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Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Research Article

ORF7a Palsies Macrophage to Worsen Diabetes by SMB/BPI/ABC Domains and PARP/Cap/Cyclin Enzyme System

Author(s): Wenzhong Liu* and Hualan Li

Volume 20, Issue 1, 2023

Published on: 18 April, 2023

Page: [19 - 38] Pages: 20

DOI: 10.2174/1570164620666230314102530

Price: $65

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Abstract

Background: Such factors as diabetes and obesity can dramatically worsen COVID-19 symptoms. In addition, macrophage accumulation in adipose tissue is related to obesity. Therefore, macrophages play a significant role in raising COVID-19 susceptibility and severity in diabetes and obese patients.

Methods: In this study, the functional impact of SARS-CoV-2 ORF7a on macrophages was analyzed using a domain-searching bioinformatics technique. Ca2+ binding domain, kinase and phosphatase, SMB/SRCR, LBP/BPI/CETP, ABC, TIR,PARP, Flavivirus Cap enzyme, Cyclin, and other domains have been identified in SARS-CoV-2 ORF7a. ORF7a binds to oxidized low-density lipoprotein cholesterol particles by the macrophage receptor-like domains such as SMB/SRCR and enters macrophages via macropinocytosis. Then, ORF7a prevents 18 S rRNA maturation and adds flavivirus cap 0/1/2 to mRNA to interfere with transcription and translation via PARP, Flavivirus Cap enzyme, and other associated domains.

Results: ORF7a activates and promotes G2/M phase transition via cyclin-related enzymatic activity domains.

Conclusion: The destructive activity of ORF7a hijacks the nitric oxide release pathway of macrophages and promotes macrophage death, enabling the virus to elude the innate immune system and aggravate diabetes-related problems in patients.

Graphical Abstract

[1]
Kruglikov, I.L.; Shah, M.; Scherer, P.E. Obesity and diabetes as comorbidities for COVID-19: Underlying mechanisms and the role of viral–bacterial interactions. eLife, 2020, 9, e61330.
[http://dx.doi.org/10.7554/eLife.61330] [PMID: 32930095]
[2]
Kruglikov, I.L.; Scherer, P.E. The role of adipocytes and adipocyte-like cells in the severity of COVID-19 infections. Obesity (Silver Spring), 2020, 28(7), 1187-1190.
[http://dx.doi.org/10.1002/oby.22856] [PMID: 32339391]
[3]
Lim, S.; Bae, J.H.; Kwon, H-S.; Nauck, M.A. COVID-19 and diabetes mellitus: From pathophysiology to clinical management. Nat. Rev. Endocrinol., 2020, 1-20.
[PMID: 33188364]
[4]
Jimenez-Duran, G.; Luque-Martin, R.; Patel, M.; Koppe, E.; Bernard, S.; Sharp, C.; Buchan, N.; Rea, C.; de Winther, M.P.J.; Turan, N.; Angell, D.; Wells, C.A.; Cousins, R.; Mander, P.K.; Masters, S.L. Pharmacological validation of targets regulating CD14 during macrophage differentiation. EBioMedicine, 2020, 61, 103039.
[http://dx.doi.org/10.1016/j.ebiom.2020.103039] [PMID: 33038762]
[5]
Pence, B.D. Severe COVID-19 and aging: are monocytes the key? Geroscience, 2020, 42(4), 1051-1061.
[http://dx.doi.org/10.1007/s11357-020-00213-0] [PMID: 32556942]
[6]
Huang, C.; Wang, Y.; Li, X.; Ren, L.; Zhao, J.; Hu, Y.; Zhang, L.; Fan, G.; Xu, J.; Gu, X.; Cheng, Z.; Yu, T.; Xia, J.; Wei, Y.; Wu, W.; Xie, X.; Yin, W.; Li, H.; Liu, M.; Xiao, Y.; Gao, H.; Guo, L.; Xie, J.; Wang, G.; Jiang, R.; Gao, Z.; Jin, Q.; Wang, J.; Cao, B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 2020, 395(10223), 497-506.
[http://dx.doi.org/10.1016/S0140-6736(20)30183-5] [PMID: 31986264]
[7]
Yuki, K.; Fujiogi, M.; Koutsogiannaki, S. COVID-19 pathophysiology: A review. Clin. Immunol., 2020, 215, 108427.
[http://dx.doi.org/10.1016/j.clim.2020.108427] [PMID: 32325252]
[8]
Xu, E.; Xie, Y.; Al-Aly, Z. Risks and burdens of incident dyslipidaemia in long COVID: A cohort study. Lancet, 2023, 11(2), 120-128.
[http://dx.doi.org/10.1016/S2213-8587(22)00355-2]
[9]
Dai, J.; Wang, H.; Liao, Y.; Tan, L.; Sun, Y.; Song, C.; Liu, W.; Qiu, X.; Ding, C. Coronavirus infection and cholesterol metabolism. Front. Immunol., 2022, 13, 791267.
[http://dx.doi.org/10.3389/fimmu.2022.791267] [PMID: 35529872]
[10]
Fan, J.; Wang, H.; Ye, G.; Cao, X.; Xu, X.; Tan, W. Low-density lipoprotein is a potential predictor of poor prognosis in patients with coronavirus disease 2019. Metabolism, 2020, 107, 154243.
[11]
Zhao, T.; Wang, C.; Duan, B.; Yang, P.; Wu, J.; Zhang, Q. Altered lipid profile in COVID-19 patients and metabolic reprogramming. Front. Microbiol., 2022, 13, 863802.
[http://dx.doi.org/10.3389/fmicb.2022.863802] [PMID: 35633693]
[12]
Kowalska, K.; Sabatowska, Z.; Forycka, J. Młynarska, E.; Franczyk, B.; Rysz, J. The influence of sars-cov-2 infection on lipid metabolism—the potential use of lipid-lowering agents in COVID-19 management. Biomedicines, 2022, 10(9), 2320.
[http://dx.doi.org/10.3390/biomedicines10092320]
[13]
Nesto, R.W. LDL cholesterol lowering in type 2 diabetes: What is the optimum approach? Clin. Diabetes, 2008, 26(1), 8-13.
[http://dx.doi.org/10.2337/diaclin.26.1.8]
[14]
Chang, C.K.; Tso, T.K.; Snook, J.T.; Huang, Y.S.; Lozano, R.A.; Zipf, W.B. Cholesteryl ester transfer and cholesterol esterification in type 1 diabetes: Relationships with plasma glucose. Acta Diabetol., 2001, 38(1), 37-42.
[http://dx.doi.org/10.1007/s005920170027] [PMID: 11487175]
[15]
Park, Y.M.R.; Kashyap, S.A.; Major, J.; Silverstein, R.L. Insulin promotes macrophage foam cell formation: Potential implications in diabetes-related atherosclerosis. Lab. Invest., 2012, 92(8), 1171-1180.
[http://dx.doi.org/10.1038/labinvest.2012.74] [PMID: 22525426]
[16]
Vergès, B. Lipid modification in type 2 diabetes: The role of LDL and HDL. Fundam. Clin. Pharmacol., 2009, 23(6), 681-685.
[http://dx.doi.org/10.1111/j.1472-8206.2009.00739.x] [PMID: 19650852]
[17]
Lesnik, P.; Rouis, M.; Skarlatos, S.; Kruth, H.S.; Chapman, M.J. Uptake of exogenous free cholesterol induces upregulation of tissue factor expression in human monocyte-derived macrophages. Proc. Natl. Acad. Sci. USA, 1992, 89(21), 10370-10374.
[http://dx.doi.org/10.1073/pnas.89.21.10370] [PMID: 1438222]
[18]
Mahlberg, F.H.; Glick, J.M.; Jerome, W.G.; Rothblat, G.H. Metabolism of cholesteryl ester lipid droplets in a J774 macrophage foam cell model. Biochim. Biophys. Acta Lipids Lipid Metab., 1990, 1045(3), 291-298.
[http://dx.doi.org/10.1016/0005-2760(90)90133-I] [PMID: 2386801]
[19]
Yu, X.H.; Fu, Y.C.; Zhang, D.W.; Yin, K.; Tang, C.K. Foam cells in atherosclerosis. Clin. Chim. Acta, 2013, 424, 245-252.
[http://dx.doi.org/10.1016/j.cca.2013.06.006] [PMID: 23782937]
[20]
Moore, K.J.; Freeman, M.W. Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler. Thromb. Vasc. Biol., 2006, 26(8), 1702-1711.
[http://dx.doi.org/10.1161/01.ATV.0000229218.97976.43] [PMID: 16728653]
[21]
Miller, Y.I.; Viriyakosol, S.; Binder, C.J.; Feramisco, J.R.; Kirkland, T.N.; Witztum, J.L. Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. J. Biol. Chem., 2003, 278(3), 1561-1568.
[http://dx.doi.org/10.1074/jbc.M209634200] [PMID: 12424240]
[22]
Nagy, L.; Tontonoz, P.; Alvarez, J.G.A.; Chen, H.; Evans, R.M. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell, 1998, 93(2), 229-240.
[http://dx.doi.org/10.1016/S0092-8674(00)81574-3] [PMID: 9568715]
[23]
Zhou, Z.; Huang, C.; Zhou, Z.; Huang, Z.; Su, L.; Kang, S.; Chen, X.; Chen, Q.; He, S.; Rong, X.; Xiao, F.; Chen, J.; Chen, S. Structural insight reveals SARS-CoV-2 ORF7a as an immunomodulating factor for human CD14+ monocytes. iScience, 2021, 24(3), 102187.
[http://dx.doi.org/10.1016/j.isci.2021.102187] [PMID: 33615195]
[24]
Nizamudeen, Z.A.; Xu, E.R.; Karthik, V.; Halawa, M.; Arkill, K.P.; Jackson, A.M.; Bates, D.O.; Emsley, J. Structural assessment of SARS-CoV2 accessory protein ORF7a predicts LFA-1 and Mac-1 binding potential. Biosci. Rep., 2021, 41(1), BSR20203837.
[http://dx.doi.org/10.1042/BSR20203837] [PMID: 33305306]
[25]
Arshad, N.; Laurent-Rolle, M.; Ahmed, W.S.; Hsu, J.C.C.; Mitchell, S.M.; Pawlak, J.; Sengupta, D.; Biswas, K.H.; Cresswell, P. SARS-CoV-2 accessory proteins ORF7a and ORF3a use distinct mechanisms to down-regulate MHC-I surface expression. Proc. Natl. Acad. Sci. USA, 2023, 120(1), e2208525120.
[http://dx.doi.org/10.1073/pnas.2208525120] [PMID: 36574644]
[26]
García-García, T.; Fernández-Rodríguez, R.; Redondo, N.; de Lucas-Rius, A.; Zaldívar-López, S.; López-Ayllón, B.D.; Suárez-Cárdenas, J.M.; Jiménez-Marín, Á.; Montoya, M.; Garrido, J.J. Impairment of antiviral immune response and disruption of cellular functions by SARS-CoV-2 ORF7a and ORF7b. iScience, 2022, 25(11), 105444.
[http://dx.doi.org/10.1016/j.isci.2022.105444] [PMID: 36310646]
[27]
Kluftinger, J.L.; Kelly, N.M.; Jost, B.H.; Hancock, R.E. Fibronectin as an enhancer of nonopsonic phagocytosis of Pseudomonas aeruginosa by macrophages. Infect. Immun., 1989, 57(9), 2782-2785.
[http://dx.doi.org/10.1128/iai.57.9.2782-2785.1989] [PMID: 2503446]
[28]
Proctor, R.A. Fibronectin: an enhancer of phagocyte function. Clin. Infect. Dis., 1987, 9(Suppl. 4), S412-S419.
[http://dx.doi.org/10.1093/clinids/9.Supplement_4.S412] [PMID: 3326137]
[29]
Abraham, L.C.; Dice, J.F.; Lee, K.; Kaplan, D.L. Phagocytosis and remodeling of collagen matrices. Exp. Cell Res., 2007, 313(5), 1045-1055.
[http://dx.doi.org/10.1016/j.yexcr.2006.12.019] [PMID: 17276428]
[30]
Mylvaganam, S.; Freeman, S.A.; Grinstein, S. The cytoskeleton in phagocytosis and macropinocytosis. Curr. Biol., 2021, 31(10), R619-R632.
[http://dx.doi.org/10.1016/j.cub.2021.01.036] [PMID: 34033794]
[31]
de Villiers, W.J.S.; Smart, E.J. Macrophage scavenger receptors and foam cell formation. J. Leukoc. Biol., 1999, 66(5), 740-746.
[http://dx.doi.org/10.1002/jlb.66.5.740] [PMID: 10577503]
[32]
Wang, N.; Westerterp, M. ABC Transporters, Cholesterol Efflux, and Implications for Cardiovascular Diseases.In: Lipid Transfer in Lipoprotein Metabolism and Cardiovascular Disease; Jiang, X-C., Ed.; Springer Singapore: Singapore, 2020, pp. 67-83.
[http://dx.doi.org/10.1007/978-981-15-6082-8_6]
[33]
Schmitz, G.; Kaminski, W.E. ABC transporters and cholesterol metabolism. Front. Biosci., 2001, 6(3), A622.
[http://dx.doi.org/10.2741/A622] [PMID: 11229879]
[34]
Xu, Y.; Du, X.; Turner, N.; Brown, A.J.; Yang, H. Enhanced acyl-CoA:cholesterol acyltransferase activity increases cholesterol levels on the lipid droplet surface and impairs adipocyte function. J. Biol. Chem., 2019, 294(50), 19306-19321.
[http://dx.doi.org/10.1074/jbc.RA119.011160] [PMID: 31727739]
[35]
Katz, S.S.; Shipley, G.G.; Small, D.M. Physical chemistry of the lipids of human atherosclerotic lesions. Demonstration of a lesion intermediate between fatty streaks and advanced plaques. J. Clin. Invest., 1976, 58(1), 200-211.
[http://dx.doi.org/10.1172/JCI108450] [PMID: 932206]
[36]
Katsuren, K.; Tamura, T.; Arashiro, R.; Takata, K.; Matsuura, T.; Niikawa, N.; Ohta, T. Structure of the human acyl-CoA:cholesterol acyltransferase-2 (ACAT-2) gene and its relation to dyslipidemia. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2001, 1531(3), 230-240.
[http://dx.doi.org/10.1016/S1388-1981(01)00106-8] [PMID: 11325614]
[37]
Chatterjee, B.; Thakur, S.S. SARS-CoV-2 Infection Triggers Phosphorylation: Potential Target for Anti-COVID-19 Therapeutics. Front. Immunol., 2022, 13, 829474.
[http://dx.doi.org/10.3389/fimmu.2022.829474] [PMID: 35251015]
[38]
Martin-Sancho, L.; Lewinski, M.K.; Pache, L.; Stoneham, C.A.; Yin, X. Pratt, D Functional Landscape of SARS-CoV-2 Cellular Restriction. SSRN Electronic J, 2020.
[http://dx.doi.org/10.2139/ssrn.3698891]
[39]
Wang, J.; Yannie, P.J.; Ghosh, S.S.; Ghosh, S. Regulation of interleukin‐ 1 beta secretion from macrophages via modulation of potassium ion (K+) channel activity. FEBS Lett., 2019, 593(11), 1873-3468.13395.
[http://dx.doi.org/10.1002/1873-3468.13395] [PMID: 31026357]
[40]
Duewell, P.; Kono, H.; Rayner, K.J.; Sirois, C.M.; Vladimer, G.; Bauernfeind, F.G.; Abela, G.S.; Franchi, L.; Nuñez, G.; Schnurr, M.; Espevik, T.; Lien, E.; Fitzgerald, K.A.; Rock, K.L.; Moore, K.J.; Wright, S.D.; Hornung, V.; Latz, E. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature, 2010, 464(7293), 1357-1361.
[http://dx.doi.org/10.1038/nature08938] [PMID: 20428172]
[41]
Hänel, K.; Willbold, D. SARS-CoV accessory protein 7a directly interacts with human LFA-1. Biol. Chem., 2007, 388(12), 1325-1332.
[42]
Nemudryi, A.; Nemudraia, A.; Wiegand, T.; Nichols, J.; Snyder, D.T.; Hedges, J.F.; Cicha, C.; Lee, H.; Vanderwood, K.K.; Bimczok, D.; Jutila, M.A.; Wiedenheft, B. SARS-CoV-2 genomic surveillance identifies naturally occurring truncation of ORF7a that limits immune suppression. Cell Rep., 2021, 35(9), 109197.
[http://dx.doi.org/10.1016/j.celrep.2021.109197] [PMID: 34043946]
[43]
Cao, Z.; Xia, H.; Rajsbaum, R.; Xia, X.; Wang, H.; Shi, P.Y. Ubiquitination of SARS-CoV-2 ORF7a promotes antagonism of interferon response. Cell. Mol. Immunol., 2021, 18(3), 746-748.
[http://dx.doi.org/10.1038/s41423-020-00603-6] [PMID: 33473190]
[44]
Timilsina, U.; Umthong, S.; Ivey, E.B.; Waxman, B.; Stavrou, S. SARS-CoV-2 ORF7a potently inhibits the antiviral effect of the host factor SERINC5. Nat. Commun., 2022, 13(1), 2935.
[http://dx.doi.org/10.1038/s41467-022-30609-9] [PMID: 35618710]
[45]
Nelson, C.A.; Pekosz, A.; Lee, C.A.; Diamond, M.S.; Fremont, D.H. Structure and intracellular targeting of the SARS-coronavirus Orf7a accessory protein. Structure, 2005, 13(1), 75-85.
[http://dx.doi.org/10.1016/j.str.2004.10.010] [PMID: 15642263]
[46]
Zhu, J.; Lee, J.G.; van de Leemput, J.; Lee, H.; Han, Z. Functional analysis of SARS-CoV-2 proteins in Drosophila identifies Orf6-induced pathogenic effects with Selinexor as an effective treatment. Cell Biosci., 2021, 11(1), 59.
[http://dx.doi.org/10.1186/s13578-021-00567-8] [PMID: 33766136]
[47]
Tan, Y.X.; Tan, T.H.P.; Lee, M.J.R.; Tham, P.Y.; Gunalan, V.; Druce, J.; Birch, C.; Catton, M.; Fu, N.Y.; Yu, V.C.; Tan, Y.J. Induction of apoptosis by the severe acute respiratory syndrome coronavirus 7a protein is dependent on its interaction with the Bcl-XL protein. J. Virol., 2007, 81(12), 6346-6355.
[http://dx.doi.org/10.1128/JVI.00090-07] [PMID: 17428862]
[48]
Jackman, M.; Firth, M.; Pines, J. Human cyclins B1 and B2 are localized to strikingly different structures: B1 to microtubules, B2 primarily to the Golgi apparatus. EMBO J., 1995, 14(8), 1646-1654.
[http://dx.doi.org/10.1002/j.1460-2075.1995.tb07153.x] [PMID: 7737117]
[49]
Sui, L.; Li, L.; Zhao, Y.; Zhao, Y.; Hao, P.; Guo, X.; Wang, W.; Wang, G.; Li, C.; Liu, Q. Host cell cycle checkpoint as antiviral target for SARS-CoV-2 revealed by integrative transcriptome and proteome analyses. Signal Transduct. Target. Ther., 2023, 8(1), 21.
[http://dx.doi.org/10.1038/s41392-022-01296-1] [PMID: 36596760]
[50]
Yuan, X.; Wu, J.; Shan, Y.; Yao, Z.; Dong, B.; Chen, B.; Zhao, Z.; Wang, S.; Chen, J.; Cong, Y. SARS coronavirus 7a protein blocks cell cycle progression at G0/G1 phase via the cyclin D3/pRb pathway. Virology, 2006, 346(1), 74-85.
[http://dx.doi.org/10.1016/j.virol.2005.10.015] [PMID: 16303160]
[51]
Kanzawa, N.; Nishigaki, K.; Hayashi, T.; Ishii, Y.; Furukawa, S.; Niiro, A.; Yasui, F.; Kohara, M.; Morita, K.; Matsushima, K.; Le, M.Q.; Masuda, T.; Kannagi, M. Augmentation of chemokine production by severe acute respiratory syndrome coronavirus 3a/X1 and 7a/X4 proteins through NF-κB activation. FEBS Lett., 2006, 580(30), 6807-6812.
[http://dx.doi.org/10.1016/j.febslet.2006.11.046] [PMID: 17141229]
[52]
Kopecky-Bromberg, S.A.; Martinez-Sobrido, L.; Palese, P. 7a protein of severe acute respiratory syndrome coronavirus inhibits cellular protein synthesis and activates p38 mitogen-activated protein kinase. J. Virol., 2006, 80(2), 785-793.
[http://dx.doi.org/10.1128/JVI.80.2.785-793.2006] [PMID: 16378980]
[53]
Tan, Y.J.; Fielding, B.C.; Goh, P.Y.; Shen, S.; Tan, T.H.P.; Lim, S.G.; Hong, W. Overexpression of 7a, a protein specifically encoded by the severe acute respiratory syndrome coronavirus, induces apoptosis via a caspase-dependent pathway. J. Virol., 2004, 78(24), 14043-14047.
[http://dx.doi.org/10.1128/JVI.78.24.14043-14047.2004] [PMID: 15564512]
[54]
Hofmann, A.; Putz, F.; Büttner-Herold, M.; Hecht, M.; Fietkau, R.; Distel, L.V. Increase in non-professional phagocytosis during the progression of cell cycle. PLoS One, 2021, 16(2), e0246402.
[http://dx.doi.org/10.1371/journal.pone.0246402] [PMID: 33544774]
[55]
Gordon, D.E.; Jang, G.M.; Bouhaddou, M.; Xu, J.; Obernier, K.; White, K.M.; O’Meara, M.J.; Rezelj, V.V.; Guo, J.Z.; Swaney, D.L.; Tummino, T.A.; Hüttenhain, R.; Kaake, R.M.; Richards, A.L.; Tutuncuoglu, B.; Foussard, H.; Batra, J.; Haas, K.; Modak, M.; Kim, M.; Haas, P.; Polacco, B.J.; Braberg, H.; Fabius, J.M.; Eckhardt, M.; Soucheray, M.; Bennett, M.J.; Cakir, M.; McGregor, M.J.; Li, Q.; Meyer, B.; Roesch, F.; Vallet, T.; Mac Kain, A.; Miorin, L.; Moreno, E.; Naing, Z.Z.C.; Zhou, Y.; Peng, S.; Shi, Y.; Zhang, Z.; Shen, W.; Kirby, I.T.; Melnyk, J.E.; Chorba, J.S.; Lou, K.; Dai, S.A.; Barrio-Hernandez, I.; Memon, D.; Hernandez-Armenta, C.; Lyu, J.; Mathy, C.J.P.; Perica, T.; Pilla, K.B.; Ganesan, S.J.; Saltzberg, D.J.; Rakesh, R.; Liu, X.; Rosenthal, S.B.; Calviello, L.; Venkataramanan, S.; Liboy-Lugo, J.; Lin, Y.; Huang, X.P.; Liu, Y.; Wankowicz, S.A.; Bohn, M.; Safari, M.; Ugur, F.S.; Koh, C.; Savar, N.S.; Tran, Q.D.; Shengjuler, D.; Fletcher, S.J.; O’Neal, M.C.; Cai, Y.; Chang, J.C.J.; Broadhurst, D.J.; Klippsten, S.; Sharp, P.P.; Wenzell, N.A.; Kuzuoglu-Ozturk, D.; Wang, H.Y.; Trenker, R.; Young, J.M.; Cavero, D.A.; Hiatt, J.; Roth, T.L.; Rathore, U.; Subramanian, A.; Noack, J.; Hubert, M.; Stroud, R.M.; Frankel, A.D.; Rosenberg, O.S.; Verba, K.A.; Agard, D.A.; Ott, M.; Emerman, M.; Jura, N.; von Zastrow, M.; Verdin, E.; Ashworth, A.; Schwartz, O.; d’Enfert, C.; Mukherjee, S.; Jacobson, M.; Malik, H.S.; Fujimori, D.G.; Ideker, T.; Craik, C.S.; Floor, S.N.; Fraser, J.S.; Gross, J.D.; Sali, A.; Roth, B.L.; Ruggero, D.; Taunton, J.; Kortemme, T.; Beltrao, P.; Vignuzzi, M.; García-Sastre, A.; Shokat, K.M.; Shoichet, B.K.; Krogan, N.J.A. SARS-CoV-2 protein interaction map reveals targets for drug repurposing. Nature, 2020, 583(7816), 459-468.
[http://dx.doi.org/10.1038/s41586-020-2286-9] [PMID: 32353859]
[56]
Bock, F.J.; Todorova, T.T.; Chang, P. RNA Regulation by Poly(ADP-Ribose). Polymerases. Mol. Cell, 2015, 58(6), 959-969.
[http://dx.doi.org/10.1016/j.molcel.2015.01.037] [PMID: 26091344]
[57]
Saxena, N.; Chandra, N.C. Cholesterol: A Prelate in Cell Nucleus and its Serendipity. Curr. Mol. Med., 2021, 20(9), 692-707.
[http://dx.doi.org/10.2174/1566524020666200413112030] [PMID: 32282300]
[58]
Torres, A.G.; Perna, N.T.; Burland, V.; Ruknudin, A.; Blattner, F.R.; Kaper, J.B. Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol. Microbiol., 2002, 45(4), 951-966.
[http://dx.doi.org/10.1046/j.1365-2958.2002.03094.x] [PMID: 12180916]
[59]
Saurin, W.; Hofnung, M.; Dassa, E. Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J. Mol. Evol., 1999, 48(1), 22-41.
[http://dx.doi.org/10.1007/PL00006442] [PMID: 9873074]
[60]
Holland, I.B.; Blight, M.A. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol., 1999, 293(2), 381-399.
[http://dx.doi.org/10.1006/jmbi.1999.2993] [PMID: 10529352]
[61]
Higgins, C.F. ABC transporters: physiology, structure and mechanism – an overview. Res. Microbiol., 2001, 152(3-4), 205-210.
[http://dx.doi.org/10.1016/S0923-2508(01)01193-7] [PMID: 11421269]
[62]
Reizer, J.; Reizer, A.; Saier, M.H. Jr A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Protein Sci., 1992, 1(10), 1326-1332.
[63]
Higgins, C.F.; Gallagher, M.P.; Mimmack, M.L.; Pearce, S.R. A family of closely related ATP-binding subunits from prokaryotic and eukaryotic cells. BioEssays, 1988, 8(4), 111-116.
[http://dx.doi.org/10.1002/bies.950080406] [PMID: 3288195]
[64]
Murina, V.; Kasari, M.; Takada, H.; Hinnu, M.; Saha, C.K.; Grimshaw, J.W.; Seki, T.; Reith, M.; Putrinš, M.; Tenson, T.; Strahl, H.; Hauryliuk, V.; Atkinson, G.C. ABCF ATPases Involved in Protein Synthesis, Ribosome Assembly and Antibiotic Resistance: Structural and Functional Diversification across the Tree of Life. J. Mol. Biol., 2019, 431(18), 3568-3590.
[http://dx.doi.org/10.1016/j.jmb.2018.12.013] [PMID: 30597160]
[65]
Wang, L.; Haeusler, R.A.; Good, P.D.; Thompson, M.; Nagar, S.; Engelke, D.R. Silencing near tRNA genes requires nucleolar localization. J. Biol. Chem., 2005, 280(10), 8637-8639.
[http://dx.doi.org/10.1074/jbc.C500017200] [PMID: 15654076]
[66]
Sgarlata, C.; Pérez-Martín, J. The cdc25 phosphatase is essential for the G2/M phase transition in the basidiomycete yeast Ustilago maydis. Mol. Microbiol., 2005, 58(5), 1482-1496.
[http://dx.doi.org/10.1111/j.1365-2958.2005.04925.x] [PMID: 16313631]
[67]
Wang, R.; He, G.; Nelman-Gonzalez, M.; Ashorn, C.L.; Gallick, G.E.; Stukenberg, P.T.; Kirschner, M.W.; Kuang, J. Regulation of Cdc25C by ERK-MAP kinases during the G2/M transition. Cell, 2007, 128(6), 1119-1132.
[http://dx.doi.org/10.1016/j.cell.2006.11.053] [PMID: 17382881]
[68]
Das, S.; Chandrasekaran, A.P.; Suresh, B.; Haq, S.; Kang, J.H.; Lee, S.J.; Kim, J.; Kim, J.; Lee, S.; Kim, H.H.; Kim, K.S.; Ramakrishna, S. Genome-scale screening of deubiquitinase subfamily identifies USP3 as a stabilizer of Cdc25A regulating cell cycle in cancer. Cell Death Differ., 2020, 27(11), 3004-3020.
[http://dx.doi.org/10.1038/s41418-020-0557-5] [PMID: 32415280]
[69]
Spanakis, N.; Kassela, K.; Dovrolis, N.; Bampali, M.; Gatzidou, E.; Kafasi, A.; Froukala, E.; Stavropoulou, A.; Lilakos, K.; Veletza, S.; Tsiodras, S.; Tsakris, A.; Karakasiliotis, I. A main event and multiple introductions of SARS‐CoV‐2 initiated the COVID-19 epidemic in Greece. J. Med. Virol., 2021, 93(5), 2899-2907.
[http://dx.doi.org/10.1002/jmv.26778] [PMID: 33410223]
[70]
Huang, C.; Ito, N.; Tseng, C.T.K.; Makino, S. Severe acute respiratory syndrome coronavirus 7a accessory protein is a viral structural protein. J. Virol., 2006, 80(15), 7287-7294.
[http://dx.doi.org/10.1128/JVI.00414-06] [PMID: 16840309]
[71]
Addetia, A.; Xie, H.; Roychoudhury, P.; Shrestha, L.; Loprieno, M.; Huang, M.L.; Jerome, K.R.; Greninger, A.L. Identification of multiple large deletions in ORF7a resulting in in-frame gene fusions in clinical SARS-CoV-2 isolates. J. Clin. Virol., 2020, 129, 104523-104523.
[http://dx.doi.org/10.1016/j.jcv.2020.104523] [PMID: 32623351]
[72]
Hänel, K.; Stangler, T.; Stoldt, M.; Willbold, D. Solution structure of the X4 protein coded by the SARS related coronavirus reveals an immunoglobulin like fold and suggests a binding activity to integrin I domains. J. Biomed. Sci., 2006, 13(3), 281-293.
[http://dx.doi.org/10.1007/s11373-005-9043-9] [PMID: 16328780]
[73]
Lau, S.Y.; Wang, P.; Mok, B.W.Y.; Zhang, A.J.; Chu, H.; Lee, A.C.Y.; Deng, S.; Chen, P.; Chan, K.H.; Song, W.; Chen, Z.; To, K.K.W.; Chan, J.F.W.; Yuen, K.Y.; Chen, H. Attenuated SARS-CoV-2 variants with deletions at the S1/S2 junction. Emerg. Microbes Infect., 2020, 9(1), 837-842.
[http://dx.doi.org/10.1080/22221751.2020.1756700] [PMID: 32301390]
[74]
Feron, O.; Dessy, C.; Moniotte, S.; Desager, J.P.; Balligand, J.L. Hypercholesterolemia decreases nitric oxide production by promoting the interaction of caveolin and endothelial nitric oxide synthase. J. Clin. Invest., 1999, 103(6), 897-905.
[http://dx.doi.org/10.1172/JCI4829] [PMID: 10079111]
[75]
O’Donnell, V.B.; Freeman, B.A. Interactions between nitric oxide and lipid oxidation pathways: implications for vascular disease. Circ. Res., 2001, 88(1), 12-21.
[http://dx.doi.org/10.1161/01.RES.88.1.12] [PMID: 11139468]
[76]
Palmieri, E.M.; McGinity, C.; Wink, D.A.; McVicar, D.W. Nitric Oxide in Macrophage Immunometabolism: Hiding in Plain Sight. Metabolites, 2020, 10(11), 429.
[http://dx.doi.org/10.3390/metabo10110429] [PMID: 33114647]

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