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Hydrogel modulate macrophages to promote myocardial repair after myocardial infarction

Published on Jun. 01, 2024Total Views: 197 timesTotal Downloads: 105 timesDownloadMobile

Author: HUANG Huihui 1 CAI Yongxiang 1 DU Huan 1 CHENG Panke 1, 2 LI Gang 1, 2 TAO Jianhong 1, 2

Affiliation: 1 School of Medicine, University of Electronic Science and Technology of China, Chengdu 611731, China 2 Department of Cardiovascular Medicine, Sichuan Academy of Medical Sciences/Sichuan Provincial People's Hospital, Chengdu 610072, China

Keywords: Myocardial infarction Myocardial repair Hydrogels Macrophage

DOI: 10.12173/j.issn.1004-5511.202401097

Reference: Huang HH, Cai YX, Du H, Cheng PK, Li G, Tao JH. Hydrogel modulate macrophages to promote myocardial repair after myocardial infarction[J]. Yixue Xinzhi Zazhi, 2024, 34(5): 572-581. DOI: 10.12173/j.issn.1004-5511.202401097.[Article in Chinese]

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Abstract

Myocardial infarction (MI) is the necrosis of cardiomyocytes caused by insufficient coronary blood supply. The inflammatory response induced by necrotic cells alters the myocardial microenvironment and participates in the process of myocardial injury and repair. Macrophages are important executors of the inflammatory response and participate in the myocardial injury and healing process by secreting cytokines with different functions through different subtypes. Modulation of macrophage subtypes has emerged as a potential therapeutic strategy for myocardial repair. In recent years, hydrogel materials have been widely used in MI repair due to its good biocompatibility and functionalized modification ability. Functionalized hydrogels not only provide mechanical support, but also modulate macrophage subtypes, improve the immune microenvironment at the infarct site, and promote myocardial repair and regeneration. This article reviews the pivotal role of macrophages in MI and the current state of hydrogels in modulating macrophages to promote myocardial repair after MI.

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References

1.Roth GA, Mensah GA, Johnson CO, et al. Global burden of cardiovascular diseases and risk factors, 1990-2019: update from the GBD 2019 study[J]. J Am Coll Cardiol, 2020, 76(25): 2982-3021. DOI: 10.1016/j.jacc.2020. 11.010.

2.中国心血管健康与疾病报告编写组. 中国心血管健康与疾病报告2022概要[J]. 中国循环杂志, 2023, 38(6): 583-612. [The Writing Committee of the Report on Cardiovascular Health and Diseases in China. Report on cardiovascular health and diseases in China 2022[J] Chinese Circulation Journal, 2023, 38(6): 583-612. DOI: 10.3969/j.issn.1000-3614.2023.06.001.

3.宁玉珍, 斯日古楞, 白相君, 等. 不同剂量瑞舒伐他汀对冠脉介入术后急性心肌梗死患者心室重构、心功能、炎症反应及血脂的影响[J]. 中国药师, 2023, 26(10): 90-96. [Ning YZ, Siri GL, Bai XJ, et al. Effects of different doses of rosuvastatin on ventricular remodeling, cardiac function, inflammatory response and serum lipids in patients with acute myocardial infarction after coronary intervention[J]. China Pharmacist, 2023, 26(10): 90-96.] DOI: 10.12173/j.issn.1008-049X.202310026.

4.Yap J, Irei J, Lozano-Gerona J, et al. Macrophages in cardiac remodelling after myocardial infarction[J]. Nat Rev Cardiol, 2023, 20(6): 373-385. DOI: 10.1038/s41569-022-00823-5.

5.Mouton AJ, DeLeon-Pennell KY, Rivera Gonzalez OJ, et al. Mapping macrophage polarization over the myocardial infarction time continuum[J]. Basic Res Cardiol, 2018, 113(4): 26. DOI: 10.1007/s00395-018-0686-x.

6.Wang Y, Li J, Han H, et al. Application of locally responsive design of biomaterials based on microenvironmental changes in myocardial infarction[J]. iScience, 2023, 26(9): 107662. DOI: 10.1016/j.isci.2023.107662.

7.Murray PJ. Macrophage Polarization[J]. Annu Rev Physiol, 2017, 79: 541-566. DOI: 10.1146/annurev-physiol-022516-034339.

8.Locati M, Curtale G, Mantovani A. Diversity, mechanisms, and significance of macrophage plasticity[J]. Annu Rev Pathol, 2020, 15: 123-147. DOI: 10.1146/annurev-pathmechdis-012418-012718.

9.Bosurgi L, Cao YG, Cabeza-Cabrerizo M, et al. Macrophage function in tissue repair and remodeling requires IL-4 or IL-13 with apoptotic cells[J]. Science, 2017, 356(6342): 1072-1076. DOI: 10.1126/science.aai8132.

10.Dick SA, Macklin JA, Nejat S, et al. Self-renewing resident cardiac macrophages limit adverse remodeling following myocardial infarction[J]. Nat Immunol, 2019, 20(1): 29-39. DOI: 10.1038/s41590-018-0272-2.

11.Lörchner H, Pöling J, Gajawada P, et al. Myocardial healing requires Reg3β-dependent accumulation of macrophages in the ischemic heart[J]. Nat Med, 2015, 21(4): 353-362. DOI: 10.1038/nm.3816.

12.Franca CN, Izar MCO, Hortencio MNS, et al. Monocyte subtypes and the CCR2 chemokine receptor in cardiovascular disease[J]. Clin Sci (Lond), 2017, 131(12): 1215-1224. DOI: 10.1042/CS20170009.

13.Ben-Mordechai T, Holbova R, Landa-Rouben N, et al. Macrophage subpopulations are essential for infarct repair with and without stem cell therapy[J]. J Am Coll Cardiol, 2013, 62(20): 1890-1901. DOI: 10.1016/j.jacc.2013.07.057.

14.Javadov S, Jang S, Agostini B. Crosstalk between mitogen-activated protein kinases and mitochondria in cardiac diseases: therapeutic perspectives[J]. Pharmacol Ther, 2014, 144(2): 202-225. DOI: 10.1016/j.pharmthera.2014.05.013.

15.Leblond AL, Klinkert K, Martin K, et al. Systemic and cardiac depletion of M2 macrophage through CSF-1R signaling inhibition alters cardiac function post myocardial infarction[J]. PLoS One, 2015, 10(9): e0137515. DOI: 10.1371/journal.pone.0137515.

16.Biemmi V, Milano G, Ciullo A, et al. Inflammatory extracellular vesicles prompt heart dysfunction via TRL4-dependent NF-κB activation [J]. Theranostics, 2020, 10(6): 2773-2790. DOI: 10.7150/thno.39072.

17.Witherel CE, Sao K, Brisson BK, et al. Regulation of extracellular matrix assembly and structure by hybrid M1/M2 macrophages[J]. Biomaterials, 2021, 269: 120667. DOI: 10.1016/j.biomaterials.2021.120667.

18.Liu S, Chen J, Shi J, et al. M1-like macrophage-derived exosomes suppress angiogenesis and exacerbate cardiac dysfunction in a myocardial infarction microenvironment[J]. Basic Res Cardiol, 2020, 115(2): 22. DOI: 10.1007/s00395-020-0781-7.

19.Peet C, Ivetic A, Bromage DI, et al. Cardiac monocytes and macrophages after myocardial infarction[J]. Cardiovasc Res, 2020, 116(6): 1101-1112. DOI: 10.1093/cvr/cvz336.

20.Li L, Cao J, Li S, et al. M2 macrophage-derived sEV regulate pro-inflammatory CCR2+ macrophage subpopulations to favor post-AMI cardiac repair[J]. Adv Sci (Weinh), 2023, 10(14): e2202964. DOI: 10.1002/advs.202202964.

21.Ferraro B, Leoni G, Hinkel R, et al. Pro-angiogenic macrophage phenotype to promote myocardial repair[J]. J Am Coll Cardiol, 2019, 73(23): 2990-3002. DOI: 10.1016/j.jacc.2019.03.503.

22.Hulsmans M, Clauss S, Xiao L, et al. Macrophages facilitate electrical conduction in the heart[J]. Cell, 2017, 169(3): 510-522, e20. DOI: 10.1016/j.cell.2017.03.050.

23.Wlaschek M, Singh K, Sindrilaru A, et al. Iron and iron-dependent reactive oxygen species in the regulation of macrophages and fibroblasts in non-healing chronic wounds[J]. Free Radic Biol Med, 2019, 133: 262-275. DOI: 10.1016/j.freeradbiomed.2018.09.036.

24.Ma F, Li Y, Jia L, et al. Macrophage-stimulated cardiac fibroblast production of IL-6 is essential for TGF β/Smad activation and cardiac fibrosis induced by angiotensin II[J]. PLoS One, 2012, 7(5): e35144. DOI: 10.1371/journal.pone.0035144.

25.Haider N, Boscá L, Zandbergen HR, et al. Transition of macrophages to fibroblast-like cells in healing myocardial infarction[J]. J Am Coll Cardiol, 2019, 74(25): 3124-3135. DOI: 10.1016/j.jacc.2019.10.036.

26.Lim SY, Cho DI, Jeong HY, et al. Adjuvant role of macrophages in stem cell-induced cardiac repair in rats[J]. Exp Mol Med, 2018, 50(11): 1-10. DOI: 10.1038/s12276-018-0171-5.

27.Zhao J, Li X, Hu J, et al. Mesenchymal stromal cell-derived exosomes attenuate myocardial ischaemia-reperfusion injury through miR-182-regulated macrophage polarization[J]. Cardiovasc Res, 2019, 115(7): 1205-1216. DOI: 10.1093/cvr/cvz040.

28.Cortés-Morales VA, Vázquez-González WG, Montesinos JJ, et al. Human bone marrow mesenchymal stem cells promote the M2 phenotype in macrophages derived from STEMI patients[J]. Int J Mol Sci, 2023, 24(22): 16257. DOI: 10.3390/ijms242216257.

29.van der Laan AM, Ter Horst EN, Delewi R, et al. Monocyte subset accumulation in the human heart following acute myocardial infarction and the role of the spleen as monocyte reservoir[J]. Eur Heart J, 2014, 35(6): 376-385.DOI: 10.1093/eurheartj/eht331.

30.Dick SA, Macklin JA, Nejat S, et al. Self-renewing resident cardiac macrophages limit adverse remodeling following myocardial infarction[J]. Nat Immunol, 2019, 20(1): 29-39. DOI: 10.1038/s41590-018-0272-2.

31.Bajpai G, Bredemeyer A, Li W, et al. Tissue resident CCR2- and CCR2+ cardiac macrophages differentially orchestrate monocyte recruitment and fate specification following myocardial injury[J]. Circ Res, 2019, 124(2): 263-278. DOI: 10.1161/Circresaha.118.314028.

32.Peet C, Ivetic A, Bromage DI, et al. Cardiac monocytes and macrophages after myocardial infarction[J]. Cardiovasc Res, 2020, 116(6): 1101-1112. DOI: 10.1093/cvr/cvz336.

33.Chung L, Maestas DR Jr, Housseau F, et al. Key players in the immune response to biomaterial scaffolds for regenerative medicine[J]. Adv Drug Deliver Rev, 2017, 114: 184-192. DOI: 10.1016/j.addr.2017.07.006.

34.Wang D, Hu Y, Zhang L, et al. Dual delivery of an NF-κB inhibitor and IL-10 through supramolecular hydrogels polarizes macrophages and promotes cardiac repair after myocardial infarction[J]. Acta Biomater, 2023, 164: 111-123. DOI: 10.1016/j.actbio.2023.03.035.

35.Hu C, Liu W, Long L, et al. Regeneration of infarcted hearts by myocardial infarction-responsive injectable hydrogels with combined anti-apoptosis, anti-inflammatory and pro-angiogenesis properties[J]. Biomaterials, 2022, 290: 121849. DOI: 10.1016/j.biomaterials.2022.121849.

36.Xie X, Li Z, Yang X, et al. Biomimetic nanofibrillar hydrogel with cell-adaptable network for enhancing cellular mechanotransduction, metabolic energetics, and bone regeneration[J]. J Am Chem Soc, 2023, 145(28): 15218-15229. DOI: 10.1021/jacs.3c02210.

37.Shen H, Xu B, Yang C, et al. A DAMP-scavenging, IL-10-releasing hydrogel promotes neural regeneration and motor function recovery after spinal cord injury[J]. Biomaterials, 2022, 280: 121279. DOI: 10.1016/j.biomaterials.2021.121279.

38.Sadtler K, Allen BW, Estrellas K, et al. The scaffold immune microenvironment: biomaterial-mediated immune polarization in traumatic and nontraumatic applications[J]. Tissue Eng Part A, 2016, 23 (19-20): 1044-1053. DOI: 10.1089/ten.TEA.2016.0304.

39.Liang JL, Jin XK, Luo GF, et al. Immunostimulant hydrogel-guided tumor microenvironment reprogramming to efficiently potentiate macrophage-mediated cellular phagocytosis for systemic cancer immunotherapy[J]. ACS Nano, 2023, 17(17): 17217-17232. DOI: 10.1021/acsnano.3c05093.

40.崔璟怡, 崔亚洲, 赵燕. 水凝胶在治疗类风湿关节炎和骨关节炎中的研究进展[J]. 生物医学工程研究, 2022, 41(4): 405-410. [Cui JY, Cui YZ, Zhao Y. Research progess of hydrogel in the treatment of rheumatoid arthritis and osteoarthritis[J]. Journal of Biomedical Engineering Research, 2022, 41(4): 405-410.] DOI: 10.19529/j.cnki.1672-6278.2022.04.09.

41.Wang Y, Li J, Han H, et al. Application of locally responsive design of biomaterials based on microenvironmental changes in myocardial infarction[J]. iScience, 2023, 26(9): 107662. DOI: 10.1016/j.isci.2023.107662.

42.Mouton AJ, DeLeon-Pennell KY, Rivera Gonzalez OJ, et al. Mapping macrophage polarization over the myocardial infarction time continuum[J]. Basic Res Cardiol, 2018, 113(4): 26. DOI: 10.1007/s00395-018-0686-x.

43.Villarreal-Leal RA, Healey GD, Corradetti B. Biomimetic immunomodulation strategies for effective tissue repair and restoration[J]. Adv Drug Deliv Rev, 2021, 179: 113913. DOI: 10.1016/j.addr.2021.113913.

44.Wang X, Senapati S, Akinbote A, et al. Microenvironment stiffness requires decellularized cardiac extracellular matrix to promote heart regeneration in the neonatal mouse heart[J]. Acta Biomater, 2020, 113: 380-392. DOI: 10.1016/j.actbio.2020.06.032.

45.Kong P, Dong J, Li W, et al. Extracellular matrix/glycopeptide hybrid hydrogel as an immunomodulatory niche for endogenous cardiac repair after myocardial infarction[J]. Adv Sci (Weinh), 2023, 10(23): e2301244. DOI: 10.1002/advs.202301244.

46.付小兵, Nicholas A. Pepas, 顾晓松.再生医学:生物材料与组织再生[M]. 北京: 人民卫生出版社, 2020: 12. [Fu XB, Nicholas A·Peppas, Gu XS, et al. Regenerative Medicine Biomaterials and Tissue Regeneration[M]. Beijing: People's Medical Publishing House, 2020: 12.]

47.Tapeinos C, Gao H, Bauleth-Ramos T, et al. Progress in stimuli-responsive biomaterials for treating cardiovascular and cerebrovascular diseases[J]. Small, 2022, 18(36): e2200291. DOI: 10.1002/smll.202200291.

48.Ding J, Yao Y, Li J, et al. A reactive oxygen species scavenging and O2 generating injectable hydrogel for myocardial infarction treatment in vivo[J]. Small, 2020, 16(48): e2005038. DOI: 10.1002/smll.202005038.

49.Zhang L, Bei Z, Li T, et al. An injectable conductive hydrogel with dual responsive release of rosmarinic acid improves cardiac function and promotes repair after myocardial infarction[J]. Bioact Mater, 2023, 29: 132-150. DOI: 10.1016/j.bioactmat.2023.07.007.

50.Zhou J, Liu W, Zhao X, et al. Natural melanin/alginate hydrogels achieve cardiac repair through ROS scavenging and macrophage polarization[J]. Adv Sci (Weinh), 2021, 8(20): e2100505. DOI: 10.1002/advs.202100505.

51.Podaru MN, Fields L, Kainuma S, et al. Reparative macrophage transplantation for myocardial repair: a refinement of bone marrow mononuclear cell-based therapy[J]. Basic Res Cardiol, 2019, 114(5): 34. DOI: 10.1007/s00395-019-0742-1.

52.Li Y, Chen X, Jin R, et al. Injectable hydrogel with MSNs/microRNA-21-5p delivery enables both immuno modification and enhanced angiogenesis for myocardial infarction therapy in pigs[J]. Sci Adv, 2021, 7(9): eabd6740. DOI: 10.1126/sci adv.abd6740.

53.Jung M, Ma Y, Iyer RP, et al. IL-10 improves cardiac remodeling after myocardial infarction by stimulating M2 macrophage polarization and fibroblast activation[J]. Basic Res Cardiol, 2017, 112(3): 33. DOI: 10.1007/s00395-017-0622-5.

54.Garikipati VNS, Verma SK, Jolardarashi D, et al. Therapeutic inhibition of miR-375 attenuates post-myocardial infarction inflammatory response and left ventricular dysfunction via PDK-1-AKT signalling axis[J]. Cardiovasc Res, 2017, 113(8): 938-949. DOI: 10.1093/cvr/cvx052.

55.Sridharan R, Cavanagh B, Cameron AR, et al. Material stiffness influences the polarization state, function and migration mode of macrophages[J]. Acta Biomater, 2019, 89: 47-59. DOI: 10.1016/j.actbio.2019.02.048.

56.Shiraishi M, Shintani Y, Shintani Y, et al. Alternatively activated macrophages determine repair of the infarcted adult murine heart[J]. J Clin Invest, 2016, 126(6): 2151-2166. DOI: 10.1172/JCI85782.

57.Hao T, Qian M, Zhang Y, et al. An injectable dual-function hydrogel protects against myocardial ischemia/reperfusion injury by modulating ROS/NO disequilibrium[J]. Adv Sci (Weinh), 2022, 9(15): e2105408. DOI: 10.1002/advs.202105408.

58.Wang D, Hu Y, Zhang L, et al. Dual delivery of an NF-κB inhibitor and IL-10 through supramolecular hydrogels polarizes macrophages and promotes cardiac repair after myocardial infarction[J]. Acta Biomater, 2023, 164: 111-123. DOI: 10.1016/j.actbio.2023.03.035.

59.Cicuéndez M, Fernandes M, Ayán-Varela M, et al. Macrophage inflammatory and metabolic responses to graphene-based nanomaterials differing in size and functionalization[J]. Colloids Surf B Biointerfaces, 2020, 186: 110709. DOI: 10.1016/j.colsurfb.2019.110709.

60.Lee M, Kim YS, Park J, et al. A paintable and adhesive hydrogel cardiac patch with sustained release of ANGPTL4 for infarcted heart repair[J]. Bioact Mater, 2023, 31: 395-407. DOI: 10.1016/j.bioactmat.2023.08.020.

61.Han C, Zhou J, Liang C, et al. Human umbilical cord mesenchymal stem cell derived exosomes encapsulated in functional peptide hydrogels promote cardiac repair[J]. Biomater Sci, 2019, 7(7): 2920-2933. DOI: 10.1039/c9bm00101h.

62.Wang X, Shi H, Huang S, et al. Localized delivery of anti-inflammatory agents using extracellular matrix-nanostructured lipid carriers hydrogel promotes cardiac repair post-myocardial infarction[J]. Biomaterials, 2023, 302: 122364. DOI: 10.1016/j.biomaterials.2023.122364.

63.Chen Y, Shi J, Zhang Y, et al. An injectable thermosensitive hydrogel loaded with an ancient natural drug colchicine for myocardial repair after infarction[J].  J Mater Chem B, 2020, 8(5): 980-992. DOI: 10.1039/c9tb02523e.

64.Shin EY, Wang L, Zemskova M, et al. Adenosine production by biomaterial-supported mesenchymal stromal cells reduces the innate inflammatory response in myocardial ischemia/reperfusion injury[J]. J Am Heart Assoc, 2018, 7(2): e006949. DOI: 10.1161/Jaha.117.006949.

65.Chen S, Luo X, Sun Y, et al. A novel metabolic reprogramming strategy for the treatment of targeting to heart injury-mediated macrophages[J]. Int Immunopharmacol, 2023, 122: 110377. DOI: 10.1016/j.intimp.2023.110377.

66.Chen W, Wang C, Liu W, et al. A matrix-metalloproteinase-responsive hydrogel system for modulating the immune microenvironment in myocardial infarction[J]. Adv Mater, 2023, 35(13): e2209041. DOI: 10.1002/adma.202209041.

67.Luo L, Li Y, Bao Z, et al. Pericardial delivery of SDF-1α puerarin hydrogel promotes heart repair and electrical coupling[J]. Adv Mater, 2024, 36(1): e2302686. DOI: 10.1002/adma.202302686.

68.Jiang X, Feng T, An B, et al. A Bi-layer hydrogel cardiac patch made of recombinant functional proteins[J]. Adv Mater, 2022, 34(19): e2201411. DOI: 10.1002/adma.202201411.

69.Monguió-Tortajada M, Prat-Vidal C, Martínez-Falguera D, et al. Acellular cardiac scaffolds enriched with MSC-derived extracellular vesicles limit ventricular remodelling and exert local and systemic immunomodulation in a myocardial infarction porcine model[J]. Theranostics, 2022, 12(10): 4656-4670. DOI: 10.7150/thno.72289.

70.Huang K, Ozpinar EW, Su T, et al. An off-the-shelf artificial cardiac patch improves cardiac repair after myocardial infarction in rats and pigs[J]. Sci Transl Med, 2020, 12(538): eaat9683. DOI: 10.1126/scitranslmed.aat9683.

71.Monguió-Tortajada M, Prat-Vidal C, Moron-Font M, et al. Local administration of porcine immunomodulatory, chemotactic and angiogenic extracellular vesicles using engineered cardiac scaffolds for myocardial infarction[J]. Bioact Mater, 2021, 6(10): 3314-3327. DOI: 10.1016/j.bioactmat.2021.02.026.