Cardioimmunology in Health and Diseases: Impairment of the Cardio-Spleno-Bone Marrow Axis Following Myocardial Infarction in Diabetes Mellitus
Abstract
1. Introduction
2. Results
2.1. Animal Characteristics
2.2. Neutrophils Kinetics After Onset MI
2.3. Macrophages Dynamics
2.4. Dendritic Cells Dynamics
2.5. T Cells Distribution
2.6. B Cells Distribution
2.7. Endothelial Progenitor Cells Colony Formation Assay (EPC-CFA)
3. Discussion
3.1. Neutrophils
3.2. Macrophages
3.3. Dendritic Cells
3.4. T Cells and Its Subsets
3.5. B Cells
3.6. Endothelial Progenitor Cells
4. Materials and Methods
4.1. Animal Sample Size and Randomization
4.2. Myocardial Infarction Induction
4.3. Preparation of a Single-Cell Suspension
4.4. Flow Cytometry Analysis
4.5. EPC Colony-Forming Assay
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Pluijmert, N.J.; Atsma, D.E.; Quax, P.H. Post-ischemic myocardial inflammatory response: A complex and dynamic process susceptible to immunomodulatory therapies. Front. Cardiovasc. Med. 2021, 8, 647785. [Google Scholar] [CrossRef] [PubMed]
- Mann, D.L. The emerging role of innate immunity in the heart and vascular system: For whom the cell tolls. Circ. Res. 2011, 108, 1133–1145. [Google Scholar] [CrossRef] [PubMed]
- Adamo, L.; Rocha-Resende, C.; Prabhu, S.D.; Mann, D.L. Reappraising the role of inflammation in heart failure. Nat. Rev. Cardiol. 2020, 17, 269–285. [Google Scholar] [CrossRef] [PubMed]
- Swirski, F.K.; Nahrendorf, M.; Etzrodt, M.; Wildgruber, M.; Cortez-Retamozo, V.; Panizzi, P.; Figueiredo, J.-L.; Kohler, R.H.; Chudnovskiy, A.; Waterman, P. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009, 325, 612–616. [Google Scholar] [CrossRef] [PubMed]
- Emami, H.; Singh, P.; MacNabb, M.; Vucic, E.; Lavender, Z.; Rudd, J.H.; Fayad, Z.A.; Lehrer-Graiwer, J.; Korsgren, M.; Figueroa, A.L.; et al. Splenic metabolic activity predicts risk of future cardiovascular events: Demonstration of a cardiosplenic axis in humans. JACC. Cardiovasc. Imaging 2015, 8, 121–130. [Google Scholar] [CrossRef]
- Kolaczkowska, E.; Kubes, P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 2013, 13, 159–175. [Google Scholar] [CrossRef]
- Iwasaki, A.; Medzhitov, R. Regulation of adaptive immunity by the innate immune system. Science 2010, 327, 291–295. [Google Scholar] [CrossRef]
- Murray, P.J.; Wynn, T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11, 723–737. [Google Scholar] [CrossRef]
- Bratton, D.L.; Henson, P.M. Neutrophil clearance: When the party is over, clean-up begins. Trends Immunol. 2011, 32, 350–357. [Google Scholar] [CrossRef]
- Ma, Y.; Yabluchanskiy, A.; Lindsey, M.L. Neutrophil roles in left ventricular remodeling following myocardial infarction. Fibrogenesis Tissue Repair 2013, 6, 1–10. [Google Scholar] [CrossRef]
- Ma, Y.; Yabluchanskiy, A.; Iyer, R.P.; Cannon, P.L.; Flynn, E.R.; Jung, M.; Henry, J.; Cates, C.A.; Deleon-Pennell, K.Y.; Lindsey, M.L. Temporal neutrophil polarization following myocardial infarction. Cardiovasc. Res. 2016, 110, 51–61. [Google Scholar] [CrossRef] [PubMed]
- Frangogiannis, N.G. Regulation of the inflammatory response in cardiac repair. Circ. Res. 2012, 110, 159–173. [Google Scholar] [CrossRef] [PubMed]
- Nahrendorf, M.; Swirski, F.K.; Aikawa, E.; Stangenberg, L.; Wurdinger, T.; Figueiredo, J.-L.; Libby, P.; Weissleder, R.; Pittet, M.J. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 2007, 204, 3037–3047. [Google Scholar] [CrossRef] [PubMed]
- Troidl, C.; Möllmann, H.; Nef, H.; Masseli, F.; Voss, S.; Szardien, S.; Willmer, M.; Rolf, A.; Rixe, J.; Troidl, K. Classically and alternatively activated macrophages contribute to tissue remodelling after myocardial infarction. J. Cell. Mol. Med. 2009, 13, 3485–3496. [Google Scholar] [CrossRef]
- Fadini, G.; de Kreutzenberg, S.V.; Boscaro, E.; Albiero, M.; Cappellari, R.; Kränkel, N.; Landmesser, U.; Toniolo, A.; Bolego, C.; Cignarella, A. An unbalanced monocyte polarisation in peripheral blood and bone marrow of patients with type 2 diabetes has an impact on microangiopathy. Diabetologia 2013, 56, 1856–1866. [Google Scholar] [CrossRef]
- Swirski, F.K.; Nahrendorf, M. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science 2013, 339, 161–166. [Google Scholar] [CrossRef]
- Torres-Castro, I.; Arroyo-Camarena, Ú.D.; Martínez-Reyes, C.P.; Gómez-Arauz, A.Y.; Dueñas-Andrade, Y.; Hernández-Ruiz, J.; Béjar, Y.L.; Zaga-Clavellina, V.; Morales-Montor, J.; Terrazas, L.I. Human monocytes and macrophages undergo M1-type inflammatory polarization in response to high levels of glucose. Immunol. Lett. 2016, 176, 81–89. [Google Scholar] [CrossRef]
- Nagareddy, P.R.; Murphy, A.J.; Stirzaker, R.A.; Hu, Y.; Yu, S.; Miller, R.G.; Ramkhelawon, B.; Distel, E.; Westerterp, M.; Huang, L.-S.; et al. Hyperglycemia Promotes Myelopoiesis and Impairs the Resolution of Atherosclerosis. Cell Metab. 2013, 17, 695–708. [Google Scholar] [CrossRef]
- Monnerat, G.; Alarcón, M.L.; Vasconcellos, L.R.; Hochman-Mendez, C.; Brasil, G.; Bassani, R.A.; Casis, O.; Malan, D.; Travassos, L.H.; Sepúlveda, M. Macrophage-dependent IL-1β production induces cardiac arrhythmias in diabetic mice. Nat. Commun. 2016, 7, 13344. [Google Scholar] [CrossRef]
- Yilmaz, A.; Weber, J.; Cicha, I.; Stumpf, C.; Klein, M.; Raithel, D.; Daniel, W.G.; Garlichs, C.D. Decrease in Circulating Myeloid Dendritic Cell Precursors in Coronary Artery Disease. J. Am. Coll. Cardiol. 2006, 48, 70–80. [Google Scholar] [CrossRef]
- Zhang, J.; Yu, Z.; Fujita, S.; Yamaguchi, M.; Ferrans, V. Interstitial dendritic cells of the rat heart. Quantitative and ultrastructural changes in experimental myocardial infarction. Circulation 1993, 87, 909–920. [Google Scholar] [CrossRef] [PubMed]
- Anzai, A.; Anzai, T.; Nagai, S.; Maekawa, Y.; Naito, K.; Kaneko, H.; Sugano, Y.; Takahashi, T.; Abe, H.; Mochizuki, S. Regulatory role of dendritic cells in postinfarction healing and left ventricular remodeling. Circulation 2012, 125, 1234–1245. [Google Scholar] [CrossRef] [PubMed]
- Naito, K.; Anzai, T.; Sugano, Y.; Maekawa, Y.; Kohno, T.; Yoshikawa, T.; Matsuno, K.; Ogawa, S. Differential effects of GM-CSF and G-CSF on infiltration of dendritic cells during early left ventricular remodeling after myocardial infarction. J. Immunol. 2008, 181, 5691–5701. [Google Scholar] [CrossRef] [PubMed]
- Gallo, P.M.; Gallucci, S. The dendritic cell response to classic, emerging, and homeostatic danger signals. Implications for autoimmunity. Front. Immunol. 2013, 4, 138. [Google Scholar] [CrossRef]
- Tel, J.; Schreibelt, G.; Sittig, S.P.; Mathan, T.S.; Buschow, S.I.; Cruz, L.J.; Lambeck, A.J.; Figdor, C.G.; de Vries, I.J.M. Human plasmacytoid dendritic cells efficiently cross-present exogenous Ags to CD8+ T cells despite lower Ag uptake than myeloid dendritic cell subsets. Blood J. Am. Soc. Hematol. 2013, 121, 459–467. [Google Scholar] [CrossRef]
- Liang, C.; Yang, K.Y.; Chan, V.W.; Li, X.; Fung, T.H.W.; Wu, Y.; Tian, X.Y.; Huang, Y.; Qin, L.; Lau, J.Y.W.; et al. CD8(+) T-cell plasticity regulates vascular regeneration in type-2 diabetes. Theranostics 2020, 10, 4217–4232. [Google Scholar] [CrossRef]
- Santos-Zas, I.; Lemarié, J.; Zlatanova, I.; Cachanado, M.; Seghezzi, J.-C.; Benamer, H.; Goube, P.; Vandestienne, M.; Cohen, R.; Ezzo, M.; et al. Cytotoxic CD8+ T cells promote granzyme B-dependent adverse post-ischemic cardiac remodeling. Nat. Commun. 2021, 12, 1483. [Google Scholar] [CrossRef]
- Ma, F.; Feng, J.; Zhang, C.; Li, Y.; Qi, G.; Li, H.; Wu, Y.; Fu, Y.; Zhao, Y.; Chen, H. The requirement of CD8+ T cells to initiate and augment acute cardiac inflammatory response to high blood pressure. J. Immunol. 2014, 192, 3365–3373. [Google Scholar] [CrossRef]
- Abdullah, C.S.; Li, Z.; Wang, X.; Jin, Z.-Q. Depletion of T lymphocytes ameliorates cardiac fibrosis in streptozotocin-induced diabetic cardiomyopathy. Int. Immunopharmacol. 2016, 39, 251–264. [Google Scholar] [CrossRef]
- Zouggari, Y.; Ait-Oufella, H.; Bonnin, P.; Simon, T.; Sage, A.P.; Guérin, C.; Vilar, J.; Caligiuri, G.; Tsiantoulas, D.; Laurans, L. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat. Med. 2013, 19, 1273–1280. [Google Scholar] [CrossRef]
- Jiao, J.; He, S.; Wang, Y.; Lu, Y.; Gu, M.; Li, D.; Tang, T.; Nie, S.; Zhang, M.; Lv, B.; et al. Regulatory B cells improve ventricular remodeling after myocardial infarction by modulating monocyte migration. Basic Res. Cardiol. 2021, 116, 46. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Jiang, K.; Chen, F.; Qian, J.; Wang, D.; Wu, Y.; Zhou, C.; Yu, Y.; Chen, K.; Hwa, J.; et al. Bone marrow-derived naïve B lymphocytes improve heart function after myocardial infarction: A novel cardioprotective mechanism for empagliflozin. Basic Res. Cardiol. 2022, 117, 47. [Google Scholar] [CrossRef] [PubMed]
- Salybekov, A.A.; Kobayashi, S.; Asahara, T. Characterization of endothelial progenitor cell: Past, present, and future. Int. J. Mol. Sci. 2022, 23, 7697. [Google Scholar] [CrossRef] [PubMed]
- António, N.; Fernandes, R.; Soares, A.; Soares, F.; Lopes, A.; Carvalheiro, T.; Paiva, A.; Pêgo, G.M.; Providência, L.A.; Gonçalves, L. Reduced levels of circulating endothelial progenitor cells in acute myocardial infarction patients with diabetes or pre-diabetes: Accompanying the glycemic continuum. Cardiovasc. Diabetol. 2014, 13, 101. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.-Y.; Zhai, L.; Li, Q.-L.; Ye, J.-X.; Kang, L.-N.; Xie, J.; Xu, B. Effects of ACE inhibition on endothelial progenitor cell mobilization and prognosis after acute myocardial infarction in type 2 diabetic patients. Clinics 2013, 68, 665–673. [Google Scholar] [CrossRef]
- Ling, L.; Shen, Y.; Wang, K.; Jiang, C.; Fang, C.; Ferro, A.; Kang, L.; Xu, B. Worse clinical outcomes in acute myocardial infarction patients with type 2 diabetes mellitus: Relevance to impaired endothelial progenitor cells mobilization. PLoS ONE 2012, 7, e50739. [Google Scholar] [CrossRef]
- Marfella, R.; Rizzo, M.R.; Siniscalchi, M.; Paolisso, P.; Barbieri, M.; Sardu, C.; Savinelli, A.; Angelico, N.; Del Gaudio, S.; Esposito, N. Peri-procedural tight glycemic control during early percutaneous coronary intervention up-regulates endothelial progenitor cell level and differentiation during acute ST-elevation myocardial infarction: Effects on myocardial salvage. Int. J. Cardiol. 2013, 168, 3954–3962. [Google Scholar] [CrossRef]
- Rigato, M.; Avogaro, A.; Fadini, G.P. Levels of circulating progenitor cells, cardiovascular outcomes and death: A meta-analysis of prospective observational studies. Circ. Res. 2016, 118, 1930–1939. [Google Scholar] [CrossRef]
- Salybekov, A.A.; Masuda, H.; Miyazaki, K.; Sheng, Y.; Sato, A.; Shizuno, T.; Iida, Y.; Okada, Y.; Asahara, T. Dipeptidyl dipeptidase-4 inhibitor recovered ischemia through an increase in vasculogenic endothelial progenitor cells and regeneration-associated cells in diet-induced obese mice. PLoS ONE 2019, 14, e0205477. [Google Scholar] [CrossRef]
- Kawaguchi, A.T.; Salybekov, A.A.; Yamano, M.; Kitagishi, H.; Sekine, K.; Tamaki, T. PEGylated carboxyhemoglobin bovine (SANGUINATE) ameliorates myocardial infarction in a rat model. Artif. Organs 2018, 42, 1174–1184. [Google Scholar] [CrossRef]
- Pinto, A.R.; Ilinykh, A.; Ivey, M.J.; Kuwabara, J.T.; D’antoni, M.L.; Debuque, R.; Chandran, A.; Wang, L.; Arora, K.; Rosenthal, N.A. Revisiting cardiac cellular composition. Circ. Res. 2016, 118, 400–409. [Google Scholar] [CrossRef] [PubMed]
- Salybekov, A.A.; Kawaguchi, A.T.; Masuda, H.; Vorateera, K.; Okada, C.; Asahara, T. Regeneration-associated cells improve recovery from myocardial infarction through enhanced vasculogenesis, anti-inflammation, and cardiomyogenesis. PLoS ONE 2018, 13, e0203244. [Google Scholar] [CrossRef] [PubMed]
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. |
© 2024 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
Salybekov, A.A.; Tashov, K.; Sheng, Y.; Salybekova, A.; Shinozaki, Y.; Asahara, T.; Kobayashi, S. Cardioimmunology in Health and Diseases: Impairment of the Cardio-Spleno-Bone Marrow Axis Following Myocardial Infarction in Diabetes Mellitus. Int. J. Mol. Sci. 2024, 25, 11833. https://doi.org/10.3390/ijms252111833
Salybekov AA, Tashov K, Sheng Y, Salybekova A, Shinozaki Y, Asahara T, Kobayashi S. Cardioimmunology in Health and Diseases: Impairment of the Cardio-Spleno-Bone Marrow Axis Following Myocardial Infarction in Diabetes Mellitus. International Journal of Molecular Sciences. 2024; 25(21):11833. https://doi.org/10.3390/ijms252111833
Chicago/Turabian StyleSalybekov, Amankeldi A., Kanat Tashov, Yin Sheng, Ainur Salybekova, Yoshiko Shinozaki, Takayuki Asahara, and Shuzo Kobayashi. 2024. "Cardioimmunology in Health and Diseases: Impairment of the Cardio-Spleno-Bone Marrow Axis Following Myocardial Infarction in Diabetes Mellitus" International Journal of Molecular Sciences 25, no. 21: 11833. https://doi.org/10.3390/ijms252111833
APA StyleSalybekov, A. A., Tashov, K., Sheng, Y., Salybekova, A., Shinozaki, Y., Asahara, T., & Kobayashi, S. (2024). Cardioimmunology in Health and Diseases: Impairment of the Cardio-Spleno-Bone Marrow Axis Following Myocardial Infarction in Diabetes Mellitus. International Journal of Molecular Sciences, 25(21), 11833. https://doi.org/10.3390/ijms252111833