eISSN: 1509-572x
ISSN: 1641-4640
Folia Neuropathologica
Current issue Archive Manuscripts accepted About the journal Special Issues Editorial board Reviewers Abstracting and indexing Subscription Contact Instructions for authors Ethical standards and procedures
Editorial System
Submit your Manuscript
SCImago Journal & Country Rank
2/2024
vol. 62
 
Share:
Share:
Original paper

Inhibitor of bromodomain and extraterminal domain proteins decreases transcription of Cd33 in the brain of mice subjected to systemic inflammation; a promising strategy for neuroprotection

Grzegorz A. Czapski
1
,
Marta Matuszewska
1
,
Magdalena Cieślik
1
,
Joanna B. Strosznajder
1

  1. Mossakowski Medical Research Institute, Polish Academy of Sciences, Warsaw, Poland
Folia Neuropathol 2024; 62 (2): 127-135
Online publish date: 2024/05/28
Article file
- Inhibitor (1).pdf  [0.12 MB]
Get citation
 
PlumX metrics:
 
1. Barroeta-Espar I, Weinstock LD, Perez-Nievas BG, Meltzer AC, Siao Tick Chong M, Amaral AC, Murray ME, Moulder KL, Morris JC, Cairns NJ, Parisi JE, Lowe VJ, Petersen RC, Kofler J, Ikonomovic MD, López O, Klunk WE, Mayeux RP, Frosch MP, Wood LB, Gomez-Isla T. Distinct cytokine profiles in human brains resilient to Alzheimer’s pathology. Neurobiol Dis 2019; 121: 327-337.
2. Belkina AC, Nikolajczyk BS, Denis GV. BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J Immunol 2013; 190: 3670-3678.
3. Bertram L, Lange C, Mullin K, Parkinson M, Hsiao M, Hogan MF, Schjeide BM, Hooli B, Divito J, Ionita I, Jiang H, Laird N, Moscarillo T,Ohlsen KL, Elliott K, Wang X, Hu-Lince D, Ryder M, Murphy A, Wagner SL, Blacker D, Becker KD, Tanzi RE. Genome-wide association analysis reveals putative Alzheimer’s disease susceptibility loci in addition to APOE. Am J Hum Genet 2008; 83: 623-632.
4. Bertram L, Tanzi RE. Alzheimer disease risk genes: 29 and counting. Nat Rev Neurol 2019; 15: 191-192.
5. Bertram L, Tanzi RE. Genomic mechanisms in Alzheimer’s disease. Brain Pathol 2020; 30: 966-977.
6. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol 1990; 27: 229-237.
7. Bradshaw EM, Chibnik LB, Keenan BT, Ottoboni L, Raj T, Tang A,Rosenkrantz LL, Imboywa S, Lee M, Von Korff A, Morris MC, Evans DA, Johnson K, Sperling RA, Schneider JA, Bennett DA, De Jager PL. CD33 Alzheimer’s disease locus: altered monocyte function and amyloid biology. Nat Neurosci 2013; 16: 848-850.
8. Brinkman-Van der Linden EC, Angata T, Reynolds SA, Powell LD, Hedrick SM, Varki A. CD33/Siglec-3 binding specificity, expression pattern, and consequences of gene deletion in mice. Mol Cell Biol 2003; 23: 4199-4206.
9. Brown GC. The endotoxin hypothesis of neurodegeneration. J Neuroinflammation 2019; 16: 180.
10. Bu XL, Yao XQ, Jiao SS, Zeng F, Liu YH, Xiang Y, Liang CR, Wang QH, Wang X, Cao HY, Yi X, Deng B, Liu CH, Xu J, Zhang LL, Gao CY, Xu ZQ, Zhang M, Wang L, Tan XL, Xu X, Zhou HD, Wang YJ. A study on the association between infectious burden and Alzheimer’s disease. Eur J Neurol 2015; 22: 1519-1525.
11. Cheng Y, Ma Z, Kim BH, Wu W, Cayting P, Boyle AP, Sundaram V, Xing X, Dogan N, Li J, Euskirchen G, Lin S, Lin Y, Visel A, Kawli T, Yang X, Patacsil D, Keller CA, Giardine B, Kundaje A, Wang T, Pennacchio LA, Weng Z, Hardison RC, Snyder MP. Principles of regulatory information conservation between mouse and human. Nature 2014; 515: 371-375.
12. Cheung KL, Kim C, Zhou MM. The functions of BET proteins in gene transcription of biology and diseases. Front Mol Biosci 2021; 8: 728777.
13. Côté S, Carmichael PH, Verreault R, Lindsay J, Lefebvre J, Laurin D. Nonsteroidal anti-inflammatory drug use and the risk of cognitive impairment and Alzheimer’s disease. Alzheimers Dement 2012; 8: 219-226.
14. Crocker PR, Paulson JC, Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol 2007; 7: 255-266.
15. Czapski GA, Adamczyk A, Strosznajder RP, Strosznajder JB. Expression and activity of PARP family members in the hippocampus during systemic inflammation: their role in the regulation of prooxidative genes. Neurochem Int 2013; 62: 664-673.
16. Czapski GA, Cakala M, Chalimoniuk M, Gajkowska B, Strosznajder JB. Role of nitric oxide in the brain during lipopolysaccharide-evoked systemic inflammation. J Neurosci Res 2007; 85: 1694-1703.
17. Czapski GA, Cakala M, Gajkowska B, Strosznajder JB. Poly(ADPribose) polymerase-1 inhibition protects the brain against systemic inflammation. Neurochem Int 2006; 49: 751-755.
18. Czapski GA, Cieślik M, Białopiotrowicz E, Lukiw WJ, Strosznajder JB. Down-regulation of cyclin D2 in amyloid b toxicity, inflammation, and Alzheimer’s disease. PLoS One 2021; 16: e0259740.
19. Czapski GA, Gajkowska B, Strosznajder JB. Systemic administration of lipopolysaccharide induces molecular and morphological alterations in the hippocampus. Brain Res 2010; 1356: 85-94.
20. Czapski GA, Gassowska M, Wilkaniec A, Chalimoniuk M, Strosznajder JB, Adamczyk A. The mechanisms regulating cyclindependent kinase 5 in hippocampus during systemic inflammatory response: The effect on inflammatory gene expression. Neurochem Int 2016; 93: 103-112.
21. Czapski GA, Zhao Y, Lukiw WJ, Strosznajder JB. Acute systemic inflammatory response alters transcription profile of genes related to immune response and Ca(2+) homeostasis in hippocampus; relevance to neurodegenerative disorders. Int J Mol Sci 2020; 21: 7838.
22. Douros A, Santella C, Dell’Aniello S, Azoulay L, Renoux C, Suissa S, Brassard P. Infectious disease burden and the risk of Alzheimer’s disease: A population-based study. J Alzheimers Dis 2021; 81: 329-338.
23. Engler-Chiurazzi EB, Russell AE, Povroznik JM, McDonald KO, Porter KN, Wang DS, Hammock J, Billig BK, Felton CC, Yilmaz A, Schreurs BG, O’Callaghan JD, Zwezdaryk KJ, Simpkins JW. Intermittent systemic exposure to lipopolysaccharide-induced inflammation disrupts hippocampal long-term potentiation and impairs cognition in aging male mice. Brain Behav Immun 2023; 108: 279-291.
24. Eskandari-Sedighi G, Crichton M, Zia S, Gomez E, Laurent CDS, Cortez LM, Patel ZH, Sidhu G, Sarkar S, Aghanya V, Sim VL, Tan Q, Julien O, Plemel JR, Macauley MS. Alzheimer’s disease associated isoforms of human CD33 distinctively modulate microglial cell responses in 5XFAD mice. bioRxiv 2023 [Preprint]; July 4, 2023 (cited 2024 Jan 9). Available from: https://doi.org/10.1101/2023.07.04.547548.
25. Eskandari-Sedighi G, Jung J, Macauley MS. CD33 isoforms in microglia and Alzheimer’s disease: Friend and foe. Mol Aspects Med 2023; 90: 101111.
26. Ganz T, Fainstein N, Elad A, Lachish M, Goldfarb S, Einstein O, Ben-Hur T. Microbial pathogens induce neurodegeneration in Alzheimer’s disease mice: protection by microglial regulation.
27. J Neuroinflammation 2022; 19: 5.
28. Godbout JP, Chen J, Abraham J, Richwine AF, Berg BM, Kelley KW, Johnson RW. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J 2005; 19: 1329-1331.
29. Gonzalez-Gil A, Porell RN, Fernandes SM, Maenpaa E, Li TA, Li T, Wong PC, Aoki K, Tiemeyer M, Yu ZJ, Orsburn BC, Bumpus NN, Matthews RT, Schnaar RL. Human brain sialoglycan ligand for CD33, a microglial inhibitory Siglec implicated in Alzheimer’s disease. J Biol Chem 2022; 298: 101960.
30. Griciuc A, Federico AN, Natasan J, Forte AM, McGinty D, Nguyen H, Volak A, LeRoy S, Gandhi S, Lerner EP, Hudry E, Tanzi RE, Maguire CA. Gene therapy for Alzheimer’s disease targeting CD33 reduces amyloid beta accumulation and neuroinflammation. Hum Mol Genet 2020; 29: 2920-2935.
31. Griciuc A, Serrano-Pozo A, Parrado AR, Lesinski AN, Asselin CN, Mullin K, Hooli B, Choi SH, Hyman BT, Tanzi RE. Alzheimer’s disease risk gene CD33 inhibits microglial uptake of amyloid beta. Neuron 2013; 78: 631-643.
32. Griciuc A, Tanzi RE. The role of innate immune genes in Alzheimer’s disease. Curr Opin Neurol 2021; 34: 228-236.
33. Hoffner O’Connor M, Berglind A, Kennedy Ng MM, Keith BP, Lynch ZJ, Schaner MR, Steinbach EC, Herzog J, Trad OK, Jeck WR, Arthur JC, Simon JM, Sartor RB, Furey TS, Sheikh SZ. BET protein inhibition regulates macrophage chromatin accessibility and microbiota-dependent colitis. Front Immunol 2022; 13: 856966.
34. in t’ Veld BA, Ruitenberg A, Hofman A, Launer LJ, van Duijn CM, Stijnen T, Breteler MM, Stricker BH. Nonsteroidal antiinflammatory drugs and the risk of Alzheimer’s disease. N Engl J Med 2001; 345: 1515-1521.
35. Jacewicz M, Czapski GA, Katkowska I, Strosznajder RP. Systemic administration of lipopolysaccharide impairs glutathione redox state and object recognition in male mice. The effect of PARP-1 inhibitor. Folia Neuropathol 2009; 47: 321-328.
36. Jostes S, Nettersheim D, Fellermeyer M, Schneider S, Hafezi F, Honecker F, Schumacher V, Geyer M, Kristiansen G, Schorle H. The bromodomain inhibitor JQ1 triggers growth arrest and apoptosis in testicular germ cell tumours in vitro and in vivo. J Cell Mol Med 2017; 21: 1300-1314.
37. Kim HS, Kim S, Shin SJ, Park YH, Nam Y, Kim CW, Lee KW, Kim SM, Jung ID, Yang HD, Park YM, Moon M. Gram-negative bacteria and their lipopolysaccharides in Alzheimer’s disease: pathologic roles and therapeutic implications. Transl Neurodegener 2021; 10: 49.
38. Kirk RA, Kesner RP, Wang LM, Wu Q, Towner RA, Hoffman JM, Morton KA. Lipopolysaccharide exposure in a rat sepsis model results in hippocampal amyloid-b plaque and phosphorylated tau deposition and corresponding behavioral deficits. Geroscience 2019; 41: 467-481.
39. Kwon SB, Ernst J. Learning a genome-wide score of human-mouse conservation at the functional genomics level. Nat Commun 2021; 12: 2495.
40. Li J, Zhao L, Urabe G, Fu Y, Guo LW. Epigenetic intervention with a BET inhibitor ameliorates acute retinal ganglion cell death in mice. Mol Vis 2017; 23: 149-159.
41. Lin S, Lin Y, Nery JR, Urich MA, Breschi A, Davis CA, Dobin A, Zaleski C, Beer MA, Chapman WC, Gingeras TR, Ecker JR, Snyder MP. Comparison of the transcriptional landscapes between human and mouse tissues. Proc Natl Acad Sci U S A 2014; 111: 17224-17229.
42. Lu T, Aron L, Zullo J, Pan Y, Kim H, Chen Y, Yang TH, Kim HM, Drake D, Liu XS, Bennett DA, Colaiácovo MP, Yankner BA. REST and stress resistance in ageing and Alzheimer’s disease. Nature 2014; 507: 448-454.
43. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA. Gene regulation and DNA damage in the ageing human brain. Nature 2004; 429: 883-891.
44. Magistri M, Velmeshev D, Makhmutova M, Patel P, Sartor GC, Volmar CH, Wahlestedt C, Faghihi MA. The BET-bromodomain inhibitor JQ1 reduces inflammation and tau phosphorylation at Ser396 in the brain of the 3xTg model of Alzheimer’s disease. Curr Alzheimer Res 2016; 13: 985-995.
45. Matuszewska M, Cieślik M, Wilkaniec A, Strawski M, Czapski GA. The role of bromodomain and extraterminal (BET) proteins in controlling the phagocytic activity of microglia in vitro: Relevance to Alzheimer’s disease. Int J Mol Sci 2022; 24: 13.
46. Matzuk MM, McKeown MR, Filippakopoulos P, Li Q, Ma L, Agno JE, Lemieux ME, Picaud S, Yu RN, Qi J, Knapp S, Bradner JE. Small-molecule inhibition of BRDT for male contraception. Cell 2012; 150: 673-684.
47. McGeer PL, McGeer EG. NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies. Neurobiol Aging 2007; 28: 639-647.
48. McGeer PL, Rogers J, McGeer EG. Inflammation, antiinflammatory agents, and Alzheimer’s disease: The last 22 years. J Alzheimers Dis 2016; 54: 853-857.
49. Mertz JA, Conery AR, Bryant BM, Sandy P, Balasubramanian S, Mele DA, Bergeron L, Sims RJ, 3rd. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc Natl Acad Sci U S A 2011; 108: 16669-16674.
50. Nicodeme E, Jeffrey KL, Schaefer U, Beinke S, Dewell S, Chung CW, Chandwani R, Marazzi I, Wilson P, Coste H, White J, Kirilovsky J, Rice CM, Lora JM, Prinjha RK, Lee K, Tarakhovsky A. Suppression of inflammation by a synthetic histone mimic. Nature 2010; 468: 1119-1123.
51. Peeters JG, Vervoort SJ, Tan SC, Mijnheer G, de Roock S, Vastert SJ, Nieuwenhuis EE, van Wijk F, Prakken BJ, Creyghton MP, Coffer PJ, Mokry M, van Loosdregt J. Inhibition of super-enhancer activity in autoinflammatory site-derived T cells reduces disease-associated gene expression. Cell Rep 2015; 12: 1986-1996.
52. Podleśny-Drabiniok A, Marcora E, Goate AM. Microglial Phagocytosis: A disease-associated process emerging from Alzheimer’s disease genetics. Trends Neurosci 2020; 43: 965-979.
53. Raj T, Ryan KJ, Replogle JM, Chibnik LB, Rosenkrantz L, Tang A, Rothamel K, Stranger BE, Bennett DA, Evans DA, De Jager PL, Bradshaw EM. CD33: increased inclusion of exon 2 implicates the Ig V-set domain in Alzheimer’s disease susceptibility. Hum Mol Genet 2014; 23: 2729-2736.
54. Schwarz F, Springer SA, Altheide TK, Varki NM, Gagneux P, Varki A. Human-specific derived alleles of CD33 and other genes protect against postreproductive cognitive decline. Proc Natl Acad Sci U S A 2016; 113: 74-79.
55. Sun J, Ludvigsson JF, Ingre C, Piehl F, Wirdefeldt K, Zagai U, Ye W, Fang F. Hospital-treated infections in early- and mid-life and risk of Alzheimer’s disease, Parkinson’s disease, and amyotrophic lateral sclerosis: A nationwide nested case-control study in Sweden. PLoS Med 2022; 19: e1004092.
56. Tortora F, Rendina A, Angiolillo A, Di Costanzo A, Aniello F, Donizetti A, Febbraio F, Vitale E. CD33 rs2455069 SNP: Correlation with Alzheimer’s disease and hypothesis of functional role. Int J Mol Sci 2022; 23: 3629.
57. Wang LM, Wu Q, Kirk RA, Horn KP, Ebada Salem AH, Hoffman JM, Yap JT, Sonnen JA, Towner RA, Bozza FA, Rodrigues RS, Morton KA. Lipopolysaccharide endotoxemia induces amyloid-b and p-tau formation in the rat brain. Am J Nucl Med Mol Imaging 2018; 8: 86-99.
58. Wang N, Wu R, Tang D, Kang R. The BET family in immunity and disease. Signal Transduct Target Ther 2021; 6: 23.
59. Wightman DP, Jansen IE, Savage JE, Shadrin AA, Bahrami S, Holland D, Rongve A, Børte S, Winsvold BS, Drange OK, Martinsen AE, Skogholt AH, Willer C, Bråthen G, Bosnes I, Nielsen JB, Fritsche LG, Thomas LF, Pedersen LM, Gabrielsen ME, Johnsen MB, Meisingset TW, Zhou W, Proitsi P, Hodges A, Dobson R, Velayudhan L, Heilbron K, Auton A, Sealock JM, Davis LK, Pedersen NL, Reynolds CA, Karlsson IK, Magnusson S, Stefansson H, Thordardottir S, Jonsson PV, Snaedal J, Zettergren A, Skoog I, Kern S, Waern M, Zetterberg H, Blennow K, Stordal E, Hveem K, Zwart JA, Athanasiu L, Selnes P, Saltvedt I, Sando SB, Ulstein I, Djurovic S, Fladby T, Aarsland D, Selbæk G, Ripke S, Stefansson K, Andreassen OA, Posthuma D. A genome-wide association study with 1,126,563 individuals identifies new risk loci for Alzheimer’s disease. Nat Genet 2021; 53: 1276-1282.
60. Wilkaniec A, Gassowska-Dobrowolska M, Strawski M, Adamczyk A, Czapski GA. Inhibition of cyclin-dependent kinase 5 affects early neuroinflammatory signalling in murine model of amyloid beta toxicity. J Neuroinflammation 2018; 15: 1.
61. Zhao Y, Jaber V, Lukiw WJ. Secretory products of the human GI tract microbiome and their potential impact on Alzheimer’s disease (AD): Detection of lipopolysaccharide (LPS) in AD hippocampus. Front Cell Infect Microbiol 2017; 7: 318.
62. Zhao Y, Jaber VR, Pogue AI, Sharfman NM, Taylor C, Lukiw WJ. Lipopolysaccharides (LPSs) as potent neurotoxic glycolipids in Alzheimer’s disease (AD). Int J Mol Sci 2022; 23: 12671.
Copyright: © 2024 Mossakowski Medical Research Centre Polish Academy of Sciences and the Polish Association of Neuropathologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) License (http://creativecommons.org/licenses/by-nc-sa/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited and states its license.
Quick links
© 2024 Termedia Sp. z o.o.
Developed by Bentus.