Chronic high-fat diet consumption exacerbates pyroptosis- and necroptosis-mediated HMGB1 signaling in the brain after ischemia and reperfusion injury.


Journal

Journal of physiology and biochemistry
ISSN: 1877-8755
Titre abrégé: J Physiol Biochem
Pays: Spain
ID NLM: 9812509

Informations de publication

Date de publication:
Nov 2022
Historique:
received: 04 11 2021
accepted: 12 06 2022
pubmed: 25 6 2022
medline: 26 11 2022
entrez: 24 6 2022
Statut: ppublish

Résumé

Obesity is categorized as a common comorbidity found in people who experience an ischemic stroke. However, the mechanisms to explain this correlation have still not been elucidated fully. Pyroptosis and necroptosis are novel forms of programmed cell death that occur upon intracellular danger signals. The major feature of pyroptosis and necroptosis is damage to the lipid membrane, which consequently results in lytic cell death and allows the release of high mobility group box protein 1 (HMGB1) into the extracellular space. We aimed to investigate the influences of high-fat diet (HFD) consumption on cerebral ischemia and reperfusion (I/R) injury and hypothesized that HFD consumption exacerbated the activation of pyroptosis, necroptosis, and HMGB1 signaling pathways. All rats received normal diet (ND) or HFD for 16 weeks. Subsequently, both groups were divided into either a sham- or an I/R-operated group. Twenty-four hours after the surgery, all rats were evaluated for neurological deficits and then sacrificed. After I/R injury, there were more severe functional deficits and larger brain infarcts in the HFD compared with the ND group. The histological observation revealed an increase in tissue abnormalities in the HFD group, consistent with the massive reduction of intact neurons along the peri-infarct region. Furthermore, cerebral I/R injury dramatically activated the pyroptotic, necroptotic, and HMGB1 signaling pathways in HFD-fed rats compared with ND-fed rats. These findings suggest that chronic HFD consumption worsens ischemic brain pathology and leads to poor post-stroke outcomes by exacerbating pyroptotic and necroptotic cell death.

Identifiants

pubmed: 35749032
doi: 10.1007/s13105-022-00906-4
pii: 10.1007/s13105-022-00906-4
doi:

Substances chimiques

HMGB1 Protein 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

833-844

Subventions

Organisme : Royal Golden Jubilee (RGJ) Ph.D. Programme
ID : PHD/0104/2561

Informations de copyright

© 2022. The Author(s) under exclusive licence to University of Navarra.

Références

Arenillas JF, Sandoval P, Perez de la Ossa N, Millan M, Guerrero C, Escudero D, Dorado L, Lopez-Cancio E, Castillo J, Davalos A (2009) The metabolic syndrome is associated with a higher resistance to intravenous thrombolysis for acute ischemic stroke in women than in men. Stroke 40:344–349. https://doi.org/10.1161/STROKEAHA.108.531079
doi: 10.1161/STROKEAHA.108.531079 pubmed: 19109538
Boaru SG, Borkham-Kamphorst E, Van de Leur E, Lehnen E, Liedtke C, Weiskirchen R (2015) NLRP3 inflammasome expression is driven by NF-κB in cultured hepatocytes. Biochem Biophys Res Commun 458:700–706. https://doi.org/10.1016/j.bbrc.2015.02.029
doi: 10.1016/j.bbrc.2015.02.029 pubmed: 25686493
Chen J, Kos R, Garssen J, Redegeld F (2019) Molecular insights into the mechanism of necroptosis: the necrosome as a potential therapeutic target. Cells 8:1486. https://doi.org/10.3390/cells8121486
doi: 10.3390/cells8121486 pubmed: 31766571 pmcid: 6952807
Chen J, Yang C, Xu X, Yang Y, Xu B (2018) The effect of focal cerebral ischemia-reperfusion injury on TLR4 and NF-κB signaling pathway. Exp Ther Med 15:897–903. https://doi.org/10.3892/etm.2017.5463
doi: 10.3892/etm.2017.5463 pubmed: 29399096
Datta A, Sarmah D, Mounica L, Kaur H, Kesharwani R, Verma G, Veeresh P, Kotian V, Kalia K, Borah A et al (2020) Cell death pathways in ischemic stroke and targeted pharmacotherapy. Transl Stroke Res 11:1185–1202. https://doi.org/10.1007/s12975-020-00806-z
doi: 10.1007/s12975-020-00806-z pubmed: 32219729
Deguchi I, Ohe Y, Fukuoka T, Dembo T, Nagoya H, Kato Y, Maruyama H, Horiuchi Y, Tanahashi N (2012) Relationship of obesity to recanalization after hyperacute recombinant tissue-plasminogen activator infusion therapy in patients with middle cerebral artery occlusion. J Stroke Cerebrovasc Dis 21:161–164. https://doi.org/10.1016/j.jstrokecerebrovasdis.2011.11.003
doi: 10.1016/j.jstrokecerebrovasdis.2011.11.003 pubmed: 22285386
Del Re DP, Amgalan D, Linkermann A, Liu Q, Kitsis RN (2019) Fundamental mechanisms of regulated cell death and implications for heart disease. Physiol Rev 99:1765–1817. https://doi.org/10.1152/physrev.00022.2018
doi: 10.1152/physrev.00022.2018 pubmed: 31364924 pmcid: 6890986
Deng XX, Li SS, Sun FY (2019) Necrostatin-1 prevents necroptosis in brains after ischemic stroke via inhibition of RIPK1-mediated RIPK3/MLKL signaling. Aging Dis 10:807–817. https://doi.org/10.14336/AD.2018.0728
doi: 10.14336/AD.2018.0728 pubmed: 31440386 pmcid: 6675533
Donkor ES (2018) Stroke in the 21(st) century: a snapshot of the burden, epidemiology, and quality of life. Stroke Res Treat 2018:3238165. https://doi.org/10.1155/2018/3238165
doi: 10.1155/2018/3238165 pubmed: 30598741 pmcid: 6288566
Frank D, Vince JE (2019) Pyroptosis versus necroptosis: Similarities, differences, and crosstalk. Cell Death Differ 26:99–114. https://doi.org/10.1038/s41418-018-0212-6
doi: 10.1038/s41418-018-0212-6 pubmed: 30341423
Gauberti M, Lapergue B, Martinez de Lizarrondo S, Vivien D, Richard S, Bracard S, Piotin M, Gory B (2018) Ischemia-reperfusion injury after endovascular thrombectomy for ischemic stroke. Stroke 49:3071–3074. https://doi.org/10.1161/STROKEAHA.118.022015
doi: 10.1161/STROKEAHA.118.022015 pubmed: 30571423
Gou X, Xu D, Li F, Hou K, Fang W, Li Y (2021) Pyroptosis in stroke-new insights into disease mechanisms and therapeutic strategies. J Physiol Biochem. https://doi.org/10.1007/s13105-021-00817-w
doi: 10.1007/s13105-021-00817-w pubmed: 33942252
Gray N, Picone G, Sloan F, Yashkin A (2015) Relation between BMI and diabetes mellitus and its complications among us older adults. South Med J 108:29–36. https://doi.org/10.14423/SMJ.0000000000000214
doi: 10.14423/SMJ.0000000000000214 pubmed: 25580754 pmcid: 4457375
Grisotto C, Taile J, Planesse C, Diotel N, Gonthier MP, Meilhac O, Couret D (2021) High-fat diet aggravates cerebral infarct, hemorrhagic transformation and neuroinflammation in a mouse stroke model. Int J Mol Sci 22:4571. https://doi.org/10.3390/ijms22094571
doi: 10.3390/ijms22094571 pubmed: 33925459 pmcid: 8123851
Hribljan V, Lisjak D, Petrovic DJ, Mitrecic D (2019) Necroptosis is one of the modalities of cell death accompanying ischemic brain stroke: From pathogenesis to therapeutic possibilities. Croat Med J 60:121–126. https://doi.org/10.3325/cmj.2019.60.121
doi: 10.3325/cmj.2019.60.121 pubmed: 31044583 pmcid: 6509625
Jaikumkao K, Pongchaidecha A, Chueakula N, Thongnak L, Wanchai K, Chatsudthipong V, Chattipakorn N, Lungkaphin A (2018) Renal outcomes with sodium glucose cotransporter 2 (SGLT2) inhibitor, dapagliflozin, in obese insulin-resistant model. Biochim Biophys Acta Mol Basis Dis 1864:2021–2033. https://doi.org/10.1016/j.bbadis.2018.03.017
doi: 10.1016/j.bbadis.2018.03.017 pubmed: 29572114
Jaikumkao K, Promsan S, Thongnak L, Swe MT, Tapanya M, Htun KT, Kothan S, Intachai N, Lungkaphin A (2021) Dapagliflozin ameliorates pancreatic injury and activates kidney autophagy by modulating the AMPK/mTOR signaling pathway in obese rats. J Cell Physiol 9:6424–6440. https://doi.org/10.1002/jcp.30316
doi: 10.1002/jcp.30316
Kim EH, Wong SW, Martinez J (2019) Programmed necrosis and disease: we interrupt your regular programming to bring you necroinflammation. Cell Death Differ 26:25–40. https://doi.org/10.1038/s41418-018-0179-3
doi: 10.1038/s41418-018-0179-3 pubmed: 30349078
Kuriakose D, Xiao Z (2020) Pathophysiology and treatment of stroke: present status and future perspectives. Int J Mol Sci 21. https://doi.org/10.3390/ijms21207609
Lin L, Wang X, Yu Z (2016) Ischemia-reperfusion injury in the brain: mechanisms and potential therapeutic strategies. Biochem Pharmacol (Los Angel) 5.  https://doi.org/10.4172/2167-0501.1000213
Lee HJ, Choi EK, Lee SH, Kim YJ, Han KD, Oh S (2018) Risk of ischemic stroke in metabolically healthy obesity: a nationwide population-based study. PLoS ONE 13:e0195210. https://doi.org/10.1371/journal.pone.0195210
doi: 10.1371/journal.pone.0195210 pubmed: 29601602 pmcid: 5877885
Lee RM, Choi H, Shin JS, Kim K, Yoo KH (2009) Distinguishing between apoptosis and necrosis using a capacitance sensor. Biosens Bioelectron 24:2586–2591. https://doi.org/10.1016/j.bios.2009.01.028
doi: 10.1016/j.bios.2009.01.028 pubmed: 19233636
Litwin M, Kulaga Z (2021) Obesity, metabolic syndrome, and primary hypertension. Pediatr Nephrol 36:825–837. https://doi.org/10.1007/s00467-020-04579-3
doi: 10.1007/s00467-020-04579-3 pubmed: 32388582
Liu T, Zhang L, Joo D, Sun SC (2017) Nf-kappab signaling in inflammation. Signal Transduct Target Ther 2:17023. https://doi.org/10.1038/sigtrans.2017.23
doi: 10.1038/sigtrans.2017.23 pubmed: 29158945 pmcid: 5661633
Maysami S, Haley MJ, Gorenkova N, Krishnan S, McColl BW, Lawrence CB (2015) Prolonged diet-induced obesity in mice modifies the inflammatory response and leads to worse outcome after stroke. J Neuroinflamm 12:140. https://doi.org/10.1186/s12974-015-0359-8
doi: 10.1186/s12974-015-0359-8
Mostafa DG, Satti HH, Khaleel EF, Badi RM (2020) A high-fat diet rich in corn oil exaggerates the infarct size and memory impairment in rats with cerebral ischemia and is associated with suppressing osteopontin and Akt, and activating GS3Kβ, iNOS, and NF-κB. J Physiol Biochem 76:393–406. https://doi.org/10.1007/s13105-020-00744-2
doi: 10.1007/s13105-020-00744-2 pubmed: 32488539
Ryan F, Khodagholi F, Dargahi L, Minai-Tehrani D, Ahmadiani A (2018) Temporal pattern and crosstalk of necroptosis markers with autophagy and apoptosis associated proteins in ischemic hippocampus. Neurotox Res 34:79–92. https://doi.org/10.1007/s12640-017-9861-3
doi: 10.1007/s12640-017-9861-3 pubmed: 29313217
Shahjouei S, Cai PY, Ansari S, Sharififar S, Azari H, Ganji S, Zand R (2016) Middle cerebral artery occlusion model of stroke in rodents: a step-by-step approach. J Vasc Interv Neurol 8:1–8
pubmed: 26958146 pmcid: 4762402
Shi Z, Yuan S, Shi L, Li J, Ning G, Kong X, Feng S (2021) Programmed cell death in spinal cord injury pathogenesis and therapy. Cell Prolif 54:e12992. https://doi.org/10.1111/cpr.12992
doi: 10.1111/cpr.12992 pubmed: 33506613 pmcid: 7941236
Sivasinprasasn S, Wikan N, Tocharus J, Pantan R, Chaichompoo W, Suksamrarn A, Tocharus C (2019) Synergistic effects of the capsaicinoid nonivamide and rosuvastatin on obesity-related endothelial dysfunction in rat fed a high-fat diet. Phytother Res 33:1815–1826. https://doi.org/10.1002/ptr.6369
doi: 10.1002/ptr.6369 pubmed: 31141276
Srinivasan K, Viswanad B, Asrat L, Kaul CL, Ramarao P (2005) Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol Res 52:313–320. https://doi.org/10.1016/j.phrs.2005.05.004
doi: 10.1016/j.phrs.2005.05.004 pubmed: 15979893
Wang H, Chen H, Jin J, Liu Q, Zhong D, Li G (2020) Inhibition of the NLRP3 inflammasome reduces brain edema and regulates the distribution of aquaporin-4 after cerebral ischaemia-reperfusion. Life Sci 251:117638. https://doi.org/10.1016/j.lfs.2020.117638
doi: 10.1016/j.lfs.2020.117638 pubmed: 32251636
Wikan N, Tocharus J, Sivasinprasasn S, Kongkaew A, Chaichompoo W, Suksamrarn A, Tocharus C (2020) Capsaicinoid nonivamide improves nonalcoholic fatty liver disease in rats fed a high-fat diet. J Pharmacol Sci 143:188–198. https://doi.org/10.1016/j.jphs.2020.03.008
doi: 10.1016/j.jphs.2020.03.008 pubmed: 32414691
Yawoot N, Govitrapong P, Tocharus C, Tocharus J (2021) Ischemic stroke, obesity, and the anti-inflammatory role of melatonin. BioFactors 47:41–58. https://doi.org/10.1002/biof.1690
doi: 10.1002/biof.1690 pubmed: 33135223
Ye Y, Zeng Z, Jin T, Zhang H, Xiong X, Gu L (2019) The role of high mobility group box 1 in ischemic stroke. Front Cell Neurosci 13:127. https://doi.org/10.3389/fncel.2019.00127
doi: 10.3389/fncel.2019.00127 pubmed: 31001089 pmcid: 6454008
Zhang D, Qian J, Zhang P, Li H, Shen H, Li X, Chen G (2019) Gasdermin D serves as a key executioner of pyroptosis in experimental cerebral ischemia and reperfusion model both in vivo and in vitro. J Neurosci Res 97:645–660. https://doi.org/10.1002/jnr.24385
doi: 10.1002/jnr.24385 pubmed: 30600840
Zhao H, Chen Z, Xie LJ, Liu GF (2018) Suppression of TLR4/NF-κB signaling pathway improves cerebral ischemia-reperfusion injury in rats. Mol Neurobiol 55:4311–4319. https://doi.org/10.1007/s12035-017-0552-0
doi: 10.1007/s12035-017-0552-0 pubmed: 28624894

Auteurs

Nuttapong Yawoot (N)

Department of Physiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand.
Graduate School, Chiang Mai University, Chiang Mai, 50200, Thailand.

Wijitra Chumboatong (W)

Department of Physiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand.

Jirakhamon Sengking (J)

Department of Anatomy, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand.

Chainarong Tocharus (C)

Department of Anatomy, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand.

Jiraporn Tocharus (J)

Department of Physiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand. jiraporn.tocharus@cmu.ac.th.
Functional Food Research Center for Well-Being, Chiang Mai University, Chiang Mai, 50200, Thailand. jiraporn.tocharus@cmu.ac.th.

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