S100B Inhibitor Pentamidine Attenuates Reactive Gliosis and Reduces Neuronal Loss in a Mouse Model of Alzheimer's Disease - PubMed (original) (raw)
S100B Inhibitor Pentamidine Attenuates Reactive Gliosis and Reduces Neuronal Loss in a Mouse Model of Alzheimer's Disease
Carla Cirillo et al. Biomed Res Int. 2015.
Abstract
Among the different signaling molecules released during reactive gliosis occurring in Alzheimer's disease (AD), the astrocyte-derived S100B protein plays a key role in neuroinflammation, one of the hallmarks of the disease. The use of pharmacological tools targeting S100B may be crucial to embank its effects and some of the pathological features of AD. The antiprotozoal drug pentamidine is a good candidate since it directly blocks S100B activity by inhibiting its interaction with the tumor suppressor p53. We used a mouse model of amyloid beta- (Aβ-) induced AD, which is characterized by reactive gliosis and neuroinflammation in the brain, and we evaluated the effect of pentamidine on the main S100B-mediated events. Pentamidine caused the reduction of glial fibrillary acidic protein, S100B, and RAGE protein expression, which are signs of reactive gliosis, and induced p53 expression in astrocytes. Pentamidine also reduced the expression of proinflammatory mediators and markers, thus reducing neuroinflammation in AD brain. In parallel, we observed a significant neuroprotection exerted by pentamidine on CA1 pyramidal neurons. We demonstrated that pentamidine inhibits Aβ-induced gliosis and neuroinflammation in an animal model of AD, thus playing a role in slowing down the course of the disease.
Figures
Figure 1
(a) Western blot and (b–f) densitometric analysis (arbitrary units normalized on the expression of the housekeeping protein β_-actin) showing the effect of 7 days of intrahippocampal injection of pentamidine (0.05–5 μ_g/mL/day) on GFAP (b), iNOS (c), p-p38 MAPK (d), COX-2 (e), and RAGE (f) expression in A_β_-injected mice. Results are expressed as mean ± SEM of n = 5 experiments performed in triplicate. ∗∗∗ P < 0.001 versus vehicle-treated mice; °_P < 0.05, °°_P < 0.01 and °°°P < 0.001 versus A_β_-treated mice.
Figure 2
(a) Electrophoretic mobility shift assay (EMSA) and the relative (b) densitometric analysis showing the effect following 7 days of intrahippocampal injection of pentamidine (0.05–5 μ_g/mL/day) on the expression of NF-κ_B in A_β_-injected mice. Results are expressed as mean ± SEM of n = 5 experiments performed in triplicate. ∗∗∗ P < 0.001 versus vehicle-treated mice; °°_P < 0.01 and °°°_P < 0.001 versus A_β_-treated mice.
Figure 3
Effect of pentamidine on release of nitrites (a), MDA (b), PGE2 (c), IL-1_β_ (d), and S100B (e) in hippocampal homogenates of A_β_-injected mice. Results are expressed as mean ± SEM of n = 5 experiments performed in triplicate. ∗∗∗ P < 0.001 versus vehicle-treated mice; °P < 0.05, °°P < 0.01 and °°°P < 0.001 versus A_β_-treated mice.
Figure 4
(a) Immunohistochemistry analysis showing the effect of pentamidine in hippocampal coronal sections after A_β_ injection. The upper panel shows GFAP-positive cells (astrocytes) infiltrating the hippocampi. Note the increased number of GFAP-positive cells in A_β_-treated (2) compared to vehicle-treated mice (1) and the dose-dependent reduction after pentamidine treatment (3-4-5). Scale bar: 200 μ_m. (b) Nissl staining showing the effect of pentamidine on pyramidal neuron loss in the CA1 area after A_β injection. Note the reduced number of neurons stained in A_β_-treated (2) compared to vehicle-treated mice (1) and the dose-dependent reduction of neuronal loss after pentamidine treatment (3-4-5). Scale bar: 200 μ_m. (c) Immunofluorescence analysis showing the effect of pentamidine in hippocampal coronal sections after A_β injection. Note the reduced number of neurons after A_β_ injection (2) compared to vehicle-treated mice (1) and the dose-dependent neuroprotection after pentamidine treatment (3-4-5). Scale bar: 200 μ_m. (d) Relative quantification of GFAP expression, (e) extent of CA1 damage measurement, and (f) number of neurons stained with Fluorojade B (FJB) in the hippocampi. Results are expressed as mean ± SEM of n = 5 experiments performed in triplicate. ∗∗∗ P < 0.001 versus vehicle-treated mice; °°_P < 0.01 and °°°P < 0.001 versus A_β_-treated mice.
Figure 5
Effect of pentamidine (0.05–5 μ_g/mL/day) on GFAP and p53 expression in astrocyte in the hippocampi of A_β_-injected mice. (a) Immunofluorescence analysis of hippocampal coronal sections. Note the increased GFAP expression in hippocampal astrocytes of A_β_-treated (2) compared to vehicle-treated mice (1) and the dose-dependent reduction after pentamidine treatment (3-4-5). Scale bar: 50 μ_m. (b) Relative quantification of p53-positive/GFAP-positive (open bars) and p53-positive/GFAP-positive (filled bars) astrocytes in the CA1 area of the brain. Results are expressed as mean ± SEM of n = 4 experiments performed in triplicate. ∗∗∗ P < 0.001 versus vehicle-treated mice; °_P < 0.05 and °°°_P < 0.001 versus A_β_-treated mice. §§ P < 0.01 versus vehicle-treated mice; ## P < 0.01, ### P < 0.001 versus A_β_-treated mice.
Similar articles
- PSAPP mice exhibit regionally selective reductions in gliosis and plaque deposition in response to S100B ablation.
Roltsch E, Holcomb L, Young KA, Marks A, Zimmer DB. Roltsch E, et al. J Neuroinflammation. 2010 Nov 16;7:78. doi: 10.1186/1742-2094-7-78. J Neuroinflammation. 2010. PMID: 21080947 Free PMC article. - The difference in gliosis induced by β-amyloid and Tau treatments in astrocyte cultures derived from senescence accelerated and normal mouse strains.
Lü L, Mak YT, Fang M, Yew DT. Lü L, et al. Biogerontology. 2009 Dec;10(6):695-710. doi: 10.1007/s10522-009-9217-3. Biogerontology. 2009. PMID: 19221889 - Pentamidine protects mice from cecal ligation and puncture-induced brain damage via inhibiting S100B/RAGE/NF-κB.
Huang L, Zhang L, Liu Z, Zhao S, Xu D, Li L, Peng Q, Ai Y. Huang L, et al. Biochem Biophys Res Commun. 2019 Sep 17;517(2):221-226. doi: 10.1016/j.bbrc.2019.07.045. Epub 2019 Jul 20. Biochem Biophys Res Commun. 2019. PMID: 31331643 - Astrocytes: implications for neuroinflammatory pathogenesis of Alzheimer's disease.
Li C, Zhao R, Gao K, Wei Z, Yin MY, Lau LT, Chui D, Yu AC. Li C, et al. Curr Alzheimer Res. 2011 Feb;8(1):67-80. doi: 10.2174/156720511794604543. Curr Alzheimer Res. 2011. PMID: 21143158 Review. - Neuroinflammation in Alzheimer's Disease: The Preventive and Therapeutic Potential of Polyphenolic Nutraceuticals.
Sawikr Y, Yarla NS, Peluso I, Kamal MA, Aliev G, Bishayee A. Sawikr Y, et al. Adv Protein Chem Struct Biol. 2017;108:33-57. doi: 10.1016/bs.apcsb.2017.02.001. Epub 2017 Mar 22. Adv Protein Chem Struct Biol. 2017. PMID: 28427563 Review.
Cited by
- Damage-Associated Molecular Patterns in Inflammatory Diseases.
Roh JS, Sohn DH. Roh JS, et al. Immune Netw. 2018 Aug 13;18(4):e27. doi: 10.4110/in.2018.18.e27. eCollection 2018 Aug. Immune Netw. 2018. PMID: 30181915 Free PMC article. Review. - The S100B Inhibitor Pentamidine Ameliorates Clinical Score and Neuropathology of Relapsing-Remitting Multiple Sclerosis Mouse Model.
Di Sante G, Amadio S, Sampaolese B, Clementi ME, Valentini M, Volonté C, Casalbore P, Ria F, Michetti F. Di Sante G, et al. Cells. 2020 Mar 18;9(3):748. doi: 10.3390/cells9030748. Cells. 2020. PMID: 32197530 Free PMC article. - Targeting neuroinflammation in Alzheimer's disease.
Bronzuoli MR, Iacomino A, Steardo L, Scuderi C. Bronzuoli MR, et al. J Inflamm Res. 2016 Nov 3;9:199-208. doi: 10.2147/JIR.S86958. eCollection 2016. J Inflamm Res. 2016. PMID: 27843334 Free PMC article. Review. - Chitosan Glutamate-Coated Niosomes: A Proposal for Nose-to-Brain Delivery.
Rinaldi F, Hanieh PN, Chan LKN, Angeloni L, Passeri D, Rossi M, Wang JT, Imbriano A, Carafa M, Marianecci C. Rinaldi F, et al. Pharmaceutics. 2018 Mar 22;10(2):38. doi: 10.3390/pharmaceutics10020038. Pharmaceutics. 2018. PMID: 29565809 Free PMC article. - The Many Faces of Astrocytes in Alzheimer's Disease.
Monterey MD, Wei H, Wu X, Wu JQ. Monterey MD, et al. Front Neurol. 2021 Aug 31;12:619626. doi: 10.3389/fneur.2021.619626. eCollection 2021. Front Neurol. 2021. PMID: 34531807 Free PMC article. Review.
References
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical
Research Materials
Miscellaneous