Might Gut Microbiota Be a Target for a Personalized Therapeutic Approach in Patients Affected by Atherosclerosis Disease?
Abstract
:1. Introduction
2. The Gut Microbiota
3. Development of the Gut Microbiota
4. Gut Microbiota as an Endocrine Organ
5. Gut Microbiota Dysbiosis and Atherosclerosis
6. Potential Therapeutic Targets
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Singh, R.B.; Mengi, S.A.; Xu, Y.-J.; Arneja, A.S.; Dhalla, N.S. Pathogenesis of atherosclerosis: A multifactorial process. Exp. Clin. Cardiol. 2002, 7, 40–53. [Google Scholar]
- Tousoulis, D.; Kampoli, A.M.; Papageorgiou, N.; Androulakis, E.; Antoniades, C.; Toutouzas, K.; Stefanadis, C. Pathophysiology of atherosclerosis: The role of inflammation. Curr. Pharm. Des. 2011, 17, 4089–4110. [Google Scholar] [CrossRef]
- Dalen, J.E.; Alpert, J.S.; Goldberg, R.J.; Weinstein, R.S. The epidemic of the 20(th) century: Coronary heart disease. Am. J. Med. 2014, 127, 807–812. [Google Scholar] [CrossRef] [PubMed]
- World Heart Federation. World Heart Report 2023 Confronting the World’s Number One Killer. Available online: https://world-heart-federation.org/wp-content/uploads/World-Heart-Report-2023.pdf (accessed on 20 July 2023).
- Siasos, G.; Tousoulis, D.; Oikonomou, E.; Zaromitidou, M.; Stefanadis, C.; Papavassiliou, A.G. Inflammatory markers in hyperlipidemia: From experimental models to clinical practice. Curr. Pharm. Des. 2011, 17, 4132–4146. [Google Scholar] [CrossRef] [PubMed]
- Caiati, C.; Stanca, A.; Lepera, M.E. Free Radicals and Obesity-Related Chronic Inflammation Contrasted by Antioxidants: A New Perspective in Coronary Artery Disease. Metabolites 2023, 13, 712. [Google Scholar] [CrossRef]
- Guaricci, A.I.; Lorenzoni, V.; Guglielmo, M.; Mushtaq, S.; Muscogiuri, G.; Cademartiri, F.; Rabbat, M.; Andreini, D.; Serviddio, G.; Gaibazzi, N.; et al. Prognostic relevance of subclinical coronary and carotid atherosclerosis in a diabetic and nondiabetic asymptomatic population. Clin. Cardiol. 2018, 41, 769–777. [Google Scholar] [CrossRef] [PubMed]
- Lim, H.Y.; Burrell, L.M.; Brook, R.; Nandurkar, H.H.; Donnan, G.; Ho, P. The Need for Individualized Risk Assessment in Cardiovascular Disease. J. Pers. Med. 2022, 12, 1140. [Google Scholar] [CrossRef] [PubMed]
- Jebari-Benslaiman, S.; Galicia-García, U.; Larrea-Sebal, A.; Olaetxea, J.R.; Alloza, I.; Vandenbroeck, K.; Benito-Vicente, A.; Martín, C. Pathophysiology of Atherosclerosis. Int. J. Mol. Sci. 2022, 23, 3346. [Google Scholar] [CrossRef] [PubMed]
- Ciccone, M.M.; Scicchitano, P.; Zito, A.; Cortese, F.; Boninfante, B.; Falcone, V.A.; Quaranta, V.N.; Ventura, V.A.; Zucano, A.; Di Serio, F.; et al. Correlation between inflammatory markers of atherosclerosis and carotid intima-media thickness in Obstructive Sleep Apnea. Molecules 2014, 19, 1651–1662. [Google Scholar] [CrossRef]
- Chan, Y.H.; Ramji, D.P. Atherosclerosis: Pathogenesis and Key Cellular Processes, Current and Emerging Therapies, Key Challenges, and Future Research Directions. Methods Mol. Biol. 2022, 2419, 3–19. [Google Scholar] [CrossRef]
- Boudoulas, K.D.; Triposciadis, F.; Geleris, P.; Boudoulas, H. Coronary Atherosclerosis: Pathophysiologic Basis for Diagnosis and Management. Prog. Cardiovasc. Dis. 2016, 58, 676–692. [Google Scholar] [CrossRef]
- Kloc, M.; Uosef, A.; Kubiak, J.Z.; Ghobrial, R.M. Role of Macrophages and RhoA Pathway in Atherosclerosis. Int. J. Mol. Sci. 2020, 22, 216. [Google Scholar] [CrossRef] [PubMed]
- Spagnoli, L.G.; Bonanno, E.; Sangiorgi, G.; Mauriello, A. Role of inflammation in atherosclerosis. J. Nucl. Med. 2007, 48, 1800–1815. [Google Scholar] [CrossRef] [PubMed]
- Ciccone, M.M.; Bilianou, E.; Balbarini, A.; Gesualdo, M.; Ghiadoni, L.; Metra, M.; Palmiero, P.; Pedrinelli, R.; Salvetti, M.; Scicchitano, P.; et al. Task force on: ‘Early markers of atherosclerosis: Influence of age and sex’. J. Cardiovasc. Med. 2013, 14, 757–766. [Google Scholar] [CrossRef]
- Moriya, J. Critical roles of inflammation in atherosclerosis. J. Cardiol. 2019, 73, 22–27. [Google Scholar] [CrossRef]
- De Pergola, G.; Cortese, F.; Termine, G.; Meliota, G.; Carbonara, R.; Masiello, M.; Cortese, A.M.; Silvestris, F.; Caccavo, D.; Ciccone, M.M. Uric Acid, Metabolic Syndrome and Atherosclerosis: The Chicken or the Egg, Which Comes First? Endocr. Metab. Immune Disord. Drug Targets 2018, 18, 251–259. [Google Scholar] [CrossRef] [PubMed]
- Stary, H.C.; Chandler, A.B.; Dinsmore, R.E.; Fuster, V.; Glagov, S.; Insull, W., Jr.; Rosenfeld, M.E.; Schwartz, C.J.; Wagner, W.D.; Wissler, R.W. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 1995, 92, 1355–1374. [Google Scholar] [CrossRef]
- Cook-Mills, J.M.; Marchese, M.E.; Abdala-Valencia, H. Vascular cell adhesion molecule-1 expression and signaling during disease: Regulation by reactive oxygen species and antioxidants. Antioxid Redox Signal. 2011, 15, 1607–1638. [Google Scholar] [CrossRef]
- Lorey, M.B.; Öörni, K.; Kovanen, P.T. Modified Lipoproteins Induce Arterial Wall Inflammation During Atherogenesis. Front. Cardiovasc. Med. 2022, 9, 841545. [Google Scholar] [CrossRef]
- Libby, P. Inflammation during the life cycle of the atherosclerotic plaque. Cardiovasc. Res. 2021, 117, 2525–2536. [Google Scholar] [CrossRef]
- Epstein, S.E.; Zhou, Y.F.; Zhu, J. Infection and atherosclerosis: Emerging mechanistic paradigms. Circulation 1999, 100, e20–e28. [Google Scholar] [CrossRef] [PubMed]
- Charitos, I.A.; Topi, S.; Castellaneta, F.; D’Agostino, D. Current Issues and Perspectives in Patients with Possible Sepsis at Emergency Departments. Antibiotics 2019, 8, 56. [Google Scholar] [CrossRef] [PubMed]
- Di Serio, F.; Lovero, R.; D’Agostino, D.; Nisi, L.; Miragliotta, G.; Contino, R.; Man, A.; Ciccone, M.M.; Santacroce, L. Evaluation of procalcitonin, Vitamin D and C-reactive protein levels in septic patients with positive emocoltures. Our preliminary experience. Acta Med. Mediterr. 2016, 32, 1911–1914. [Google Scholar] [CrossRef]
- Neish, A.S. Microbes in gastrointestinal health and disease. Gastroenterology 2009, 136, 65–80. [Google Scholar] [CrossRef] [PubMed]
- Bäckhed, F.; Roswall, J.; Peng, Y.; Feng, Q.; Jia, H.; Kovatcheva-Datchary, P.; Li, Y.; Xia, Y.; Xie, H.; Zhong, H.; et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe. 2015, 17, 690–703, Erratum in Cell Host Microbe. 2015, 17, 852. [Google Scholar] [CrossRef]
- Chang, C.; Lin, H. Dysbiosis in gastrointestinal disorders. Best Pract. Res. Clin. Gastroenterol. 2016, 30, 3–15. [Google Scholar] [CrossRef] [PubMed]
- Eckburg, P.B.; Bik, E.M.; Bernstein, C.N.; Purdom, E.; Dethlefsen, L.; Sargent, M.; Gill, S.R.; Nelson, K.E.; Relman, D.A. Diversity of the human intestinal microbial flora. Science 2005, 308, 1635–1638. [Google Scholar] [CrossRef] [PubMed]
- Santacroce, L.; Man, A.; Charitos, I.A.; Haxhirexha, K.; Topi, S. Current knowledge about the connection between health status and gut microbiota from birth to elderly. A narrative review. Front. Biosci. 2021, 26, 135–148. [Google Scholar] [CrossRef]
- Kundu, P.; Blacher, E.; Elinav, E.; Pettersson, S. Our Gut Microbiome: The Evolving Inner Self. Cell 2017, 171, 1481–1493. [Google Scholar] [CrossRef]
- Mizrahi-Man, O.; Davenport, E.R.; Gilad, Y. Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: Evaluation of effective study designs. PLoS ONE 2013, 8, e53608. [Google Scholar] [CrossRef]
- Schluter, J.; Foster, K.R. The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol. 2012, 10, e1001424. [Google Scholar] [CrossRef] [PubMed]
- Valdes, A.M.; Walter, J.; Segal, E.; Spector, T.D. Role of the gut microbiota in nutrition and health. BMJ 2018, 361, k2179. [Google Scholar] [CrossRef]
- Charitos, I.A.; Topi, S.; Gagliano-Candela, R.; De Nitto, E.; Polimeno, L.; Montagnani, M.; Santacroce, L. The Toxic Effects of Endocrine Disrupting Chemicals (EDCs) on Gut Microbiota: Bisphenol A (BPA) A Review. Endocr. Metab. Immune Disord. Drug Targets 2022, 22, 716–727. [Google Scholar] [CrossRef]
- Di Domenico, M.; Ballini, A.; Boccellino, M.; Scacco, S.; Lovero, R.; Charitos, I.A.; Santacroce, L. The Intestinal Microbiota May Be a Potential Theranostic Tool for Personalized Medicine. J. Pers. Med. 2022, 12, 523. [Google Scholar] [CrossRef] [PubMed]
- La, X.; Wang, Y.; Xiong, X.; Shen, L.; Chen, W.; Zhang, L.; Yang, F.; Cai, X.; Zheng, H.; Jiang, H. The Composition of Placental Microbiota and Its Association with Adverse Pregnancy Outcomes. Front. Microbiol. 2022, 13, 911852. [Google Scholar] [CrossRef]
- Rinninella, E.; Raoul, P.; Cintoni, M.; Franceschi, F.; Miggiano, G.A.D.; Gasbarrini, A.; Mele, M.C. What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms 2019, 7, 14. [Google Scholar] [CrossRef]
- Guinane, C.M.; Cotter, P.D. Role of the gut microbiota in health and chronic gastrointestinal disease: Understanding a hidden metabolic organ. Ther. Adv. Gastroenterol. 2013, 6, 295–308. [Google Scholar] [CrossRef] [PubMed]
- Salazar, N.; Arboleya, S.; Fernández-Navarro, T.; de Los Reyes-Gavilán, C.G.; Gonzalez, S.; Gueimonde, M. Age-Associated Changes in Gut Microbiota and Dietary Components Related with the Immune System in Adulthood and Old Age: A Cross-Sectional Study. Nutrients 2019, 11, 1765. [Google Scholar] [CrossRef]
- Silva, Y.P.; Bernardi, A.; Frozza, R.L. The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication. Front. Endocrinol. 2020, 11, 25. [Google Scholar] [CrossRef]
- Montagnani, M.; Bottalico, L.; Potenza, M.A.; Charitos, I.A.; Topi, S.; Colella, M.; Santacroce, L. The Crosstalk between Gut Microbiota and Nervous System: A Bidirectional Interaction between Microorganisms and Metabolome. Int. J. Mol. Sci. 2023, 24, 10322. [Google Scholar] [CrossRef]
- Clarke, G.; Stilling, R.M.; Kennedy, P.J.; Stanton, C.; Cryan, J.F.; Dinan, T.G. Minireview: Gut microbiota: The neglected endocrine organ. Mol. Endocrinol. 2014, 28, 1221–1238. [Google Scholar] [CrossRef] [PubMed]
- Org, E.; Mehrabian, M.; Lusis, A.J. Unraveling the environmental and genetic interactions in atherosclerosis: Central role of the gut microbiota. Atherosclerosis 2015, 241, 387–399. [Google Scholar] [CrossRef] [PubMed]
- Ghasemzadeh, M.; Ahmadi, J.; Hosseini, E. Platelet-leukocyte crosstalk in COVID-19: How might the reciprocal links between thrombotic events and inflammatory state affect treatment strategies and disease prognosis? Thromb. Res. 2022, 213, 179–194. [Google Scholar] [CrossRef] [PubMed]
- Caesar, R.; Fak, F.; Backhed, F. Effects of gut microbiota on obesity and atherosclerosis via modulation of inflammation and lipid metabolism. J. Intern. Med. 2010, 268, 320–328. [Google Scholar] [CrossRef]
- Sanchez, M.; Panahi, S.; Tremblay, A. Childhood obesity: A role for gut microbiota? Int. J. Environ. Res. Public Health 2014, 12, 162–175. [Google Scholar] [CrossRef]
- Ahmadmehrabi, S.; Tang, W.H.W. Gut microbiome and its role in cardiovascular diseases. Curr. Opin. Cardiol. 2017, 32, 761–766. [Google Scholar] [CrossRef]
- Kanevskiy, L.M.; Telford, W.G.; Sapozhnikov, A.M.; Kovalenko, E.I. Lipopolysaccharide induces IFN-γ production in human NK cells. Front. Immunol. 2013, 4, 11. [Google Scholar] [CrossRef]
- Ghosh, S.S.; Bie, J.; Wang, J.; Ghosh, S. Oral supplementation with non-absorbable antibiotics or curcumin attenuates western diet induced atherosclerosis and glucose intolerance in LDLR−/− mice—Role of intestinal permeability and macrophage activation. PLoS ONE 2014, 9, e108577. [Google Scholar] [CrossRef]
- Jonsson, A.L.; Backhed, F. Role of gut microbiota in atherosclerosis. Nat. Rev. Cardiol. 2017, 14, 79–87. [Google Scholar] [CrossRef]
- Ramezani, A.; Raj, D.S. The gut microbiome, kidney disease, and targeted interventions. J. Am. Soc. Nephrol. 2014, 25, 657–670. [Google Scholar] [CrossRef]
- Sowmiya, T.; Silambanan, S. Association of Gut Microbiota and Diabetes Mellitus. Curr. Diabetes Rev. 2023, 19, e211122211066. [Google Scholar] [CrossRef] [PubMed]
- Koren, O.; Spor, A.; Felin, J.; Fak, F.; Stombaugh, J.; Tremaroli, V.; Behre, C.J.; Knight, R.; Fagerberg, B.; Ley, R.E.; et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc. Natl. Acad. Sci. USA 2011, 108 (Suppl. S1), 4592–4598. [Google Scholar] [CrossRef] [PubMed]
- Chen, M.L.; Yi, L.; Zhang, Y.; Zhou, X.; Ran, L.; Yang, J.; Zhu, J.D.; Zhang, Q.Y.; Mi, M.T. Resveratrol Attenuates Trimethylamine-N-Oxide (TMAO)-Induced Atherosclerosis by Regulating TMAO Synthesis and Bile Acid Metabolism via Remodeling of the Gut Microbiota. mBio 2016, 7, e02210–e02215. [Google Scholar] [CrossRef]
- Spence, J.D. Intestinal Microbiome and Atherosclerosis. eBioMedicine 2016, 13, 17–18. [Google Scholar] [CrossRef] [PubMed]
- Abu El Haija, M.; Ye, Y.; Chu, Y.; Herz, H.; Linden, B.; Shahi, S.K.; Zarei, K.; Mangalam, A.K.; Mcelroy, S.J.; Mokadem, M. Toll-like receptor 4 and myeloid differentiation factor 88 are required for gastric bypass-induced metabolic effects. Surg. Obes. Relat. Dis. 2021, 17, 1996–2006. [Google Scholar] [CrossRef]
- Yin, J.; Liao, S.X.; He, Y.; Wang, S.; Xia, G.H.; Liu, F.T.; Zhu, J.J.; You, C.; Chen, Q.; Zhou, L.; et al. Dysbiosis of Gut Microbiota with Reduced Trimethylamine-N-Oxide Level in Patients With Large-Artery Atherosclerotic Stroke or Transient Ischemic Attack. J. Am. Heart Assoc. 2015, 4, e002699. [Google Scholar] [CrossRef]
- Hou, K.; Wu, Z.X.; Chen, X.Y.; Wang, J.Q.; Zhang, D.; Xiao, C.; Zhu, D.; Koya, J.B.; Wei, L.; Li, J.; et al. Microbiota in health and diseases. Signal Transduct Target Ther. 2022, 7, 135. [Google Scholar] [CrossRef]
- Ie, Z.; Xia, H.; Zhong, S.L.; Feng, Q.; Li, S.; Liang, S.; Zhong, H.; Liu, Z.; Gao, Y.; Zhao, H.; et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat. Commun. 2017, 8, 845. [Google Scholar] [CrossRef]
- Yamashita, T. Intestinal Immunity and Gut Microbiota in Atherogenesis. J. Atheroscler. Thromb. 2017, 24, 110–119. [Google Scholar] [CrossRef]
- Zeisel, S.H.; Warrier, M. Trimethylamine N-Oxide, the Microbiome, and Heart and Kidney Disease. Annu. Rev. Nutr. 2017, 37, 157–181. [Google Scholar] [CrossRef]
- Koeth, R.A.; Wang, Z.; Levison, B.S.; Buffa, J.A.; Org, E.; Sheehy, B.T.; Britt, E.B.; Fu, X.; Wu, Y.; Li, L.; et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 2013, 19, 576–585. [Google Scholar] [CrossRef] [PubMed]
- Skagen, K.; Troseid, M.; Ueland, T.; Holm, S.; Abbas, A.; Gregersen, I.; Kummen, M.; Bjerkeli, V.; Reier-Nilsen, F.; Russell, D.; et al. The Carnitine-butyrobetaine-trimethylamine-N-oxide pathway and its association with cardiovascular mortality in patients with carotid atherosclerosis. Atherosclerosis 2016, 247, 64–69. [Google Scholar] [CrossRef]
- Bhuiya, J.; Notsu, Y.; Kobayashi, H.; Shibly, A.Z.; Sheikh, A.M.; Okazaki, R.; Yamaguchi, K.; Nagai, A.; Nabika, T.; Abe, T.; et al. Neither Trimethylamine-N-Oxide nor Trimethyllysine Is Associated with Atherosclerosis: A Cross-Sectional Study in Older Japanese Adults. Nutrients 2023, 15, 759. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Li, Q.; Jiang, H. Gut microbiota in atherosclerosis: Focus on trimethylamine N-oxide. APMIS 2020, 128, 353–366. [Google Scholar] [CrossRef]
- Postler, T.S.; Ghosh, S. Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System. Cell Metab. 2017, 26, 110–130. [Google Scholar] [CrossRef]
- Ussher, J.R.; Lopaschuk, G.D.; Arduini, A. Gut microbiota metabolism of L-carnitine and cardiovascular risk. Atherosclerosis 2013, 231, 456–461. [Google Scholar] [CrossRef] [PubMed]
- Serino, M.; Blasco-Baque, V.; Nicolas, S.; Burcelin, R. Far from the eyes, close to the heart: Dysbiosis of gut microbiota and cardiovascular consequences. Curr. Cardiol. Rep. 2014, 16, 540. [Google Scholar] [CrossRef]
- Chistiakov, D.A.; Bobryshev, Y.V.; Kozarov, E.; Sobenin, I.A.; Orekhov, A.N. Role of gut microbiota in the modulation of atherosclerosis-associated immune response. Front. Microbiol. 2015, 6, 671. [Google Scholar] [CrossRef] [PubMed]
- Gregory, J.C.; Buffa, J.A.; Org, E.; Wang, Z.; Levison, B.S.; Zhu, W.; Wagner, M.A.; Bennett, B.J.; Li, L.; DiDonato, J.A.; et al. Transmission of atherosclerosis susceptibility with gut microbial transplantation. J. Biol. Chem. 2015, 290, 5647–5660. [Google Scholar] [CrossRef]
- Ghosh, S.S.; He, H.; Wang, J.; Gehr, T.W.; Ghosh, S. Curcumin-mediated regulation of intestinal barrier function: The mechanism underlying its beneficial effects. Tissue Barriers 2018, 6, e1425085. [Google Scholar] [CrossRef]
- Koeth, R.A.; Lam-Galvez, B.R.; Kirsop, J.; Wang, Z.; Levison, B.S.; Gu, X.; Copeland, M.F.; Bartlett, D.; Cody, D.B.; Dai, H.J.; et al. l-Carnitine in omnivorous diets induces an atherogenic gut microbial pathway in humans. J. Clin. Investig. 2019, 129, 373–387. [Google Scholar] [CrossRef] [PubMed]
- Nayor, M.; Brown, K.J.; Vasan, R.S. The Molecular Basis of Predicting Atherosclerotic Cardiovascular Disease Risk. Circ. Res. 2021, 128, 287–303. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Zhang, J.; Wu, C.; Cai, S.; Huang, W.; Chen, J.; Xi, X.; Liang, Z.; Hou, Q.; Zhou, B.; et al. Unique Features of Ethnic Mongolian Gut Microbiome revealed by metagenomic analysis. Sci. Rep. 2016, 6, 34826. [Google Scholar] [CrossRef]
- Tang, W.H.; Kitai, T.; Hazen, S.L. Gut Microbiota in Cardiovascular Health and Disease. Circ. Res. 2017, 120, 1183–1196. [Google Scholar] [CrossRef] [PubMed]
- Wilson, A.; McLean, C.; Kim, R.B. Trimethylamine-N-oxide: A link between the gut microbiome, bile acid metabolism, and atherosclerosis. Curr. Opin. Lipidol. 2016, 27, 148–154. [Google Scholar] [CrossRef]
- Papandreou, C.; Moré, M.; Bellamine, A. Trimethylamine N-Oxide in Relation to Cardiometabolic Health-Cause or Effect? Nutrients 2020, 12, 1330. [Google Scholar] [CrossRef]
- Krueger, E.S.; Lloyd, T.S.; Tessem, J.S. The Accumulation and Molecular Effects of Trimethylamine N-Oxide on Metabolic Tissues: It’s Not All Bad. Nutrients 2021, 13, 2873. [Google Scholar] [CrossRef]
- Wang, Z.; Klipfell, E.; Bennett, B.J.; Koeth, R.; Levison, B.S.; Dugar, B.; Feldstein, A.E.; Britt, E.B.; Fu, X.; Chung, Y.M.; et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011, 472, 57–63. [Google Scholar] [CrossRef]
- Wang, B.; Qiu, J.; Lian, J.; Yang, X.; Zhou, J. Gut Metabolite Trimethylamine-N-Oxide in Atherosclerosis: From Mechanism to Therapy. Front. Cardiovasc. Med. 2021, 8, 723886. [Google Scholar] [CrossRef]
- Lyu, M.; Wang, Y.F.; Fan, G.W.; Wang, X.Y.; Xu, S.Y.; Zhu, Y. Balancing Herbal Medicine and Functional Food for Prevention and Treatment of Cardiometabolic Diseases through Modulating Gut Microbiota. Front. Microbiol. 2017, 8, 2146. [Google Scholar] [CrossRef]
- Zhu, L.; Zhang, D.; Zhu, H.; Zhu, J.; Weng, S.; Dong, L.; Liu, T.; Hu, Y.; Shen, X. Berberine treatment increases Akkermansia in the gut and improves high-fat diet-induced atherosclerosis in Apoe(−/−) mice. Atherosclerosis 2018, 268, 117–126. [Google Scholar] [CrossRef] [PubMed]
- Gebrayel, P.; Nicco, C.; Al Khodor, S.; Bilinski, J.; Caselli, E.; Comelli, E.M.; Egert, M.; Giaroni, C.; Karpinski, T.M.; Loniewski, I.; et al. Microbiota medicine: Towards clinical revolution. J. Transl. Med. 2022, 20, 111. [Google Scholar] [CrossRef] [PubMed]
- Schoeler, M.; Caesar, R. Dietary lipids, gut microbiota and lipid metabolism. Rev. Endocr. Metab. Disord. 2019, 20, 461–472. [Google Scholar] [CrossRef] [PubMed]
- Witkowski, M.; Witkowski, M.; Friebel, J.; Buffa, J.A.; Li, X.S.; Wang, Z.; Sangwan, N.; Li, L.; DiDonato, J.A.; Tizian, C.; et al. Vascular endothelial tissue factor contributes to trimethylamine N-oxide-enhanced arterial thrombosis. Cardiovasc. Res. 2022, 118, 2367–2384. [Google Scholar] [CrossRef]
- Talmor-Barkan, Y.; Kornowski, R. The gut microbiome and cardiovascular risk: Current perspective and gaps of knowledge. Future Cardiol. 2017, 13, 191–194. [Google Scholar] [CrossRef] [PubMed]
- Ghasemzadeh, M.; Hosseini, E.; Shahbaz Ghasabeh, A.; Mousavi Hosseini, K. Reactive Oxygen Species Generated by CD45-Cells Distinct from Leukocyte Population in Platelet Concentrates Is Correlated with the Expression and Release of Platelet Activation Markers during Storage. Transfus. Med. Hemother. 2018, 45, 33–41. [Google Scholar] [CrossRef] [PubMed]
- Kuhlencordt, P.J.; Rosel, E.; Gerszten, R.E.; Morales-Ruiz, M.; Dombkowski, D.; Atkinson, W.J.; Han, F.; Preffer, F.; Rosenzweig, A.; Sessa, W.C.; et al. Role of endothelial nitric oxide synthase in endothelial activation: Insights from eNOS knockout endothelial cells. Am. J. Physiol. Cell. Physiol. 2004, 286, C1195–C1202. [Google Scholar] [CrossRef]
- Andersen, G.N.; Caidahl, K.; Kazzam, E.; Petersson, A.S.; Waldenström, A.; Mincheva-Nilsson, L.; Rantapää-Dahlqvist, S. Correlation between increased nitric oxide production and markers of endothelial activation in systemic sclerosis: Findings with the soluble adhesion molecules E-selectin, intercellular adhesion molecule 1, and vascular cell adhesion molecule 1. Arthritis Rheum. 2000, 43, 1085–1093. [Google Scholar] [CrossRef]
- Hartiala, J.; Bennett, B.J.; Tang, W.H.; Wang, Z.; Stewart, A.F.; Roberts, R.; McPherson, R.; Lusis, A.J.; Hazen, S.L.; Allayee, H.; et al. Comparative genome-wide association studies in mice and humans for trimethylamine N-oxide, a proatherogenic metabolite of choline and L-carnitine. Arterioscler. Thromb. Vasc. Biol. 2014, 34, 1307–1313. [Google Scholar] [CrossRef]
- Janeiro, M.H.; Ramírez, M.J.; Milagro, F.I.; Martínez, J.A.; Solas, M. Implication of Trimethylamine N-Oxide (TMAO) in Disease: Potential Biomarker or New Therapeutic Target. Nutrients 2018, 10, 1398. [Google Scholar] [CrossRef]
- de Moreno de LeBlanc, A.; LeBlanc, J.G. Effect of probiotic administration on the intestinal microbiota, current knowledge and potential applications. World J. Gastroenterol. 2014, 20, 16518–16528. [Google Scholar] [CrossRef] [PubMed]
- Cafiero, C.; Re, A.; Pisconti, S.; Trombetti, M.; Perri, M.; Colosimo, M.; D’Amato, G.; Gallelli, L.; Cannataro, R.; Molinario, C.; et al. Dysbiosis in intestinal microbiome linked to fecal blood determined by direct hybridization. 3Biotech 2020, 10, 358. [Google Scholar] [CrossRef] [PubMed]
- Miele, L.; Giorgio, V.; Alberelli, M.A.; De Candia, E.; Gasbarrini, A.; Grieco, A. Impact of Gut Microbiota on Obesity, Diabetes, and Cardiovascular Disease Risk. Curr. Cardiol. Rep. 2015, 17, 120. [Google Scholar] [CrossRef]
- Yamashita, T.; Kasahara, K.; Emoto, T.; Matsumoto, T.; Mizoguchi, T.; Kitano, N.; Sasaki, N.; Hirata, K. Intestinal Immunity and Gut Microbiota as Therapeutic Targets for Preventing Atherosclerotic Cardiovascular Diseases. Circ. J. 2015, 79, 1882–1890. [Google Scholar] [CrossRef] [PubMed]
- Yamashita, T.; Emoto, T.; Sasaki, N.; Hirata, K.I. Gut Microbiota and Coronary Artery Disease. Int. Heart J. 2016, 57, 663–671. [Google Scholar] [CrossRef] [PubMed]
- Rune, I.; Rolin, B.; Lykkesfeldt, J.; Nielsen, D.S.; Krych, L.; Kanter, J.E.; Bornfeldt, K.E.; Kihl, P.; Buschard, K.; Josefsen, K.; et al. Long-term Western diet fed apolipoprotein E-deficient rats exhibit only modest early atherosclerotic characteristics. Sci. Rep. 2018, 8, 5416. [Google Scholar] [CrossRef]
- Ballini, A.; Charitos, I.A.; Cantore, S.; Topi, S.; Bottalico, L.; Santacroce, L. About Functional Foods: The Probiotics and Prebiotics State of Art. Antibiotics 2023, 12, 635. [Google Scholar] [CrossRef]
- Valcheva, R.; Dieleman, L.A. Prebiotics: Definition and protective mechanisms. Best Pract. Res. Clin. Gastroenterol. 2016, 30, 27–37. [Google Scholar] [CrossRef]
- Brugere, J.F.; Borrel, G.; Gaci, N.; Tottey, W.; O’Toole, P.W.; Malpuech-Brugere, C. Archaebiotics: Proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes 2014, 5, 5–10. [Google Scholar] [CrossRef]
- Rom, O.; Korach-Rechtman, H.; Hayek, T.; Danin-Poleg, Y.; Bar, H.; Kashi, Y.; Aviram, M. Acrolein increases macrophage atherogenicity in association with gut microbiota remodeling in atherosclerotic mice: Protective role for the polyphenol-rich pomegranate juice. Arch. Toxicol. 2017, 91, 1709–1725. [Google Scholar] [CrossRef]
- Ryan, P.M.; London, L.E.E.; Bjorndahl, T.C.; Mandal, R.; Murphy, K.; Fitzgerald, G.F.; Shanahan, F.; Ross, R.P.; Wishart, D.S.; Caplice, N.M.; et al. Microbiome and metabolome modifying effects of several cardiovascular disease interventions in apo-E−/− mice. Microbiome 2017, 5, 30. [Google Scholar] [CrossRef]
- Lau, K.; Srivatsav, V.; Rizwan, A.; Nashed, A.; Liu, R.; Shen, R.; Akhtar, M. Bridging the Gap between Gut Microbial Dysbiosis and Cardiovascular Diseases. Nutrients 2017, 9, 859. [Google Scholar] [CrossRef] [PubMed]
- Deng, B.; Tao, L.; Wang, Y. Natural products against inflammation and atherosclerosis: Targeting on gut microbiota. Front. Microbiol. 2022, 13, 997056. [Google Scholar] [CrossRef] [PubMed]
- Centner, A.M.; Khalili, L.; Ukhanov, V.; Kadyan, S.; Nagpal, R.; Salazar, G. The Role of Phytochemicals and Gut Microbiome in Atherosclerosis in Preclinical Mouse Models. Nutrients 2023, 15, 1212. [Google Scholar] [CrossRef] [PubMed]
- El Hage, R.; Al-Arawe, N.; Hinterseher, I. The Role of the Gut Microbiome and Trimethylamine Oxide in Atherosclerosis and Age-Related Disease. Int. J. Mol. Sci. 2023, 24, 2399. [Google Scholar] [CrossRef]
- Momin, E.S.; Khan, A.A.; Kashyap, T.; Pervaiz, M.A.; Akram, A.; Mannan, V.; Sanusi, M.; Elshaikh, A.O. The Effects of Probiotics on Cholesterol Levels in Patients with Metabolic Syndrome: A Systematic Review. Cureus 2023, 15, e37567. [Google Scholar] [CrossRef]
- Kuka, J.; Liepinsh, E.; Makrecka-Kuka, M.; Liepins, J.; Cirule, H.; Gustina, D.; Loza, E.; Zharkova-Malkova, O.; Grinberga, S.; Pugovics, O.; et al. Suppression of intestinal microbiota-dependent production of pro-atherogenic trimethylamine N-oxide by shifting L-carnitine microbial degradation. Life Sci. 2014, 117, 84–92. [Google Scholar] [CrossRef]
- Liao, Z.-L.; Zeng, B.-H.; Wang, W.; Li, G.-H.; Wu, F.; Wang, L.; Zhong, Q.P.; Wei, H.; Fang, X. Impact of the Consumption of Tea Polyphenols on Early Atherosclerotic Lesion Formation and Intestinal Bifidobacteria in High-Fat-Fed ApoE(−/−) Mice. Front. Nutr. 2016, 3, 42. [Google Scholar] [CrossRef]
- Colella, M.; Charitos, I.A.; Ballini, A.; Cafiero, C.; Topi, S.; Palmirotta, R.; Santacroce, L. Microbiota revolution: How gut microbes regulate our lives. World J. Gastroenterol. 2023, 29, 4368–4383. [Google Scholar] [CrossRef]
- Lu, Z.Y.; Feng, L.; Jiang, W.D.; Wu, P.; Liu, Y.; Jin, X.W.; Ren, H.M.; Kuang, S.Y.; Li, S.W.; Tang, L.; et al. An Antioxidant Supplement Function Exploration: Rescue of Intestinal Structure Injury by Mannan Oligosaccharides after Aeromonas hydrophila Infection in Grass Carp (Ctenopharyngodon idella). Antioxidants 2022, 11, 806. [Google Scholar] [CrossRef]
- Matziouridou, C.; Marungruang, N.; Nguyen, T.D.; Nyman, M.; Fak, F. Lingonberries reduce atherosclerosis in Apoe(−/−) mice in association with altered gut microbiota composition and improved lipid profile. Mol. Nutr. Food Res. 2016, 60, 1150–1160. [Google Scholar] [CrossRef] [PubMed]
- Trøseid, M.; Ueland, T.; Hov, J.R.; Svardal, A.; Gregersen, I.; Dahl, C.P.; Aakhus, S.; Gude, E.; Bjørndal, B.; Halvorsen, B.; et al. Microbiota-dependent metabolite trimethylamine-N-oxide is associated with disease severity and survival of patients with chronic heart failure. J. Intern. Med. 2015, 277, 717–726. [Google Scholar] [CrossRef] [PubMed]
- Kadam, I.; Dalloul, M.; Hausser, J.; Huntley, M.; Hoepner, L.; Fordjour, L.; Hittelman, J.; Saxena, A.; Liu, J.; Futterman, I.D.; et al. Associations between nutrients in one-carbon metabolism and fetal DNA methylation in pregnancies with or without gestational diabetes mellitus. Clin. Epigenet. 2023, 15, 137. [Google Scholar] [CrossRef] [PubMed]
- Mansuri, N.M.; Mann, N.K.; Rizwan, S.; Mohamed, A.E.; Elshafey, A.E.; Khadka, A.; Mosuka, E.M.; Thilakarathne, K.N.; Mohammed, L. Role of Gut Microbiome in Cardiovascular Events: A Systematic Review. Cureus 2022, 14, e32465. [Google Scholar] [CrossRef] [PubMed]
- Sato, S.; Kudo, F.; Kuzuyama, T.; Hammerschmidt, F.; Eguchi, T. C-Methylation Catalyzed by Fom3, a Cobalamin-Dependent Radical S-adenosyl-l-methionine Enzyme in Fosfomycin Biosynthesis, Proceeds with Inversion of Configuration. Biochemistry 2018, 57, 4963–4966. [Google Scholar] [CrossRef] [PubMed]
- Mackay, R.J.; McEntyre, C.J.; Henderson, C.; Lever, M.; George, P.M. Trimethylaminuria: Causes and diagnosis of a socially distressing condition. Clin. Biochem. Rev. 2011, 32, 33–43. [Google Scholar]
- Trøseid, M.; Hov, J.R.; Nestvold, T.K.; Thoresen, H.; Berge, R.K.; Svardal, A.; Lappegård, K.T. Major Increase in Microbiota-Dependent Proatherogenic Metabolite TMAO One Year After Bariatric Surgery. Metab. Syndr. Relat. Disord. 2016, 14, 197–201. [Google Scholar] [CrossRef]
- Wang, M.; Huang, Y.; Xin, M.; Li, T.; Wang, X.; Fang, Y.; Liang, S.; Cai, T.; Xu, X.; Dong, L.; et al. The impact of microbially modified metabolites associated with obesity and bariatric surgery on antitumor immunity. Front. Immunol. 2023, 14, 1156471. [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
Ciccone, M.M.; Lepera, M.E.; Guaricci, A.I.; Forleo, C.; Cafiero, C.; Colella, M.; Palmirotta, R.; Santacroce, L. Might Gut Microbiota Be a Target for a Personalized Therapeutic Approach in Patients Affected by Atherosclerosis Disease? J. Pers. Med. 2023, 13, 1360. https://doi.org/10.3390/jpm13091360
Ciccone MM, Lepera ME, Guaricci AI, Forleo C, Cafiero C, Colella M, Palmirotta R, Santacroce L. Might Gut Microbiota Be a Target for a Personalized Therapeutic Approach in Patients Affected by Atherosclerosis Disease? Journal of Personalized Medicine. 2023; 13(9):1360. https://doi.org/10.3390/jpm13091360
Chicago/Turabian StyleCiccone, Marco Matteo, Mario Erminio Lepera, Andrea Igoren Guaricci, Cinzia Forleo, Concetta Cafiero, Marica Colella, Raffele Palmirotta, and Luigi Santacroce. 2023. "Might Gut Microbiota Be a Target for a Personalized Therapeutic Approach in Patients Affected by Atherosclerosis Disease?" Journal of Personalized Medicine 13, no. 9: 1360. https://doi.org/10.3390/jpm13091360