Loss of Niemann Pick type C proteins 1 and 2 greatly enhances HIV infectivity and is associated with accumulation of HIV Gag and cholesterol in late endosomes/lysosomes

Virology Journal

Volumn 9, Issue , 2012, Pages

  Coleman, Ebony M ^a,b   Walker, Tiffany N ^a   Hildreth, James E K ^a,b  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; GAG PROTEIN; NIEMANN PICK TYPE C PROTEIN 1; NIEMANN PICK TYPE C PROTEIN 2; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; CARRIER PROTEIN; GLYCOPROTEIN; MEMBRANE PROTEIN; NPC1 PROTEIN, HUMAN; NPC2 PROTEIN, HUMAN;

ARTICLE; CELL LINE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENDOSOME; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYSOSOME; NIEMANN PICK DISEASE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VIRUS INFECTIVITY; VIRUS RELEASE; VIRUS REPLICATION; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PATHOGENICITY; VIRION; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CARRIER PROTEINS; CHOLESTEROL; ENDOSOMES; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GLYCOPROTEINS; HIV-1; HUMANS; MEMBRANE GLYCOPROTEINS; VIRION;

EID: 84856073405     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-9-31     Document Type: Article

References (54)

1. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. Nguyen DH, Hildreth JE, J Virol 2000 74 3264 3272 10.1128/JVI.74.7.3264-3272.2000 10708443 (Pubitemid 30143751)
2. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Aloia RC, Tian H, Jensen FC, Proc Natl Acad Sci USA 1993 90 5181 5185 10.1073/pnas.90.11.5181 8389472 (Pubitemid 23183001)
3. Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. Manes S, del Real G, Lacalle RA, Lucas P, Gomez-Mouton C, Sanchez-Palomino S, Delgado R, Alcami J, Mira E, Martinez AC, EMBO Rep 2000 1 190 196 10.1093/embo-reports/kvd025 11265761
4. Human immunodeficiency virus type 1 uses lipid raft-colocalized CD4 and chemokine receptors for productive entry into CD4(+) T cells. Popik W, Alce TM, Au WC, J Virol 2002 76 4709 4722 10.1128/JVI.76.10.4709-4722.2002 11967288 (Pubitemid 34441677)
5. Nef induces multiple genes involved in cholesterol synthesis and uptake in human immunodeficiency virus type 1-infected T cells. van 't Wout AB, Swain JV, Schindler M, Rao U, Pathmajeyan MS, Mullins JI, Kirchhoff F, J Virol 2005 79 10053 10058 10.1128/JVI.79.15.10053-10058.2005 16014965 (Pubitemid 41022346)
6. Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1 progeny virions. Zheng YH, Plemenitas A, Fielding CJ, Peterlin BM, Proc Natl Acad Sci USA 2003 100 8460 8465 10.1073/pnas.1437453100 12824470 (Pubitemid 36842567)
7. Cholesterol depletion of human immunodeficiency virus type 1 and simian immunodeficiency virus with beta-cyclodextrin inactivates and permeabilizes the virions: evidence for virion-associated lipid rafts. Graham DR, Chertova E, Hilburn JM, Arthur LO, Hildreth JE, J Virol 2003 77 8237 8248 10.1128/JVI.77.15.8237-8248.2003 12857892 (Pubitemid 36871451)
8. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Ono A, Freed EO, Proc Natl Acad Sci USA 2001 98 13925 13930 10.1073/pnas.241320298 11717449 (Pubitemid 33116000)
9. Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. Guyader M, Kiyokawa E, Abrami L, Turelli P, Trono D, J Virol 2002 76 10356 10364 10.1128/JVI.76.20.10356-10364.2002 12239312
10. HIV entry in macrophages is dependent on intact lipid rafts. Carter GC, Bernstone L, Sangani D, Bee JW, Harder T, James W, Virology 2009 386 192 202 10.1016/j.virol.2008.12.031 19185899
11. Human immunodeficiency virus impairs reverse cholesterol transport from macrophages. Mujawar Z, Rose H, Morrow MP, Pushkarsky T, Dubrovsky L, Mukhamedova N, Fu Y, Dart A, Orenstein JM, Bobryshev YV, et al. PLoS Biol 2006 4 365 10.1371/journal.pbio.0040365 17076584 (Pubitemid 44760013)
12. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, et al. Science 1997 277 228 231 10.1126/science.277.5323.228 9211849 (Pubitemid 27446076)
13. Identification of HE1 as the second gene of Niemann-Pick C disease. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, Jadot M, Lobel P, Science 2000 290 2298 2301 10.1126/science.290.5500.2298 11125141 (Pubitemid 32041569)
14. Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Puri V, Watanabe R, Dominguez M, Sun X, Wheatley CL, Marks DL, Pagano RE, Nat Cell Biol 1999 1 386 388 10.1038/14084 10559968 (Pubitemid 129493583)
15. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Sleat DE, Wiseman JA, El-Banna M, Price SM, Verot L, Shen MM, Tint GS, Vanier MT, Walkley SU, Lobel P, Proc Natl Acad Sci USA 2004 101 5886 5891 10.1073/pnas.0308456101 15071184 (Pubitemid 38520498)
16. NPC1/NPC2 function as a tag team duo to mobilize cholesterol. Subramanian K, Balch WE, Proc Natl Acad Sci USA 2008 105 15223 15224 10.1073/pnas. 0808256105 18832164
17. NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Infante RE, Wang ML, Radhakrishnan A, Kwon HJ, Brown MS, Goldstein JL, Proc Natl Acad Sci USA 2008 105 15287 15292 10.1073/pnas.0807328105 18772377
18. Type-C Niemann-Pick disease: low density lipoprotein uptake is associated with premature cholesterol accumulation in the Golgi complex and excessive cholesterol storage in lysosomes. Blanchette-Mackie EJ, Dwyer NK, Amende LM, Kruth HS, Butler JD, Sokol J, Comly ME, Vanier MT, August JT, Brady RO, et al. Proc Natl Acad Sci USA 1988 85 8022 8026 10.1073/pnas.85.21.8022 3186703
19. The Niemann-Pick C lesion and its relationship to the intracellular distribution and utilization of LDL cholesterol. Pentchev PG, Brady RO, Blanchette-Mackie EJ, Vanier MT, Carstea ED, Parker CC, Goldin E, Roff CF, Biochim Biophys Acta 1994 1225 235 243 8312368 (Pubitemid 24066572)
20. Co-cultivation of Niemann-Pick disease type C fibroblasts belonging to complementation groups alpha and beta stimulates LDL-derived cholesterol esterification. Steinberg SJ, Mondal D, Fensom AH, J Inherit Metab Dis 1996 19 769 774 10.1007/BF01799171 8982950 (Pubitemid 26405465)
21. Genetic heterogeneity in Niemann-Pick C disease: a study using somatic cell hybridization and linkage analysis. Vanier MT, Duthel S, Rodriguez-Lafrasse C, Pentchev P, Carstea ED, Am J Hum Genet 1996 58 118 125 8554047
22. Deficiency of niemann-pick type C-1 protein impairs release of human immunodeficiency virus type 1 and results in Gag accumulation in late endosomal/lysosomal compartments. Tang Y, Leao IC, Coleman EM, Broughton RS, Hildreth JE, J Virol 2009 83 7982 7995 10.1128/JVI.00259-09 19474101
23. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. Nguyen DG, Booth A, Gould SJ, Hildreth JE, J Biol Chem 2003 278 52347 52354 10.1074/jbc.M309009200 14561735 (Pubitemid 38035824)
24. Infectious HIV-1 assembles in late endosomes in primary macrophages. Pelchen-Matthews A, Kramer B, Marsh M, J Cell Biol 2003 162 443 455 10.1083/jcb.200304008 12885763 (Pubitemid 36988553)
25. HIV-1 egress is gated through late endosomal membranes. Nydegger S, Foti M, Derdowski A, Spearman P, Thali M, Traffic 2003 4 902 910 10.1046/j.1600-0854. 2003.00145.x 14617353 (Pubitemid 37540592)
26. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Ono A, Ablan SD, Lockett SJ, Nagashima K, Freed EO, Proc Natl Acad Sci USA 2004 101 14889 14894 10.1073/pnas.0405596101 15465916 (Pubitemid 39410770)
27. Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. Cantin R, Methot S, Tremblay MJ, J Virol 2005 79 6577 6587 10.1128/JVI.79.11.6577-6587.2005 15890896 (Pubitemid 40677289)
28. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. Chertova E, Chertov O, Coren LV, Roser JD, Trubey CM, Bess JW Jr, Sowder RC, Barsov E, Hood BL, Fisher RJ, et al. J Virol 2006 80 9039 9052 10.1128/JVI.01013-06 16940516 (Pubitemid 44359978)
29. SREBP2 Couples HIV-1 Transcription to Cholesterol Homeostasis and T Cell Activation. Taylor HE, Linde ME, Khatua AK, Popik W, Hildreth JE, J Virol 2011 85 7699 7709 10.1128/JVI.00337-11 21613400
30. Annexin A6 is recruited into lipid rafts of Niemann-Pick type C disease fibroblasts in a Ca2 + -dependent manner. Domon MM, Besson F, Bandorowicz-Pikula J, Pikula S, Biochem Biophys Res Commun 2011 405 192 196 10.1016/j.bbrc.2010. 12.138 21216236
31. Functional rafts in cell membranes. Simons K, Ikonen E, Nature 1997 387 569 572 10.1038/42408 9177342 (Pubitemid 27248754)
32. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Parton RG, Richards AA, Traffic 2003 4 724 738 10.1034/j.1600-0854.2003.00128.x 14617356 (Pubitemid 37361854)
33. Independent segregation of human immunodeficiency virus type 1 Gag protein complexes and lipid rafts. Ding L, Derdowski A, Wang JJ, Spearman P, J Virol 2003 77 1916 1926 10.1128/JVI.77.3.1916-1926.2003 12525626 (Pubitemid 36110004)
34. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. Lindwasser OW, Resh MD, J Virol 2001 75 7913 7924 10.1128/JVI.75.17.7913-7924.2001 11483736 (Pubitemid 32743663)
35. Human immunodeficiency virus type 1 assembly and lipid rafts: Pr55(gag) associates with membrane domains that are largely resistant to Brij98 but sensitive to Triton X-100. Holm K, Weclewicz K, Hewson R, Suomalainen M, J Virol 2003 77 4805 4817 10.1128/JVI.77.8.4805-4817.2003 12663787 (Pubitemid 36402830)
36. Nef increases infectivity of HIV via lipid rafts. Zheng YH, Plemenitas A, Linnemann T, Fackler OT, Peterlin BM, Curr Biol 2001 11 875 879 10.1016/S0960-9822(01)00237-8 11516650 (Pubitemid 32532814)
37. Human immunodeficiency virus type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains. Brugger B, Krautkramer E, Tibroni N, Munte CE, Rauch S, Leibrecht I, Glass B, Breuer S, Geyer M, Krausslich HG, et al. Retrovirology 2007 4 70 10.1186/1742-4690-4-70 17908312 (Pubitemid 350066536)
38. Lipid rafts and HIV pathogenesis: virion-associated cholesterol is required for fusion and infection of susceptible cells. Liao Z, Graham DR, Hildreth JE, AIDS Res Hum Retroviruses 2003 19 675 687 10.1089/ 088922203322280900 13678470 (Pubitemid 37047093)
39. The raft-promoting property of virion-associated cholesterol, but not the presence of virion-associated Brij 98 rafts, is a determinant of human immunodeficiency virus type 1 infectivity. Campbell S, Gaus K, Bittman R, Jessup W, Crowe S, Mak J, J Virol 2004 78 10556 10565 10.1128/JVI.78.19.10556-10565. 2004 15367622 (Pubitemid 39258381)
40. Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. Liao Z, Cimakasky LM, Hampton R, Nguyen DH, Hildreth JE, AIDS Res Hum Retroviruses 2001 17 1009 1019 10.1089/ 088922201300343690 11485618 (Pubitemid 32881320)
41. Virion-associated cholesterol is critical for the maintenance of HIV-1 structure and infectivity. Campbell SM, Crowe SM, Mak J, AIDS 2002 16 2253 2261 10.1097/00002030-200211220-00004 12441796 (Pubitemid 35449010)
42. Effects of a novel compound (AL 721) on HTLV-III infectivity in vitro. Sarin PS, Gallo RC, Scheer DI, Crews F, Lippa AS, N Engl J Med 1985 313 1289 1290 2414659 (Pubitemid 16217055)
43. Correction of apolipoprotein A-I-mediated lipid efflux and high density lipoprotein particle formation in human Niemann-Pick type C disease fibroblasts. Boadu E, Choi HY, Lee DW, Waddington EI, Chan T, Asztalos B, Vance JE, Chan A, Castro G, Francis GA, J Biol Chem 2006 281 37081 37090 10.1074/jbc.M606890200 17020879 (Pubitemid 46042178)
44. Stimulation of the liver × receptor pathway inhibits HIV-1 replication via induction of ATP-binding cassette transporter A1. Morrow MP, Grant A, Mujawar Z, Dubrovsky L, Pushkarsky T, Kiselyeva Y, Jennelle L, Mukhamedova N, Remaley AT, Kashanchi F, et al. Mol Pharmacol 2010 78 215 225 10.1124/mol.110.065029 20479131
45. Lipid rafts and HIV-1: from viral entry to assembly of progeny virions. Campbell SM, Crowe SM, Mak J, J Clin Virol: the official publication of the Pan American Society for Clinical Virology 2001 22 217 227 10.1016/S1386-6532(01) 00193-7 (Pubitemid 32846552)
46. Jamming the endosomal system: lipid rafts and lysosomal storage diseases. Simons K, Gruenberg J, Trends Cell Biol 2000 10 459 462 10.1016/S0962-8924(00) 01847-X 11050411
47. Depletion of rafts in late endocytic membranes is controlled by NPC1-dependent recycling of cholesterol to the plasma membrane. Lusa S, Blom TS, Eskelinen EL, Kuismanen E, Mansson JE, Simons K, Ikonen E, J Cell Sci 2001 114 1893 1900 11329376
48. The sterol-sensing domain: multiple families, a unique role? Kuwabara PE, Labouesse M, Trends Genet: TIG 2002 18 193 201 10.1016/S0168-9525(02)02640-9 11932020 (Pubitemid 34273740)
49. The Niemann-Pick C1 gene is downregulated by feedback inhibition of the SREBP pathway in human fibroblasts. Garver WS, Jelinek D, Francis GA, Murphy BD, J Lipid Res 2008 49 1090 1102 10.1194/jlr.M700555-JLR200 18272927
50. Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes. Shimano H, Prog Lipid Res 2001 40 439 452 10.1016/S0163-7827(01)00010-8 11591434 (Pubitemid 32929966)
51. MiR-33 contributes to the regulation of cholesterol homeostasis. Rayner KJ, Suarez Y, Davalos A, Parathath S, Fitzgerald ML, Tamehiro N, Fisher EA, Moore KJ, Fernandez-Hernando C, Science 2010 328 1570 1573 10.1126/science. 1189862 20466885
52. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, Naar AM, Science 2010 328 1566 1569 10.1126/science.1189123 20466882
53. 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. Mujawar Z, Tamehiro N, Grant A, Sviridov D, Bukrinsky M, Fitzgerald ML, Biochemistry 2010 49 8338 8349 10.1021/bi100466q 20731376
54. CD4 receptor localized to non-raft membrane microdomains supports HIV-1 entry. Identification of a novel raft localization marker in CD4. Popik W, Alce TM, J Biol Chem 2004 279 704 712 14570906 (Pubitemid 38044875)