2,417
Views
24
CrossRef citations to date
0
Altmetric
Research Paper - Basic Science

Induction of a Na+/K+-ATPase-dependent form of autophagy triggers preferential cell death of human immunodeficiency virus type-1-infected macrophages

, , , & ORCID Icon
Pages 1359-1375 | Received 02 Oct 2017, Accepted 08 May 2018, Published online: 23 Jul 2018

References

  • Gulick RM, Hirsch MS, Lane HC, et al. Guidelines for the use of antiretroviral agents in adults and adolescents living with HIV. Department of health and human services. AIDSinfonihgov. 2018 Mar 27. Available from: https://aidsinfo.nih.gov/contentfiles/lvguidelines/AdultandAdolescentGL.pdf
  • Walmsley SL, Antela A, Clumeck N, et al. Dolutegravir plus abacavir-lamivudine for the treatment of HIV-1 infection. N Engl J Med. 2013 Nov 7;369(19):1807–1818. PubMed PMID: 24195548.
  • Group ISS, Lundgren JD, Babiker AG, et al. Initiation of antiretroviral therapy in early asymptomatic HIV infection. N Engl J Med. 2015 Aug 27;373(9):795–807. PubMed PMID: 26192873; PubMed Central PMCID: PMCPMC4569751.
  • Le T, Wright EJ, Smith DM, et al. Enhanced CD4+ T-cell recovery with earlier HIV-1 antiretroviral therapy. N Engl J Med. 2013 Jan 17;368(3):218–230. PubMed PMID: 23323898; PubMed Central PMCID: PMCPMC3657555.
  • International ASSWGoHIVC, Deeks SG, Autran B, et al. Towards an HIV cure: a global scientific strategy. Nat Rev Immunol. 2012 Jul 20;12(8):607–614. PubMed PMID: 22814509; PubMed Central PMCID: PMCPMC3595991.
  • Gama L, Abreu CM, Shirk EN, et al. Reactivation of simian immunodeficiency virus reservoirs in the brain of virally suppressed macaques. AIDS. 2017 Jan 2;31(1):5–14. PubMed PMID: WOS:000390240700002; English.
  • Spector SA, Rappaport J. HIV cure strategists: ignore the central nervous system at your patients’ peril. AIDS. 2017 Jan 2;31(1):167–168. PubMed PMID: WOS:000390240700018; English.
  • Barton K, Winckelmann A, Palmer S. HIV-1 reservoirs during suppressive therapy. Trends Microbiol. 2016 May;24(5):345–355. PubMed PMID: 26875617; PubMed Central PMCID: PMC5319871.
  • Lorenzo-Redondo R, Fryer HR, Bedford T, et al. Persistent HIV-1 replication maintains the tissue reservoir during therapy. Nature. 2016 Feb 4;530(7588):51–56. PubMed PMID: 26814962; PubMed Central PMCID: PMCPMC4865637.
  • Martinez-Picado J, Deeks SG. Persistent HIV-1 replication during antiretroviral therapy. Curr Opin HIV AIDS. 2016 Jul;11(4):417–423. PubMed PMID: 27078619; PubMed Central PMCID: PMCPMC4900428.
  • Chun TW, Stuyver L, Mizell SB, et al. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13193–13197. PubMed PMID: 9371822; PubMed Central PMCID: PMC24285.
  • Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013 Oct;13(10):722–737. PubMed PMID: 24064518; PubMed Central PMCID: PMC5340150.
  • Schmid D, Munz C. Innate and adaptive immunity through autophagy. Immunity. 2007 Jul;27(1):11–21. PubMed PMID: 17663981.
  • Tsujimoto Y, Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ. 2005 Nov;12(Suppl 2):1528–1534. PubMed PMID: 16247500.
  • Kyei GB, Dinkins C, Davis AS, et al. Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol. 2009 Jul 27;186(2):255–268. PubMed PMID: 19635843; PubMed Central PMCID: PMCPMC2717652.
  • Campbell GR, Rawat P, Bruckman RS, et al. Human immunodeficiency virus type 1 nef inhibits autophagy through transcription factor EB sequestration. PLoS Pathog. 2015 Jun;11(6):e1005018. PubMed PMID: 26115100; PubMed Central PMCID: PMC4482621.
  • Zhou D, Spector SA. Human immunodeficiency virus type-1 infection inhibits autophagy. AIDS. 2008 Mar 30;22(6):695–699. PubMed PMID: 18356598; PubMed Central PMCID: PMCPMC2764485.
  • Alimonti JB, Ball TB, Fowke KR. Mechanisms of CD4+ T lymphocyte cell death in human immunodeficiency virus infection and AIDS. J Gen Virol. 2003 Jul;84(Pt 7):1649–1661. PubMed PMID: 12810858.
  • Doitsh G, Greene WC. Dissecting how CD4 T cells are lost during HIV infection. Cell Host Microbe. 2016 Mar 9;19(3):280–291. PubMed PMID: WOS:000372457500006; English.
  • Dahabieh MS, Battivelli E, Verdin E. Understanding HIV latency: the road to an HIV cure. Annu Rev Med. 2015;66:407–421. PubMed PMID: 25587657; PubMed Central PMCID: PMCPMC4381961.
  • Castellano P, Prevedel L, Eugenin EA. HIV-infected macrophages and microglia that survive acute infection become viral reservoirs by a mechanism involving Bim. Sci Rep. 2017 Oct 9;7(1):12866. PubMed PMID: 28993666; PubMed Central PMCID: PMCPMC5634422.
  • Lennemann NJ, Coyne CB. Catch me if you can: the link between autophagy and viruses. PLoS Pathog. 2015 Mar;11(3):e1004685. PubMed PMID: 25811485; PubMed Central PMCID: PMC4374752.
  • Jackson WT, Giddings TH Jr., Taylor MP, et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005 May;3(5):e156. PubMed PMID: 15884975; PubMed Central PMCID: PMC1084330.
  • Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008 Dec;9(12):1004–1010. PubMed PMID: 18971948; PubMed Central PMCID: PMCPMC2727358.
  • He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67–93. PubMed PMID: 19653858; PubMed Central PMCID: PMCPMC2831538.
  • Liu Y, Shoji-Kawata S, Sumpter RM Jr., et al. Autosis is a Na+,K+-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxia-ischemia. Proc Natl Acad Sci U S A. 2013 Dec 17;110(51):20364–20371. PubMed PMID: 24277826; PubMed Central PMCID: PMCPMC3870705.
  • Shoji-Kawata S, Sumpter R, Leveno M, et al. Identification of a candidate therapeutic autophagy-inducing peptide. Nature. 2013 Feb 14;494(7436):201–206. PubMed PMID: 23364696; PubMed Central PMCID: PMC3788641.
  • Lee JS, Li Q, Lee JY, et al. FLIP-mediated autophagy regulation in cell death control. Nat Cell Biol. 2009 Nov;11(11):1355–1362. PubMed PMID: 19838173; PubMed Central PMCID: PMCPMC2802862.
  • Ho DD, Rota TR, Hirsch MS. Infection of monocyte/macrophages by human T lymphotropic virus type III. J Clin Invest. 1986 May;77(5):1712–1715. PubMed PMID: 2422213; PubMed Central PMCID: PMCPMC424579.
  • Campbell GR, Spector SA. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog. 2012;8(5):e1002689. PubMed PMID: 22589721; PubMed Central PMCID: PMCPMC3349755.
  • Zhang G, Guo D, Dash PK, et al. The mixed lineage kinase-3 inhibitor URMC-099 improves therapeutic outcomes for long-acting antiretroviral therapy. Nanomedicine. 2016 Jan;12(1):109–122. PubMed PMID: 26472049; PubMed Central PMCID: PMC4728028.
  • Liu Y, Levine B. Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ. 2015 Mar;22(3):367–376. PubMed PMID: 25257169; PubMed Central PMCID: PMCPMC4326571.
  • Laird GM, Eisele EE, Rabi SA, et al. A novel cell-based high-throughput screen for inhibitors of HIV-1 gene expression and budding identifies the cardiac glycosides. J Antimicrob Chemother. 2014 Apr;69(4):988–994. PubMed PMID: 24275119; PubMed Central PMCID: PMCPMC3956374.
  • Wong RW, Balachandran A, Ostrowski MA, et al. Digoxin suppresses HIV-1 replication by altering viral RNA processing. PLoS Pathog. 2013 Mar;9(3):e1003241. PubMed PMID: 23555254; PubMed Central PMCID: PMCPMC3610647.
  • Spector SA, Zhou D. Autophagy: an overlooked mechanism of HIV-1 pathogenesis and neuroAIDS? Autophagy. 2008;4(5):704–706. 6105 [pii]. PubMed PMID: 18424919.
  • Zhou D, Masliah E, Spector SA. Autophagy is increased in postmortem brains of persons with HIV-1-associated encephalitis. J Infect Dis. 2011 Jun 1;203(11):1647–1657. PubMed PMID: 21592995; PubMed Central PMCID: PMC3096793. eng.
  • Borel S, Robert-Hebmann V, Alfaisal J, et al. HIV-1 viral infectivity factor interacts with microtubule-associated protein light chain 3 and inhibits autophagy. AIDS. 2015 Jan 28;29(3):275–286. PubMed PMID: 25490467.
  • Espert L, Denizot M, Grimaldi M, et al. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest. 2006 Aug;116(8):2161–2172. PubMed PMID: 16886061; PubMed Central PMCID: PMC1523410.
  • Nardacci R, Amendola A, Ciccosanti F, et al. Autophagy plays an important role in the containment of HIV-1 in nonprogressor-infected patients. Autophagy. 2014 Jul;10(7):1167–1178. PubMed PMID: 24813622; PubMed Central PMCID: PMC4203545.
  • Sagnier S, Daussy CF, Borel S, et al. Autophagy restricts HIV-1 infection by selectively degrading Tat in CD4+ T lymphocytes. J Virol. 2015 Jan;89(1):615–625. PubMed PMID: 25339774; PubMed Central PMCID: PMC4301118.
  • Valera MS, De Armas-Rillo L, Barroso-Gonzalez J, et al. The HDAC6/APOBEC3G complex regulates HIV-1 infectiveness by inducing Vif autophagic degradation. Retrovirology. 2015 Jun 24;12:53. PubMed PMID: 26105074; PubMed Central PMCID: PMC4479245.
  • Gao W, Zhang L. Coating nanoparticles with cell membranes for targeted drug delivery. J Drug Target. 2015 Aug;23(7–8):619–626. PubMed PMID: 26453159.
  • Luk BT, Zhang L. Current advances in polymer-based nanotheranostics for cancer treatment and diagnosis. ACS Appl Mater Interfaces. 2014 Dec 24;6(24):21859–21873. PubMed PMID: 25014486; PubMed Central PMCID: PMC4278687.
  • Zhao L, Li N, Wang K, et al. A review of polypeptide-based polymersomes. Biomaterials. 2014 Jan;35(4):1284–1301. PubMed PMID: 24211077.
  • Alexis F, Pridgen E, Molnar LK, et al. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharm. 2008 Jul-Aug;5(4):505–515. PubMed PMID: 18672949; PubMed Central PMCID: PMC2663893.
  • Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol. 2015 Sep;33(9):941–951. PubMed PMID: 26348965; PubMed Central PMCID: PMC4978509.
  • Dehaini D, Fang RH, Luk BT, et al. Ultra-small lipid-polymer hybrid nanoparticles for tumor-penetrating drug delivery. Nanoscale. 2016 Aug 14;8(30):14411–14419. PubMed PMID: 27411852; PubMed Central PMCID: PMC4977227.
  • Bramini M, Ye D, Hallerbach A, et al. Imaging approach to mechanistic study of nanoparticle interactions with the blood-brain barrier. ACS Nano. 2014 May 27;8(5):4304–4312. PubMed PMID: 24773217.
  • Jo DH, Kim JH, Lee TG, et al. Size, surface charge, and shape determine therapeutic effects of nanoparticles on brain and retinal diseases. Nanomedicine. 2015 Oct;11(7):1603–1611. PubMed PMID: 25989200.
  • Hu CM, Kaushal S, Tran Cao HS, et al. Half-antibody functionalized lipid-polymer hybrid nanoparticles for targeted drug delivery to carcinoembryonic antigen presenting pancreatic cancer cells. Mol Pharm. 2010 Jun 07;7(3):914–920. PubMed PMID: 20394436; PubMed Central PMCID: PMC2884057.
  • Rawat P, Spector SA. Development and characterization of a human microglia cell model of HIV-1 infection. J Neurovirol. 2017 Feb;23(1):33–46. PubMed PMID: 27538994; PubMed Central PMCID: PMCPMC5593752.
  • Aquaro S, Svicher V, Schols D, et al. Mechanisms underlying activity of antiretroviral drugs in HIV-1-infected macrophages: new therapeutic strategies. J Leukoc Biol. 2006 Nov;80(5):1103–1110. PubMed PMID: 16931601.
  • Gavegnano C, Schinazi RF. Antiretroviral therapy in macrophages: implication for HIV eradication. Antivir Chem Chemother. 2009 Oct 19;20(2):63–78. PubMed PMID: 19843977; PubMed Central PMCID: PMC2978531.
  • Cribbs SK, Lennox J, Caliendo AM, et al. Healthy HIV-1-infected individuals on highly active antiretroviral therapy harbor HIV-1 in their alveolar macrophages. AIDS Res Hum Retroviruses. 2015 Jan;31(1):64–70. PubMed PMID: 25134819; PubMed Central PMCID: PMC4287110.
  • Liang XH, Kleeman LK, Jiang HH, et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol. 1998 Nov;72(11):8586–8596. PubMed PMID: 9765397; PubMed Central PMCID: PMC110269.
  • Liu Y, Schiff M, Czymmek K, et al. Autophagy regulates programmed cell death during the plant innate immune response. Cell. 2005 May 20;121(4):567–577. PubMed PMID: 15907470.
  • Shelly S, Lukinova N, Bambina S, et al. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity. 2009 Apr 17;30(4):588–598. PubMed PMID: 19362021; PubMed Central PMCID: PMC2754303.
  • Talloczy Z, Virgin H, Levine B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy. 2006 Jan-Mar;2(1):24–29. PubMed PMID: 16874088.
  • Orvedahl A, MacPherson S, Sumpter R Jr., et al. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe. 2010 Feb 18;7(2):115–127. PubMed PMID: 20159618; PubMed Central PMCID: PMC2860265.
  • Won M, Jun EJ, Khim M, et al. Antiviral protection against enterovirus 71 mediated by autophagy induction following FLICE-inhibitory protein inactivation. Virus Res. 2012 Oct;169(1):316–320. PubMed PMID: 22960766.
  • Moy RH, Gold B, Molleston JM, et al. Antiviral autophagy restrictsRift Valley fever virus infection and is conserved from flies to mammals. Immunity. 2014 Jan 16;40(1):51–65. PubMed PMID: 24374193; PubMed Central PMCID: PMC3951734.
  • Kobayashi S, Orba Y, Yamaguchi H, et al. Autophagy inhibits viral genome replication and gene expression stages in West Nile virus infection. Virus Res. 2014 Oct;13(191):83–91. PubMed PMID: 25091564.
  • Griffin LM, Cicchini L, Pyeon D. Human papillomavirus infection is inhibited by host autophagy in primary human keratinocytes. Virology. 2013 Mar 01;437(1):12–19. PubMed PMID: 23290079; PubMed Central PMCID: PMC3615978.
  • Pennarun B, Gaidos G, Bucur O, et al. killerFLIP: a novel lytic peptide specifically inducing cancer cell death. Cell Death Dis. 2013 Oct;31(4):e894. PubMed PMID: 24176852; PubMed Central PMCID: PMC3920952.
  • Kaplan JH. Biochemistry of Na,K-ATPase. Annu Rev Biochem. 2002;71:511–535. PubMed PMID: 12045105.
  • Choi B, Fermin CD, Comardelle AM, et al. Alterations in intracellular potassium concentration by HIV-1 and SIV Nef. Virol J. 2008 May;19(5):60. PubMed PMID: 18489774; PubMed Central PMCID: PMCPMC2396157.
  • Voss TG, Fermin CD, Levy JA, et al. Alteration of intracellular potassium and sodium concentrations correlates with induction of cytopathic effects by human immunodeficiency virus. J Virol. 1996 Aug;70(8):5447–5454. PubMed PMID: 8764056; PubMed Central PMCID: PMCPMC190502.
  • Yang J, Hu D, Xia J, et al. Enhancement of NMDA receptor-mediated excitatory postsynaptic currents by gp120-treated macrophages: implications for HIV-1-associated neuropathology. J Neuroimmune Pharmacol. 2013 Sep;8(4):921–933. PubMed PMID: 23660833; PubMed Central PMCID: PMC3740075.
  • Brown AM. Use of a macrophage-tropic GFP-tagged human immunodeficiency virus type 1 (HIV-1) to study viral reservoirs. Methods Mol Biol. 2009;515:165–175. PubMed PMID: 19378134.
  • Li T, Gendelman HE, Zhang G, et al. Magnetic resonance imaging of folic acid-coated magnetite nanoparticles reflects tissue biodistribution of long-acting antiretroviral therapy. Int J Nanomedicine. 2015;10:3779–3790. PubMed PMID: 26082630; PubMed Central PMCID: PMC4461087.
  • Puligujja P, Balkundi SS, Kendrick LM, et al. Pharmacodynamics of long-acting folic acid-receptor targeted ritonavir-boosted atazanavir nanoformulations. Biomaterials. 2015 Feb;41:141–150. PubMed PMID: 25522973; PubMed Central PMCID: PMC4272445.
  • Zhang G, Kiyota T, Batrakova EV, et al. Inhibitory effect of nanozymes on amyloid beta aggregation and oxidative stress: a new therapeutic implication for alzheimer’s disease. J Neuroimmune Pharm. 2012 Apr;7:S61–S61. PubMed PMID: WOS:000302288800143; English.
  • Guo D, Zhang G, Wysocki TA, et al. Endosomal trafficking of nanoformulated antiretroviral therapy facilitates drug particle carriage and HIV clearance. J Virol. 2014 Sep 01;88(17):9504–9513. PubMed PMID: 24920821; PubMed Central PMCID: PMC4136325.
  • Kiyota T, Zhang G, Morrison CM, et al. AAV2/1 CD74 gene transfer reduces beta-amyloidosis and improves learning and memory in a mouse model of alzheimer’s disease. Mol Ther. 2015 Nov;23(11):1712–1721. PubMed PMID: 26227349; PubMed Central PMCID: PMC4817947.
  • Kiyota T, Gendelman HE, Weir RA, et al. CCL2 affects beta-amyloidosis and progressive neurocognitive dysfunction in a mouse model of Alzheimer’s disease. Neurobiol Aging. 2013 Apr;34(4):1060–1068. PubMed PMID: 23040664; PubMed Central PMCID: PMC4011558.
  • Kiyota T, Morrison CM, Tu G, et al. Presenilin-1 familial Alzheimer’s disease mutation alters hippocampal neurogenesis and memory function in CCL2 null mice. Brain Behav Immun. 2015 Oct;49:311–321. PubMed PMID: 26112421; PubMed Central PMCID: PMC4567522.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.