · cites this paper as [170]
Oxidative damage-induced poly(ADP-ribose) can mediate neuroinflammatory activity in AD.
“can mediate neuroinflammatory activity in AD (Kauppinen et al, 2011)”
From Mechanisms of DNA damage-mediated neurotoxicity in neurodegenerative disease (2022) · cites this paper as Kauppinen 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.

Measurement of protein using bicinchoninic acid
Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., & Klenk, D. C. (1985) · Analytical Biochemistry · doi:10.1016/0003-2697(85)90442-7 · Cited by 18,482 · see citing works
The Amyloid Hypothesis of Alzheimer’s Disease: Progress and Problems on the Road to Therapeutics
Hardy, J., & Selkoe, D. J. (2002) · Science · doi:10.1126/science.1072994 · Cited by 13,864 · see citing works
Function and Activation of NF-kappaB in the Immune System
Baeuerle, P. A., & Henkel, T. (1994) · Annual Review of Immunology · doi:10.1146/annurev.iy.12.040194.001041 · Cited by 4,745 · see citing works
Inflammation and Alzheimer’s disease
Akiyama, H. (2000) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00124-x · Cited by 4,514 · see citing works
Microglia: a sensor for pathological events in the CNS
Kreutzberg, G. W. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)10049-7 · Cited by 4,396 · see citing works
NF-κB regulation in the immune system
Li, Q., & Verma, I. M. (2002) · Nature Reviews Immunology · doi:10.1038/nri910 · Cited by 4,007 · see citing works
Microglial physiology: unique stimuli, specialized responses
Ransohoff, R. M., & Perry, V. H. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132528 · Cited by 1,858 · see citing works
High-Level Neuronal Expression of Aβ<sub>1–42</sub>in Wild-Type Human Amyloid Protein Precursor Transgenic Mice: Synaptotoxicity without Plaque Formation
Mucke, L., Masliah, E., Yu, G.-Q., Mallory, M., Rockenstein, E. M., Tatsuno, G., Hu, K., Kholodenko, D., Johnson-Wood, K., & McConlogue, L. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04050.2000 · Cited by 1,856 · see citing works
Amyloid-β–induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks
Palop, J. J., & Mucke, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2583 · Cited by 1,651 · see citing works
Bone Marrow-Derived Microglia Play a Critical Role in Restricting Senile Plaque Formation in Alzheimer's Disease
Simard, A. R., Soulet, D., Gowing, G., Julien, J.-P., & Rivest, S. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.022 · Cited by 1,265 · see citing works
Novel Inhibitors of Cytokine-induced IκBα Phosphorylation and Endothelial Cell Adhesion Molecule Expression Show Anti-inflammatory Effects in Vivo
Pierce, J. W., Schoenleber, R. W., Jesmok, G. J., Best, J. L., Moore, S. A., Collins, T., & Gerritsen, M. E. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.34.21096 · Cited by 1,044 · see citing works
Recognition memory and the medial temporal lobe: a new perspective
Squire, L. R., Wixted, J. T., & Clark, R. E. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2154 · Cited by 1,013 · see citing works
Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia
Tikka, T., Fiebich, B. L., Goldsteins, G., Keinänen, R., & Koistinaho, J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02580.2001 · Cited by 958 · see citing works
Microglia as neuroprotective, immunocompetent cells of the CNS
Streit, W. J. (2002) · Glia · doi:10.1002/glia.10154 · Cited by 919 · see citing works
Heterogeneity of Microglial Activation in the Innate Immune Response in the Brain
Colton, C. A. (2009) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-009-9164-4 · Cited by 871 · see citing works
Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death
Boje, K. M., & Arora, P. K. (1992) · Brain Research · doi:10.1016/0006-8993(92)91004-x · Cited by 786 · see citing works
Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease.Preprint
Wang, Z. Q., Auer, B., Stingl, L., Berghammer, H., Haidacher, D., Schweiger, M. R., & Wagner, E. F. (1995) · Genes & Development · doi:10.1101/gad.9.5.509 · Cited by 774 · see citing works
SIRT1 Protects against Microglia-dependent Amyloid-β Toxicity through Inhibiting NF-κB Signaling
Chen, J., Zhou, Y., Mueller-Steiner, S., Chen, L.-F., Kwon, H., Yi, S., Mucke, L., & Gan, L. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509329200 · Cited by 740 · see citing works
Self-citation
β-Amyloid Stimulation of Microglia and Monocytes Results in TNFα-Dependent Expression of Inducible Nitric Oxide Synthase and Neuronal Apoptosis
Combs, C. K., Karlo, J. C., Kao, S.-C., & Landreth, G. E. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-04-01179.2001 · Cited by 721 · see citing works
Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function
Elkabes, S., Dicicco-Bloom, E., & Black, I. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02508.1996 · Cited by 697 · see citing works
Amyloid precursor protein processing and Aβ 42 deposition in a transgenic mouse model of Alzheimer disease
Johnson‐Wood, K., Lee, M., Motter, R. N., Hu, K., Gordon, G., Barbour, R., Khan, K., Gordon, M. N., Tan, H. T., Games, D., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1550 · Cited by 634 · see citing works
TGF-β1 promotes microglial amyloid-β clearance and reduces plaque burden in transgenic mice
Wyss-Coray, T., Lin, C., Yan, F., Yu, G.-Q., Rohde, M., McConlogue, L., Masliah, E., & Mucke, L. (2001) · Nature Medicine · doi:10.1038/87945 · Cited by 587 · see citing works
Activated Macrophages and Microglia Induce Dopaminergic Sprouting in the Injured Striatum and Express Brain-Derived Neurotrophic Factor and Glial Cell Line-Derived Neurotrophic Factor
Batchelor, P., Liberatore, G. T., Wong, J. Y. F., Porritt, M. J., Frerichs, F., Donnan, G. A., & Howells, D. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01708.1999 · Cited by 576 · see citing works
PARP Goes Transcription
Kraus, W. L., & Lis, J. T. (2003) · Cell · doi:10.1016/s0092-8674(03)00433-1 · Cited by 547 · see citing works
Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification
Guillemin, G. J., & Brew, B. J. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0303114 · Cited by 520 · see citing works
NSAIDs and Alzheimer disease: Epidemiological, animal model and clinical studies
McGeer, P. L., & McGeer, E. G. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.03.013 · Cited by 498 · see citing works
The microglial "activation" continuum: from innate to adaptive responses
Town, T., Nikolic, V., & Tan, J. (2005) · Journal of Neuroinflammation · doi:10.1186/1742-2094-2-24 · Cited by 456 · see citing works
Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory
Wan, H., Aggleton, J. P., & Brown, M. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-03-01142.1999 · Cited by 449 · see citing works
Blocking TGF-β–Smad2/3 innate immune signaling mitigates Alzheimer-like pathology
Town, T., Laouar, Y., Pittenger, C., Mori, T., Szekely, C. A., Tan, J., Duman, R. S., & Flavell, R. A. (2008) · Nature Medicine · doi:10.1038/nm1781 · Cited by 422 · see citing works
Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits
Palop, J. J., Jones, B., Kekonius, L., Chin, J., Yu, G.-Q., Raber, J., Masliah, E., & Mucke, L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1133381100 · Cited by 402 · see citing works
Microglial Activation in Stroke: Therapeutic Targets
Yenari, M. A., Kauppinen, T. M., & Swanson, R. A. (2010) · Neurotherapeutics · doi:10.1016/j.nurt.2010.07.005 · Cited by 390 · see citing works
Self-citation
Cognitive Function Over Time in the Alzheimer's Disease Anti-inflammatory Prevention Trial (ADAPT): Results of a Randomized, Controlled Trial of Naproxen and Celecoxib
(2008) · Archives of Neurology · doi:10.1001/archneur.2008.65.7.nct70006 · Cited by 387 · see citing works
DNA-Independent PARP-1 Activation by Phosphorylated ERK2 Increases Elk1 Activity: A Link to Histone Acetylation
Cohen-Armon, M., Visochek, L., Rozensal, D., Kalal, A., Geistrikh, I., Klein, R., Bendetz-Nezer, S., Yao, Z., & Seger, R. (2007) · Molecular Cell · doi:10.1016/j.molcel.2006.12.012 · Cited by 329 · see citing works
The Enzymatic and DNA Binding Activity of PARP-1 Are Not Required for NF-κB Coactivator Function
Hassa, P. O., Covic, M., Hasan, S., Imhof, R., & Hottiger, M. O. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106528200 · Cited by 296 · see citing works
Minocycline Attenuates Neuronal Cell Death and Improves Cognitive Impairment in Alzheimer's Disease Models
Choi, Y., Kim, H., Shin, K. Y., Kim, E., Kim, M., Kim, H.-S., Park, C. H., Jeong, Y. H., Yoo, J., Lee, J., et al. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301377 · Cited by 290 · see citing works
Amyloid-β Protein Oligomer at Low Nanomolar Concentrations Activates Microglia and Induces Microglial Neurotoxicity
Maezawa, I., Zimin, P. I., Wulff, H., & Jin, L. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.135244 · Cited by 279 · see citing works
Poly(ADP-ribose) polymerase-1 dependence of stress-induced transcription factors and associated gene expression in glia
Ha, H. C., Hester, L. D., & Snyder, S. H. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052712399 · Cited by 255 · see citing works
Increased poly(ADP-ribosyl)ation of nuclear proteins in Alzheimer's disease
Love, S., Barber, R., & Wilcock, G. K. (1999) · Brain · doi:10.1093/brain/122.2.247 · Cited by 254 · see citing works
β-Amyloid-Stimulated Microglia Induce Neuron Death via Synergistic Stimulation of Tumor Necrosis Factor α and NMDA Receptors
Floden, A. M., Li, S., & Combs, C. K. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4998-04.2005 · Cited by 246 · see citing works
Transcriptional Coactivation of Nuclear Factor-κB-dependent Gene Expression by p300 Is Regulated by Poly(ADP)-ribose Polymerase-1
Hassa, P. O., Buerki, C., Lombardi, C., Imhof, R., & Hottiger, M. O. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307957200 · Cited by 236 · see citing works
Minocycline inhibits poly(ADP-ribose) polymerase-1 at nanomolar concentrations
Alano, C. C., Kauppinen, T. M., Valls, A. V., & Swanson, R. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600554103 · Cited by 229 · see citing works
Self-citation
Minocycline affects microglia activation, Aβ deposition, and behavior in APP‐tg mice
Seabrook, T. J., Jiang, L., Maier, M., & Lemere, C. A. (2006) · Glia · doi:10.1002/glia.20338 · Cited by 223 · see citing works
Poly(ADP‐ribose) polymerase‐1 activity promotes NF‐κB‐driven transcription and microglial activation: implication for neurodegenerative disorders
Chiarugi, A., & Moskowitz, M. A. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01684.x · Cited by 216 · see citing works
Hypoglycemic Neuronal Death and Cognitive Impairment Are Prevented by Poly(ADP-Ribose) Polymerase Inhibitors Administered after Hypoglycemia
Suh, S. W., Aoyama, K., Chen, Y., Garnier, P. E., Matsumori, Y., Gum, E. T., Liu, J., & Swanson, R. A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-33-10681.2003 · Cited by 210 · see citing works
Self-citation
The glutamate transporters EAAT2 and EAAT3 mediate cysteine uptake in cortical neuron cultures
Chen, Y., & Swanson, R. A. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01630.x · Cited by 195 · see citing works
Self-citation
Vascular endothelial growth factor in Alzheimer's disease and experimental cerebral ischemia
Kalaria, R. N., Cohen, D., Premkumar, D. R., Nag, S., LaManna, J. C., & Lust, W. D. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(98)00190-9 · Cited by 190 · see citing works
Poly(ADP-Ribose) Polymerase-1 Promotes Microglial Activation, Proliferation, and Matrix Metalloproteinase-9-Mediated Neuron Death
Kauppinen, T. M., & Swanson, R. A. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.4.2288 · Cited by 181 · see citing works
Self-citation
Decrease in the Numbers of Dendritic Cells and CD4+ T Cells in Cerebral Perivascular Spaces Due to Natalizumab
Martin, M. D. P. (2008) · Archives of Neurology · doi:10.1001/archneur.65.12.noc80051 · Cited by 181 · see citing works
Regulation of microglial expression of integrins by poly(ADP-ribose) polymerase-1
Ullrich, O., Diestel, A., Eyüpoglu, I. Y., & Nitsch, R. (2001) · Nature Cell Biology · doi:10.1038/ncb1201-1035 · Cited by 175 · see citing works
Zinc Triggers Microglial Activation
Kauppinen, T. M., Higashi, Y., Suh, S. W., Escartin, C., Nagasawa, K., & Swanson, R. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1236-08.2008 · Cited by 174 · see citing works
Self-citation
Dynamic Complexity of the Microglial Activation Response in Transgenic Models of Amyloid Deposition: Implications for Alzheimer Therapeutics
Morgan, D., Gordon, M. N., Tan, J., Wilcock, D. M., & Rojiani, A. M. (2005) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000178444.33972.e0 · Cited by 174 · see citing works
The Sequence-specific DNA Binding of NF-κB Is Reversibly Regulated by the Automodification Reaction of Poly (ADP-ribose) Polymerase 1
Chang, W.-J., & Álvarez-González, R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104666200 · Cited by 134 · see citing works
Qualitatively different modes of perirhinal–hippocampal engagement when rats explore novel vs. familiar objects as revealed by c‐Fos imaging
Albasser, M. M., Poirier, G. L., & Aggleton, J. P. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07042.x · Cited by 131 · see citing works
Minocycline reduces the development of abnormal tau species in models of Alzheimer's disease
Noble, W., Garwood, C., Stephenson, J., Kinsey, A. M., Hanger, D., & Anderton, B. (2009) · The FASEB Journal · doi:10.1096/fj.08-113795 · Cited by 123 · see citing works
Microglial VEGF Receptor Response Is an Integral Chemotactic Component in Alzheimer's Disease Pathology
Ryu, J. K., Cho, T., Choi, H. B., Wang, Y. T., & McLarnon, J. G. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2888-08.2009 · Cited by 121 · see citing works
β-Amyloid Stimulates Murine Postnatal and Adult Microglia Cultures in a Unique Manner
Floden, A. M., & Combs, C. K. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4822-05.2006 · Cited by 118 · see citing works
Insulin‐like growth factor‐1 mRNA is increased in deafferented hippocampus: Spatiotemporal correspondence of a trophic event with axon sprouting
Guthrie, K. M., Nguyen, T., & Gall, C. M. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903520111 · Cited by 113 · see citing works
Critical Role of the Automodification of Poly(ADP-ribose) Polymerase-1 in Nuclear Factor-κB-dependent Gene Expression in Primary Cultured Mouse Glial Cells
Nakajima, H., Nagaso, H., Kakui, N., Ishikawa, M., Hiranuma, T., & Hoshiko, S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407923200 · Cited by 97 · see citing works
Nuclear translocation of p65 NF-κB is sufficient for VCAM-1, but not ICAM-1, expression in TNF-stimulated smooth muscle cells: Differential requirement for PARP-1 expression and interaction
Zerfaoui, M., Suzuki, Y., Naura, A. S., Hans, C. P., Nichols, C. D., & Boulares, A. H. (2007) · Cellular Signalling · doi:10.1016/j.cellsig.2007.10.007 · Cited by 93 · see citing works
TGF-&#946; Pathway as a Potential Target in Neurodegeneration and Alzheimers
Wyss-Coray, T. (2006) · Current Alzheimer Research · doi:10.2174/156720506777632916 · Cited by 85 · see citing works
Inhibition of Poly(ADP-Ribose) Polymerase Suppresses Inflammation and Promotes Recovery after Ischemic Injury
Kauppinen, T. M., Suh, S. W., Berman, A., Hamby, A. M., & Swanson, R. A. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.9 · Cited by 84 · see citing works
Self-citation
Regulation of NFAT by poly(ADP-ribose) polymerase activity in T cells
Valdor, R., Schreiber, V., Saenz, L., Martı́nez, T., Muñoz-Suano, A., Dominguez‐Villar, M., Ramı́rez, P., Parrilla, P., Aguado, E., & Garcia-Cozar, F. J. (2008) · Molecular Immunology · doi:10.1016/j.molimm.2007.10.044 · Cited by 78 · see citing works
Transforming growth factor beta expression in reactive spinal cord microglia and meningeal inflammatory cells during experimental allergic neuritis
Kiefer, R., Gold, R., Gehrmann, J., Lindholm, D., Wekerle, H., & Kreutzberg, G. W. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490360405 · Cited by 55 · see citing works
Microglial activation depends on beta‐amyloid conformation: role of the formylpeptide receptor 2
Heurtaux, T., Michelucci, A., Losciuto, S., Gallotti, C., Felten, P., Dorban, G., Grandbarbe, L., Morga, E., & Heuschling, P. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06783.x · Cited by 54 · see citing works
Minocycline does not affect amyloid β phagocytosis by human microglial cells
Familian, A., Eikelenboom, P., & Veerhuis, R. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.01.052 · Cited by 53 · see citing works
Minocycline reduces engraftment and activation of bone marrow‐derived cells but sustains their phagocytic activity in a mouse model of Alzheimer's disease
Malm, T., Magga, J. M., Kuh, G. F., Vatanen, T., Koistinaho, M., & Koıstınaho, J. (2008) · Glia · doi:10.1002/glia.20726 · Cited by 53 · see citing works
Poly (ADP‐ribose) polymerases (PARPs) 1‐3 regulate astrocyte activation
Phulwani, N. K., & Kielian, T. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05403.x · Cited by 51 · see citing works
Activation and Nuclear translocation of p65 NF-kappaB are sufficient for VCAM-1, but insufficient for ICAM-1, expression in TNF-stimulated primary smooth muscle cells: differential requirement for PARP-1 expression and interaction
Boulares, H. A., Suzuki, Y., Zerfaoui, M., Naura, A. S., Hans, C. P., & Nichols, C. B. (2007) · The Journal of Immunology · Cited by 18 · see citing works
Induction of angiogenesis by platelet-activating factor in the rat striatum
Tran, K., Ryu, J., & McLarnon, J. (2005) · NeuroReport · doi:10.1097/01.wnr.0000179073.24412.7b · Cited by 10 · see citing works

Flagged first, then by citations

1 of the 70 references couldn’t be matched to a known paper.

Sorted by citations

NAD+ metabolism and its roles in cellular processes during ageing
Covarrubias, A. J., Perrone, R., Grozio, A., & Verdin, E. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00313-x · Cited by 1,617 · see citing works
Triggering receptor expressed on myeloid cells 2 (TREM2) deficiency attenuates phagocytic activities of microglia and exacerbates ischemic damage in experimental stroke
Kawabori, M., Kacimi, R., Kauppinen, T., Calosing, C., Kim, J. Y., Hsieh, C. L., Nakamura, M. C., & Yenari, M. A. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2620-14.2015 · Cited by 375 · see citing works
Self-citation
Oxidative and nitrative stress in neurodegeneration
Cobb, C. A., & Cole, M. P. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.04.020 · Cited by 300 · see citing works
Caspase-1 inhibition alleviates cognitive impairment and neuropathology in an Alzheimer’s disease mouse model
Flores, J., Noël, A., Foveau, B., Lynham, J., Lecrux, C., & LeBlanc, A. C. (2018) · Nature Communications · doi:10.1038/s41467-018-06449-x · Cited by 288 · see citing works
Neuronal cell death mechanisms in Alzheimer’s disease: An insight
Goel, P., Chakrabarti, S., Goel, K., Bhutani, K., Chopra, T., & Bali, S. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.937133 · Cited by 235 · see citing works
PARP-1 involvement in neurodegeneration: A focus on Alzheimer’s and Parkinson’s diseases
Martire, S., Mosca, L., & D’Erme, M. (2015) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2015.04.001 · Cited by 228 · see citing works
Molecular Mechanisms of Parthanatos and Its Role in Diverse Diseases
Huang, P., Chen, G., Jin, W., Mao, K., Wan, H., & He, Y. T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137292 · Cited by 193 · see citing works
The role of PARP1 in neurodegenerative diseases and aging
Mao, K., & Zhang, G. (2022) · The FEBS Journal · doi:10.1111/febs.15716 · Cited by 172 · see citing works
The Important Role of Zinc in Neurological Diseases
Li, Z., Liu, Y., Wei, R., Yong, V. W., & Xue, M. (2022) · Biomolecules · doi:10.3390/biom13010028 · Cited by 163 · see citing works
Exposure to gestational diabetes mellitus induces neuroinflammation, derangement of hippocampal neurons, and cognitive changes in rat offspring
Vuong, B., Odero, G., Rozbacher, S., Stevenson, M., Kereliuk, S. M., Pereira, T. J., Dolinsky, V. W., & Kauppinen, T. M. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0859-9 · Cited by 147 · see citing works
Self-citation
Mechanisms of DNA damage-mediated neurotoxicity in neurodegenerative disease
Welch, G., & Tsai, L. (2022) · The EMBO Reports · doi:10.15252/embr.202154217 · Cited by 129 · see citing works
PARP-1 Inhibition Attenuates Neuronal Loss, Microglia Activation and Neurological Deficits after Traumatic Brain Injury
Stoica, B. A., Loane, D. J., Zhao, Z., Kabadi, S. V., Hanscom, M., Byrnes, K. R., & Faden, A. I. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2013.3194 · Cited by 122 · see citing works
The Safety and Antiaging Effects of Nicotinamide Mononucleotide in Human Clinical Trials: an Update
Song, Q., Zhou, X., Xu, K., Liu, S., Zhu, X., & Yang, J. J. (2023) · Advances in Nutrition · doi:10.1016/j.advnut.2023.08.008 · Cited by 122 · see citing works
Cell Death Mechanisms of Neurodegeneration
Fan, J., Dawson, T. M., & Dawson, V. L. (2017) · Advances in neurobiology · doi:10.1007/978-3-319-57193-5_16 · Cited by 112 · see citing works
Nuclear poly(ADP-ribose) activity is a therapeutic target in amyotrophic lateral sclerosis
McGurk, L., Mojsilovic‐Petrovic, J., Deerlin, V. M. V., Shorter, J., Kalb, R. G., Lee, V. M., Trojanowski, J. Q., Lee, E. B., & Bonini, N. M. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0586-1 · Cited by 112 · see citing works
Poly(ADP-ribose) Polymerase-1 in Amyloid Beta Toxicity and Alzheimer's Disease
Strosznajder, J. B., Czapski, G. A., Adamczyk, A., & Strosznajder, R. P. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8258-9 · Cited by 109 · see citing works
Poly (ADP-ribose) (PAR)-dependent cell death in neurodegenerative diseases
Park, H., Kam, T., Dawson, T. M., & Dawson, V. L. (2020) · International review of cytology · doi:10.1016/bs.ircmb.2019.12.009 · Cited by 105 · see citing works
ADP-ribosylation signalling and human disease
Palazzo, L., Mikolčević, P., Mikoč, A., & Ahel, I. (2019) · Open Biology · doi:10.1098/rsob.190041 · Cited by 104 · see citing works
A critical role of TRPM2 channel in Aβ42‐induced microglial activation and generation of tumor necrosis factor‐α
Mortadza, S. A. S., Sim, J. A., Neubrand, V. E., & Jiang, L. (2017) · Glia · doi:10.1002/glia.23265 · Cited by 99 · see citing works
Brain Response to Injuries: When Microglia Go Sexist
Rahimian, R., Cordeau, P., & Križ, J. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.02.048 · Cited by 95 · see citing works
Pathologic role of glial nitric oxide in adult and pediatric neuroinflammatory diseases
Ghasemi, M., & Fatemi, A. S. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.06.002 · Cited by 95 · see citing works
Poly (ADP-ribose) polymerase-1 as a promising drug target for neurodegenerative diseases
Thapa, K., Khan, H., Sharma, U., Grewal, A. K., & Singh, T. G. (2021) · Life Sciences · doi:10.1016/j.lfs.2020.118975 · Cited by 92 · see citing works
Nicotinamide, a Poly [ADP-Ribose] Polymerase 1 (PARP-1) Inhibitor, as an Adjunctive Therapy for the Treatment of Alzheimer’s Disease
Salech, F., Ponce, D. P., Paula-Lima, A. C., SanMartín, C. D., & Behrens, M. I. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00255 · Cited by 89 · see citing works
Microglial NMDA receptors drive pro‐inflammatory responses via PARP‐1/TRMP2 signaling
Raghunatha, P., Vosoughi, A. R., Kauppinen, T. M., & Jackson, M. F. (2020) · Glia · doi:10.1002/glia.23790 · Cited by 87 · see citing works
Self-citation
The key players of parthanatos: opportunities for targeting multiple levels in the therapy of parthanatos-based pathogenesis
Liu, L., Li, J., Ke, Y., Zeng, X., Gao, J., Ba, X., & Wang, R. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-04109-w · Cited by 86 · see citing works
Therapeutic potential of boosting NAD+ in aging and age-related diseases
Aman, Y., Qiu, Y., Tao, J., & Fang, E. F. (2018) · Translational Medicine of Aging · doi:10.1016/j.tma.2018.08.003 · Cited by 85 · see citing works
Whole-exome sequencing and imaging genetics identify functional variants for rate of change in hippocampal volume in mild cognitive impairment
Nho, K. T., Corneveaux, J. J., Kim, S., Lin, H., Risacher, S. L., Shen, L., Swaminathan, S., Ramanan, V. K., Liu, Y., Foroud, T., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.24 · Cited by 81 · see citing works
Significance of Programmed Cell Death Pathways in Neurodegenerative Diseases
Guo, D., Liu, Z., Zhou, J., Ke, C., & Li, D. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25189947 · Cited by 81 · see citing works
Poly(ADP-ribose)polymerase-1 hyperactivation in neurodegenerative diseases: The death knell tolls for neurons
Narne, P., Pandey, V., Simhadri, P. K., & Phanithi, P. B. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.11.007 · Cited by 80 · see citing works
Activation of PARP by Oxidative Stress Induced by β-Amyloid: Implications for Alzheimer’s Disease
Abeti, R., & Duchen, M. R. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0895-x · Cited by 78 · see citing works
Nicotinamide Adenine Dinucleotide Metabolism and Neurodegeneration
Pehar, M., Harlan, B. A., Killoy, K. M., & Vargas, M. R. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7145 · Cited by 77 · see citing works
Parthanatos in the pathogenesis of nervous system diseases
Wang, X., & Ge, P. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.09.049 · Cited by 75 · see citing works
Inhibition of NADPH oxidase activation reduces EAE-induced white matter damage in mice
Choi, B. Y., Kim, J. H., Kho, A. R., Kim, I. Y., Lee, S. H., Lee, B. E., Choi, E., Sohn, M., Stevenson, M., Chung, T. N., et al. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0325-5 · Cited by 74 · see citing works
Self-citation
NF-κB transcriptional activation by TNFα requires phospholipase C, extracellular signal-regulated kinase 2 and poly(ADP-ribose) polymerase-1
Vuong, B., Hogan-Cann, A. D., Alano, C. C., Stevenson, M., Chan, W., Anderson, C. M., Swanson, R. A., & Kauppinen, T. M. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0448-8 · Cited by 71 · see citing works
Self-citation
Poly (ADP-Ribose) polymerase 1 and parthanatos in neurological diseases: From pathogenesis to therapeutic opportunities
Xu, X., Sun, B., & Zhao, C. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106314 · Cited by 70 · see citing works
Evaluation of the NAD+ biosynthetic pathway in ALS patients and effect of modulating NAD+ levels in hSOD1-linked ALS mouse models
Harlan, B. A., Killoy, K. M., Pehar, M., Liu, L., Auwerx, J. H., & Vargas, M. R. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113219 · Cited by 70 · see citing works
Plasma and Brain Concentrations of Doxycycline after Single and Repeated Doses in Wild-Type and APP23 Mice
Lucchetti, J., Fracasso, C., Balducci, C., Passoni, A., Forloni, G., Salmona, M., & Gobbi, M. (2018) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.118.252064 · Cited by 67 · see citing works
Parthanatos: Mechanisms, modulation, and therapeutic prospects in neurodegenerative disease and stroke
Liu, Y., Guttman, L. C., Dawson, V. L., & Dawson, T. M. (2024) · Biochemical Pharmacology · doi:10.1016/j.bcp.2024.116174 · Cited by 64 · see citing works
The balance between NAD+ biosynthesis and consumption in ageing
Strømland, Ø., Diab, J., Ferrario, E., Sverkeli, L. J., & Ziegler, M. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111569 · Cited by 63 · see citing works
Bioenergetic Impairment in Animal and Cellular Models of Alzheimer’s Disease: PARP-1 Inhibition Rescues Metabolic Dysfunctions
Martire, S., Fuso, A., Mosca, L., Forte, E., Correani, V., Fontana, M., Scarpa, S., Maras, B., & D’Erme, M. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-151040 · Cited by 62 · see citing works
Poly(ADP-ribose) polymerase-1-induced NAD+ depletion promotes nuclear factor-κB transcriptional activity by preventing p65 de-acetylation
Kauppinen, T. M., Gan, L., & Swanson, R. A. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.04.005 · Cited by 60 · see citing works
Self-citation
Poly(ADP-ribose) polymerase-1 regulates microglia mediated decrease of endothelial tight junction integrity
Mehrabadi, A. R., Korolainen, M. A., Odero, G. L., Miller, D. W., & Kauppinen, T. M. (2017) · Neurochemistry International · doi:10.1016/j.neuint.2017.04.014 · Cited by 60 · see citing works
Self-citation
Dementia in Diabetes: The Role of Hypoglycemia
Husain, K. H., Sarhan, S. F., AlKhalifa, H. K. A. A., Buhasan, A., Moin, A. S. M., & Butler, A. E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24129846 · Cited by 52 · see citing works
Microglia-Mediated Neurovascular Unit Dysfunction in Alzheimer’s Disease
Huang, W., Xia, Q., Zheng, F., Zhao, X. L., Ge, F., Xiao, J., Liu, Z., Shen, Y., Ye, K., Wang, D., et al. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-221064 · Cited by 46 · see citing works
PARP1-mediated PARylation activity is essential for oligodendroglial differentiation and CNS myelination
Wang, Y., Zhang, Y., Zhang, S., Kim, B., Hull, V. L., Xu, J., Prabhu, P., Gregory, M., Martínez‐Cerdeño, V., Zhan, X., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109695 · Cited by 46 · see citing works
Poly (ADP-ribose) polymerase 1 and neurodegenerative diseases: past, present, and future
Hu, M.-L., Pan, Y.-R., Yong, Y.-Y., Liu, Y., Yu, L., Qin, D.-L., Qiao, G., Law, B. Y.-K., Wu, J.-M., Zhou, X.-G., et al. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102078 · Cited by 44 · see citing works
Targeting NAD+ degradation: The therapeutic potential of flavonoids for Alzheimer's disease and cognitive frailty
Ruan, Q., Ruan, J., Zhang, W., Qian, F., & Yu, Z. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.08.010 · Cited by 44 · see citing works
Txnip mediates glucocorticoid-activated NLRP3 inflammatory signaling in mouse microglia
Bharti, V., Tan, H. T., Zhou, H., & Wang, J. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.104564 · Cited by 41 · see citing works
Neuroprotective Effects of PARP Inhibitors in Drosophila Models of Alzheimer’s Disease
Maggiore, A., Casale, A. M., Toscanelli, W., Cappucci, U., Rotili, D., Grieco, M., Gagné, J.-P., Poirier, G. G., d’Erme, M., & Piacentini, L. (2022) · Cells · doi:10.3390/cells11081284 · Cited by 40 · see citing works
Regulation of Biomolecular Condensates by Poly(ADP-ribose)
Rhine, K., Odeh, H. M., Shorter, J., & Myong, S. (2023) · Chemical Reviews · doi:10.1021/acs.chemrev.2c00851 · Cited by 39 · see citing works
Natural Inhibitors of Poly(ADP-ribose) Polymerase-1
Banasik, M., Stedeford, T. J., & Strosznajder, R. P. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8257-x · Cited by 37 · see citing works
The Enemy within: Innate Surveillance-Mediated Cell Death, the Common Mechanism of Neurodegenerative Disease
Richards, R. I., Robertson, S. A., O’Keefe, L. V., Fornarino, D. L., Scott, A., Lardelli, M. T., & Baune, B. T. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00193 · Cited by 37 · see citing works
Selective Sparing of Striatal Interneurons after Poly (ADP-Ribose) Polymerase 1 Inhibition in the R6/2 Mouse Model of Huntington’s Disease
Paldino, E., Cardinale, A., D’Angelo, V., Sauve, I., Giampà, C., & Fusco, F. R. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00061 · Cited by 37 · see citing works
Particulate matter increases beta-amyloid and activated glial cells in hippocampal tissues of transgenic Alzheimer's mouse: Involvement of PARP-1
Jang, S., Kim, E. W., Zhang, Y., Lee, J., Cho, S. Y., Ha, J.-H., Kim, H., & Kim, E. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.04.068 · Cited by 37 · see citing works
Self-citation
Roles of vitamin D in amyotrophic lateral sclerosis: possible genetic and cellular signaling mechanisms
Lương, K. V. Q., & Nguyễn, L. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-16 · Cited by 37 · see citing works
Crosstalk between Different DNA Repair Pathways Contributes to Neurodegenerative Diseases
Gupta, S., You, P., SenGupta, T., Nilsen, H. L., & Sharma, K. (2021) · Biology · doi:10.3390/biology10020163 · Cited by 34 · see citing works
Aberrant cardiolipin metabolism is associated with cognitive deficiency and hippocampal alteration in tafazzin knockdown mice
Cole, L., Kim, J. H., Amoscato, A. A., Tyurina, Y. Y., Bayır, H., Karimi, B., Siddiqui, T. J., Kagan, V. E., Hatch, G. M., & Kauppinen, T. M. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.07.022 · Cited by 31 · see citing works
Self-citation
PARP overactivation in neurological disorders
Arruri, V. K., Gundu, C., Khan, I., Khatri, D. K., & Singh, S. B. (2021) · Molecular Biology Reports · doi:10.1007/s11033-021-06285-1 · Cited by 26 · see citing works
Nicotinamide N-Methyltransferase (NNMT): A New Hope for Treating Aging and Age-Related Conditions
Li, J., Sun, W.-D., Zhu, X., Mei, Y.-Z., Li, W.-S., & Li, J.-H. (2024) · Metabolites · doi:10.3390/metabo14060343 · Cited by 26 · see citing works
The new insight on the regulatory role of the vitamin D3 in metabolic pathways characteristic for cancerogenesis and neurodegenerative diseases
Kubis-Kubiak, A., & Piwowar, A. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.07.008 · Cited by 26 · see citing works
Recent advances in preventing neurodegenerative diseases
Chou, S.-C., Aggarwal, A., Dawson, V. L., Dawson, T. M., & Kam, T. (2021) · Faculty Reviews · doi:10.12703/r/10-81 · Cited by 24 · see citing works
Pathobiochemistry of Aging and Neurodegeneration: Deregulation of NAD+ Metabolism in Brain Cells
Kolotyeva, N. A., Groshkov, A. A., Rozanova, N. A., Berdnikov, A. K., Novikova, S. V., Komleva, Y. K., Salmina, A. B., Illarioshkin, S. N., & Пирадов, М. А. (2024) · Biomolecules · doi:10.3390/biom14121556 · Cited by 22 · see citing works
Therapeutic Potentials of Poly (ADP‐Ribose) Polymerase 1 (PARP1) Inhibition in Multiple Sclerosis and Animal Models: Concept Revisiting
Wang, Y., Pleasure, D., Deng, W., & Guo, F. (2021) · Advanced Science · doi:10.1002/advs.202102853 · Cited by 22 · see citing works
Radiation-induced neuroinflammation: a potential protective role for poly(ADP-ribose) polymerase inhibitors?
Gutierrez‐Quintana, R., Walker, D. J., Williams, K. J., Forster, D. M., & Chalmers, A. J. (2022) · Neuro-Oncology Advances · doi:10.1093/noajnl/vdab190 · Cited by 22 · see citing works
Poly(ADP-ribose) polymerase is not involved in the neuroprotection exerted by azithromycin against ischemic stroke in mice
Petrelli, F., Muzzi, M., Chiarugi, A., Bagetta, G., & Amantea, D. (2016) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2016.09.030 · Cited by 21 · see citing works
Recent Understanding of the Molecular Mechanisms of Alzheimer?s Disease
Grimm, M. O. W., & Hartmann, T. (2011) · Journal of Addiction Research & Therapy · doi:10.4172/2155-6105.s5-004 · Cited by 19 · see citing works
Age-Dependent Alterations of the Hippocampal Cell Composition and Proliferative Potential in the hAβPPSwInd-J20 Mouse
Fu, Y., Rusznák, Z., Kwok, J. B., Kim, W. S., & Paxinos, G. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-132717 · Cited by 18 · see citing works
Vulnerability to a Metabolic Challenge Following Perinatal Asphyxia Evaluated by Organotypic Cultures: Neonatal Nicotinamide Treatment
Pérez-Lobos, R., Lespay‐Rebolledo, C., Tapia-Bustos, A., Palacios, E., Vío, V., Bustamante, D., Morales, P., & Herrera‐Marschitz, M. (2017) · Neurotoxicity Research · doi:10.1007/s12640-017-9755-4 · Cited by 17 · see citing works
Oxidative Stress in HIV-Associated Neurodegeneration: Mechanisms of Pathogenesis and Therapeutic Targets
Gagliardi, S., Hotchkin, T., Hillmer, G., Engelbride, M., Diggs, A., Tibebe, H., Izumi, C., Sullivan, C., Cropp, C., Lantz, O., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26146724 · Cited by 16 · see citing works
Extra Virgin Olive Oil consumption from Mild Cognitive Impairment patients attenuates oxidative and nitrative stress reflecting on the reduction of the PARP levels and DNA damage
Tzekaki, E. E., Tsolaki, M., Geromichalos, G. D., & Pantazaki, Α. A. (2021) · Experimental Gerontology · doi:10.1016/j.exger.2021.111621 · Cited by 16 · see citing works
Effects of Amyloid-β-Mimicking Peptide Hydrogel Matrix on Neuronal Progenitor Cell Phenotype for the in vitro Modeling of Alzheimer's Disease
Mathes, T. G., Monirizad, M., Ermis, M., de Barros, N. R., Rodriguez, M., Kraatz, H., Jucaud, V., Khademhosseini, A., & Falcone, N. (2023) · Acta Biomaterialia · doi:10.1016/j.actbio.2024.05.020 · Cited by 15 · see citing works
Oxidized cholesterol species as signaling molecules in the brain: diabetes and Alzheimer’s disease
Weigel, T. K., Kulas, J. A., & Ferris, H. A. (2019) · Neuronal Signaling · doi:10.1042/ns20190068 · Cited by 15 · see citing works
PARkinson's: From cellular mechanisms to potential therapeutics
Lengyel‐Zhand, Z., Puentes, L. N., & Mach, R. H. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107968 · Cited by 15 · see citing works
Attenuation of zinc-enhanced inflammatory M1 phenotype of microglia by peridinin protects against short-term spatial-memory impairment following cerebral ischemia in mice
Ueba, Y., Aratake, T., Onodera, K., Higashi, Y., Hamada, T., Shimizu, T., Shimizu, S., Yawata, T., Nakamura, R., Akizawa, T., et al. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.11.067 · Cited by 15 · see citing works
Self-citation
Computational Analysis Indicates That PARP1 Acts as a Histone Deacetylases Interactor Sharing Common Lysine Residues for Acetylation, Ubiquitination, and SUMOylation in Alzheimer’s and Parkinson’s Disease
Gupta, R. V., & Kumar, P. (2021) · ACS Omega · doi:10.1021/acsomega.0c06168 · Cited by 15 · see citing works
PARP-DNA trapping ability of PARP inhibitors jeopardizes astrocyte viability: Implications for CNS disease therapeutics
Sinha, A., Katyal, S., & Kauppinen, T. M. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108502 · Cited by 14 · see citing works
Self-citation
Life-threatening risk factors contribute to the development of diseases with the highest mortality through the induction of regulated necrotic cell death
Zsuzsa, M., Jenei, V., Mácsik, R., Mezhonova, E., Diyab, S., Csősz, R., Bácsi, A., Mázló, A., & Koncz, G. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-07563-7 · Cited by 13 · see citing works
ADP-ribosylation, a multifaceted modification: Functions and mechanisms in aging and aging-related diseases
Hao, W., Jialong, Z., Jiuzhi, Y., Yang, Y. S., Lv, C., & Jin-cai, L. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102347 · Cited by 13 · see citing works
A Novel Probiotic Formula, BIOCG, Protects Against Alzheimer’s-Related Cognitive Deficits via Regulation of Dendritic Spine Dynamics
Sun, M., Bao, W., Huang, C., Xia, Z., Zhang, C., Wang, G., Wang, R., Li, J., Roux, S., Li, Q., et al. (2021) · Current Alzheimer Research · doi:10.2174/1567205018666211022091110 · Cited by 13 · see citing works
A Review of PARP-1 Inhibitors: Assessing Emerging Prospects and Tailoring Therapeutic Strategies
Ramesh, S., Almeida, S. D., Hammigi, S., Radhakrishna, G. K., Sireesha, G., Theivendren, P., Vellingiri, S., Kunjiappan, S., Ammunje, D. N., & Pavadai, P. (2023) · Drug Research · doi:10.1055/a-2181-0813 · Cited by 12 · see citing works
Nicotinamide Adenine Dinucleotide (NAD + )-Dependent Signaling in Neurological Disorders
Bresque, M., Esteve, D., Pehar, M., & Vargas, M. R. (2023) · Antioxidants and Redox Signaling · doi:10.1089/ars.2023.0241 · Cited by 12 · see citing works
Oxidative Stress Events and Neuronal Dysfunction in Alzheimer’s Disease: Focus on APE1/Ref-1-Mediated Survival Strategies
Kaur, N., Sarkar, B., Mittal, S., Dhiman, M., Taglialatela, G., Perez‐Polo, R. J., & Mantha, A. K. (2014) · Springer eBooks · doi:10.1007/978-81-322-2035-0_13 · Cited by 12 · see citing works
A high-refined carbohydrate diet facilitates compulsive-like behavior in mice through the nitric oxide pathway
Gomes, J. A. S., Oliveira, M. C., Gobira, P. H., da Silva, G. C., Marçal, A. P., Gomes, G. F., Ferrari, C. Z., Lemos, V. S., de Oliveira, A. C. P., Vieira, L. B., et al. (2018) · Nitric Oxide · doi:10.1016/j.niox.2018.08.008 · Cited by 11 · see citing works
Aggregability of the SQSTM1/p62-based aggresome-like induced structures determines the sensitivity to parthanatos
Hamano, S., Noguchi, T., Asai, Y., Ito, R., Komatsu, R., Sato, T., Inoue, A., Maruyama, T., Kudo, T., Hirata, Y., et al. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-01838-2 · Cited by 10 · see citing works
Doxycycline rescues recognition memory and circadian motor rhythmicity but does not prevent terminal disease in fatal familial insomnia mice
Lavigna, G., Masone, A., Bouybayoune, I., Bertani, I., Lucchetti, J., Gobbi, M., Porcu, L., Zordan, S., Rigamonti, M., Imeri, L., et al. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105455 · Cited by 10 · see citing works
Glitches in the brain: the dangerous relationship between radiotherapy and brain fog
Marino, N., Bedeschi, M., Vaccari, M. E., Cambiaghi, M., & Tesei, A. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1328361 · Cited by 9 · see citing works
Fruquintinib/HMPL-013 ameliorates cognitive impairments and pathology in a mouse model of cerebral amyloid angiopathy (CAA)
Zhou, G., Xiang, T., Xu, Y., He, B., Wu, L., Zhu, G., Xie, J., Yao, L., & Xiao, Z. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175446 · Cited by 8 · see citing works
PARP1 Gene Variation and Microglial Activity on [11C]PBR28 PET in Older Adults at Risk for Alzheimer’s Disease
Kim, S., Nho, K. T., Risacher, S. L., Inlow, M. H., Swaminathan, S., Yoder, K. K., Shen, L., West, J. D., McDonald, B. C., Tallman, E. F., et al. (2013) · Lecture notes in computer science · doi:10.1007/978-3-319-02126-3_15 · Cited by 8 · see citing works
Alzheimer’s disease: a jigsaw puzzle comprised of different types of programmed cell death pieces
Wang, Y., Mu, D., Li, Y., Liu, C., Feng, J., Lai, Y., & Lou, G. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149861 · Cited by 7 · see citing works
PARP1 deficiency mitigates amyloid pathology, neurodegeneration, and cognitive decline in a familial Alzheimer’s disease model
Jhaldiyal, A., Kumari, M., Guttman, L. C., Tripathi, T., Khan, M. R., Wang, J., Biswas, D., Pasupuleti, A., Aggarwal, A., Pandya, S., et al. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2525028123 · Cited by 6 · see citing works
Wild Bitter Melon Extract Abrogates Hypoxia-Induced Cell Death via the Regulation of Ferroptosis, ER Stress, and Apoptosis in Microglial BV2 Cells
Lin, C., Wu, J., Hsieh, P., Chiu, V. J.-Y., Lan, C., & Kuo, C. (2022) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2022/1072600 · Cited by 5 · see citing works
Retracted
The Role of Caffeine in Neurodegenerative Diseases
Lương, K. V. Q., & Nguyễn, L. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-411462-3.00028-x · Cited by 5 · see citing works
PARP inhibitors target cellular energy metabolism: Mechanisms of action and clinical implications
Li, J., Mu, D., Jin, L. P., Lan, M., Wu, W., Zhang, S., & Dai, Y. (2026) · Translational Oncology · doi:10.1016/j.tranon.2026.102757 · Cited by 4 · see citing works
Possible Therapeutic Potential of Flavonoids and Phenolic Acids from Honey in Age-Related Neurodegenerative Diseases Via Targeting NAD+ Degradation
Khan, A., Alshahrani, S., Arafah, A. M., Qamar, W., Shoaib, A., Wali, A. F., Amin, I., Alqahtani, S. S., & Rehman, M. U. (2020) · Springer eBooks · doi:10.1007/978-981-15-7305-7_2 · Cited by 3 · see citing works
Protective action of glutamate antibodies on increased expression of genes of programmed death of rat brain cells induced by injection of a β-amyloid fragment (25–35)
Викторович, К. В., Davydova, T. V., & Fomina, V. G. (2014) · Biology Bulletin · doi:10.1134/s1062359014020034 · Cited by 3 · see citing works
NAD + ‒circadian rhythm coupling in dementia
Zhang, S., Lee, J., Pan, J., Enger, R., Hrubos‐Strøm, H., Musiek, E. S., Fang, E. F., & Le, W. (2026) · Alzheimer s & Dementia · doi:10.1002/alz.71360 · Cited by 2 · see citing works
Membrane-Spanning 4-Domains Subfamily A, MS4A Cluster
Brown, K. S., Turton, J. C., & Morgan, K. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7309-1_8 · Cited by 2 · see citing works
The Effects Of Oil Palm Phenolics On Inflammation And Oxidative Stress In Relation To Amyloid Beta Plaques In Fad-Mutant And Wild Type B103 Cells
Godsey, L. M. (2012) · Human Biology · Cited by 2 · see citing works
Role of Zinc in Brain Functions, and Brain Zinc Dyshomeostasis
Higashi, Y., & Aratake, T. (2025) · Royal Society of Chemistry eBooks · doi:10.1039/9781837676583-00187 · Cited by 1 · see citing works
Self-citation
NF-κB across the Alzheimer disease spectrum: Context-dependent protective and pathogenic roles
Azargoonjahromi, A., Abutalebian, F., & Nasiri, H. (2026) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2026.08.008 · Cited by 1 · see citing works

The role of microglial PARP-1 in Alzheimer’s disease
Rezaeian Mehrabadi, A. (2017) · Mspace (University of Manitoba)
P4–092: Regulation of NF–κB and AP–1 by poly(ADP–ribose) polymerase–1 in astrocytes of Alzheimer's disease
Tanaka, S., & Ueda, K. (2006) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2006.05.1830
Poly(ADP-ribose) Polymerase 1 Deficiency Attenuates Amyloid Pathology, Neurodegeneration, and Cognitive Decline in a Familial Alzheimer’s Disease ModelPreprint
Jhaldiyal, A., Kumari, M., Tripathi, T., Khan, R. H., Wang, J. L., Guttman, L. C., Biswas, D., Pasupuleti, A., Aggarwal, A., Pandya, S., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.06.674313 · Cited by 3 · see citing works
Poly(ADP-Ribose) Polymerase-1 Promotes Microglial Activation, Proliferation, and Matrix Metalloproteinase-9-Mediated Neuron Death
Kauppinen, T. M., & Swanson, R. A. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.4.2288 · Cited by 181 · see citing works
Self-citation
Poly(ADP‐ribose) polymerase‐1 activity promotes NF‐κB‐driven transcription and microglial activation: implication for neurodegenerative disorders
Chiarugi, A., & Moskowitz, M. A. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01684.x · Cited by 216 · see citing works

Authors: Kauppinen, T. M., Suh, S., Higashi, Y., Berman, A. E., Escartin, C., Won, S., Wang, C., Cho, S.-H., Gan, L., & Swanson, R. A.
Affiliations: San Francisco VA Medical Center (US)
University of California, San Francisco (US)
Corresponding author: Kauppinen, Tiina M
ORCID: Kauppinen, Tiina M
Suh, Sang
Higashi, Youichirou
Escartin, Carole
Won, Seok
Wang, Chao
Gan, Li
Swanson, Raymond A
Venue: Journal of Neuroinflammation
Publisher: Springer Science and Business Media LLC
Published: 2011
Volume: 8
Issue: 1
Pages: 152
ISSN: 1742-2094 (ISSN-L)
DOI: 10.1186/1742-2094-8-152
PMC: PMC3247192
OpenAlex: W2147930131
Cited by: 112
References: 70
Citations by year: 2026: 7 · 2025: 6 · 2024: 10 · 2023: 11 · 2022: 9 · 2021: 13 · 2020: 8 · 2019: 3 · 2018: 9 · 2017: 8 · 2016: 5 · 2015: 6 · 2014: 6 · 2013: 6 · 2012: 4
FWCI: 3.01
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Journal of Neuroinflammation (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
HAL (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: U.S. Department of Veterans Affairs
American Heart Association (SDG 0835222N)
National Institutes of Health
University of California, San Francisco
National Institute on Aging (R01AG030207, AG030207-A2, R21AG029483, AG029483)
National Institute of Neurological Disorders and Stroke (NS 041421, R01NS041421)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: PARP1, amyloid-beta, microglial activation, Alzheimer's disease, NF-κB, PARP1 inhibition, neuroinflammation, neurotoxicity, cognitive impairment, TNF-α, nitric oxide, TGF-beta, vascular endothelial growth factor, microglia-neuron co-culture
MeSH terms: Poly (ADP-Ribose) Polymerase-1, Animals, Behavior, Animal, Cells, Cultured, Hippocampus, Memory, Mice, Inbred C57BL, Neurons, Phagocytosis, Poly(ADP-ribose) Polymerases, Cytokines, Amyloid beta-Peptides, NF-kappa B, Microglia, Mice, Knockout, Coculture Techniques, Mice, Calbindins, S100 Calcium Binding Protein G

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

Poly(ADP-ribose)polymerase-1 modulates microglial responses to amyloid β

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks