Electron Tomography of HIV-1 Infection in Gut-Associated Lymphoid Tissue

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Ladinsky, Mark S ^a   Kieffer, Collin ^a   Olson, Gregory ^b   Deruaz, Maud ^c   Vrbanac, Vladimir ^c   Tager, Andrew M ^c   Kwon, Douglas S ^b   Bjorkman, Pamela J ^a,d  

^a California Institute of Technology   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; CLINICAL TRIAL; ELECTRON TOMOGRAPHY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INTESTINE; KNOCKOUT MOUSE; LYMPHOID TISSUE; MALE; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; VIRION; VIROLOGY;

ANIMALS; ELECTRON MICROSCOPE TOMOGRAPHY; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; INTESTINES; LYMPHOID TISSUE; MALE; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; VIRION;

EID: 84893724876     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003899     Document Type: Article

References (72)

1. UNAIDS (2012) http://www.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2012/gr2012/20121120_UNAIDS_Global_Report_2012_with_annexes_en.pdf.
2. Haase AT, (2011) Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu Rev Med 62: 127-139.
3. Brenchley JM, Douek DC, (2008) HIV infection and the gastrointestinal immune system. Mucosal Immunol 1: 23-30.
4. Douek DC, Roederer M, Koup RA, (2009) Emerging concepts in the immunopathogenesis of AIDS. Annu Rev Med 60: 471-484.
5. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, et al. (1998) Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280: 427-431.
6. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, et al. (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200: 749-759.
7. Lackner AA, Lederman MM, Rodriguez B, (2012) HIV Pathogenesis: The Host. Cold Spring Harb Perspect Med 2: a007005.
8. Haase AT, (2005) Perils at mucosal front lines for HIV and SIV and their hosts. Nat Rev Immunol 5: 783-792.
9. Guy-Grand D, Vassalli P, (1993) Gut intraepithelial T lymphocytes. Curr Opin Immunol 5: 247-252.
10. Douek D, (2007) HIV disease progression: immune activation, microbes, and a leaky gut. Top HIV Med 15: 114-117.
11. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
12. Denton PW, Garcia JV, (2012) Mucosal HIV-1 transmission and prevention strategies in BLT humanized mice. Trends in microbiology 20: 268-274.
13. Brainard DM, Seung E, Frahm N, Cariappa A, Bailey CC, et al. (2009) Induction of robust cellular and humoral virus-specific adaptive immune responses in human immunodeficiency virus-infected humanized BLT mice. J Virol 83: 7305-7321.
14. Denton PW, Garcia JV, (2011) Humanized mouse models of HIV infection. AIDS Rev 13: 135-148.
15. Denton PW, Estes JD, Sun Z, Othieno FA, Wei BL, et al. (2008) Antiretroviral pre-exposure prophylaxis prevents vaginal transmission of HIV-1 in humanized BLT mice. PLoS Med 5: e16.
16. Sun Z, Denton PW, Estes JD, Othieno FA, Wei BL, et al. (2007) Intrarectal transmission, systemic infection, and CD4+ T cell depletion in humanized mice infected with HIV-1. J Exp Med 204: 705-714.
17. Lan P, Tonomura N, Shimizu A, Wang S, Yang YG, (2006) Reconstitution of a functional human immune system in immunodeficient mice through combined human fetal thymus/liver and CD34+ cell transplantation. Blood 108: 487-492.
18. Rajesh D, Zhou Y, Jankowska-Gan E, Roenneburg DA, Dart ML, et al. (2010) Th1 and Th17 immunocompetence in humanized NOD/SCID/IL2rgammanull mice. Human immunology 71: 551-559.
19. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, et al. (1983) Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220: 868-871.
20. Gallo RC, Sarin PS, Gelmann EP, Robert-Guroff M, Richardson E, et al. (1983) Isolation of human T-cell leukemia virus in acquired immune deficiency syndrome (AIDS). Science 220: 865-867.
21. Orenstein JM, (2007) Replication of HIV-1 in vivo and in vitro. Ultrastruct Pathol 31: 151-167.
22. Briggs JA, Riches JD, Glass B, Bartonova V, Zanetti G, et al. (2009) Structure and assembly of immature HIV. Proc Natl Acad Sci U S A 106: 11090-11095.
23. Benjamin J, Ganser-Pornillos BK, Tivol WF, Sundquist WI, Jensen GJ, (2005) Three-dimensional structure of HIV-1 virus-like particles by electron cryotomography. J Mol Biol 346: 577-588.
24. Wright ER, Schooler JB, Ding HJ, Kieffer C, Fillmore C, et al. (2007) Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J 26: 2218-2226.
25. Carlson LA, de Marco A, Oberwinkler H, Habermann A, Briggs JA, et al. (2010) Cryo electron tomography of native HIV-1 budding sites. PLoS Pathog 6: e1001173.
26. Carlson LA, Briggs JA, Glass B, Riches JD, Simon MN, et al. (2008) Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis. Cell Host Microbe 4: 592-599.
27. Felts RL, Narayan K, Estes JD, Shi D, Trubey CM, et al. (2010) 3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells. Proc Natl Acad Sci U S A 107: 13336-13341.
28. Sougrat R, Bartesaghi A, Lifson JD, Bennett AE, Bess JW, et al. (2007) Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog 3: e63.
29. Walker MR, Patel KK, Stappenbeck TS, (2009) The stem cell niche. J Pathol 217: 169-180.
30. McIntosh JR, Nicastro D, Mastronarde DN, (2005) New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol 15: 43-51.
31. Gilkey JC, Staehelin LA, (1986) Advances in Ultrarapid Freezing for the Preservation of Cellular Ultrastructure. J Elect Microsc Tech 3: 177-210.
32. Morphew M, He W, Bjorkman PJ, McIntosh JR, (2008) Silver enhancement of Nanogold particles during freeze substitution for electron microscopy. J Microsc 230: 263-267.
33. Ladinsky MS, Howell KE, (2007) Electron tomography of immunolabeled cryosections. Methods Cell Biol 79: 543-558.
34. Luther PK, Lawrence MC, Crowther RA, (1988) A method for monitoring the collapse of plastic sections as a function of electron dose. Ultramicroscopy 24: 7-18.
35. Fuller SD, Wilk T, Gowen BE, Krausslich HG, Vogt VM, (1997) Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle. Curr Biol 7: 729-738.
36. Wilk T, Gross I, Gowen BE, Rutten T, de Haas F, et al. (2001) Organization of immature human immunodeficiency virus type 1. J Virol 75: 759-771.
37. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI, (1999) Assembly and analysis of conical models for the HIV-1 core. Science 283: 80-83.
38. Hockley DJ, Wood RD, Jacobs JP, Garrett AJ, (1988) Electron microscopy of human immunodeficiency virus. J Gen Virol 69: 2455-2469.
39. Zhu P, Liu J, Bess J Jr, Chertova E, Lifson JD, et al. (2006) Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441: 847-852.
40. Chertova E, Bess Jr JW, Crise BJ, Sowder IR, Schaden TM, et al. (2002) Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol 76: 5315-5325.
41. Magadan JG, Perez-Victoria FJ, Sougrat R, Ye Y, Strebel K, et al. (2010) Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS Pathog 6: e1000869.
42. Briggs JA, Simon MN, Gross I, Krausslich HG, Fuller SD, et al. (2004) The stoichiometry of Gag protein in HIV-1. Nat Struct Mol Biol 11: 672-675.
43. Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M, (2007) In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J Cell Biol 177: 329-341.
44. Bennett AE, Narayan K, Shi D, Hartnell LM, Gousset K, et al. (2009) Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages. PLoS Pathog 5: e1000591.
45. Pelchen-Matthews A, Kramer B, Marsh M, (2003) Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol 162: 443-455.
46. Raposo G, Moore M, Innes D, Leijendekker R, Leigh-Brown A, et al. (2002) Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic 3: 718-729.
47. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ, (2004) HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J Exp Med 199: 283-293.
48. Hioe CE, Chien PC Jr, Lu C, Springer TA, Wang XH, et al. (2001) LFA-1 expression on target cells promotes human immunodeficiency virus type 1 infection and transmission. J Virol 75: 1077-1082.
49. Rizzuto CD, Sodroski JG, (1997) Contribution of virion ICAM-1 to human immunodeficiency virus infectivity and sensitivity to neutralization. J Virol 71: 4847-4851.
50. Robertson DL, Anderson JP, Bradac JA, Carr JK, Foley B, et al. (2000) HIV-1 nomenclature proposal. Science 288: 55-56.
51. Aggarwal A, Iemma TL, Shih I, Newsome TP, McAllery S, et al. (2012) Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog 8: e1002762.
52. Sundquist WI, Krausslich HG, (2012) HIV-1 Assembly, Budding, and Maturation. Cold Spring Harb Perspect Med 2: a006924.
53. Votteler J, Iavnilovitch E, Fingrut O, Shemesh V, Taglicht D, et al. (2009) Exploring the functional interaction between POSH and ALIX and the relevance to HIV-1 release. BMC Biochem 10: 12.
54. Carlson LA, Hurley JH, (2012) In vitro reconstitution of the ordered assembly of the endosomal sorting complex required for transport at membrane-bound HIV-1 Gag clusters. Proc Natl Acad Sci U S A 109: 16928-16933.
55. Boura E, Rozycki B, Chung HS, Herrick DZ, Canagarajah B, et al. (2012) Solution structure of the ESCRT-I and-II supercomplex: implications for membrane budding and scission. Structure 20: 874-886.
56. Lata S, Schoehn G, Jain A, Pires R, Piehler J, et al. (2008) Helical structures of ESCRT-III are disassembled by VPS4. Science 321: 1354-1357.
57. Hanson PI, Roth R, Lin Y, Heuser JE, (2008) Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J Cell Biol 180: 389-402.
58. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, et al. (2003) The protein network of HIV budding. Cell 114: 701-713.
59. Baumgartel V, Ivanchenko S, Dupont A, Sergeev M, Wiseman PW, et al. (2011) Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component. Nat Cell Biol 13: 469-474.
60. Jouvenet N, Zhadina M, Bieniasz PD, Simon SM, (2011) Dynamics of ESCRT protein recruitment during retroviral assembly. Nat Cell Biol 13: 394-401.
61. Yu Z, Gonciarz MD, Sundquist WI, Hill CP, Jensen GJ, (2008) Cryo-EM structure of dodecameric Vps4p and its 2:1 complex with Vta1p. J Mol Biol 377: 364-377.
62. Anton PA, Mitsuyasu RT, Deeks SG, Scadden DT, Wagner B, et al. (2003) Multiple measures of HIV burden in blood and tissue are correlated with each other but not with clinical parameters in aviremic subjects. AIDS 17: 53-63.
63. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, et al. (1997) Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387: 183-188.
64. Welsch S, Keppler OT, Habermann A, Allespach I, Krijnse-Locker J, et al. (2007) HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog 3: e36.
65. Chu H, Wang JJ, Qi M, Yoon JJ, Wen X, et al. (2012) The intracellular virus-containing compartments in primary human macrophages are largely inaccessible to antibodies and small molecules. PLoS One 7: e35297.
66. de Marco A, Muller B, Glass B, Riches JD, Krausslich HG, et al. (2010) Structural analysis of HIV-1 maturation using cryo-electron tomography. PLoS Pathog 6: e1001215.
67. Swartz MA, Fleury ME, (2007) Interstitial flow and its effects in soft tissues. Annu Rev Biomed Eng 9: 229-256.
68. Welsch S, Habermann A, Jager S, Muller B, Krijnse-Locker J, et al. (2006) Ultrastructural analysis of ESCRT proteins suggests a role for endosome-associated tubular-vesicular membranes in ESCRT function. Traffic 7: 1551-1566.
69. Boutwell CL, Rowley CF, Essex M, (2009) Reduced viral replication capacity of human immunodeficiency virus type 1 subtype C caused by cytotoxic-T-lymphocyte escape mutations in HLA-B57 epitopes of capsid protein. J Virol 83: 2460-2468.
70. Mastronarde DN, (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36-51.
71. Mastronarde DN, (2008) Correction for non-perpendicularity of beam and tilt axis in tomographic reconstructions with the IMOD package. J Microsc 230: 212-217.
72. Ladinsky MS, Wu CC, McIntosh S, McIntosh JR, Howell KE, (2002) Structure of the Golgi and distribution of reporter molecules at 20 degrees C reveals the complexity of the exit compartments. Mol Biol Cell 13: 2810-2825.