HIV-1 Nef mobilizes lipid rafts in macrophages through a pathway that competes with ABCA1-dependent cholesterol efflux

Journal of Lipid Research

Volumn 53, Issue 4, 2012, Pages 696-708

  Cui, Huanhuan L ^a   Grant, Angela ^b,e   Mukhamedova, Nigora ^a   Pushkarsky, Tatiana ^b   Jennelle, Lucas ^b   Dubrovsky, Larisa ^b   Gaus, Katharina ^c   Fitzgerald, Michael L ^d   Sviridov, Dmitri ^a   Bukrinsky, Michael ^b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e Harvard AIDS Institute   (United States)

Author keywords

ATP binding cassette transporter A1; Cholesterol metabolism; Cholesterol trafficking; Human immunodeficiency virus

Indexed keywords

ABC TRANSPORTER A1; NEF PROTEIN;

ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL FRACTIONATION; CELL FUNCTION; CELL SURFACE; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; INNATE IMMUNITY; INTERNALIZATION; LIPID RAFT; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; VIRUS INFECTIVITY; VIRUS REPLICATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CALCIUM CHLORIDE; CHLOROQUINE; CHOLESTEROL; HELA CELLS; HIV INFECTIONS; HIV-1; HUMANS; HYDROCARBONS, FLUORINATED; LYSOSOMES; MACROPHAGES; MEMBRANE MICRODOMAINS; MICE; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PROTEIN STABILITY; PROTEOLYSIS; RNA INTERFERENCE; SULFONAMIDES; TRANSFECTION; VIRUS REPLICATION;

EID: 84859389772     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M023119     Document Type: Article

References (38)

1. Bukrinsky, M., and D. Sviridov. 2006. Human immunodeficiency virus infection and macrophage cholesterol metabolism. J. Leukoc. Biol. 80: 1044-1051. (Pubitemid 44646310)
2. Rose, H., J. Hoy, I. Woolley, U. Tchoua, M. Bukrinsky, A. Dart, and D. Sviridov. 2008. HIV infection and high density lipoprotein metabolism. Atherosclerosis. 199: 79-86. (Pubitemid 351842701)
3. Mujawar, Z., H. Rose, M. P. Morrow, T. Pushkarsky, L. Dubrovsky, N. Mukhamedova, Y. Fu, A. Dart, J. M. Orenstein, Y. V. Bobryshev, et al. 2006. Human immunodeficiency virus impairs reverse cholesterol transport from macrophages. PLoS Biol. 4: e365.
4. Fitzgerald, M. L., Z. Mujawar, and N. Tamehiro. 2010. ABC transporters, atherosclerosis and inflammation. Atherosclerosis. 211: 361-370.
5. Asztalos, B. F., Z. Mujawar, M. P. Morrow, A. Grant, T. Pushkarsky, C. Wanke, R. Shannon, M. Geyer, F. Kirchhoff, D. Sviridov, et al. 2010. Circulating Nef induces dyslipidemia in simian immunodeficiency virus-infected macaques by suppressing cholesterol efflux. J. Infect. Dis. 202: 614-623.
6. Morrow, M. P., A. Grant, Z. Mujawar, L. Dubrovsky, T. Pushkarsky, Y. Kiselyeva, L. Jennelle, N. Mukhamedova, A. T. Remaley, F. Kashanchi, et al. 2010. Stimulation of the liver X receptor pathway inhibits HIV-1 replication via induction of ATP-binding cassette transporter A1. Mol. Pharmacol. 78: 215-225.
7. Arora, V. K., B. L. Fredericksen, and J. V. Garcia. 2002. Nef: agent of cell subversion. Microbes Infect. 4: 189-199. (Pubitemid 34183494)
8. Zheng, Y. H., A. Plemenitas, C. J. Fielding, and B. M. Peterlin. 2003. Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1 progeny virions. Proc. Natl. Acad. Sci. USA. 100: 8460-8465. (Pubitemid 36842567)
9. van't Wout, A. B., J. V. Swain, M. Schindler, U. Rao, M. S. Pathmajeyan, J. I. Mullins, and F. Kirchhoff. 2005. Nef induces multiple genes involved in cholesterol synthesis and uptake in human immunodeficiency virus type 1-infected T cells. J. Virol. 79: 10053-10058. (Pubitemid 41022346)
10. Zheng, Y. H., A. Plemenitas, T. Linnemann, O. T. Fackler, and B. M. Peterlin. 2001. Nef increases infectivity of HIV via lipid rafts. Curr. Biol. 11: 875-879.
11. Giese, S. I., I. Woerz, S. Homann, N. Tibroni, M. Geyer, and O. T. Fackler. 2006. Specific and distinct determinants mediate membrane binding and lipid raft incorporation of HIV-1(SF2) Nef. Virology. 355: 175-191. (Pubitemid 44692772)
12. Gerlach, H., V. Laumann, S. Martens, C. F. Becker, R. S. Goody, and M. Geyer. 2010. HIV-1 Nef membrane association depends on charge, curvature, composition and sequence. Nat. Chem. Biol. 6: 46-53.
13. Brügger, B., E. Krautkramer, N. Tibroni, C. E. Munte, S. Rauch, I. Leibrecht, B. Glass, S. Breuer, M. Geyer, H. G. Kräusslich, et al. 2007. Human immunodeficiency virus type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains. Retrovirology. 4: 70.
14. Cooke, S. J., K. Coates, C. H. Barton, T. E. Biggs, S. J. Barrett, A. Cochrane, K. Oliver, J. A. McKeating, M. P. Harris, and D. A. Mann. 1997. Regulated expression vectors demonstrate cell-type-specific sensitivity to human immunodeficiency virus type 1 Nef-induced cytostasis. J. Gen. Virol. 78: 381-392. (Pubitemid 27075636)
15. Mukhamedova, N., Y. Fu, M. Bukrinsky, A. T. Remaley, and D. Sviridov. 2007. The role of different regions of ATP-binding cassette transporter A1 in cholesterol efflux. Biochemistry. 46: 9388-9398. (Pubitemid 47291946)
16. Neufeld, E. B., A. T. Remaley, S. J. Demosky, J. A. Stonik, A. M. Cooney, M. Comly, N. K. Dwyer, M. Zhang, J. Blanchette-Mackie, S. Santamarina-Fojo, et al. 2001. Cellular localization and trafficking of the human ABCA1 transporter. J. Biol. Chem. 276: 27584-27590.
17. Brace, R. J., B. Sorrenson, D. Sviridov, and S. P. A. McCormick. 2010. A gel-based method for purification of apolipoprotein A-I from small volumes of plasma. J. Lipid Res. 51: 3370-3376.
18. Wei, X., J. M. Decker, H. Liu, Z. Zhang, R. B. Arani, J. M. Kilby, M. S. Saag, X. Wu, G. M. Shaw, and J. C. Kappes. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46: 1896-1905. (Pubitemid 34535213)
19. Sviridov, D., N. Fidge, G. Beaumier-Gallon, and C. Fielding. 2001. Apolipoprotein A-I stimulates the transport of intracellular cholesterol to cell-surface cholesterol-rich domains (caveolae). Biochem. J. 358: 79-86. (Pubitemid 32778100)
20. Mukhamedova, N., G. Escher, W. D'Souza, U. Tchoua, A. Grant, Z. Krozowski, M. Bukrinsky, and D. Sviridov. 2008. Enhancing apolipoprotein A-I-dependent cholesterol efflux elevates cholesterol export from macrophages in vivo. J. Lipid Res. 49: 2312-2322.
21. Patlolla, J. M., M. V. Swamy, J. Raju, and C. V. Rao. 2004. Overexpression of caveolin-1 in experimental colon adenocarcinomas and human colon cancer cell lines. Oncol. Rep. 11: 957-963.
22. Le Lay, S., Q. Li, N. Proschogo, M. Rodriguez, K. Gunaratnam, S. Cartland, C. Rentero, W. Jessup, T. Mitchell, and K. Gaus. 2009. Caveolin-1-dependent and -independent membrane domains. J. Lipid Res. 50: 1609-1620.
23. Gaus, K., T. Zech, and T. Harder. 2006. Visualizing membrane microdomains by Laurdan 2-photon microscopy. Mol. Membr. Biol. 23: 41-48.
24. Owen, D. M., C. Rentero, A. Magenau, A. Abu-Siniyeh, and K. Gaus. 2011. Quantitative imaging of membrane lipid order in cells and organisms. Nat. Protoc. 7: 24-35.
25. Nieland, T. J. F., A. Chroni, M. L. Fitzgerald, Z. Maliga, V. I. Zannis, T. Kirchhausen, and M. Krieger. 2004. Cross-inhibition of SR-BI- and ABCA1-mediated cholesterol transport by the small molecules BLT-4 and glyburide. J. Lipid Res. 45: 1256-1265. (Pubitemid 38802628)
26. Rigamonti, E., G. Chinetti-Gbaguidi, and B. Staels. 2008. Regulation of macrophage functions by PPAR-{alpha}, PPAR-{gamma}, and LXRs in mice and men. Arterioscler. Thromb. Vasc. Biol. 28: 1050-1059.
27. Rauch, S., K. Pulkkinen, K. Saksela, and O. T. Fackler. 2008. Human immunodeficiency virus type 1 Nef recruits the guanine exchange factor Vav1 via an unexpected interface into plasma membrane microdomains for association with p21-activated kinase 2 activity. J. Virol. 82: 2918-2929. (Pubitemid 351329181)
28. Djordjevic, J. T., S. D. Schibeci, G. J. Stewart, and P. Williamson. 2004. HIV type 1 Nef increases the association of T cell receptor (TCR)-signaling molecules with T cell rafts and promotes activation-induced raft fusion. AIDS Res. Hum. Retroviruses. 20: 547-555. (Pubitemid 38720969)
29. Mendez, A. J., G. Lin, D. P. Wade, R. M. Lawn, and J. F. Oram. 2001. Membrane lipid domains distinct from cholesterol/sphingomyelin-rich rafts are involved in the ABCA1-mediated lipid secretory pathway. J. Biol. Chem. 276: 3158-3166.
30. daSilva, L. L., R. Sougrat, P. V. Burgos, K. Janvier, R. Mattera, and J. S. Bonifacino. 2009. Human immunodeficiency virus type 1 Nef protein targets CD4 to the multivesicular body pathway. J. Virol. 83: 6578-6590.
31. Yvan-Charvet, L., N. Wang, and A. R. Tall. 2010. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 30: 139-143.
32. Koseki, M., K. Hirano, D. Masuda, C. Ikegami, M. Tanaka, A. Ota, J. C. Sandoval, Y. Nakagawa-Toyama, S. B. Sato, T. Kobayashi, et al. 2007. Increased lipid rafts and accelerated lipopolysaccharide-induced tumor necrosis factor-{alpha} secretion in Abca1-deficient macrophages. J. Lipid Res. 48: 299-306. (Pubitemid 46220596)
33. Landry, Y. D., M. Denis, S. Nandi, S. Bell, A. M. Vaughan, and X. Zha. 2006. ATP-binding cassette transporter A1 expression disrupts raft membrane microdomains through its ATPase-related functions. J. Biol. Chem. 281: 36091-36101. (Pubitemid 46041342)
34. Mañes, S., G. del Real, and C. Martínez-A. 2003. Pathogens: raft hijackers. Nat. Rev. Immunol. 3: 557-568. (Pubitemid 37328675)
35. Mujawar, Z., N. Tamehiro, A. Grant, D. Sviridov, M. Bukrinsky, and M. L. Fitzgerald. 2010. Mutation of the ATP cassette binding transporter A1 (ABCA1) C-terminus disrupts HIV-1 Nef binding but does not block the Nef enhancement of ABCA1 protein degradation. Biochemistry. 49: 8338-8349.
36. Nagao, G., K. Ishii, K. Hirota, K. Makino, and H. Terada. 2010. Role of lipid rafts in phagocytic uptake of polystyrene latex microspheres by macrophages. Anticancer Res. 30: 3167-3176.
37. Kedzierska, K., J. Mak, A. Jaworowski, A. Greenway, A. Violo, H. T. Chan, J. Hocking, D. Purcell, J. S. Sullivan, J. Mills, et al. 2001. Nef-deleted HIV-1 inhibits phagocytosis by monocyte-derived macrophages in vitro but not by peripheral blood monocytes in vivo. AIDS. 15: 945-955. (Pubitemid 32476661)
38. Roeth, J. F., and K. L. Collins. 2006. Human immunodeficiency virus type 1 Nef: adapting to intracellular trafficking pathways. Microbiol. Mol. Biol. Rev. 70: 548-563. (Pubitemid 43895037)