Generic placeholder image

Current Medicinal Chemistry


ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Prospects for the Use of Sialidase Inhibitors in Anti-atherosclerotic Therapy

Author(s): Igor A. Sobenin, Alexander M. Markin*, Victor Y. Glanz, Yuliya V. Markina, Wei-Kai Wu, Veronika A. Myasoedova and Alexander N. Orekhov

Volume 28 , Issue 12 , 2021

Published on: 31 August, 2020

Page: [2438 - 2450] Pages: 13

DOI: 10.2174/0929867327666200831133912

Price: $65


The most typical feature of atherogenesis in humans at its early stage is the formation of foam cells in subendothelial arterial intima, which occurs as the consequence of intracellular cholesterol deposition. The main source of lipids accumulating in the arterial wall is circulating low-density lipoprotein (LDL). However, LDL particles should undergo proatherogenic modification to acquire atherogenic properties. One of the known types of atherogenic modification of LDL is enzymatic deglycosilation, namely, desialylation, which is the earliest change in the cascade of following multiple LDL modifications. The accumulating data make sialidases an intriguing and plausible therapeutic target, since pharmacological modulation of activity of these enzymes may have beneficial effects in several pathologies, including atherosclerosis. The hypothesis exists that decreasing LDL enzymatic desialylation may result in the prevention of lipid accumulation in arterial wall, thus breaking down one of the key players in atherogenesis at the cellular level. Several drugs acting as glycomimetics and inhibiting sialidase enzymatic activity already exist, but the concept of sialidase inhibition as an anti-atherosclerosis strategy remains unexplored to date. This review is focused on the potential possibilities of the repurposing of sialidase inhibitors for pathogenetic anti-atherosclerotic therapy.

Keywords: Atherosclerosis, low density lipoprotein, atherogenic modification, deglycosylation, desialylation, intracellular cholesterol accumulation, sialidase inhibitors, drug repurposing.

« Previous
World Health Organization. Global health estimates 2016: deaths by cause, age, sex, by country and by region, 2000- 2016; Geneva, 2020. (Accessed on: March 15, 2020).
Schwartz, C.J.; Valente, A.J.; Sprague, E.A. A modern view of atherogenesis. Am. J. Cardiol., 1993, 71(6), 9B-14B.
[] [PMID: 8434561]
Orekhov, A.N. LDL and foam cell formation as the basis of atherogenesis. Curr. Opin. Lipidol., 2018, 29(4), 279-284.
[] [PMID: 29746302]
Bäck, M.; Yurdagul, A., Jr; Tabas, I.; Öörni, K.; Kovanen, P.T. Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities. Nat. Rev. Cardiol., 2019, 16(7), 389-406.
[] [PMID: 30846875]
Ellulu, M.S.; Patimah, I.; Khaza’ai, H.; Rahmat, A.; Abed, Y.; Ali, F. Atherosclerotic cardiovascular disease: a review of initiators and protective factors. Inflammopharmacology, 2016, 24(1), 1-10.
[] [PMID: 26750181]
Chistiakov, D.A.; Bobryshev, Y.V.; Orekhov, A.N. Macrophage-mediated cholesterol handling in atherosclerosis. J. Cell. Mol. Med., 2016, 20(1), 17-28.
[] [PMID: 26493158]
Morita, S.Y. Metabolism and modification of apolipoprotein B-containing lipoproteins involved in dyslipidemia and atherosclerosis. Biol. Pharm. Bull., 2016, 39(1), 1-24.
[] [PMID: 26725424]
Arnao, V.; Tuttolomondo, A.; Daidone, M.; Pinto, A. Lipoproteins in atherosclerosis process. Curr. Med. Chem., 2019, 26(9), 1525-1543.
[] [PMID: 31096892]
Nakajima, K.; Tanaka, A. Atherogenic postprandial remnant lipoproteins; VLDL remnants as a causal factor in atherosclerosis. Clin. Chim. Acta, 2018, 478, 200-215.
[] [PMID: 29307667]
Alipov, V.I.; Sukhorukov, V.N.; Karagodin, V.P.; Grechko, A.V.; Orekhov, A.N. Chemical composition of circulating native and desialylated low density lipoprotein: what is the difference? Vessel Plus, 2017, 1, 107-115.
Summerhill, V.I.; Grechko, A.V.; Yet, S.F.; Sobenin, I.A.; Orekhov, A.N. The atherogenic role of circulating modified lipids in atherosclerosis. Int. J. Mol. Sci., 2019, 20(14), 3561.
[] [PMID: 31330845]
Orekhov, A.N.; Sobenin, I.A. Modified lipoproteins as biomarkers of atherosclerosis. Front. Biosci., 2018, 23, 1422-1444.
[] [PMID: 29293443]
Afonso, C.B.; Spickett, C.M. Lipoproteins as targets and markers of lipoxidation. Redox Biol., 2019, 23, 101066.
[] [PMID: 30579928]
Orekhov, A.N.; Sobenin, I.A. Modified and dysfunctional lipoproteins in atherosclerosis: effectors or biomarkers? Curr. Med. Chem., 2019, 26(9), 1512-1524.
[] [PMID: 29557739]
Ivanova, E.A.; Myasoedova, V.A.; Melnichenko, A.A.; Grechko, A.V.; Orekhov, A.N. Small dense low-density lipoprotein as biomarker for atherosclerotic diseases. Oxid. Med. Cell. Longev., 2017, 2017, 1273042.
[] [PMID: 28572872]
Wang, H.H.; Garruti, G.; Liu, M.; Portincasa, P.; Wang, D-Q. Cholesterol and lipoprotein metabolism and atherosclerosis: recent advances in reverse cholesterol transport. Ann. Hepatol., 2017, 16(Suppl. 1), S27-S42.
[] [PMID: 31196632]
Rivas-Urbina, A.; Rull, A.; Ordóñez-Llanos, J.; Sánchez-Quesada, J.L. Electronegative LDL: an active player in atherogenesis or a by-product of atherosclerosis? Curr. Med. Chem., 2019, 26(9), 1665-1679.
[] [PMID: 29600751]
Nikiforov, N.G.; Zakiev, E.R.; Elizova, N.V.; Sukhorukov, V.N.; Orekhov, A.N. Multiple-modified low-density lipoprotein as atherogenic factor of patients’ blood: development of therapeutic approaches to reduce blood atherogenicity. Curr. Pharm. Des., 2017, 23(6), 932-936.
[] [PMID: 28120723]
Torzewski, M. Enzymatically modified LDL, atherosclerosis and beyond: paving the way to acceptance. Front. Biosci., 2018, 23, 1257-1271.
[] [PMID: 28930598]
Tertov, V.V.; Kaplun, V.V.; Sobenin, I.A.; Orekhov, A.N. Low-density lipoprotein modification occurring in human plasma possible mechanism of in vivo lipoprotein desialylation as a primary step of atherogenic modification. Atherosclerosis, 1998, 138(1), 183-195.
[] [PMID: 9678784]
Zakiev, E.R.; Sobenin, I.A.; Sukhorukov, V.N.; Myasoedova, V.A.; Ivanova, E.A.; Orekhov, A.N. Carbohydrate composition of circulating multiple-modified low-density lipoprotein. Vasc. Health Risk Manag., 2016, 12, 379-385.
[] [PMID: 27789955]
Zakiev, E.R.; Sukhorukov, V.N.; Ivanova, E.A.; Orekhov, A.N. Analysis of apolipoprotein B protein of circulating multiple-modified low-density lipoprotein. Int. J. Angiol., 2017, 26(1), 49-52.
[] [PMID: 28255216]
Tertov, V.V.; Kaplun, V.V.; Sobenin, I.A.; Boytsova, E.Y.; Bovin, N.V.; Orekhov, A.N. Human plasma trans-sialidase causes atherogenic modification of low density lipoprotein. Atherosclerosis, 2001, 159(1), 103-115.
[] [PMID: 11689212]
Glanz, V.Y.; Myasoedova, V.A.; Grechko, A.V.; Orekhov, A.N. Trans-sialidase associated with atherosclerosis: defining the identity of a key enzyme involved in the pathology. Curr. Drug Targets, 2019, 20(9), 938-941.
[] [PMID: 30848200]
Glanz, V.Y.; Myasoedova, V.A.; Grechko, A.V.; Orekhov, A.N. Sialidase activity in human pathologies. Eur. J. Pharmacol., 2019, 842, 345-350.
[] [PMID: 30439363]
Sesorova, I.S.; Karelina, N.R.; Kazakova, T.E.; Parashuraman, S.; Zdorikova, M.A.; Dimov, I.D.; Seliverstova, E.V.; Beznoussenko, G.V.; Mironov, A.A. Structure of the enterocyte transcytosis compartments during lipid absorption. Histochem. Cell Biol., 2020, 153(6), 413-429.
[] [PMID: 32162136]
Mironov, A.A.; Sesorova, I.S.; Dimov, I.D.; Karelina, N.R.; Beznoussenko, G.V. Intracellular transports and atherogenesis. Front. Biosci., 2020, 25, 1230-1258.
[PMID: 32114431]
Dousset, N.; Dousset, J.C.; Taus, M.; Ferretti, G.; Curatola, G.; Soléra, M.L.; Valdiguié, P. Effect of desialylation on low density lipoproteins: comparative study before and after oxidative stress. Biochem. Mol. Biol. Int., 1994, 32(3), 555-563.
[PMID: 8032323]
Grewal, T.; Bartlett, A.; Burgess, J.W.; Packer, N.H.; Stanley, K.K. Desialylated LDL uptake in human and mouse macrophages can be mediated by a lectin receptor. Atherosclerosis, 1996, 121(1), 151-163.
[] [PMID: 8678920]
Tanaka, K.; Tokumaru, S.; Kojo, S. Possible involvement of radical reactions in desialylation of LDL. FEBS Lett., 1997, 413(2), 202-204.
[] [PMID: 9280282]
Harada, L.M.; Carvalho, M.D.; Passarelli, M.; Quintão, E.C. Lipoprotein desialylation simultaneously enhances the cell cholesterol uptake and impairs the reverse cholesterol transport system: in vitro evidences utilizing neuraminidase-treated lipoproteins and mouse peritoneal macrophages. Atherosclerosis, 1998, 139(1), 65-75.
[] [PMID: 9699893]
Bartlett, A.L.; Grewal, T.; De Angelis, E.; Myers, S.; Stanley, K.K. Role of the macrophage galactose lectin in the uptake of desialylated LDL. Atherosclerosis, 2000, 153(1), 219-230.
[] [PMID: 11058718]
Garner, B.; Harvey, D.J.; Royle, L.; Frischmann, M.; Nigon, F.; Chapman, M.J.; Rudd, P.M. Characterization of human apolipoprotein B100 oligosaccharides in LDL subfractions derived from normal and hyperlipidemic plasma: deficiency of α-N-acetylneuraminyllactosyl-ceramide in light and small dense LDL particles. Glycobiology, 2001, 11(10), 791-802.
[] [PMID: 11588155]
Sukhorukov, V.; Gudelj, I.; Pučić-Baković, M.; Zakiev, E.; Orekhov, A.; Kontush, A.; Lauc, G. Glycosylation of human plasma lipoproteins reveals a high level of diversity, which directly impacts their functional properties. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2019, 1864(5), 643-653.
[] [PMID: 30641224]
Glanz, V.Y.; Myasoedova, V.A.; Grechko, A.V.; Orekhov, A.N. Inhibition of sialidase activity as a therapeutic approach. Drug Des. Devel. Ther., 2018, 12, 3431-3437.
[] [PMID: 30349196]
Schauer, R.; Kamerling, J.P. Exploration of the sialic acid world. Adv. Carbohydr. Chem. Biochem., 2018, 75, 1-213.
[] [PMID: 30509400]
Li, Y.; Chen, X. Sialic acid metabolism and sialyltransferases: natural functions and applications. Appl. Microbiol. Biotechnol., 2012, 94(4), 887-905.
[] [PMID: 22526796]
Mehr, K.; Withers, S.G. Mechanisms of the sialidase and trans-sialidase activities of bacterial sialyltransferases from glycosyltransferase family 80. Glycobiology, 2016, 26(4), 353-359.
[] [PMID: 26582604]
van Wyk, N.; Drancourt, M.; Henrissat, B.; Kremer, L. Current perspectives on the families of glycoside hydrolases of Mycobacterium tuberculosis: their importance and prospects for assigning function to unknowns. Glycobiology, 2017, 27(2), 112-122.
[] [PMID: 27697825]
Wilson, I. Biosynthesis and degradation of mono-, oligo-, and polysaccharides: introduction.Glycoscience; Fraser-Reid, B.O.; Tatsuta, K.; Thiem, J., Eds.; Springer: Berlin, Heidelberg, 2008, pp. 2243-2264.
Miyagi, T.; Yamaguchi, K. Mammalian sialidases: physiological and pathological roles in cellular functions. Glycobiology, 2012, 22(7), 880-896.
[] [PMID: 22377912]
Achyuthan, K.E.; Achyuthan, A.M. Comparative enzymology, biochemistry and pathophysiology of human exo-α-sialidases (neuraminidases). Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2001, 129(1), 29-64.
[] [PMID: 11337249]
Monti, E.; Preti, A.; Venerando, B.; Borsani, G. Recent development in mammalian sialidase molecular biology. Neurochem. Res., 2002, 27(7-8), 649-663.
[] [PMID: 12374200]
Miyagi, T.; Takahashi, K.; Yamamoto, K.; Shiozaki, K.; Yamaguchi, K. Biological and pathological roles of ganglioside sialidases. Prog. Mol. Biol. Transl. Sci., 2018, 156, 121-150.
[] [PMID: 29747812]
Valaperta, R.; Chigorno, V.; Basso, L.; Prinetti, A.; Bresciani, R.; Preti, A.; Miyagi, T.; Sonnino, S. Plasma membrane production of ceramide from ganglioside GM3 in human fibroblasts. FASEB J., 2006, 20(8), 1227-1229.
[] [PMID: 16645048]
Moon, S.K.; Cho, S.H.; Kim, K.W.; Jeon, J.H.; Ko, J.H.; Kim, B.Y.; Kim, C.H. Overexpression of membrane sialic acid-specific sialidase Neu3 inhibits matrix metalloproteinase-9 expression in vascular smooth muscle cells. Biochem. Biophys. Res. Commun., 2007, 356(3), 542-547.
[] [PMID: 17382908]
Finlay, T.M.; Abdulkhalek, S.; Gilmour, A.; Guzzo, C.; Jayanth, P.; Amith, S.R.; Gee, K.; Beyaert, R.; Szewczuk, M.R. Thymoquinone-induced Neu4 sialidase activates NFκB in macrophage cells and pro-inflammatory cytokines in vivo. Glycoconj. J., 2010, 27(6), 583-600.
[] [PMID: 20697956]
Tannock, L.R.; King, V.L. Proteoglycan mediated lipoprotein retention: a mechanism of diabetic atherosclerosis. Rev. Endocr. Metab. Disord., 2008, 9(4), 289-300.
[] [PMID: 18584330]
Tran-Lundmark, K.; Tran, P.K.; Paulsson-Berne, G.; Fridén, V.; Soininen, R.; Tryggvason, K.; Wight, T.N.; Kinsella, M.G.; Borén, J.; Hedin, U. Heparan sulfate in perlecan promotes mouse atherosclerosis: roles in lipid permeability, lipid retention, and smooth muscle cell proliferation. Circ. Res., 2008, 103(1), 43-52.
[] [PMID: 18596265]
Xu, Y.X.; Ashline, D.; Liu, L.; Tassa, C.; Shaw, S.Y.; Ravid, K.; Layne, M.D.; Reinhold, V.; Robbins, P.W. The glycosylation-dependent interaction of perlecan core protein with LDL: implications for atherosclerosis. J. Lipid Res., 2015, 56(2), 266-276.
[] [PMID: 25528754]
Huang, Y.L.; Chassard, C.; Hausmann, M.; von Itzstein, M.; Hennet, T. Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice. Nat. Commun., 2015, 6, 8141.
[] [PMID: 26303108]
Miklavcic, J.J.; Hart, T.D.; Lees, G.M.; Shoemaker, G.K.; Schnabl, K.L.; Larsen, B.M.; Bathe, O.F.; Thomson, A.B.; Mazurak, V.C.; Clandinin, M.T. Increased catabolism and decreased unsaturation of ganglioside in patients with inflammatory bowel disease. World J. Gastroenterol., 2015, 21(35), 10080-10090.
[] [PMID: 26401073]
Qadri, S.M.; Donkor, D.A.; Nazy, I.; Branch, D.R.; Sheffield, W.P. Bacterial neuraminidase-mediated erythrocyte desialylation provokes cell surface aminophospholipid exposure. Eur. J. Haematol., 2018, 100(5), 502-510.
[] [PMID: 29453885]
Reganon, E.; Vila, V.; Martínez-Sales, V.; Vayá, A.; Mira, Y.; Ferrando, F.; Aznar, J. Sialic acid is an inflammation marker associated with a history of deep vein thrombosis. Thromb. Res., 2007, 119(1), 73-78.
[] [PMID: 16500696]
Chrostek, L.; Cylwik, B.; Gindzienska-Sieskiewicz, E.; Gruszewska, E.; Szmitkowski, M.; Sierakowski, S. Sialic acid level reflects the disturbances of glycosylation and acute-phase reaction in rheumatic diseases. Rheumatol. Int., 2014, 34(3), 393-399.
[] [PMID: 24346772]
Rajendiran, K.S.; Ananthanarayanan, R.H.; Satheesh, S.; Rajappa, M. Elevated levels of serum sialic acid and high-sensitivity C-reactive protein: markers of systemic inflammation in patients with chronic heart failure. Br. J. Biomed. Sci., 2014, 71(1), 29-32.
[] [PMID: 24693572]
Khalili, P.; Sundström, J.; Jendle, J.; Lundin, F.; Jungner, I.; Nilsson, P.M. Sialic acid and incidence of hospitalization for diabetes and its complications during 40-years of follow-up in a large cohort: the Värmland survey. Prim. Care Diabetes, 2014, 8(4), 352-357.
[] [PMID: 24996911]
Kara, A.E.; Guney, G.; Tokmak, A.; Ozaksit, G. The role of inflammatory markers hs-CRP, sialic acid, and IL-6 in the pathogenesis of preeclampsia and intrauterine growth restriction. Eur. Cytokine Netw., 2019, 30(1), 29-33.
[] [PMID: 31074415]
Nigam, P.K.; Narain, V.S.; Kumar, A. Sialic acid in cardiovascular diseases. Indian J. Clin. Biochem., 2006, 21(1), 54-61.
[] [PMID: 23105570]
Süer Gökmen, S.; Kazezoğlu, C.; Sunar, B.; Ozçelik, F.; Güngör, O.; Yorulmaz, F.; Gülen, S. Relationship between serum sialic acids, sialic acid-rich inflammation-sensitive proteins and cell damage in patients with acute myocardial infarction. Clin. Chem. Lab. Med., 2006, 44(2), 199-206.
[] [PMID: 16475908]
Sasaki, A.; Hata, K.; Suzuki, S.; Sawada, M.; Wada, T.; Yamaguchi, K.; Obinata, M.; Tateno, H.; Suzuki, H.; Miyagi, T. Overexpression of plasma membrane-associated sialidase attenuates insulin signaling in transgenic mice. J. Biol. Chem., 2003, 278(30), 27896-27902.
[] [PMID: 12730204]
Samraj, A.N.; Läubli, H.; Varki, N.; Varki, A. Involvement of a non-human sialic Acid in human cancer. Front. Oncol., 2014, 4, 33.
[] [PMID: 24600589]
Yoshizumi, S.; Suzuki, S.; Hirai, M.; Hinokio, Y.; Yamada, T.; Yamada, T.; Tsunoda, U.; Aburatani, H.; Yamaguchi, K.; Miyagi, T.; Oka, Y. Increased hepatic expression of ganglioside-specific sialidase, NEU3, improves insulin sensitivity and glucose tolerance in mice. Metabolism, 2007, 56(3), 420-429.
[] [PMID: 17292733]
Kabayama, K.; Sato, T.; Saito, K.; Loberto, N.; Prinetti, A.; Sonnino, S.; Kinjo, M.; Igarashi, Y.; Inokuchi, J. Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc. Natl. Acad. Sci. USA, 2007, 104(34), 13678-13683.
[] [PMID: 17699617]
Cross, A.S.; Hyun, S.W.; Miranda-Ribera, A.; Feng, C.; Liu, A.; Nguyen, C.; Zhang, L.; Luzina, I.G.; Atamas, S.P.; Twaddell, W.S.; Guang, W.; Lillehoj, E.P.; Puché, A.C.; Huang, W.; Wang, L.X.; Passaniti, A.; Goldblum, S.E. NEU1 and NEU3 sialidase activity expressed in human lung microvascular endothelia: NEU1 restrains endothelial cell migration, whereas NEU3 does not. J. Biol. Chem., 2012, 287(19), 15966-15980.
[] [PMID: 22403397]
Tertov, V.V.; Orekhov, A.N.; Sobenin, I.A.; Morrisett, J.D.; Gotto, A.M., Jr; Guevara, J.G. Jr. Carbohydrate composition of protein and lipid components in sialic acid-rich and -poor low density lipoproteins from subjects with and without coronary artery disease. J. Lipid Res., 1993, 34(3), 365-375.
[PMID: 8468522]
Orekhov, A.N.; Tertov, V.V.; Mukhin, D.N.; Mikhailenko, I.A. Modification of low density lipoprotein by desialylation causes lipid accumulation in cultured cells: discovery of desialylated lipoprotein with altered cellular metabolism in the blood of atherosclerotic patients. Biochem. Biophys. Res. Commun., 1989, 162(1), 206-211.
[] [PMID: 2751649]
Tertov, V.V.; Sobenin, I.A.; Tonevitsky, A.G.; Orekhov, A.N.; Smirnov, V.N. Isolation of atherogenic modified (desialylated) low density lipoprotein from blood of atherosclerotic patients: separation from native lipoprotein by affinity chromatography. Biochem. Biophys. Res. Commun., 1990, 167(3), 1122-1127.
[] [PMID: 2322261]
Orekhov, A.N.; Tertov, V.V.; Mukhin, D.N. Desialylated low density lipoprotein--naturally occurring modified lipoprotein with atherogenic potency. Atherosclerosis, 1991, 86(2-3), 153-161.
[] [PMID: 1872910]
Orekhov, A.N.; Tertov, V.V.; Sobenin, I.A.; Smirnov, V.N.; Via, D.P.; Guevara, J., Jr; Gotto, A.M., Jr; Morrisett, J.D. Sialic acid content of human low density lipoproteins affects their interaction with cell receptors and intracellular lipid accumulation. J. Lipid Res., 1992, 33(6), 805-817.
[PMID: 1512508]
Sobenin, I.A.; Galitsyna, E.V.; Grechko, A.V.; Orekhov, A.N. Small dense and desialylated low density lipoprotein in diabetic patients. Vessel Plus, 2017, 1, 29-37.
Orekhov, A.N.; Ivanova, E.A.; Melnichenko, A.A.; Sobenin, I.A. Circulating desialylated low density lipoprotein. Cor et Vasa, 2017, 59(2), e149-e156.
Aksenov, D.V.; Medvedeva, L.A.; Skalbe, T.A.; Sobenin, I.A.; Tertov, V.V.; Gabbasov, Z.A.; Popov, E.V.; Orekhov, A.N. Deglycosylation of apo B-containing lipoproteins increase their ability to aggregate and to promote intracellular cholesterol accumulation in vitro. Arch. Physiol. Biochem., 2008, 114(5), 349-356.
[] [PMID: 19085234]
Padarti, A.; Zhang, J. Recent advances in cerebral cavernous malformation research. Vessel Plus, 2018, 2, 21.
[] [PMID: 31360916]
Orekhov, A.N.; Oishi, Y.; Nikiforov, N.G.; Zhelankin, A.V.; Dubrovsky, L.; Sobenin, I.A.; Kel, A.; Stelmashenko, D.; Makeev, V.J.; Foxx, K.; Jin, X.; Kruth, H.S.; Bukrinsky, M. Modified LDL particles activate inflammatory pathways in monocyte-derived macrophages: transcriptome analysis. Curr. Pharm. Des., 2018, 24(26), 3143-3151.
[] [PMID: 30205792]
Glanz, V.; Myasoedova, V.A.; Sukhorukov, V.; Grechko, A.; Zhang, D.; Romaneneko, E.B.; Orekhova, V.A.; Orekhov, A. Transcriptional characteristics of activated macrophages. Curr. Pharm. Des., 2019, 25(3), 213-217.
[] [PMID: 30892154]
Orekhov, A.N.; Nikiforov, N.G.; Sukhorukov, V.N.; Kubekina, M.V.; Sobenin, I.A.; Wu, W.K.; Foxx, K.K.; Pintus, S.; Stegmaier, P.; Stelmashenko, D.; Kel, A.; Gratchev, A.N.; Melnichenko, A.A.; Wetzker, R.; Summerhill, V.I.; Manabe, I.; Oishi, Y. Role of phagocytosis in the pro-inflammatory response in LDL-induced foam cell formation: a transcriptome analysis. Int. J. Mol. Sci., 2020, 21(3), 817.
[] [PMID: 32012706]
Tertov, V.V.; Nikonova, E.Y.; Nifant’ev, N.E.; Bovin, N.V.; Orekhov, A.N. Human plasma trans-sialidase donor and acceptor specificity. Biochemistry (Mosc.), 2002, 67(8), 908-913.
[] [PMID: 12223090]
Nikonova, E.Y.; Tertov, V.V.; Sato, C.; Kitajima, K.; Bovin, N.V. Specificity of human trans-sialidase as probed with gangliosides. Bioorg. Med. Chem. Lett., 2004, 14(20), 5161-5164.
[] [PMID: 15380219]
Mel’nichenko, A.A.; Tertov, V.V.; Ivanova, O.A.; Aksenov, D.V.; Sobenin, I.A.; Popov, E.V.; Kaplun, V.V.; Suprun, I.V.; Panasenko, O.M.; Orekhov, A.N. Desialylation decreases the resistance of apo B-containing lipoproteins to aggregation and increases their atherogenic potential. Bull. Exp. Biol. Med., 2005, 140(1), 51-54.
[] [PMID: 16254619]
Oztürk, Z.; Sönmez, H.; Görgün, F.M.; Ekmekçi, H.; Bilgen, D.; Ozen, N.; Sözer, V.; Altuğ, T.; Kökoğlu, E. The Relationship Between Lipid Peroxidation and LDL Desialylation in Experimental Atherosclerosis. Toxicol. Mech. Methods, 2007, 17(5), 265-273.
[] [PMID: 20020949]
Aksenov, D.V.; Kaplun, V.V.; Tertov, V.V.; Sobenin, I.A.; Orekhov, A.N. Effect of plant extracts on trans-sialidase activity in human blood plasma. Bull. Exp. Biol. Med., 2007, 143(1), 46-50.
[] [PMID: 18019010]
Wang, N.; Tall, A.R. Cholesterol in platelet biogenesis and activation. Blood, 2016, 127(16), 1949-1953.
[] [PMID: 26929273]
Grozovsky, R.; Giannini, S.; Falet, H.; Hoffmeister, K.M. Regulating billions of blood platelets: glycans and beyond. Blood, 2015, 126(16), 1877-1884.
[] [PMID: 26330242]
Mendoza, S.; Trenchevska, O.; King, S.M.; Nelson, R.W.; Nedelkov, D.; Krauss, R.M.; Yassine, H.N. Changes in low-density lipoprotein size phenotypes associate with changes in apolipoprotein C-III glycoforms after dietary interventions. J. Clin. Lipidol., 2017, 11(1), 224-233.e2.
[] [PMID: 28391889]
Yassine, H.N.; Trenchevska, O.; Ramrakhiani, A.; Parekh, A.; Koska, J.; Walker, R.W.; Billheimer, D.; Reaven, P.D.; Yen, F.T.; Nelson, R.W.; Goran, M.I.; Nedelkov, D. The Association of Human Apolipoprotein C-III Sialylation Proteoforms with Plasma Triglycerides. PLoS One, 2015, 10(12), e0144138.
[] [PMID: 26633899]
Savinova, O.V.; Fillaus, K.; Jing, L.; Harris, W.S.; Shearer, G.C. Reduced apolipoprotein glycosylation in patients with the metabolic syndrome. PLoS One, 2014, 9(8), e104833.
[] [PMID: 25118169]
Lee, Y.; Kockx, M.; Raftery, M.J.; Jessup, W.; Griffith, R.; Kritharides, L. Glycosylation and sialylation of macrophage-derived human apolipoprotein E analyzed by SDS-PAGE and mass spectrometry: evidence for a novel site of glycosylation on Ser290. Mol. Cell. Proteomics, 2010, 9(9), 1968-1981.
[] [PMID: 20511397]
Yang, A.; Gyulay, G.; Mitchell, M.; White, E.; Trigatti, B.L.; Igdoura, S.A. Hypomorphic sialidase expression decreases serum cholesterol by downregulation of VLDL production in mice. J. Lipid Res., 2012, 53(12), 2573-2585.
[] [PMID: 22984145]
Altay, M.; Karakoç, M.A.; Çakır, N.; Yılmaz Demirtaş, C.; Cerit, E.T.; Aktürk, M.; Ateş, İ.; Bukan, N.; Arslan, M. Serum total sialic acid level is elevated in hypothyroid patients as an atherosclerotic risk factor. J. Clin. Lab. Anal., 2017, 31(2), e22034.
[] [PMID: 27457058]
Tanigaki, K.; Sacharidou, A.; Peng, J.; Chambliss, K.L.; Yuhanna, I.S.; Ghosh, D.; Ahmed, M.; Szalai, A.J.; Vongpatanasin, W.; Mattrey, R.F.; Chen, Q.; Azadi, P.; Lingvay, I.; Botto, M.; Holland, W.L.; Kohler, J.J.; Sirsi, S.R.; Hoyt, K.; Shaul, P.W.; Mineo, C. Hyposialylated IgG activates endothelial IgG receptor FcγRIIB to promote obesity-induced insulin resistance. J. Clin. Invest., 2018, 128(1), 309-322.
[] [PMID: 29202472]
Belfiore, A.; Malaguarnera, R.; Vella, V.; Lawrence, M.C.; Sciacca, L.; Frasca, F.; Morrione, A.; Vigneri, R. Insulin receptor isoforms in physiology and disease: an updated view. Endocr. Rev., 2017, 38(5), 379-431.
[] [PMID: 28973479]
Aikawa, M.; Libby, P. Lipid lowering therapy in atherosclerosis. Semin. Vasc. Med., 2004, 4(4), 357-366.
[] [PMID: 15861316]
Pasta, A.; Cremonini, A.L.; Pisciotta, L.; Buscaglia, A.; Porto, I.; Barra, F.; Ferrero, S.; Brunelli, C.; Rosa, G.M. PCSK9 inhibitors for treating hypercholesterolemia. Expert Opin. Pharmacother., 2020, 21(3), 353-363.
[] [PMID: 31893957]
Reiter-Brennan, C.; Osei, A.D.; Iftekhar Uddin, S.M.; Orimoloye, O.A.; Obisesan, O.H.; Mirbolouk, M.; Blaha, M.J.; Dzaye, O. ACC/AHA lipid guidelines: personalized care to prevent cardiovascular disease. Cleve. Clin. J. Med., 2020, 87(4), 231-239.
[] [PMID: 32238379]
Nordestgaard, B.G.; Langlois, M.R.; Langsted, A.; Chapman, M.J.; Aakre, K.M.; Baum, H.; Borén, J.; Bruckert, E.; Catapano, A.; Cobbaert, C.; Collinson, P.; Descamps, O.S.; Duff, C.J.; von Eckardstein, A.; Hammerer-Lercher, A.; Kamstrup, P.R.; Kolovou, G.; Kronenberg, F.; Mora, S.; Pulkki, K.; Remaley, A.T.; Rifai, N.; Ros, E.; Stankovic, S.; Stavljenic-Rukavina, A.; Sypniewska, G.; Watts, G.F.; Wiklund, O.; Laitinen, P. European Atherosclerosis Society (EAS) and the European Federation of Clinical Chemistry and Laboratory Medicine (EFLM) Joint Consensus Initiative. Quantifying atherogenic lipoproteins for lipid-lowering strategies: consensus-based recommendations from EAS and EFLM. Atherosclerosis, 2020, 294, 46-61.
[] [PMID: 31928713]
Feig, J.E.; Hewing, B.; Smith, J.D.; Hazen, S.L.; Fisher, E.A. High-density lipoprotein and atherosclerosis regression: evidence from preclinical and clinical studies. Circ. Res., 2014, 114(1), 205-213.
[] [PMID: 24385513]
White, E.J.; Gyulay, G.; Lhoták, Š.; Szewczyk, M.M.; Chong, T.; Fuller, M.T.; Dadoo, O.; Fox-Robichaud, A.E.; Austin, R.C.; Trigatti, B.L.; Igdoura, S.A. Sialidase down-regulation reduces non-HDL cholesterol, inhibits leukocyte transmigration, and attenuates atherosclerosis in ApoE knockout mice. J. Biol. Chem., 2018, 293(38), 14689-14706.
[] [PMID: 30097518]
Hata, K.; Koseki, K.; Yamaguchi, K.; Moriya, S.; Suzuki, Y.; Yingsakmongkon, S.; Hirai, G.; Sodeoka, M.; von Itzstein, M.; Miyagi, T. Limited inhibitory effects of oseltamivir and zanamivir on human sialidases. Antimicrob. Agents Chemother., 2008, 52(10), 3484-3491.
[] [PMID: 18694948]
Richards, M.R.; Guo, T.; Hunter, C.D.; Cairo, C.W. Molecular dynamics simulations of viral neuraminidase inhibitors with the human neuraminidase enzymes: Insights into isoenzyme selectivity. Bioorg. Med. Chem., 2018, 26(19), 5349-5358.
[] [PMID: 29903413]
Magesh, S.; Moriya, S.; Suzuki, T.; Miyagi, T.; Ishida, H.; Kiso, M. Design, synthesis, and biological evaluation of human sialidase inhibitors. Part 1: selective inhibitors of lysosomal sialidase (NEU1). Bioorg. Med. Chem. Lett., 2008, 18(2), 532-537.
[] [PMID: 18068975]
Khedri, Z.; Li, Y.; Cao, H.; Qu, J.; Yu, H.; Muthana, M.M.; Chen, X. Synthesis of selective inhibitors against V. cholerae sialidase and human cytosolic sialidase NEU2. Org. Biomol. Chem., 2012, 10(30), 6112-6120.
[] [PMID: 22641268]
Kim, J-H.; Resende, R.; Wennekes, T.; Chen, H-M.; Bance, N.; Buchini, S.; Watts, A.G.; Pilling, P.; Streltsov, V.A.; Petric, M.; Liggins, R.; Barrett, S.; McKimm-Breschkin, J.L.; Niikura, M.; Withers, S.G. Mechanism-based covalent neuraminidase inhibitors with broad-spectrum influenza antiviral activity. Science, 2013, 340(6128), 71-75.
[] [PMID: 23429702]
Cairo, C.W. Inhibitors of the human neuraminidase enzymes. MedChemComm, 2014, 5(8), 1067-1074.
Guo, T.; Dätwyler, P.; Demina, E.; Richards, M.R.; Ge, P.; Zou, C.; Zheng, R.; Fougerat, A.; Pshezhetsky, A.V.; Ernst, B.; Cairo, C.W. Selective inhibitors of human neuraminidase 3. J. Med. Chem., 2018, 61(5), 1990-2008.
[] [PMID: 29425031]
Guo, T.; Héon-Roberts, R.; Zou, C.; Zheng, R.; Pshezhetsky, A.V.; Cairo, C.W. Selective inhibitors of human neuraminidase 1 (NEU1). J. Med. Chem., 2018, 61(24), 11261-11279.
[] [PMID: 30457869]
Li, J.; van der Wal, D.E.; Zhu, G.; Xu, M.; Yougbare, I.; Ma, L.; Vadasz, B.; Carrim, N.; Grozovsky, R.; Ruan, M.; Zhu, L.; Zeng, Q.; Tao, L.; Zhai, Z.M.; Peng, J.; Hou, M.; Leytin, V.; Freedman, J.; Hoffmeister, K.M.; Ni, H. Desialylation is a mechanism of Fc-independent platelet clearance and a therapeutic target in immune thrombocytopenia. Nat. Commun., 2015, 6(6), 7737.
[] [PMID: 26185093]
Dupont, A.; Soukaseum, C.; Cheptou, M.; Adam, F.; Nipoti, T.; Lourenco-Rodrigues, M.D.; Legendre, P.; Proulle, V.; Rauch, A.; Kawecki, C.; Bryckaert, M.; Rosa, J.P.; Paris, C.; Ternisien, C.; Boisseau, P.; Goudemand, J.; Borgel, D.; Lasne, D.; Maurice, P.; Lenting, P.J.; Denis, C.V.; Susen, S.; Kauskot, A. Relevance of platelet desialylation and thrombocytopenia in type 2B von Willebrand disease: preclinical and clinical evidence. Haematologica, 2019, 104(12), 2493-2500.
[] [PMID: 30819911]
Hyun, S.W.; Liu, A.; Liu, Z.; Cross, A.S.; Verceles, A.C.; Magesh, S.; Kommagalla, Y.; Kona, C.; Ando, H.; Luzina, I.G.; Atamas, S.P.; Piepenbrink, K.H.; Sundberg, E.J.; Guang, W.; Ishida, H.; Lillehoj, E.P.; Goldblum, S.E. The NEU1-selective sialidase inhibitor, C9-butyl-amide-DANA, blocks sialidase activity and NEU1-mediated bioactivities in human lung in vitro and murine lung in vivo. Glycobiology, 2016, 26(8), 834-849.
[] [PMID: 27226251]
Sasaki, N.; Itakura, Y.; Toyoda, M. Gangliosides contribute to vascular insulin resistance. Int. J. Mol. Sci., 2019, 20(8), 1819.
[] [PMID: 31013778]
Hevey, R. Strategies for the development of glycomimetic drug candidates. Pharmaceuticals (Basel), 2019, 12(2), 55.
[] [PMID: 30978966]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy