UDC

611-018.2:616.127-005.8-002.17-06:612.67

Authors

Anna N. Putyatina*, Lena B. Kim*
*Research Institute of Experimental and Clinical Medicine (Novosibirsk, Russian Federation)

Abstract

Complications of myocardial infarction quite often cause deaths and make the treatment of myocardial infarction much more difficult, especially in the elderly. Age-dependent modification of reparative fibrosis seems to underlie a worse prognosis in complicated myocardial infarction. This review attempts to characterize the most frequent complications of the disease on the basis of selected markers of reparative fibrosis. The mechanisms involved in the development of myocardial infarction complications are also covered. In addition, the article points out the changes in the levels of individual markers of reparative fibrosis and local regulation system in human and animal tissue and biological liquids. These changes cause modifications in postinfarction reparative fibrosis. In particular, collagen metabolism is increased in acute heart failure; at the same time the content of sulfated glycosaminoglycans rises when matrix metalloproteinase-2 and tissue inhibitor of matrix metalloproteinase-1 are activated. Moreover, increased collagen and proteoglycan metabolism as well as lower fibronectin content are observed against the background of higher level of tissue inhibitor of matrix metalloproteinase-1 when heart rhythm is disturbed. In heart aneurism, there is an accelerated degradation of collagen with low levels of sulfated glycosaminoglycans and matrix metalloproteinase-9 and a high level of tissue inhibitor of matrix metalloproteinase-1. In cardiac rupture, possibly due to tenascin C stimulation, the content of matrix metalloproteinase-8 and -9 increases, which may disrupt the connection between cardiomyocytes and the extracellular matrix. Further, it was shown that changes in titin level and in its association with cardiomyocyte contractile proteins and collagen can promote fibrosis as well as diastolic and systolic dysfunction. These findings provide completely new insights into the role of reparative fibrosis markers in pathological remodelling of cardiac extracellular matrix in complicated disease. To find pharmacological targets and develop a timely treatment strategy in adverse outcomes we need to study metabolism regulation of extracellular matrix components in complicated myocardial infarction.

Keywords

myocardial infarction complications, reparative fibrosis, collagens, proteoglycans, fibronectin

References

1. Latfullin I.A., Podol’skaya A.A., Aglullina E.I. Infarkt miokarda u lits pozhilogo i starcheskogo vozrasta [Myocardial Infarction in the Elderly and the Senile]. Klinicheskaya gerontologiya, 2002, vol. 8, no. 7, pp. 40–45.
   
2. Pankin O.A. Dogospital’nye faktory bol’nichnoy letal’nosti pri infarkte miokarda [Prehospital Factors of Hospital Lethality in Myocardial Infarction]. Klinicheskaya meditsina, 2004, vol. 82, no. 4, pp. 36–40.
   
3. Rich M.W. Epidemiology, Clinical Features, and Prognosis of Acute Myocardial Infarction in the Elderly. Am. J. Geriatr. Cardiol., 2008, vol. 15, no. 1, pp. 7–13.
   
4. Savilova V.V., Kondrat’ev A.I., Dolgikh V.T., Toropov A.V. Kriticheskie sostoyaniya pri infarkte miokarda [Critical Conditions During Myocardial Infarction]. Kazanskiy meditsinskiy zhurnal, 2007, vol. 88, no. S5, pp. 177–179.
   
5. Rukovodstvo po kardiologii [Guidelines on Cardiology]. Vol. 1. Ed. by G.I. Strozhakov, A.A. Gorbachenkov. Moscow, 2008. 672 p.
   
6. Kim L.B. Sposob prognozirovaniya razvitiya oslozhneniy infarkta miokarda [A Method for Predicting Complications of Myocardial Infarction]. Patent RF 2373542, 2009.
   
7. Kim L.B., Putyatina A.N. Dinamika biokhimicheskikh markerov reparativnogo fibroza pri oslozhnennom techenii infarkta miokarda [Dynamics of Biochemical Markers of Reparative Fibrosis in Uncomplicated Course of Myocardial Infarction]. Kardiologiya, 2010, vol. 50, no. 12, pp. 10–14.
   
8. Sabatin M.S., O’Gara P.T., Lili L.S. Ostryy infarkt miokarda [Acute Myocardial Infarction]. Patofiziologiya zabolevaniy serdechno-sosudistoy sistemy [Pathophysiology of Cardiovascular Diseases]. Moscow, 2003, pp. 199–234.
   
9. Sutton M.G., Sharpe N. Left Ventricular Remodeling After Myocardial Infarction: Pathophysiology and Therapy. Circulation, 2000, vol. 101, no. 25, pp. 2981–2988.
   
10. Jugdutt B.I. Extracellular Matrix and Cardiac Remodeling. Interstitial Fibrosis in Heart Failure. Ed. by F.J. Villarreal. New York, 2005. Vol. 253, pp. 23–55.
    
11. Malaya L.T., Vlasenko M.A., Miklyaev I.Yu. Infarkt miokarda [Myocardial Infarction]. Moscow, 1981. 487 p.
    
12. Valeeva R.M., Leshchinskiy L.A. Osobennosti kliniki, diagnostiki i terapii infarkta miokarda u lits starshey vozrastnoy gruppy [Clinical Features, Diagnosis and Treatment of Myocardial Infarction in Older Adults]. Klinicheskaya gerontologiya, 2001, vol. 7, no. 5–6, pp. 53–56.
    
13. Govorin A.V., Ratsina E.V., Fetisova N.V., Sokolova N.A. Soderzhanie v krovi biomarkerov kollagena i sul’fatirovannykh glikozaminoglikanov u bol’nykh ostrym transmural’nym infarktom miokarda [Blood Level of Collagen Biomarkers and Sulfated Glycosaminoglycans in Acute Transmural Myocardial Infarction]. Rossiyskiy kardiologicheskiy zhurnal, 2016, no. 3, pp. 75–79.
    
14. Biolo A., Fisch M., Balog J., Chao T., Schulze P.C., Ooi H., Siwik D., Colucci W.S. Episodes of Acute Heart Failure Syndrome Are Associated with Increased Levels of Troponin and Extracellular Matrix Markers. Circ. Heart Fail., 2010, vol. 3, no. 1, pp. 44–50.
    
15. Kolesnik M.Yu. Osobennosti ekspressii regulyatornogo belka taytina i kollagena I tipa v miokarde spontanno gipertenzivnykh krys s eksperimental’nym sakharnym diabetom [Peculiarities of the Expression of Regulatory Protein Titin and Collagen I in Myocardium of Spontaneously Hypertensive Rats with Experimental Diabetes Mellitus]. Patologiya, 2013, no. 2, pp. 31–35.
    
16. Fukuda N., Terui T., Ishiwata S., Kurihara S. Titin-Based Regulations of Diastolic and Systolic Functions of Mammalian Cardiac Muscle. J. Mol. Cell. Cardiol., 2010, vol. 48, no. 5, pp. 876–881.
    
17. Visse R., Nagase H. Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases: Structure, Function, and Biochemistry. Circ. Res., 2003, vol. 92, no. 8, pp. 827–839.
    
18. Sawicki G. Intracellular Regulation of Matrix Metalloproteinase-2 Activity: New Strategies in Treatment and Protection of Heart Subjected to Oxidative Stress. Scientifica (Cairo), 2013, vol. 2013. Art. ID 130451.
    
19. Bogomolovas J., Gasch A., Bajoras V., Karčiauskaitė D., Šerpytis P., Grabauskienė V., Labeit D., Labeit S. Cardiac Specific Titin N2B Exon Is a Novel Sensitive Serological Marker for Cardiac Injury. Int. J. Cardiol., 2016, vol. 212, pp. 232–234.
    
20. Chatzikyriakou S.V., Tziakas D.N., Chalikias G.K., Stakos D.A., Thomaidi A.K., Mitrousi K., Lantzouraki A.E., Kotsiou S., Maltezos E., Boudoulas H. Resolution of Symptoms and Serum Peptides of Collagen Type I Turnover in Acute Heart Failure Patients. Acta Cardiol., 2009, vol. 64, no. 1, pp. 29–33.
    
21. Høst N.B., Jensen L.T., Bendixen P.M., Jensen S.E., Koldkjaer O.G., Simonsen E.E. The Aminoterminal Propeptide of Type III Procollagen Provides New Information on Prognosis After Acute Myocardial Infarction. Am. J. Cardiol., 1995, vol. 76, no. 12, pp. 869–873.
    
22. Hortells Aznar J.L., Ibáñez Estella J.A., Pérez de Viñaspre Adrados S., Atance Martínez J.C., Larraz Mur L., Lasierra Díaz M.P. Plasma Concentrations of Fibronectin in Septic, Hypovolemic, and Cardiogenic Shock. Prognostic Usefulness of Their Variation. Med. Clin. (Barc.), 1992, vol. 99, no. 5, pp. 172–174.
    
23. Voevodina N.Yu., Zhuravleva I.A., Nikiforova L.A., Arutyunov G.P. Rol’ markerov vospaleniya v otsenke klinicheskogo techeniya infarkta miokarda [The Role of Inflammatory Markers in the Evaluation of the Clinical Course of Myocardial Infarction]. Kardiologiya, 1990, vol. 30, no. 9, pp. 20–22.
    
24. Akchurin R.S., Borisenko A.P., Burakovskiy V.I. Bolezni serdtsa i sosudov: v 4 t. T. 2 [Cardiovascular Diseases: In 4 Vols. Vol. 2]. Moscow, 1992. 512 p.
    
25. Semisotova E.F. Infarkt miokarda u lyudey pozhilogo i starcheskogo vozrasta [Myocardial Infarction in the Elderly and the Senile]. Vladivostok, 1994. 167 p.
    
26. Banerjee I., Yekkala K., Borg T.K., Baudino T.A. Dynamic Interactions Between Myocytes, Fibroblasts, and Extracellular Matrix. Ann. N. Y. Acad. Sci., 2006, vol. 1080, pp. 76–84.
    
27. Zhang P., Su J., Mende U. Cross Talk Between Cardiac Myocytes and Fibroblasts: From Multiscale Investigative Approaches to Mechanisms and Functional Consequences. Am. J. Physiol. Heart Circ. Physiol., 2012, vol. 303, no. 12, pp. H1385–H1396.
    
28. Camelliti P., Borg T.K., Kohl P. Structural and Functional Characterisation of Cardiac Fibroblasts. Cardiovasc. Res., 2005, vol. 65, no. 1, pp. 40–51.
    
29. Porter K.E., Turner N.A. Cardiac Fibroblasts: At the Heart of Myocardial Remodeling. Pharmacol. Ther., 2009, vol. 123, no. 2, pp. 255–278.
    
30. Fan D., Takawale A., Lee J., Kassiri Z. Cardiac Fibroblasts, Fibrosis and Extracellular Matrix Remodeling in Heart Disease. Fibrogenesis Tissue Repair, 2012, vol. 5, no. 1, p. 15.
    
31. Stolyarov V.V., Usynin A.F., Zuevskiy V.P. Patomorfologicheskiy analiz provodyashchey sistemy serdtsa pri infarkte miokarda [Pathomorphological Analysis of the Cardiac Conduction System in Myocardial Infarction]. Sibirskiy konsilium, 2005, no. 4, pp. 29–31.
    
32. Elmas E., Lang S., Dempfle C.E., Kälsch T., Hannak D., Sueselbeck T., Wolpert C., Borggrefe M., Brueckmann M. High Plasma Levels of Tissue Inhibitor of Metalloproteinase-1 (TIMP-1) and Interleukin-8 (IL-8) Characterize Patients Prone to Ventricular Fibrillation Complicating Myocardial Infarction. Clin. Chem. Lab. Med., 2007, vol. 45, no. 10, pp. 1360–1365.
    
33. Flevari P., Theodorakis G., Leftheriotis D., Kroupis C., Kolokathis F., Dima K., Anastasiou-Nana M., Kremastinos D. Serum Markers of Deranged Myocardial Collagen Turnover: Their Relation to Malignant Ventricular Arrhythmias in Cardioverter-Defibrillator Recipients with Heart Failure. Am. Heart J., 2012, vol. 164, no. 4, pp. 530–537.
    
34. Heymans S., Schroen B., Vermeersch P., Milting H., Gao F., Kassner A., Gillijns H., Herijgers P., Flameng W., Carmeliet P., Van de Werf F., Pinto Y.M., Janssens S. Increased Cardiac Expression of Tissue Inhibitor of Metalloproteinase-1 and Tissue Inhibitor of Metalloproteinase-2 Is Related to Cardiac Fibrosis and Dysfunction in the Chronic Pressure-Overloaded Human Heart. Circulation, 2005, vol. 112, no. 8, pp. 1136–1344.
    
35. Knowlton A.A., Connelly C.M., Romo G.M., Mamuya W., Apstein C.S., Brecher P. Rapid Expression of Fibronectin in the Rabbit Heart After Myocardial Infarction with and Without Reperfusion. J. Clin. Invest., 1992, vol. 89, no. 4, pp. 1060–1068.
    
36. Ohkawa S.I., Sugiura M., Hata R., Nagai Y. Acidic Glycosaminoglycans in Urine, Serum and Myocardium of Aged Patients with Myocardial Infarction. J. Mol. Cell. Cardiol., 1977, vol. 9, no. 7, pp. 541–550.
    
37. Castagnino H.E., Toranzos F.A. Ventricular Aneurysms: A Geometrical-Dynamical Model. Jpn. J. Exp. Med., 1989, vol. 59, no. 3, pp. 89–102.
    
38. Weis S.M., Zimmerman S.D., Shah M., Covell J.W., Omens J.H., Ross J. Jr., Dalton N., Jones Y., Reed C.C., Iozzo R.V., McCulloch A.D. A Role for Decorin in the Remodeling of Myocardial Infarction. Matrix Biol., 2005, vol. 24, no. 4, pp. 313–324.
    
39. Shekhonin B.V., Gurevich S.B., Irdashev Sh.B., Kotelyanskiy V.E. Fibronektin i fibrinogen/fibrin v ochage eksperimental’nogo infarkta miokarda [Fibronectin and Fibrinogen/Fibrin in the Focus of Experimental Myocardial Infarction]. Arkh. patologii, 1989, vol. 51, no. 9, pp. 14–20.
    
40. Branishte T.A., Sokolova R.I., Zhdanov V.S., Cherpachenko N.M., Khodareva E.N., Tsyplenkova V.G., Skridlevskaya E.A., Naumov V.G., Akchurin R.S. Apoptoz i gibernatsiya kardiomiotsitov perirubtsovoy zony kak faktor progressirovaniya khronicheskoy anevrizmy serdtsa [Apoptosis and Hibernation of Cardiomyocytes of Periscar Zone as Factor of Chronic Cardiac Aneurysm Progression]. Kardiologiya, 2004, vol. 44, no. 5, pp. 4–7.
    
41. Beltrami A.P., Urbanek K., Kajstura J., Yan S.M., Finato N., Bussani R., Nadal-Ginard B., Silvestri F., Leri A., Beltrami C.A., Anversa P. Evidence that Human Cardiac Myocytes Divide After Myocardial Infarction. N. Engl. J. Med. 2001, vol. 344, no. 23, pp. 1750–1757.
    
42. Jensen L.T., Hørslev-Petersen K., Toft P., Bentsen K.D., Grande P., Simonsen E.E., Lorenzen I. Serum Aminoterminal Type III Procollagen Peptide Reflects Repair After Acute Myocardial Infarction. Circulation, 1990, vol. 81, no. 1, pp. 52–57.
    
43. Kyselov S.M. Gender Peculiarities and Prognostic Value of Matrix Metalloproteinase and Their Inhibitors System in Patients with Acute Q-Wave Left Ventricle Myocardial Infarction. Zaporozhye Med. J., 2015, no. 1, pp. 9–13.
    
44. Govorin A.V., Ratsina E.V., Sokolova N.A., Fetisova N.V. Soderzhanie v krovi matriksnoy metalloproteinazy-9, tkanevogo ingibitora metalloproteinaz-1 i biomarkerov kollagena u patsientov s ostrym transmural’nym infarktom miokarda, oslozhnennym anevrizmoy [Blood Levels of Matrix Metalloproteinase-9, Tissue Inhibitor of Metalloproteases-1, and Collagen Biomarkers in Patients with Acute Transmural Myocardial Infarction Complicated with Aneurysm]. Serdtse: zhurnal dlya praktikuyushchikh vrachey, 2015, vol. 14, no. 1, pp. 30–33.
    
45. Zeltyn’-Abramov E.M. Razryvy serdtsa pri ostrom infarkte miokarda (obzor literatury) [Cardiac Rupture in Acute Myocardial Infarction (Review)]. Sibirskiy medisinskiy zhurnal, 2010, vol. 25, no. 4-1, pp. 14–22.
    
46. Anzai T. Post-Infarction Inflammation and Left Ventricular Remodeling: A Double-Edged Sword. Circ. J., 2013, vol. 77, no. 3, pp. 580–587.
    
47. Golofeevskiy V.Yu., Inozemtsev S.A., Sotnikov A.V., Yakovlev V.V., Bessonova N.A. Faktory riska infarkta miokarda u patsientov molodogo i srednego vozrasta [Myocardial Infarction Development Hazards in Young and Middle-Aged Patients]. Vestnik Sankt-Peterburgskogo universiteta. Ser. 11: Meditsina, 2007, no. 3, pp. 3–10.
    
48. van den Borne S.W., Cleutjens J.P., Hanemaaijer R., Creemers E.E., Smits J.F., Daemen M.J., Blankesteijn W.M. Increased Matrix Metalloproteinase-8 and -9 Activity in Patients with Infarct Rupture After Myocardial Infarction. Cardiovasc. Pathol., 2009, vol. 18, no. 1, pp. 37–43.
    
49. Tao Z.Y., Cavasin M.A., Yang F., Liu Y.H., Yang X.P. Temporal Changes in Matrix Metalloproteinase Expression and Inflammatory Response Associated with Cardiac Rupture After Myocardial Infarction in Mice. Life Sci., 2004, vol. 74, no. 12, pp 1561–1572.
    
50. Berezin A.E. Regulyatory aktivnosti matriksnykh metalloproteinaz kak novye biologicheskie markery kardiovaskulyarnogo remodelirovaniya (obzor literatury) [Matrix Metalloproteinase Activity Regulators as New Biological Markers of Cardiovascular Remodelling (Literature Review)]. Ukrainskiy meditsinskiy zhurnal, 2011, no. 1, pp. 36–42.
    
51. Matsui Y., Morimoto J., Uede T. Role of Matricellular Proteins in Cardiac Tissue Remodeling After Myocardial Infarction. World J. Biol. Chem., 2010, vol. 1, no. 5, pp. 69–80.
    
52. Cavasin M.A., Tao Z., Menon S., Yang X.P. Gender Differences in Cardiac Function During Early Remodeling After Acute Myocardial Infarction in Mice. Life Sci., 2004, vol. 75, no. 18, pp. 2181–2192.
    
53. Fang L., Gao X.M., Moore X.L., Kiriazis H., Su Y., Ming Z., Lim Y.L., Dart A.M., Du X.J. Differences in Inflammation, MMP Activation and Collagen Damage Account for Gender Difference in Murine Cardiac Rupture Following Myocardial Infarction. J. Mol. Cell. Cardiol., 2007, vol. 43, no. 5, pp. 535–544.
    
54. Kim L.B. Biokhimicheskie aspekty postinfarktnogo remodelirovaniya levogo zheludochka pri arterial’noy gipertenzii i nedifferentsirovannoy displazii soedinitel’noy tkani [Biochemical Aspects of Post-Infarction Remodelling of Left Ventricle in Arterial Hypertension and Non-Differentiated Dysplasia of Connective Tissue]. Kazanskiy meditsinskiy zhurnal, 2007, vol. 88, no. S5, pp. 48–50.
    
55. Kim L.B., Putyatina A.N. Postinfarktnyy reparativnyy fibroz pri lechenii ingibitorami angiotenzinprevrashchayushchego fermenta [Dynamics of Markers of Postinfarction Reparative Fibrosis in Early Treatment with ACE Inhibitors]. Vestnik Novosibirskogo gosudarstvennogo universiteta. Ser.: Biologiya, klinicheskaya meditsina, 2010, vol. 8, no. 1, pp. 79–85.
    
56. Kim L.B., Layvin A.N., Berezovskaya G.A., Tsyba L.P., Bakhtina I.A. Vliyanie organicheskikh nitratov na skorost’ reparativnogo fibroza i aktivnost’ reaktsii perekisnogo okisleniya lipidov u bol’nykh infarktom miokarda [The Influence of Organic Nitrates on the Rate of Reparative Fibrosis and Reaction of Lipid Peroxidation in Patients with Myocardial Infarction]. Sibirskiy konsilium, 2003, no. 2–3, pp. 9–12.
    
57. Ertl G., Frantz S. Healing After Myocardial Infarction. Cardiovasc. Res., 2005, vol. 66, no. 1, pp. 22–32.
    
58. Kopitsa N.P., Belaya N.V., Titarenko N.V. Rol’ matriksnykh metalloproteinaz v patogeneze postinfarktnogo remodelirovaniya levogo zheludochka [The Role of Matrix Metalloproteinases in the Pathogenesis of Post-Infarction Left Ventricular Remodelling]. Mezhdunarodnyy meditsinskiy zhurnal, 2010, vol. 16, no. 4, pp. 55–58.
    
59. Lindsey M.L., Gannon J., Aikawa M., Schoen F.J., Rabkin E., Lopresti-Morrow L., Crawford J., Black S., Libby P., Mitchell P.G., Lee R.T. Selective Matrix Metalloproteinase Inhibition Reduces Left Ventricular Remodeling but Does Not Inhibit Angiogenesis After Myocardial Infarction. Circulation, 2002, vol. 105, no. 6, pp. 753–758.
    
60. Kruglyakov P.V., Sokolova I.B., Polyntseva D.G. Kletochnaya terapiya infarkta miokarda [Cell Therapy for Myocardial Infarction]. Tsitologiya, 2008, vol. 50, no. 6, pp. 521–527.