Andrey G. ALEKSANDROV, Tatyana N. SAVATEEVA-LYUBIMOVA, Konstantin V. SIVAK, Kira I. STOSMAN, Irina N. ZHILINSKAYA

Protective effect of aminoguanidine against acute lung injury induced by influenza А(H1N1)pdm09 (mouseadapted) virus in mice with diabetes mellitus

Advanced glycation end products (AGEs) formation is a reason for protein dysfunction and inflammatory response during acute lung injury (ALI) and diabetes mellitus (DM). Previous studies showed the efficacy of AGEs blockers against inflammatory response and protein dysfunction. But the efficacy of AGEs blockers against ALI with combined pathology stays unclear. This study was performed on albino female mice with DM. Virus-induced ALI was induced by the pandemic strain of influenza virus A(H1N1)pdm09. Experimental DM was induced by a single subcutaneous injection of alloxan monohydrate (180 mg/kg). Aminoguanidine bicarbonate (25 mg/kg, subcutaneously) was administered during 7 days post-infection. In our research, we evaluated parameters of ALI during influenza infection such as survival rate, blood-oxygen saturation, levels of cytokines in lung tissue, specific hematological parameters, lung tissue morphology, and AGEs level in the lungs. The protective effect of aminoguanidine was confirmed by reduction mortality, decreasing of hypoxia and limitation of lung damage(p

PDF

___

[1] Kalil A.C., Thomas P.G. Influenza virus-related critical illness: pathophysiology and epidemiology. Crit Care. 2019; 23: 258. [CrossRef]
[2] Gallelli L., Zhang L., Wang T., Fu F. Severe Acute Lung Injury Related to COVID-19 Infection: A Review and the Possible Role for Escin. J ClinPharmacol.2020; 60: 815-825. [CrossRef]
[3] Grasselli G., Tonetti T., Protti A., Langer T., Girardis M., Bellani G., Laffey J., Carrafiello G., Carsana L., Rizzuto C., Zanella A., Scaravilli V., Pizzilli G., Grieco D. L., Meglio L. D., de Pascale G., Lanza E., Monteduro F., Zompatori M., Filippini C., Locatelli F., Cecconi M., Fumagalli R., Nava S., Vincent J.-L., Antonelli M., Slutsky A. S, Pesenti A., Ranieri V M., on behalf of the collaborator Pathophysiology of COVID-19-associated acute respiratory distress syndrome: a multicentre prospective observational study.Lancet Respir Med. 2020; 8: 1201-1208. [CrossRef]
[4] Lobo S.M., Watanabe A.S.A., Salomão M.L.M., Queiroz F., Gandolfi J.V., de Oliveira N.E., Covello L.H.S., Sacillotto G.H., de Godoy L.G., Simões E.S., Frini I.C.M., Da Silva Teixeira R.E.R., Furlan N.P., Dutra K.R., Nogueira M.L. Excess mortality is associated with influenza a (H1N1) in patients with severe acute respiratory infections. J ClinVirol.2019; 116: 62-68. [CrossRef]
[5] Jaber S., Conseil M., Coisel Y., Jung B., Chanques G. Grippe A (H1N1) et SDRA: caractéristiques des patients admisenréanimation et priseen charge. Revue de la littérature. Ann Fr Anesth Reanim. 2010; 29: 117–125. [CrossRef] [article in French with an abstract in English]
[6] Töpfer L., Menk M., Weber-Carstens S., Spies C., Wernecke K.D., Uhrig A., Lojewski C., Jörres A., Deja M. Influenza A (H1N1) vs non-H1N1 ARDS: Analysis of clinical course. J Crit Care.2014; 29: 340–346. [CrossRef]
[7] Gibson P.G., Qin L., Puah S.H. COVID-19 acute respiratory distress syndrome (ARDS): clinical features and differences from typical pre-COVID-19 ARDS.Med J Aust. 2020; 213: 54-56.e1. [CrossRef]
[8] Allard R., Leclerc P., Tremblay C., Tannenbaum T.N. Diabetes and the severity of pandemic influenza A (H1N1) infection. Diabetes Care.2010; 33: 1491-1493. [CrossRef]
[9] Abdi A., Jalilian M., Sarbarzeh P.A., Vlaisavljevic Z. Diabetes and COVID-19: A systematic review on the current evidences.Diabetes Res ClinPract. 2020; 166: 108347. [CrossRef]
[10] Poux C., Dondalska A., Bergenstråhle J., Pålsson S., Contreras V., Arasa C., Järver P., Albert J., Busse D. C., LeGrand R., Lundeberg J., Tregoning J. S. and Spetz A.-L. A Single-Stranded Oligonucleotide Inhibits Toll-Like Receptor 3 Activation and Reduces Influenza A (H1N1) Infection. Front Immunol.2019; 10: 2161. [CrossRef]
[11] Aeffner F., Woods P.S,. Davis I.C. Activation of A1-adenosine receptors promotes leukocyte recruitment to the lung and attenuates acute lung injury in mice infected with influenza A/WSN/33 (H1N1) virus. J Virol.2014; 88: 10214- 27. [CrossRef]
[12] Tavares L.P., Teixeira M.M., Garcia C.C. The inflammatory response triggered by Influenza virus: a two edged sword. Inflamm Res. 2017; 66: 283-302. [CrossRef]
[13] Nowotny K., Jung T., Höhn A., Weber D., Grune T. Advanced glycation end products and oxidative stress in type 2 diabetes mellitus. Biomolecules.2015; 5: 194-222. [CrossRef]
[14] Chawla D., Bansal S., Banerjee B.D., Madhu S.V., Kalra O.P., Tripathi A.K. Role of advanced glycation end product (AGE)-induced receptor (RAGE) expression in diabetic vascular complications. Microvasc Res. 2014; 95: 1-6. [CrossRef]
[15] Saadat S., Beheshti F., Askari V.R., Hosseini M., Roshan N. M., Boskabady M.H. Aminoguanidine affects systemic and lung inflammation induced by lipopolysaccharide in rats. Respir Res. 2019; 20: 96. [CrossRef]
[16] Tsuji C, Shioya S, Hirota Y., Fukuyama N., Kurita D., Tanigaki T., Ohta Y., Nakazawa H. Increased production of nitrotyrosine in lung tissue of rats with radiation-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol. 2000; 278: L719-725. [CrossRef]
[17] Singh R, Barden A, Mori T, Beilin L. Advanced glycation end-products: a review. Diabetologia.2001; 44: 129-146. [CrossRef]
[18] Lander H.M., Tauras J.M., Ogiste J.S., Hori O., Moss R.A., Schmidt A.M. Activation of the receptor for advanced glycation end products triggers a p21(ras)-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J Biol Chem. 1997; 272: 17810-17814. [CrossRef]
[19] Ren X., Ren L., Wei Q., Shao H., Chen L., Liu N. Advanced glycation end-products decreases expression of endothelial nitric oxide synthase through oxidative stress in human coronary artery endothelial cells. CardiovascDiabetol. 2017; 16: 52. [CrossRef]
[20] Rouhiainen A, Kuja-Panula J, Tumova S, Rauvala H. RAGE-mediated cell signaling. Methods Mol Biol. 2013; 963: 239-263. [CrossRef]
[21] Suratt B.T., Parsons P.E. Mechanisms of acute lung injury/acute respiratory distress syndrome. Clin Chest Med. 2006; 27: 579-589. [CrossRef]
[22] Byun K, Yoo Y., Son M., Lee J., Jeong G.B., Park Y.M., Salekdeh G.H., Lee B. Advanced glycation end-products produced systemically and by macrophages: A common contributor to inflammation and degenerative diseases. PharmacolTher. 2017; 177: 44-55. [CrossRef]
[23] Chang G.J., Yeh Y.H., Chen W.J., Ko Y.S., Pang J.S., Lee H.Y. Inhibition of Advanced Glycation End Products Formation Attenuates Cardiac Electrical and Mechanical Remodeling and Vulnerability to Tachyarrhythmias in Diabetic Rats. J PharmacolExpTher.2019; 368: 66-78. [CrossRef]
[24] Coughlan MT, Forbes JM, Cooper ME. Role of the AGE crosslink breaker, alagebrium, as a renoprotective agent in diabetes. Kidney Int Suppl. 2007; 106: S54-60. [CrossRef]
[25] Brownlee M., Vlassara H., Kooney A., Ulrich P., Cerami A. Aminoguanidine prevents diabetes-induced arterial wall protein cross-linking. Science. 1986; 232(4758): 1629–1632. [CrossRef]
[26] Forbes J.M., Soulis T., Thallas V., Panagiotopoulos S., Long D.M., Vasan S., Wagle D., Jerums G., Cooper M. E. Renoprotective effects of a novel inhibitor of advanced glycation. Diabetologia.2001; 44(1): 108–114. [CrossRef]
[27] Figarola J.L., Scott S., Loera S., Tessler C., Chu P., Weiss L., Hardy J., Rahbar S. LR-90 a new advanced glycation endproduct inhibitor prevents progression of diabetic nephropathy in streptozotocin-diabetic rats. Diabetologia.2003; 46(8): 1140-1152. [CrossRef]
[28] Vasan S, Foiles P, Founds H. Therapeutic potential of breakers of advanced glycation end product-protein crosslinks. Arch BiochemBiophys. 2003; 419 (1): 89-96. [CrossRef]
[29] Pathak P, Gupta R, Chaudhari A, Shiwalkar A, Dubey A, Mandhare AB, Gupta RC, Joshi D, Chauthaiwale V. TRC4149 a novel advanced glycation end product breaker improves hemodynamic status in diabetic spontaneously hypertensive rats. Eur J Med Res. 2008; 13 (8): 388-398. [CrossRef]
[30] Aleksandrov A.G., Savateeva-Lyubimova T.N., Stosman K.I., Muzhikyan A.A. Sivak K.V.. The effect of aminoguanidine on acute lung injury induced by influenza A/H1N1/PDM09.Medical academic journal.2020; 20(2): 33-44. [CrossRef] [article in Russian with an abstract in English]
[31] Thornalley P.J., Langborg A., Minhas H.S. Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J. 1999; 344: 109-116.
[32] Paschou S.A., Papadopoulou-Marketou N., Chrousos G.P., Kanaka-Gantenbein C. On type 1 diabetes mellitus pathogenesis. Endocr Connect. 2018; 7: R38-R46. [CrossRef]
[33] Singh V.P., Bali A., Singh N., Jaggi A.S. Advanced glycation end products and diabetic complications. Korean J Physiol Pharmacol.2014; 18: 1-14. [CrossRef]
[34] Li Y.M., Steffes M., Donnelly T., Liu C., Fuh H., Basgen J., Bucala R., Vlassara H. Prevention of cardiovascular and renal pathology of aging by the advanced glycation inhibitor aminoguanidine. Proc Natl AcadSci USA. 1996; 93: 3902-3907. [CrossRef]
[35] Kołodziej-Sobocińska M., Machnicka-Rowińska B. In vivo inhibition of inducible nitric oxide synthase by aminoguanidine influences free radicals production and macrophage activity in Trichinella spiralis infected low responders (C57BL/6) and high responders (BALB/c) mice. Helminthologia.2012; 49: 189–200. [CrossRef]
[36] Dudhgaonkar S.P., Tandan S.K., Bhat A.S., Jadhav S.H., Kumar D. Synergistic anti-inflammatory interaction between meloxicam and aminoguanidine hydrochloride in carrageenan-induced acute inflammation in rats.Life Sci. 2006; 78: 1044-1048. [CrossRef]
[37] Maillard L.-C. Action Des Acides Amine´s Sur Les Sucres.Formation Des Melanoidins Par VoieMethodique [Action of amino acids on sugars. Formation of melanoidins in a methodical way].Compt Rend. 1912; 154: 66–68. [article in French]
[38] Schmidt A.M., Yan S.D., Wautier J.L., Stern D. Activation of receptor for advanced glycation end products: a mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circ Res. 1999; 84(5): 489- 497. [CrossRef]
[39] Fournet M, Bonté F, Desmoulière A. Glycation Damage: A Possible Hub for Major Pathophysiological Disorders and Aging.Aging Dis. 2018;9(5):880-900. [CrossRef]
[40] Farhad A.R., Razavi S.M., Nejad P.A. The use of aminoguanidine, a selective inducible nitric oxide synthase inhibitor, to evaluate the role of nitric oxide on periapical healing. Dent Res J (Isfahan). 2011; 8: 197-202. [CrossRef]
[41] Kikumoto Y., Sugiyama H., Inoue T., Morinaga H., Takiue K., Kitagawa M., Fukuoka N., Saeki M., Maeshima Y., Wang D.H., Ogino K., Masuoka N., Makino H. Sensitization to alloxan-induced diabetes and pancreatic cell apoptosis in acatalasemic mice. BiochimBiophysActa. 2010; 1802: 240-246. [CrossRef]
[42] Burleson F.G., Chambers T.M., Wiedbrauk D.L. Virology: A laboratory manual. Academic press, London, UK, 1992.
[43] Killian M.L. Hemagglutination assay for influenza virus. Methods Mol Biol. 2014; 1161: 3-9. [CrossRef]
[44] Jonxis J.H.P. The determination of oxygen saturation in small amounts of blood, by means of the Pulfrich step photometer. Acta Med Scand, 1943; 115: 425–428. [CrossRef]
[45] Matute-Bello G., Downey G., Moore B.B., Groshong S.D., Matthay M.A., Slutsky A.S., Kuebler W.M. Acute Lung Injury in Animals Study Group An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol. 2011; 44: 725-738. [CrossRef]
[46] Zheng K., Wu L., He Z., Yang B., Yang Y. Measurement of the total protein in serum by biuret method with uncertainty evaluation. Measurement, 2017; 112: 16–21. [CrossRef]
[47] Yanagisawa K., Makita Z., Shiroshita K., Ueda T., Fusegawa T., Kuwajima S., Takeuchi M., Koike T. Specific fluorescence assay for advanced glycation end products in blood and urine of diabetic patients. Metabolism.1998; 47: 1348-1353. [CrossRef]