Apolipoprotein A-I inhibits the increased activities of chitotriosidase and β-glucosaminidase in the liver of mice with BCG-induced tuberculosis inflammation
https://doi.org/10.18699/SSMJ20220605
Abstract
The aim of the investigation was to study the activity of lysosomal chitinases (chitotriosidase and β-glucosaminidase) in the liver of mice using a model of BCG-induced tuberculous inflammation after intravenous administration of apolipoprotein A-I. Material and methods. The study was carried out on male CBA mice weighing 20–22 g. Disseminated tuberculous inflammation was modeled by a single intraperitoneal injection of 0.5 mg of BCG vaccine. The activity of chitinases was determined using fluorescent substrates 4-methylumbelliferyl β-D-N,N′,N′′-triacetylchitotrioside and 4-methylumbelliferyl N-acetyl-β-D-glucosaminide. Results and discussion. BCG-infection of animals after 4 weeks caused a significant increase in the activity of endogenous chitinases in comparison with the control group: chitotriosidase – 3.05 times (p <0.001), β-glucosaminidase – 1.76 times (p <0.01). Intravenous administration of apolipoprotein A-I to animals against the background of BCG infection inhibited the increased enzyme activity, values did not significantly differ from the control values. Conclusions. The results of these studies indicate the ability of apolipoprotein A-I to reduce the increased activity of endogenous lysosomal chitinases in the liver of mice with BCGinduced tuberculous inflammation.
About the Authors
L. M. PolyakovRussian Federation
Lev M. Polyakov, doctor of medical sciences, professor
630117, Novosibirsk, Timakov str., 2
M. V. Kotova
Russian Federation
Mariya V. Kotova
630117, Novosibirsk, Timakov str., 2
N. V. Trifonova
Russian Federation
Natalia V. Trifonova
630117, Novosibirsk, Timakov str., 2
E. I. Soloveva
Russian Federation
Elena I. Soloveva
630117, Novosibirsk, Timakov str., 2
R. A. Knyasev
Russian Federation
Roman A. Knyazev, candidate of biological sciences
630117, Novosibirsk, Timakov str., 2
References
1. Vergne I., Chua J., Lee H., Lucas M., Belisle J., Deretic V. Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA. 2005;102(11):4033–4038. doi: 10.1073/pnas.0409716102
2. Hmama Z., Sendide K., Talal A., Garcia R., Dobos K., Reiner N.E. Quantitative analysis of phagolysosome fusion in intact cells: inhibition by mycobacterial lipoarabinomannan and rescue by an 1alpha,25-dihydroxyvitamin D3-phosphoinositide 3-kinase pathway. J. Cell. Sci. 2004;117(Pt 10):2131–2140. doi: 10.1242/ jcs.01072
3. Pandit S., Roy S., Pillai J., Banerjee S. Formulation and intracellular trafficking of lipid-drug conjugate nanoparticles containing a hydrophilic antitubercular drug for improved intracellular delivery to human macrophages. ACS Omega. 2020;5(9):4433–4448. doi: 10.1021/acsomega.9b03523
4. Суменкова Д.В., Поляков Л.М., Панин Л.Е. Влияние комплекса изониазида с аполипопротеином А-I на активность ферментов лизосом у мышей с моделью туберкулезного воспаления. Эксперим. и клин. фармакол. 2012;75(11):28–30.
5. Sumenkova D.V., Polyakov L.M., Panin L.E. Influence of isoniazid complex with A-I apolipoprotein on activity of lysosomal enzymes in mice with tuberculous inflammation model. Eksperimental’naya i klinicheskaya farmakologiya = Experimental and Clinical Pharmacology. 2012;75(1):29–32. [In Russian].
6. Chua J., Vergne I., Master S., Deretic V. A tale of two lipids: Mycobacterium tuberculosis phagosome maturation arrest. Curr. Opin. Microbiol. 2004;7(1):71– 77. doi: 10.1016/j.mib.2003.12.011
7. Поляков Л.М., Князев Р.А., Котова М.В., Русских Г.С., Соловьева Е.И., Рябченко А.В. Аполипопротеин А-I повышает активность лизосомальных гликозидаз в печени мышей с БЦЖ-индуцированным туберкулезным воспалением. Сиб. науч. мед. ж. 2021;41(6):51–55. doi: 10.18699/ SSMJ20210605
8. Polyakov L.M., Knyazev R.A., Kotova M.V., Russkikh G.S., Solov’eva E.I., Ryabchenko A.V. Apolipoprotein A-I increases the activity of lysosomal glycosidases in the liver of mice with BCG-induced tuberculosis inflammation. Sibirskij nauchnyj medicinskij zhurnal = Siberian Scientific Medical Journal. 2021;41(6):51–55. doi:10.18699/SSMJ20210605
9. Hollak C.E., van Weely S., van Oers M.H., Aerts J.M. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J. Clin. Invest. 1994;93(3):1288–1292. doi: 10.1172/JCI117084
10. Tronsmo A., Harman G.E. Detection and quantification of N-acetyl-beta-D-glucosaminidase, chitobiosidase, and endochitinase in solutions and on gels. Anal. Biochem. 1993;208(1):74–79. doi: 10.1006/ abio.1993.1010
11. Jungbauer C.G., Uecer E., Stadler S., Birner C., Buchner S., Maier L.S., Luchner A. N-acteyl-ß-D-glucosaminidase and kidney injury molecule-1: New predictors for long-term progression of chronic kidney disease in patients with heart failure. Nephrology (Carlton). 2016;21(6):490–498. doi: 10.1111/nep.12632
12. Kim D.H., Park H.J., Lim S., Lee H.G., Koo J.H., Lee H.G., Choi J.O., Oh J.H., Ha S.J., MinJong K, … Choi J.M. Regulation of chitinase-3-like-1 in T cell elicites Th1 nad cytotoxic responses to inhibit lung metastasis. Nat. Commun. 2018;9(1):503. doi: 10.1038/s41467-017-02731-6
13. Turk J., ŞahutoĞlu A.S., Hatice H., Frese S.A., Karav S. Structural insights of two novel N-acetylglucosaminidase enzymes through in silico methods. Turk. J. Chem. 2020;44(6):1703–1712. doi: 10.3906/ kim-2006-19
14. Elmonem M.A., van den Heuvel L.P., Levtchenko E.N. Immunomodulatory effects of chitotriosidase enzyme. Enzyme Res. 2016; 2016:2682680. doi: 10.1155/2016/2682680
15. Tasci C., Tapan S., Ozkaya S., Demirer E., Deniz O., Balkan A., Ozkan M., Inan I., Kurt I., Bilgic H. Efficacy of serum chitotriosidase activity in early treatment of patients with active tuberculosis and a negative sputum smear. Ther. Clin. Risk Manag. 2012;8:369– 372. doi: 10.2147/tcrm.s31752
16. Boot R.G., Blommaart E.F., Swart E., Ghauharali-van der Vlugt K., Bijl N., Moe C., Place A., Aerts J.M. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J. Biol. Chem. 2001;276(9):6770–6778. doi: 10.1074/jbc. M009886200
17. Boot R.G., Renkema G.H., Verhoek M., Strijland A., Bliek J., de Meulemeester T.M., Mannens M.M., Aerts J.M. The human chitotriosidase gene. Nature of inherited enzyme deficiency. J. Biol. Chem. 1998;273(40):25680–25685. doi: 10.1074/ jbc.273.40.25680
18. Bargagli E., Margollicci M., Nikiforakis N., Luddi A., Perrone A., Grosso S., Rottoli G. Chitotriosidase activity in the serum of patients with sarcoidosis and pulmonary tuberculosis. Respiration. 2007;74(5):548–552. doi: 10.1159/000100555
19. Zhu Z., Zheng T., Homer R.J., Kim Y.K., Chen N.Y., Cohn L., Qutayba H.Q., Elias J.A. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science. 2004;304(5677):1678–1682. doi: 10.1126/science.1095336
20. di Rosa M., Brundo V.M., Malaguarnera L. New insights on chitinases immunologic activities. World J. Immunol. 2016;6(2):96–104. doi: 10.4049/ jimmunol.172.3.181
21. Yin K., Chen W.J., Zhou Z.G., Zhao G.J., Lv Y.C., Ouyang X.P., Yu X.H., Fu Y., Jiang Z.S., Tang C.K. Apolipoprotein A-I inhibits CD40 proinflammatory signaling via ATP-binding cassette transporter A1-mediated modulation of lipid raft in macrophages. J. Atheroscler. Thromb. 2012;19(9):823–836. doi: 10.5551/jat.12823
22. Polyakov L.M., Sumenkova D.V., Panin L.E. Effect of plasma lipoproteins and their complexes with polysaccharides on interleukin-1β concentration in macrophages of mice with HA-1 ascitic hepatoma. Bull. Exp. Biol. Med. 2009;147(4):466–468. doi: 10.1007/ s10517-009-0557-4
23. Hyka N., Dayer J.M., Modoux C., Kohno T., Edwards C.K., Roux-Lombard P., Burger D. Apolipoprotein A-I inhibits the production of interleukin-1 beta and tumor necrosis factor-alpha by blocking contact-mediated activation of monocytes by T lymphocytes. Blood. 2001;97(8):2381–2389. doi: 10.1182/ blood.v97.8.2381
24. Wadham C., Albanese N., Roberts J., Wang L., Bagley C.J., Gamble J.R., Rye K.A., Barter P.J., Vadas M.A., Xia P. High-density lipoproteins neutralize C-reactive protein proinflammatory activity. Circulation. 2004;109(17):2116–2122. doi: 10.1161/01. CIR.0000127419.45975.26
25. Burger D., Dayer J.M. High-density lipoprotein-associated apolipoprotein A-I: the missing link between infection and chronic inflammation? Autoimmun. Rev. 2002;1(1–2):111–117. doi: 10.1016/s1568- 9972(01)00018-0
26. Tada N., Sakamoto T., Kagami A., Mochizuk K., Kurosaka K. Antimicrobial activity of lipoprotein particles containing apolipoprotein Al. Mol. Cell. Biochem. 1993;119(1–2):171–178. doi: 10.1007/BF00926868.