Nerve growth factor and post-infarction cardiac remodeling
https://doi.org/10.29413/ABS.2022-7.2.13
Abstract
The prevalence of sudden death from chronic heart failure and cardiac arrhythmias caused by myocardial infarction is a complex problem in cardiology. Post-infarction cardiac remodeling occurs after myocardial infarction. This compensatory-adaptive reaction, regulated by mechanical, neurohumoral and genetic factors, includes the structural and functional changes of cardiomyocytes, stromal elements and extracellular matrix, geometry and architectonics of the left ventricular cavity. Adverse left ventricular remodeling is associated with heart failure and increased mortality. The concept of post-infarction cardiac remodeling is an urgent problem, since the mechanisms of development and progression of adverse post-infarction changes in the myocardium are completely unexplored. In recent years, the scientist attention has been focused on neurotrophic factors involved in the sympathetic nervous system and the vascular system remodeling after myocardial infarction. Nerve growth factor (NGF) is a protein from the neurotrophin family that is essential for the survival and development of sympathetic and sensory neurons, which also plays an important role in vasculogenesis. Acute myocardial infarction and heart failure are characterized by changes in the expression and activity of neurotrophic factors and their receptors, affecting the innervation of the heart muscle, as well as having a direct effect on cardiomyocytes, endothelial and smooth muscle vascular cells. The identification of the molecular mechanisms involved in the interactions between cardiomyocytes and neurons, as well as the study of the effects of NGF in the cardiovascular system, will improve understanding of the cardiac remodeling mechanism. This review summarizes the available scientific information (2019–2021) about mechanisms of the link between post-infarction cardiac remodeling and NGF functions.
About the Authors
O. Yu. KytikovaRussian Federation
Dr. Sc. (Med.), Senior Research Officer at the Laboratory of Rehabilitative Treatment
Russkaya str. 73G, Vladivostok 690105
T. P. Novgorodtseva
Russian Federation
Dr. Sc. (Biol.), Professor, Deputy Director for Science, Chief Research Officer at the Laboratory of Biomedical Research
Russkaya str. 73G, Vladivostok 690105
М. V. Antonyuk
Russian Federation
Dr. Sc. (Med.), Professor, Head of the Laboratory of Rehabilitation Treatment
Russkaya str. 73G, Vladivostok 690105
Yu. K. Denisenko
Russian Federation
Dr. Sc. (Biol.), Head of the Laboratory of Biomedical Research
Russkaya str. 73G, Vladivostok 690105
O. V. Atamas
Russian Federation
Cardiologist, Postgraduate at the Laboratory of Rehabilitation Treatment
Russkaya str. 73G, Vladivostok 690105
References
1. Virani SS, Alonso А, Benjamin EJ. Heart disease and stroke statistics-2020 update: A report from the American Heart Association. Circulation. 2020; 141(9): 139-596. doi: 10.1161/CIR.0000000000000757
2. Shih J-Y, Chen Z-C, Chang H-Y. Risks of age and sex on clinical outcomes post myocardial infarction. Int J Cardiol Heart Vasc. 2019; 23: 100350. doi: 10.1016/j.ijcha.2019.100350
3. Report on cardiovascular health and diseases in China 2019: An updated summary. Chinese Circulation Journal. 2020; 35(9): 833-854.
4. Timmis A, Townsend N, Gale CP. European Society of Cardiology: Cardiovascular disease statistics 2019. Eur Heart J. 2020; 41: 12-85. doi: 10.1093/eurheartj/ehz859
5. Maglietta G, Ardissino М, Malagoli Tagliazucchi G. Longterm outcomes after early-onset myocardial infarction. J Am Coll Cardiol. 2019; 74(16): 2113-2115. doi: 10.1016/j.jacc.2019.08.1000
6. Pfeffer MA. Survival after an experimental myocardial infarction: Beneficial effects of long-term therapy with captopril. Circulation. 1985; 2(72): 406-412.
7. Guo Y, Zhang C, Ye T, Chen X, Liu X, Chen X, et al. Pinocembrin ameliorates arrhythmias in rats with chronic ischaemic heart failure. Ann Med. 2021; 53(1): 830-840. doi: 10.1080/07853890.2021.1927168
8. Wu Y, Liu H, Wang X. Cardioprotection of pharmacological postconditioning on myocardial ischemia/reperfusion injury. Life Sci. 2021; 264: 118628. doi: 10.1016/j.lfs.2020.118628
9. Maida CD, Norrito RL, Daidone M. Neuroinflammatory mechanisms in ischemic stroke: Focus on cardioembolic stroke, background, and therapeutic approaches. Int J Mol Sci. 2020; 21(18): 6454. doi: 10.3390/ijms21186454
10. Morton AB, Jacobsen NL, Segal SS. Functionalizing biomaterials to promote neurovascular regeneration following skeletal muscle injury. Am J Physiol Cell Physiol. 2021; 320(6): C1099-C1111. doi: 10.1152/ajpcell.00501.2020
11. Gonçalves RC, Banfi A, Oliveira MB. Strategies for revascularization and promotion of angiogenesis in trauma and disease. Biomaterials. 2021; 269: 120628. doi: 10.1016/j.biomaterials.2020.120628
12. László A, Lénárt L, Illésy L. The role of neurotrophins in psychopathology and cardiovascular diseases: Psychosomatic connections. J Neural Transm (Vienna). 2019; 126(3): 265-278. doi: 10.1007/s00702-019-01973-6
13. Kotlega D, Zembron-Lacny A, Morawin B. Free fatty acids and their inflammatory derivatives affect BDNF in stroke patients. Mediators Inflamm. 2020; 2020: 6676247. doi: 10.1155/2020/6676247
14. Jamali A, Shahrbanian S, Morteza Tayebi S. The effects of exercise training on the brain-derived neurotrophic factor (BDNF) in the patients with type 2 diabetes: A systematic review of the randomized controlled trials. J Diabetes Metab Disord. 2020; 19(1): 633-643. doi: 10.1007/s40200-020-00529-w
15. Wang J, Amidfar M, Eyileten C. Nerve growth factor in metabolic complications and Alzheimer’s disease: Physiology and therapeutic potential. Biochim Biophys Acta Mol Basis Dis. 2020; 1866(10): 165858. doi: 10.1016/j.bbadis.2020.165858
16. Xue Y, Liang H, Yang R. The role of pro- and mature neurotrophins in the depression. Behav Brain Res. 2021; 404: 113162. doi: 10.1016/j.bbr.2021.113162
17. Hang PZ, Zhu H, Li PF. The emerging role of BDNF/TrkB signaling in cardiovascular diseases. Life (Basel). 2021; 11(1): 70. doi: 10.3390/life11010070
18. Halloway S, Jung M, Yeh AY. An integrative review of brain-derived neurotrophic factor and serious cardiovascular conditions. Nurs Res. 2020; 69(5): 376-390. doi: 10.1097/NNR.0000000000000454
19. Wise BL, Seidel MF, Lane NE. The evolution of nerve growth factor inhibition in clinical medicine. Nat Rev Rheumatol. 2021; 17(1): 34-46. doi: 10.1038/s41584-020-00528-4
20. Pius-Sadowska E, Machaliński B. Pleiotropic activity of nerve growth factor in regulating cardiac functions and counteracting pathogenesis. ESC Heart Fail. 2021; 8(2): 974-987. doi: 10.1002/ehf2.13138
21. Li R, Xu J, Rao Z. Facilitate angiogenesis and neurogenesis by growth factors integrated decellularized matrix hydrogel. Tissue Eng Part A. 2021; 27(11-12): 771-787. doi: 10.1089/ten.TEA.2020.0227
22. Yan T, Zhang Z, Li D. NGF receptors and PI3K/AKT pathway involved in glucose fluctuation-induced damage to neurons and alpha-lipoic acid treatment. BMC Neuroscience. 2020; 21(1): 38. doi: 10.1186/s12868-020-00588-y
23. Xu F, Na L, Li Y. Roles of the PI3K/AKT/mTOR signalling pathways in neurodegenerative diseases and tumours. Cell Biosci. 2020; 10: 54. doi: 10.1186/s13578-020-00416-0
24. Baldassarro VA, Lorenzini L, Bighinati A. NGF and endogenous regeneration: From embryology toward therapies. Adv Exp Med Biol. 2021; 1331: 51-63. doi: 10.1007/978-3-030-74046-7_5
25. Dahlström M, Nordvall G, Sundström E. Identification of amino acid residues of nerve growth factor important for neurite outgrowth in human dorsal root ganglion neurons. Eur J Neurosci. 2019; 50: 3487-3501. doi: 10.1111/ejn.14513
26. Testa G, Cattaneo A, Capsoni S. Understanding pain perception through genetic painlessness diseases: The role of NGF and proNGF. Pharmacol Res. 2021; 169: 105662. doi: 10.1016/j.phrs.2021.105662
27. Grassi G, Quarti-Trevano F, Esler MD. Sympathetic activation in congestive heart failure: An updated overview. Heart Fail Rev. 2021; 26(1): 173-182. doi: 10.1007/s10741-019-09901-2
28. Ceci FM, Ferraguti G, Petrella C, Greco A, Tirassa P, Iannitelli A, et al. Nerve growth factor, stress and diseases. Curr Med Chem. 2021; 28(15): 2943-2959. doi: 10.2174/0929867327999200818111654
29. Wang Y, Tan J, Yin J, Hu H, Shi Y, Wang Y, et al. Targeting blockade of nuclear factor-kappaB in the hypothalamus paraventricular nucleus to prevent cardiac sympathetic hyperinnervation post myocardial infarction. Neurosci Lett. 2019; 707: 134319. doi: 10.1016/j.neulet.2019.134319
30. Oliveira ÍM, Silva Júnior ELD, Martins YO, Rocha HAL, Scanavacca MI, Gutierrez PS. Cardiac autonomic nervous system remodeling may play a role in atrial fibrillation: A study of the autonomic nervous system and myocardial receptors. Arq Bras Cardiol. 2021; 117(5): 999-1007. doi: 10.36660/abc.20200725
31. Gussak G, Pfenniger A, Wren L, Gilani M, Zhang W, Yoo S, et al. Region-specific parasympathetic nerve remodeling in the left atrium contributes to creation of a vulnerable substrate for atrial fibrillation. JCI Insight. 2019; 4(20): e130532. doi: 10.1172/jci.insight.130532
32. Yang M, Zhang S, Liang J, Tang Y, Wang X, Huang C, et al. Different effects of norepinephrine and nerve growth factor on atrial fibrillation vulnerability. J Cardiol. 2019; 74: 460-465. doi: 10.1016/j.jjcc.2019.04.009
33. Wang Z, Li S, Lai H, Zhou L, Meng G, Wang M, et al. Interaction between endothelin-1 and left stellate ganglion activation: A potential mechanism of malignant ventricular arrhythmia during myocardial ischemia. Oxid Med Cell Longev. 2019; 2019: 6508328. doi: 10.1155/2019/6508328
34. Jie X, Yang H, Wang K, Zhu ZF, Wang JP, Yang LG, et al. Apocynin prevents reduced myocardial nerve growth factor, contributing to amelioration of myocardial apoptosis and failure. Clin Exp Pharmacol Physiol. 2021; 48(5): 704-716. doi: 10.1111/1440-1681.13465
35. Cheng XY, Chen C, He SF, Huang CX, Zhang L, Chen ZW, et al. Spinal NGF induces anti-intrathecal opioid-initiated cardioprotective effect via regulation of TRPV1 expression. Eur J Pharmacol. 2019; 844: 145-155. doi: 10.1016/j.ejphar.2018.12.007
36. van der Bijl P, Abou R, Goedemans L, Gersh BJ, Holmes DR Jr, Ajmone Marsan N, et al. Left ventricular post-infarct remodeling: Implications for systolic function improvement and outcomes in the modern era. JACC Heart Fail. 2020; 8(2): 131-140. doi: 10.1016/j.jchf.2019.08.014
37. Schuttler D, Clauss S, Weckbach LT, Brunner S. Molecular mechanisms of cardiac remodeling and regeneration in physical exercise. Cells. 2019; 8(10): 1128. doi: 10.3390/cells8101128
38. Smit M, Coetzee AR, Lochner A. The pathophysiology of myocardial ischemia and perioperative myocardial infarction. J Cardiothorac Vasc Anesth. 2020; 34(9): 2501-2512. doi: 10.1053/j.jvca.2019.10.00
39. Lin Y, Ding S, Chen Y, Xiang M, Xie Y. Cardiac adipose tissue contributes to cardiac repair: A review. Stem Cell Rev Rep. 2021; 17(4): 1137-1153. doi: 10.1007/s12015-020-10097-4
40. Revelo X, Parthiban P, Chen C, Barrow F, Fredrickson G, Wang H, et al. Cardiac resident macrophages prevent fibrosis and stimulate angiogenesis. Circ Res. 2021; 129(12): 1086-1101. doi: 10.1161/CIRCRESAHA.121.319737
41. Jenča D, Melenovský V, Stehlik J, Staněk V, Kettner J, Kautzner J, et al. Heart failure after myocardial infarction: Incidence and predictors. ESC Heart Fail. 2021; 8(1): 222-237. doi: 10.1002/ehf2.13144
42. Yu TS, Ge LZ, Cao JM. Research advances in sympathetic remodeling after myocardial infarction and its significance in forensic science. Fa Yi Xue Za Zhi. 2019; 35(1): 68-73. doi: 10.12116/j.issn.1004-5619.2019.01.013
43. Kosmas N, Manolis AS, Dagres N, Iliodromitis EK. Myocardial infarction or acute coronary syndrome with non-obstructive coronary arteries and sudden cardiac death: A missing connection. Europace. 2020; 22(9): 1303-1310. doi: 10.1093/europace/euaa156
44. Lyu J, Wang M, Kang X, Xu H, Cao Z, Yu T, et al. Macrophagemediated regulation of catecholamines in sympathetic neural remodeling after myocardial infarction. Basic Res Cardiol. 2020; 115(5): 56. doi: 10.1007/s00395-020-0813-3
45. Kytikova OY, Novgorodtseva TP, Antonyuk MV, Gvozdenko TA. The role of regulatory neuropeptides and neurotrophic factors in asthma pathophysiology. Russian Open Medical Journal. 2019; 8(4): e0402. doi: 10.15275/rusomj.2019.0402
46. Cuello AC. Levi-Montalcini R. NGF metabolism in health and in the Alzheimer’s pathology. Adv Exp Med Biol. 2021; 1331: 119-144. doi: 10.1007/978-3-030-74046-7_9
47. Paoletti F, Merzel F, Cassetta A, Ogris I, Covaceuszach S, Grdadolnik J, et al. Endogenous modulators of neurotrophin signaling: Landscape of the transient ATP-NGF interactions. Comput Struct Biotechnol J. 2021; 19: 2938-2949. doi: 10.1016/j.csbj.2021.05.009
48. Yamashita N. NGF signaling in endosomes. Adv Exp Med Biol. 2021; 1331: 19-29. doi: 10.1007/978-3-030-74046-7_3
49. Rowe CW, Dill T, Faulkner S, Gedye C, Paul JW, Tolosa JM, et al. The precursor for nerve growth factor (proNGF) in thyroid cancer lymph node metastases: Correlation with primary tumour and pathological variables. Int J Mol Sci. 2019; 20(5924). doi: 10.3390/ijms20235924
50. Kendall A, Nyström S, Ekman S, Hultén LM, Lindahl A, Hansson E, et al. Nerve growth factor in the equine joint. Vet J. 2021; 267: 105579. doi: 10.1016/j.tvjl.2020.105579
51. Liu Z, Wu H, Huang S. Role of NGF and its receptors in wound healing (Review). Exp Ther Med. 2021; 21(6): 599. doi: 10.3892/etm.2021.10031
52. Seidel MF, Lane NE. The evolution of nerve growth factor inhibition in clinical medicine. Nat Rev Rheumatol. 2021; 17(1): 34-46. doi: 10.1038/s41584-020-00528-4
53. Kang L, Andersen ND, Turek JW. Commentary: Connecting the dots: Coronary artery development as a combination of vasculogenesis and angiogenesis. J Thorac Cardiovasc Surg. 2021: S0022-5223(21)01224-1. doi: 10.1016/j.jtcvs.2021.08.026
54. Wu X, Reboll MR, Korf-Klingebiel M, Wollert KC. Angiogenesis after acute myocardial infarction. Cardiovasc Res. 2021; 117(5): 1257-1273. doi: 10.1093/cvr/cvaa287
55. Kurotsu S, Osakabe R, Isomi M, Tamura F, Sadahiro T, Muraoka N, et al. Distinct expression patterns of Flk1 and Flt1 in the coronary vascular system during development and after myocardial infarction. Biochem Biophys Res Commun. 2019; 495: 884-891. doi: 10.1016/j.bbrc.2017.11.094
56. Ferraro B, Leoni G, Hinkel R, Ormanns S, Paulin N, Ortega-Gomez A, et al. Pro-angiogenic macrophage phenotype to promote myocardial repair. J Am Coll Cardiol. 2019; 73: 2990-3002. doi: 10.1016/j.jacc.2019.03.503
57. Yang S, Cheng J, Man C, Jiang L, Long G, Zhao W, et al. Effects of exogenous nerve growth factor on the expression of BMP-9 and VEGF in the healing of rabbit mandible fracture with local nerve injury. J Orthop Surg Res. 2021; 16(1): 74. doi: 10.1186/s13018-021-02220-z
58. Julian K, Prichard B, Raco J, Jain R, Jain R. A review of cardiac autonomics: From pathophysiology to therapy. Future Cardiol. 2022; 18(2): 125-133. doi: 10.2217/fca-2021-0041
59. Kusayama T, Wan J, Yuan Y, Chen PS. Neural mechanisms and therapeutic opportunities for atrial fibrillation. Methodist Debakey Cardiovasc J. 2021; 17(1): 43-47. doi: 10.14797/FVDN2224
60. Shah R, Assis F, Alugubelli N, Okada DR, Cardoso R, Shivkumar K, et al. Cardiac sympathetic denervation for refractory ventricular arrhythmias in patients with structural heart disease: A systematic review. Heart Rhythm. 2019; 16(10): 1499-1505. doi: 10.1016/j.hrthm.2019.06.018
61. Aksu T, Gupta D, Pauza DH. Anatomy and physiology of intrinsic cardiac autonomic nervous system: Da Vinci anatomy card #2. JACC Case Rep. 2021; 3(4): 625-629. doi: 10.1016/j.jaccas.2021.02.018
62. Moss A, Robbins S, Achanta S, Kuttippurathu L, Turick S, Nieves S, et al. A single cell transcriptomics map of paracrine networks in the intrinsic cardiac nervous system. iScience. 2021; 24(7): 102713. doi: 10.1016/j.isci.2021.102713
63. Kusayama T, Wan J, Yuan Y, Chen PS. Neural mechanisms and therapeutic opportunities for atrial fibrillation. Methodist Debakey Cardiovasc J. 2021; 17(1): 43-47. doi: 10.14797/FVDN2224
64. Kotalczyk A, Mazurek M, Kalarus Z, Potpara TS, Lip GYH. Stroke prevention strategies in high-risk patients with atrial fibrillation. Nat Rev Cardiol. 2021; 18(4): 276-290. doi: 10.1038/s41569-020-00459-3
65. Sethwala AM, Goh I, Amerena JV. Combating inflammation in cardiovascular disease. Heart Lung Circ. 2021; 30(2): 197-206. doi: 10.1016/j.hlc.2020.09.003
66. Hutchings G, Kruszyna Ł, Nawrocki MJ, Strauss E, Bryl R, Spaczyńska J, et al. Molecular mechanisms associated with ROSdependent angiogenesis in lower extremity artery disease. Antioxidants (Basel). 2021; 10(5): 735. doi: 10.3390/antiox10050735
67. Bostan MM, Stătescu C, Anghel L, Șerban IL, Cojocaru E, Sascău R. Post-myocardial infarction ventricular remodeling biomarkers – The key link between pathophysiology and clinic. Biomolecules. 2020; 10(11): 1587. doi: 10.3390/biom10111587
68. Henning RJ. Cardiovascular exosomes and MicroRNAs in cardiovascular physiology and pathophysiology. J Cardiovasc Transl Res. 2021; 14(2): 195-212. doi: 10.1007/s12265-020-10040-5
69. Hu Y, Xiong J, Wen H, Wei H, Zeng X. MiR-98-5p promotes ischemia/reperfusion-induced microvascular dysfunction by targeting NGF and is a potential biomarker for microvascular reperfusion. Microcirculation. 2021; 28(1): e12657. doi: 10.1111/micc.12657
70. Zhao W, Zhao J, Rong J. Pharmacological modulation of cardiac remodeling after myocardial infarction. Oxid Med Cell Longev. 2020; 2020: 8815349. doi: 10.1155/2020/8815349
71. Pentz R, Iulita MF. The NGF metabolic pathway: New opportunities for biomarker research and drug target discovery: NGF pathway biomarkers and drug targets. Adv Exp Med Biol. 2021; 1331: 31-48. doi: 10.1007/978-3-030-74046-7_4
72. Gudasheva TA, Povarnina PY, Tarasiuk AV, Seredenin SB. Low-molecular mimetics of nerve growth factor and brain-derived neurotrophic factor: Design and pharmacological properties. Med Res Rev. 2020; 41(5): 2746-2774. doi: 10.1002/med.21721
73. Luo W, Gong Y, Qiu F, Yuan Y, Jia W, Liu Z, et al. NGF nanoparticles enhance the potency of transplanted human umbilical cord mesenchymal stem cells for myocardial repair. Am J Physiol Heart Circ Physiol. 2021; 320(5): H1959-H1974. doi: 10.1152/ajpheart.00855.2020
74. Saragovi HU, Galan A, Levin LA. Neuroprotection: Prosurvival and anti-neurotoxic mechanisms as therapeutic strategies in neurodegeneration. Front Cell Neurosci. 2019; 13: 231. doi: 10.3389/fncel.2019.00231
75. Dobbin SJH, Petrie MC, Myles RC, Touyz RM, Lang NN. Cardiotoxic effects of angiogenesis inhibitors. Clin Sci (Lond). 2021; 135(1): 71-100. doi: 10.1042/CS20200305
Review
For citations:
Kytikova O.Yu., Novgorodtseva T.P., Antonyuk М.V., Denisenko Yu.K., Atamas O.V. Nerve growth factor and post-infarction cardiac remodeling. Acta Biomedica Scientifica. 2022;7(2):113-124. (In Russ.) https://doi.org/10.29413/ABS.2022-7.2.13