Quantitative Proteomic Analysis Reveals the Mechanisms of Sinapine Alleviate Macrophage Foaming
Abstract
:1. Introduction
2. Results
2.1. The Effect of Extraction Methods on Sinapine
2.2. Regulatory Effects of Sinapine on Cholesterol Accumulation in Foam Cells
2.3. Differences in Differentially Expressed Proteins (DEPs) between Different Treatments
2.4. DEPs Enriched in Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG)
2.5. Effects of Sinapine on the Cholesterol Metabolism in Foam Cells
2.6. Western Blot Validation of Key Proteins
3. Discussion
4. Materials and Methods
4.1. Materials
4.2. Preparation of Rapeseed-Meal Samples and Extraction of Sinapine
4.3. Foam Cell Formation of Macrophages
4.4. Confirmation of Sinapine Effects on Macrophages
4.5. Preparation Method for Proteomic Samples
4.6. Protein Identification, Quantitation, and Bioinformatic Analysis
4.7. Western Blotting
4.8. Data Analysis
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- He, M.; Nian, B.; Shi, J.; Sun, X.; Du, R.; Tan, C.P.; Xu, Y.J.; Liu, Y. Influence of extraction technology on rapeseed oil functional quality: A study on rapeseed polyphenols. Food Funct. 2022, 13, 270–279. [Google Scholar] [CrossRef]
- Zago, E.; Lecomte, J.; Barouh, N.; Aouf, C.; Carré, P.; Fine, F.; Villeneuve, P. Influence of rapeseed meal treatments on its total phenolic content and composition in sinapine, sinapic acid and canolol. Ind. Crop. Prod. 2015, 76, 1061–1070. [Google Scholar] [CrossRef]
- Li, J.; Guo, Z. Concurrent extraction and transformation of bioactive phenolic compounds from rapeseed meal using pressurized solvent extraction system. Ind. Crops Prod. 2016, 94, 152–159. [Google Scholar] [CrossRef]
- Bhinu, V.S.; Schäfer, U.A.; Li, R.; Huang, J.; Hannoufa, A. Targeted modulation of sinapine biosynthesis pathway for seed quality improvement in Brassica napus. Transgenic Res. 2009, 18, 31–44. [Google Scholar] [CrossRef] [PubMed]
- Dubie, J.; Stancik, A.; Morra, M.; Nindo, C. Antioxidant extraction from mustard (Brassica juncea) seed meal using high-intensity ultrasound. J. Food Sci. 2013, 78, E542–E548. [Google Scholar] [CrossRef] [PubMed]
- Guo, Y.; Ding, Y.; Zhang, T.; An, H. Sinapine reverses multi-drug resistance in MCF-7/dox cancer cells by downregulating FGFR4/FRS2α-ERK1/2 pathway-mediated NF-κB activation. Phytomedicine 2016, 23, 267–273. [Google Scholar] [CrossRef]
- Gu, Y.; Zhang, Y.; Li, M.; Huang, Z.; Jiang, J.; Chen, Y.; Chen, J.; Jia, Y.; Zhang, L.; Zhou, F. Ferulic Acid Ameliorates Atherosclerotic Injury by Modulating Gut Microbiota and Lipid Metabolism. Front. Pharmacol. 2021, 12, 621339. [Google Scholar] [CrossRef]
- Marino, M.; Del Bo, C.; Tucci, M.; Venturi, S.; Mantegazza, G.; Taverniti, V.; Møller, P.; Riso, P.; Porrini, M. A mix of chlorogenic and caffeic acid reduces C/EBPß and PPAR-γ1 levels and counteracts lipid accumulation in macrophages. Eur. J. Nutr. 2022, 61, 1003–1014. [Google Scholar] [CrossRef] [PubMed]
- Koelwyn, G.J.; Corr, E.M.; Erbay, E.; Moore, K.J. Regulation of macrophage immunometabolism in atherosclerosis. Nat. Immunol. 2018, 19, 526–537. [Google Scholar] [CrossRef] [Green Version]
- Bobryshev, Y.V.; Ivanova, E.A.; Chistiakov, D.A.; Nikiforov, N.G.; Orekhov, A.N. Macrophages and Their Role in Atherosclerosis: Pathophysiology and Transcriptome Analysis. BioMed Res. Int. 2016, 2016, 9582430. [Google Scholar] [CrossRef] [Green Version]
- Burgos, V.; Paz, C.; Saavedra, K.; Saavedra, N.; Foglio, M.A.; González-Chavarría, I.; Salazar, L.A. Drimys winteri and isodrimeninol decreased foam cell formation in THP-1 derived macrophages. Food Chem. Toxicol. 2020, 146, 111842. [Google Scholar] [CrossRef]
- Kobiyama, K.; Ley, K. Atherosclerosis. Circ. Res. 2018, 123, 1118–1120. [Google Scholar] [CrossRef] [PubMed]
- Maguire, E.M.; Pearce, S.W.A.; Xiao, Q. Foam cell formation: A new target for fighting atherosclerosis and cardiovascular disease. Vasc. Pharmacol. 2019, 112, 54–71. [Google Scholar] [CrossRef] [PubMed]
- Tamminen, M.; Mottino, G.; Qiao, J.H.; Breslow, J.L.; Frank, J.S. Ultrastructure of early lipid accumulation in ApoE-deficient mice. Arter. Thromb. Vasc. Biol. 1999, 19, 847–853. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Febbraio, M.; Hajjar, D.P.; Silverstein, R.L. CD36: A class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J. Clin. Investig. 2001, 108, 785–791. [Google Scholar] [CrossRef]
- Rahaman, S.O.; Lennon, D.J.; Febbraio, M.; Podrez, E.A.; Hazen, S.L.; Silverstein, R.L. A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metab. 2006, 4, 211–221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silverstein, R.L.; Febbraio, M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal. 2009, 2, re3. [Google Scholar] [CrossRef] [Green Version]
- Moore, K.J.; Sheedy, F.J.; Fisher, E.A. Macrophages in atherosclerosis: A dynamic balance. Nat. Rev. Immunol. 2013, 13, 709–721. [Google Scholar] [CrossRef] [Green Version]
- Febbraio, M.; Podrez, E.A.; Smith, J.D.; Hajjar, D.P.; Hazen, S.L.; Hoff, H.F.; Sharma, K.; Silverstein, R.L. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Investig. 2000, 105, 1049–1056. [Google Scholar] [CrossRef] [Green Version]
- Yang, L.; Sun, J.; Li, M.; Long, Y.; Zhang, D.; Guo, H.; Huang, R.; Yan, J. Oxidized Low-Density Lipoprotein Links Hypercholesterolemia and Bladder Cancer Aggressiveness by Promoting Cancer Stemness. Cancer Res. 2021, 81, 5720–5732. [Google Scholar] [CrossRef]
- Xin, P.; Xu, X.; Deng, C.; Liu, S.; Wang, Y.; Zhou, X.; Ma, H.; Wei, D.; Sun, S. The role of JAK/STAT signaling pathway and its inhibitors in diseases. Int. Immunopharmacol. 2020, 80, 106210. [Google Scholar] [CrossRef]
- Razidlo, G.L.; Burton, K.M.; McNiven, M.A. Interleukin-6 promotes pancreatic cancer cell migration by rapidly activating the small GTPase CDC42. J. Biol. Chem. 2018, 293, 11143–11153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ferrer, B.; Prince, L.M.; Tinkov, A.A.; Santamaria, A.; Farina, M.; Rocha, J.B.; Bowman, A.B.; Aschner, M. Chronic exposure to methylmercury enhances the anorexigenic effects of leptin in C57BL/6J male mice. Food Chem. Toxicol. 2021, 147, 111924. [Google Scholar] [CrossRef]
- Bowe, B.; Gibson, A.K.; Xie, Y.; Yan, Y.; Donkelaar, A.V.; Martin, R.V.; Al-Aly, Z. Ambient Fine Particulate Matter Air Pollution and Risk of Weight Gain and Obesity in United States Veterans: An Observational Cohort Study. Environ. Health Perspect. 2021, 129, 47003. [Google Scholar] [CrossRef]
- Chen, K.; Zhao, Z.; Wang, G.; Zou, J.; Yu, X.; Zhang, D.; Zeng, G.; Tang, C. Interleukin-5 promotes ATP-binding cassette transporter A1 expression through miR-211/JAK2/STAT3 pathways in THP-1-dervied macrophages. Acta Biochim. Biophys. Sin. 2020, 52, 832–841. [Google Scholar] [CrossRef]
- Chadda, R.; Howes, M.T.; Plowman, S.J.; Hancock, J.F.; Parton, R.G.; Mayor, S. Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 2007, 8, 702–717. [Google Scholar] [CrossRef] [Green Version]
- Mukhamedova, N.; Hoang, A.; Dragoljevic, D.; Dubrovsky, L.; Pushkarsky, T.; Low, H.; Ditiatkovski, M.; Fu, Y.; Ohkawa, R.; Meikle, P.J.; et al. Exosomes containing HIV protein Nef reorganize lipid rafts potentiating inflammatory response in bystander cells. PLoS Pathog. 2019, 15, e1007907. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diederich, W.; Orsó, E.; Drobnik, W.; Schmitz, G. Apolipoprotein AI and HDL(3) inhibit spreading of primary human monocytes through a mechanism that involves cholesterol depletion and regulation of CDC42. Atherosclerosis 2001, 159, 313–324. [Google Scholar] [CrossRef]
- Heasman, S.J.; Ridley, A.J. Mammalian Rho GTPases: New insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 2008, 9, 690–701. [Google Scholar] [CrossRef]
- Low, H.; Mukhamedova, N.; Capettini, L.; Xia, Y.; Carmichael, I.; Cody, S.H.; Huynh, K.; Ditiatkovski, M.; Ohkawa, R.; Bukrinsky, M.; et al. Cholesterol Efflux-Independent Modification of Lipid Rafts by AIBP (Apolipoprotein A-I Binding Protein). Arter. Thromb. Vasc. Biol. 2020, 40, 2346–2359. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Tang, C. Regulation of ABCA1 functions by signaling pathways. Biochim. Biophys. Acta 2012, 1821, 522–529. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raptis, L.; Arulanandam, R.; Geletu, M.; Turkson, J. The R(h)oads to Stat3: Stat3 activation by the Rho GTPases. Exp. Cell Res. 2011, 317, 1787–1795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aznar, S.; Valerón, P.F.; del Rincon, S.V.; Pérez, L.F.; Perona, R.; Lacal, J.C. Simultaneous tyrosine and serine phosphorylation of STAT3 transcription factor is involved in Rho A GTPase oncogenic transformation. Mol. Biol. Cell 2001, 12, 3282–3294. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arulanandam, R.; Geletu, M.; Feracci, H.; Raptis, L. Activated Rac1 requires gp130 for Stat3 activation, cell proliferation and migration. Exp. Cell Res. 2010, 316, 875–886. [Google Scholar] [CrossRef]
- Yang, S.; Yuan, H.Q.; Hao, Y.M.; Ren, Z.; Qu, S.L.; Liu, L.S.; Wei, D.H.; Tang, Z.H.; Zhang, J.F.; Jiang, Z.S. Macrophage polarization in atherosclerosis. Clin. Chim. Acta 2020, 501, 142–146. [Google Scholar] [CrossRef]
- Petit, V.; Parcelier, A.; Mathé, C.; Barroca, V.; Torres, C.; Lewandowski, D.; Ferri, F.; Gallouët, A.S.; Dalloz, M.; Dinet, O.; et al. TRIM33 deficiency in monocytes and macrophages impairs resolution of colonic inflammation. EBioMedicine 2019, 44, 60–70. [Google Scholar] [CrossRef] [Green Version]
- Shirai, T.; Hilhorst, M.; Harrison, D.G.; Goronzy, J.J.; Weyand, C.M. Macrophages in vascular inflammation--From atherosclerosis to vasculitis. Autoimmunity 2015, 48, 139–151. [Google Scholar] [CrossRef] [Green Version]
- Colin, S.; Chinetti-Gbaguidi, G.; Staels, B. Macrophage phenotypes in atherosclerosis. Immunol. Rev. 2014, 262, 153–166. [Google Scholar] [CrossRef]
- Shapouri-Moghaddam, A.; Mohammadian, S.; Vazini, H.; Taghadosi, M.; Esmaeili, S.A.; Mardani, F.; Seifi, B.; Mohammadi, A.; Afshari, J.T.; Sahebkar, A. Macrophage plasticity, polarization, and function in health and disease. J. Cell. Physiol. 2018, 233, 6425–6440. [Google Scholar] [CrossRef]
- Wang, Y.; Liu, J.; Chen, X.; Sun, H.; Peng, S.; Kuang, Y.; Pi, J.; Zhuang, T.; Zhang, L.; Yu, Z.; et al. Dysfunctional endothelial-derived microparticles promote inflammatory macrophage formation via NF-кB and IL-1β signal pathways. J. Cell. Mol. Med. 2019, 23, 476–486. [Google Scholar] [CrossRef] [Green Version]
- Martinez, F.O.; Gordon, S. The M1 and M2 paradigm of macrophage activation: Time for reassessment. F1000Prime Rep. 2014, 6, 13. [Google Scholar] [CrossRef] [Green Version]
- Wang, N.; Liang, H.; Zen, K. Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front. Immunol. 2014, 5, 614. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hutchins, A.P.; Diez, D.; Miranda-Saavedra, D. The IL-10/STAT3-mediated anti-inflammatory response: Recent developments and future challenges. Brief. Funct. Genom. 2013, 12, 489–498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, W.; Meridew, J.A.; Aravamudhan, A.; Ligresti, G.; Tschumperlin, D.J.; Tan, Q. Targeted regulation of fibroblast state by CRISPR-mediated CEBPA expression. Respir. Res. 2019, 20, 281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nie, C.; Wang, B.; Fan, M.; Wang, Y.; Sun, Y.; Qian, H.; Li, Y.; Wang, L. Highland Barley Tea Polyphenols Extract Alleviates Skeletal Muscle Fibrosis in Mice by Reducing Oxidative Stress, Inflammation, and Cell Senescence. J. Agric. Food Chem. 2023, 71, 739–748. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, A.; Liao, B.; Yin, S.; Ye, Z.; He, M.; Li, X.; Liu, Y.; Xu, Y. Quantitative Proteomic Analysis Reveals the Mechanisms of Sinapine Alleviate Macrophage Foaming. Molecules 2023, 28, 2012. https://doi.org/10.3390/molecules28052012
Liu A, Liao B, Yin S, Ye Z, He M, Li X, Liu Y, Xu Y. Quantitative Proteomic Analysis Reveals the Mechanisms of Sinapine Alleviate Macrophage Foaming. Molecules. 2023; 28(5):2012. https://doi.org/10.3390/molecules28052012
Chicago/Turabian StyleLiu, Aiyang, Bin Liao, Shipeng Yin, Zhan Ye, Mengxue He, Xue Li, Yuanfa Liu, and Yongjiang Xu. 2023. "Quantitative Proteomic Analysis Reveals the Mechanisms of Sinapine Alleviate Macrophage Foaming" Molecules 28, no. 5: 2012. https://doi.org/10.3390/molecules28052012