Top

Published in:

01-05-2020 | Influenza | Original Article

Influence of cellular lipid content on influenza A virus replication

Published in: Archives of Virology | Issue 5/2020

Abstract

Influenza A virus (IAV) depends on the metabolism of its cellular host to provide energy and essential factors, including lipids, for viral replication. Previous studies have shown that fatty acids (FAs) play an important role in IAV replication and that inhibition of FA biosynthesis can diminish viral replication. However, cellular lipids can either be synthesized intracellularly or be imported from the extracellular environment. Interfering with FA import mechanisms may reduce the cellular lipid content and inhibit IAV replication. To test this hypothesis, MDCK and Detroit 562 cells were infected with IAV followed by exposure to palmitic acid and inhibitors of FA import. Replication of IAV significantly increased when infected cells were supplied with palmitic acid. This enhancement could be reduced by adding an FA import inhibitor. The addition of palmitic acid significantly increased the cellular lipid content, and this increased level was reduced by treatment with an FA import inhibitor. These results show that reducing the cellular lipid level might be an approach for IAV therapy.

Alvisi G, Madan V, Bartenschlager R (2011) Hepatitis c virus and host cell lipids: An intimate connection. RNA Biol 8(2):258–269CrossRefPubMed

Anschau A, Caruso CS, Kuhn RC, Franco TT (2017) Validation of the sulfo-phospho-vanillin (SPV) method for the determination of lipid content in oleaginous microorganisms. Braz J Chem Eng 34(1):19–27CrossRef

Basu J (2004) Protein palmitoylation and dynamic modulation of protein function. Curr Sci 87(2):12–17

Blanc M, Blaskovic S, van der Goot FG (2013) Palmitoylation pathogens and their host. Biochem Soc Trans 41(1):84–88CrossRefPubMed

Coe NR, Smith AJ, Frohnert BI, Watkins PA, Bernlohr DA (1999) The fatty acid transport protein (FATP1) is a very long chain acyl-CoA synthetase. J Biol Chem 274(51):36300–36304CrossRefPubMed

Cui L, Zheng D, Lee YH, Chan TK, Kumar Y, Ho WE et al (2016) Metabolomics investigation reveals metabolite mediators associated with acute lung injury and repair in a murine model of influenza pneumonia. Sci Rep 6:26076CrossRefPubMedPubMedCentral

Færgeman NJ, Dirusso CC, Elberger A, Knudsen J, Black PN (1997) Disruption of the Saccharomyces cerevisiae homologue to the murine fatty acid transport protein impairs uptake and growth on long-chain fatty acids. J Biol Chem 272(13):8531–8538CrossRefPubMed

Gao X, Wu J, Qian Y, Fu L, Wu G, Xu C et al (2014) Oxidized high-density lipoprotein impairs the function of human renal proximal tubule epithelial cells through CD36. Int J Mol Med 34(2):564–572CrossRefPubMed

Glatz JFC, Luiken JJFP (2018) Dynamic role of the transmembrane glycoprotein CD36 (SR-B2) in cellular fatty acid uptake and utilization. J Lipid Res 59(7):1084–1093CrossRefPubMedPubMedCentral

10.

Goldberg IJ, Eckel RH, Abumrad NA (2008) Regulation of fatty acid uptake into tissues: lipoprotein lipase- and CD36-mediated pathways. J Lipid Res 50(Suppl):S86–S90PubMed

11.

Hall AM, Smith AJ, Bernlohr DA (2003) Characterization of the acyl-CoA synthetase activity of purified murine fatty acid transport protein 1. J Biol Chem 278(44):43008–43013CrossRefPubMed

12.

Heaton NS, Randall G (2011) Multifaceted roles for lipids in viral infection. Trends Microbiol 19(7):368–375CrossRefPubMedPubMedCentral

13.

Holloway GP, Chou CJ, Lally J, Stellingwerff T, Maher AC, Gavrilova O et al (2011) Increasing skeletal muscle fatty acid transport protein 1 (FATP1) targets fatty acids to oxidation and does not predispose mice to diet-induced insulin resistance. Diabetologia 54(6):1457–1467CrossRefPubMed

14.

Iwao Y, Nakajou K, Nagai R, Kitamura K, Anraku M, Maruyama T et al (2008) CD36 is one of important receptors promoting renal tubular injury by advanced oxidation protein products. Am J Physiol Ren Physiol 295(6):F1871–F1880CrossRef

15.

Ibricevic A, Pekosz A, Walter MJ, Newby C, Battaile JT, Brown EG et al (2006) Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol 80(15):7469–7480CrossRefPubMedPubMedCentral

16.

Kilbourne ED (2006) Influenza pandemics of the 20th century. Emerg Infect Dis 12:9–14CrossRefPubMedPubMedCentral

17.

Kim JK, Gimeno RE, Higashimori T, Kim H-J, Choi H, Punreddy S et al (2004) Inactivation of fatty acid transport protein 1 prevents fat-induced insulin resistance in skeletal muscle. J Clin Investig 113(5):756–763CrossRefPubMedPubMedCentral

18.

Bensaad K, Harris AL (2016) Lipid metabolism. In: Koumenis C, Hammond E, Giaccia A (eds) Tumor microenvironment and cellular stress: signaling, metabolism, imaging, and therapeutic targets. Springer, New York, p 18

19.

Kuda O, Pietka TA, Demianova Z, Kudova E, Cvacka J, Kopecky J et al (2013) Sulfo-N-succinimidyl oleate (SSO) inhibits fatty acid uptake and signaling for intracellular calcium via binding CD36 lysine 164: SSO also inhibits oxidized low density lipoprotein uptake by macrophages. J Biol Chem 288(22):15547–15555CrossRefPubMedPubMedCentral

20.

Lobo S, Wiczer BM, Smith AJ, Hall AM, Bernlohr DA (2006) Fatty acid metabolism in adipocytes: functional analysis of fatty acid transport proteins 1 and 4. J Lipid Res 48(3):609–620CrossRefPubMed

21.

Glatz JFC, Luiken JJFP (2016) Myocardial fatty acid uptake. In: Lopaschuk GD, Dhalla NS (eds) Cardiac energy metabolism in health and disease. Springer, New York, p 54

22.

Lorizate M, Krausslich HG (2011) Role of lipids in virus replication. Cold Spring Harb Perspect Biol 3(10):a004820CrossRefPubMedPubMedCentral

23.

Mansor LS, Fialho MDLS, Yea G, Coumans WA, West JA, Kerr M et al (2017) Inhibition of sarcolemmal FAT/CD36 by sulfo-N-succinimidyl oleate rapidly corrects metabolism and restores function in the diabetic heart following hypoxia/reoxygenation. Cardiovasc Res 113(7):737–748CrossRefPubMedPubMedCentral

24.

Martín-Acebes Miguel A, Ángela Vázquez-Calvo, Caridi F, Sobrino F, Saiz JC (2013) Lipid involvement in viral infections: present and future perspectives for the design of antiviral strategies. INTECH Open Access Publisher, Rijeka

25.

Matsufuji T, Ikeda M, Naito A, Hirouchi M, Kanda S, Izumi M et al (2013) Arylpiperazines as fatty acid transport protein 1 (FATP1) inhibitors with improved potency and pharmacokinetic properties. Bioorg Med Chem Lett 23(9):2560–2565CrossRefPubMed

26.

Munger J, Bennett BD, Parikh A, Feng XJ, Mcardle J, Rabitz HA et al (2008) Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat Biotechnol 26(10):1179–1186CrossRefPubMedPubMedCentral

27.

Noushmehr H, Damico E, Farilla L, Hui H, Wawrowsky KA, Mlynarski W et al (2005) Fatty acid translocase (FAT/CD36) is localized on insulin-containing granules in human pancreatic β-cells and mediates fatty acid effects on insulin secretion. Diabetes 54(2):472–481CrossRefPubMed

28.

O’Hanlon R, Shaw ML (2019) Baloxavir marboxil: the new influenza drug on the market. Curr Opin Virol 35:14–18CrossRefPubMed

29.

Okamura DM, Pennathur S, Pasichnyk K, López-Guisa JM, Collins S, Febbraio M et al (2009) CD36 regulates oxidative stress and inflammation in hypercholesterolemic CKD. J Am Soc Nephrol 20(3):495–505CrossRefPubMedPubMedCentral

30.

Rocks O, Peyker A, Kahms M, Verveer PJ, Koerner C, Lumbierres M, Kuhlmann J, Waldmann H, Wittinghofer A, Bastiaens PI (2005) An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307(5716):1746–1752CrossRefPubMed

31.

Rustan AC, Drevon CA (2001) Fatty acids: structures and properties. eLS. https://doi.org/10.1038/npg.els.0003894CrossRef

32.

Schwenk RW, Holloway GP, Luiken JJ, Bonen A, Glatz JF (2010) Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins Leukot Essent Fatty Acids 82(4–6):149–154CrossRefPubMed

33.

Schaffer JE, Lodish HF (1994) Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79(3):427–436CrossRefPubMed

34.

Stapleford KA, Miller DJ (2010) Role of cellular lipids in positive-sense RNA virus replication complex assembly and function. Viruses 2(5):1055–1068CrossRefPubMedPubMedCentral

35.

Tarhda Z, Ibrahimi A (2015) Insight into the mechanism of lipids binding and uptake by CD36 receptor. Bioinformation 11(6):302–306CrossRefPubMedPubMedCentral

36.

Tomura S, Uchida M, Yonezawa T, Kobayashi M, Bonkobara M, Arai S et al (2014) Molecular cloning and gene expression of canine apoptosis inhibitor of macrophage. J Vet Med Sci 76(12):1641–1645CrossRefPubMedPubMedCentral

37.

Veit M, Serebryakova MV, Kordyukova LV (2013) Palmitoylation of influenza virus proteins. Biochem Soc Trans 41(1):50–55CrossRefPubMed

38.

Wu Q, Ortegon AM, Tsang B, Doege H, Feingold KR, Stahl A (2006) FATP1 is an insulin-sensitive fatty acid transporter involved in diet-Induced obesity. Mol Cell Biol 26(9):3455–3467CrossRefPubMedPubMedCentral

39.

Yang X, Okamura DM, Lu X, Chen Y, Moorhead J, Varghese Z et al (2017) CD36 in chronic kidney disease: novel insights and therapeutic opportunities. Nat Rev Nephrol 13(12):769–781CrossRefPubMed

Title: Influence of cellular lipid content on influenza A virus replication
Publication date: 01-05-2020
Keyword: Influenza
Published in: Archives of Virology / Issue 5/2020
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-020-04596-5

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Influence of cellular lipid content on influenza A virus replication

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2020

Fragaria vesca-associated virus 1: a new virus related to negeviruses

Metaviromic analysis reveals coinfection of papaya in western Kenya with a unique strain of Moroccan watermelon mosaic virus and a novel member of the family Alphaflexiviridae

A multiplex RT-PCR method to detect papaya meleira virus complex in adult pre-flowering plants

Molecular epidemiology of respiratory syncytial virus for 28 consecutive seasons (1990-2018) and genetic variability of the duplication region in the G gene of genotypes ON1 and BA in South Korea

Identification and complete genomic sequence of a novel sadwavirus discovered in pineapple (Ananas comosus)

Development of an antigen-capture enzyme-linked immunosorbent assay and immunochromatographic strip based on monoclonal antibodies for detection of H6 avian influenza viruses

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page