HIV-1 transforms the monocyte plasma membrane proteome

Cellular Immunology

Volumn 258, Issue 1, 2009, Pages 44-58

  Kadiu, Irena ^a   Wang, Tong ^a   Schlautman, Joshua D ^a   Dubrovsky, Larisa ^b   Ciborowski, Pawel ^a   Bukrinsky, Michael ^b   Gendelman, Howard E ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

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

Author keywords

Apoptosis; HIV 1; Monocytes; Necrosis; Oxidative stress; Phorbol myristate acetate; Plasma membrane; Proteomics; Vitamin E

Indexed keywords

BILIVERDIN REDUCTASE; CASPASE 3; CASPASE 9; CATHEPSIN B; CYSTATIN B; FREE RADICAL; HEAT SHOCK PROTEIN 70; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HYDROLASE; LEUKOTRIENE HYDROLASE A4; MEMBRANE PROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEOME; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR ETV6; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL LABELING; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; GEL ELECTROPHORESIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LIQUID CHROMATOGRAPHY; MONOCYTE; OXIDATIVE STRESS; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL DIFFERENTIAL IN GEL ELECTROPHORESIS; VIRUS CELL INTERACTION; VIRUS CELL TRANSFORMATION; VIRUS INFECTION; VIRUS REPLICATION;

CARCINOGENS; CATHEPSIN B; CELL MEMBRANE; CELL SURVIVAL; CELLS, CULTURED; EPOXIDE HYDROLASES; HIV INFECTIONS; HIV-1; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MONOCYTES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEOME; TETRADECANOYLPHORBOL ACETATE; VITAMIN E; VITAMINS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 67349121668     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2009.03.012     Document Type: Article

References (76)

1. Peirce M.J., Saklatvala J., Cope A.P., and Wait R. Mapping lymphocyte plasma membrane proteins: a proteomic approach. Methods Mol. Med. 136 (2007) 361-367
2. Peirce M.J., Wait R., Begum S., Saklatvala J., and Cope A.P. Expression profiling of lymphocyte plasma membrane proteins. Mol. Cell. Proteomics 3 (2004) 56-65
3. Santoni V., Molloy M., and Rabilloud T. Membrane proteins and proteomics: un amour impossible?. Electrophoresis 21 (2000) 1054-1070
4. Krogh A., Larsson B., Von Heijne G., and Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305 (2001) 567-580
5. Adessi C., Miege C., Albrieux C., and Rabilloud T. Two-dimensional electrophoresis of membrane proteins: a current challenge for immobilized pH gradients. Electrophoresis 18 (1997) 127-135
6. Hurley W.L., Finkelstein E., and Holst B.D. Identification of surface proteins on bovine leukocytes by a biotin-avidin protein blotting technique. J. Immunol. Methods 85 (1985) 195-202
7. Sabarth N., Lamer S., Zimny-Arndt U., Jungblut P.R., Meyer T.F., and Bumann D. Identification of surface proteins of Helicobacter pylori by selective biotinylation, affinity purification, and two-dimensional gel electrophoresis. J. Biol. Chem. 277 (2002) 27896-27902
8. Adam P.J., Boyd R., Tyson K.L., Fletcher G.C., Stamps A., Hudson L., Poyser H.R., Redpath N., Griffiths M., Steers G., Harris A.L., Patel S., Berry J., Loader J.A., Townsend R.R., Daviet L., Legrain P., Parekh R., and Terrett J.A. Comprehensive proteomic analysis of breast cancer cell membranes reveals unique proteins with potential roles in clinical cancer. J. Biol. Chem. 278 (2003) 6482-6489
9. Simpson R.J., Connolly L.M., Eddes J.S., Pereira J.J., Moritz R.L., and Reid G.E. Proteomic analysis of the human colon carcinoma cell line (LIM 1215): development of a membrane protein database. Electrophoresis 21 (2000) 1707-1732
10. Link A.J., Eng J., Schieltz D.M., Carmack E., Mize G.J., Morris D.R., Garvik B.M., and Yates III J.R. Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17 (1999) 676-682
11. Wu C.C., MacCoss M.J., Howell K.E., and Yates III J.R. A method for the comprehensive proteomic analysis of membrane proteins. Nat. Biotechnol. 21 (2003) 532-538
12. Gygi S.P., Rist B., Gerber S.A., Turecek F., Gelb M.H., and Aebersold R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17 (1999) 994-999
13. Ross P.L., Huang Y.N., Marchese J.N., Williamson B., Parker K., Hattan S., Khainovski N., Pillai S., Dey S., Daniels S., Purkayastha S., Juhasz P., Martin S., Bartlet-Jones M., He F., Jacobson A., and Pappin D.J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3 (2004) 1154-1169
14. Chevallet M., Santoni V., Poinas A., Rouquie D., Fuchs A., Kieffer S., Rossignol M., Lunardi J., Garin J., and Rabilloud T. New zwitterionic detergents improve the analysis of membrane proteins by two-dimensional electrophoresis. Electrophoresis 19 (1998) 1901-1909
15. Rabilloud T., Adessi C., Giraudel A., and Lunardi J. Improvement of the solubilization of proteins in two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 18 (1997) 307-316
16. Rabilloud T., Luche S., Santoni V., and Chevallet M. Detergents and chaotropes for protein solubilization before two-dimensional electrophoresis. Methods Mol. Biol. 355 (2007) 111-119
17. Jang J.H., and Hanash S. Profiling of the cell surface proteome. Proteomics 3 (2003) 1947-1954
18. Mayrhofer C., Krieger S., Allmaier G., and Kerjaschki D. DIGE compatible labelling of surface proteins on vital cells in vitro and in vivo. Proteomics 6 (2006) 579-585
19. Meltzer M.S., and Gendelman H.E. Mononuclear phagocytes as targets, tissue reservoirs, and immunoregulatory cells in human immunodeficiency virus disease. Curr. Top. Microbiol. Immunol. 181 (1992) 239-263
20. Zhu T., Mo H., Wang N., Nam D.S., Cao Y., Koup R.A., and Ho D.D. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261 (1993) 1179-1181
21. Cheng-Mayer C., and Levy J.A. Human immunodeficiency virus infection of the CNS: characterization of "neurotropic" strains. Curr. Top. Microbiol. Immunol. 160 (1990) 145-156
22. Heinzinger N., Baca-Regen L., Stevenson M., and Gendelman H.E. Efficient synthesis of viral nucleic acids following monocyte infection by HIV-1. Virology 206 (1995) 731-735
23. Kedzierska K., Crowe S.M., Turville S., and Cunningham A.L. The influence of cytokines, chemokines and their receptors on HIV-1 replication in monocytes and macrophages. Rev. Med. Virol. 13 (2003) 39-56
24. Schuitemaker H., Kootstra N.A., Koppelman M.H., Bruisten S.M., Huisman H.G., Tersmette M., and Miedema F. Proliferation-dependent HIV-1 infection of monocytes occurs during differentiation into macrophages. J. Clin. Invest. 89 (1992) 1154-1160
25. Lewin S.R., Kirihara J., Sonza S., Irving L., Mills J., and Crowe S.M. HIV-1 DNA and mRNA concentrations are similar in peripheral blood monocytes and alveolar macrophages in HIV-1-infected individuals. AIDS 12 (1998) 719-727
26. McElrath M.J., Pruett J.E., and Cohn Z.A. Mononuclear phagocytes of blood and bone marrow: comparative roles as viral reservoirs in human immunodeficiency virus type 1 infections. Proc. Natl. Acad. Sci. USA 86 (1989) 675-679
27. Ciborowski P., Kadiu I., Rozek W., Smith L., Bernhardt K., Fladseth M., Ricardo-Dukelow M., and Gendelman H.E. Investigating the human immunodeficiency virus type 1-infected monocyte-derived macrophage secretome. Virology 363 (2007) 198-209
28. Kadiu I., Glanzer J.G., Kipnis J., Gendelman H.E., and Thomas M.P. Mononuclear phagocytes in the pathogenesis of neurodegenerative diseases. Neurotox. Res. 8 (2005) 25-50
29. Elbim C., Pillet S., Prevost M.H., Preira A., Girard P.M., Rogine N., Matusani H., Hakim J., Israel N., and Gougerot-Pocidalo M.A. Redox and activation status of monocytes from human immunodeficiency virus-infected patients: relationship with viral load. J. Virol. 73 (1999) 4561-4566
30. Nottet H.D., Persidsky Y., Sasseville V.G., Nukuna A.N., Bock P., Zhai Q.H., Sharer L.R., McComb R.D., Swindells S., Soderland C., and Gendelman H.E. Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J. Immunol. 156 (1996) 1284-1295
31. Ricardo-Dukelow M., Kadiu I., Rozek W., Schlautman J., Persidsky Y., Ciborowski P., Kanmogne G.D., and Gendelman H.E. HIV-1 infected monocyte-derived macrophages affect the human brain microvascular endothelial cell proteome: new insights into blood-brain barrier dysfunction for HIV-1-associated dementia. J. Neuroimmunol. 185 (2007) 37-46
32. Gendelman H.E., Orenstein J.M., Martin M.A., Ferrua C., Mitra R., Phipps T., Wahl L.A., Lane H.C., Fauci A.S., Burke D.S., et al. Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes. J. Exp. Med. 167 (1988) 1428-1441
33. Gendelman H.E., Phelps W., Feigenbaum L., Ostrove J.M., Adachi A., Howley P.M., Khoury G., Ginsberg H.S., and Martin M.A. Trans-activation of the human immunodeficiency virus long terminal repeat sequence by DNA viruses. Proc. Natl. Acad. Sci. USA 83 (1986) 9759-9763
34. Gendelman H.E., Theodore T.S., Willey R., McCoy J., Adachi A., Mervis R.J., Venkatesan S., and Martin M.A. Molecular characterization of a polymerase mutant human immunodeficiency virus. Virology 160 (1987) 323-329
35. Arfi V., Riviere L., Jarrosson-Wuilleme L., Goujon C., Rigal D., Darlix J.L., and Cimarelli A. Characterization of the early steps of infection of primary blood monocytes by human immunodeficiency virus type 1. J. Virol. 82 (2008) 6557-6565
36. Hunter-Lavin C., Davies E.L., Bacelar M.M., Marshall M.J., Andrew S.M., and Williams J.H. Hsp70 release from peripheral blood mononuclear cells. Biochem. Biophys. Res. Commun. 324 (2004) 511-517
37. Gastpar R., Gehrmann M., Bausero M.A., Asea A., Gross C., Schroeder J.A., and Multhoff G. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 65 (2005) 5238-5247
38. Kadiu I., Ricardo-Dukelow M., Ciborowski P., and Gendelman H.E. Cytoskeletal protein transformation in HIV-1-infected macrophage giant cells. J. Immunol. 178 (2007) 6404-6415
39. Jolly C., Mitar I., and Sattentau Q. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J. Virol. 81 (2007) 5547-5560
40. Mor-Vaknin N., Punturieri A., Sitwala K., and Markovitz M. Vimentin is secreted by activated macrophages. Nat. Cell Biol. 5 (2003) 59-63
41. Gougerot-Pocidalo M.A., Roche Y., Fay M., Perianin A., and Bailly S. Oxidative injury amplifies interleukin-1-like activity produced by human monocytes. Int. J. Immunopharmacol. 11 (1989) 961-969
42. Israel N., Gougerot-Pocidalo M.A., Aillet F., and Virelizier J.L. Redox status of cells influences constitutive or induced NF-kappa B translocation and HIV long terminal repeat activity in human T and monocytic cell lines. J. Immunol. 149 (1992) 3386-3393
43. Israel N., Hazan U., Alcami J., Munier A., Arenzana-Seisdedos F., Bachelerie F., Israel A., and Virelizier J.L. Tumor necrosis factor stimulates transcription of HIV-1 in human T lymphocytes, independently and synergistically with mitogens. J. Immunol. 143 (1989) 3956-3960
44. Buttke T.M., and Sandstrom P.A. Oxidative stress as a mediator of apoptosis. Immunol. Today 15 (1994) 7-10
45. 2 induces monocyte apoptosis and reduces viability of Mycobacterium avium-M. intracellulare within cultured human monocytes. Infect. Immun. 64 (1996) 452-459
46. Um H.D., Orenstein J.M., and Wahl S.M. Fas mediates apoptosis in human monocytes by a reactive oxygen intermediate dependent pathway. J. Immunol. 156 (1996) 3469-3477
47. Baranano D.E., Rao M., Ferris C.D., and Snyder S.H. Biliverdin reductase: a major physiologic cytoprotectant. Proc. Natl. Acad. Sci. USA 99 (2002) 16093-16098
48. Haeggstrom J.Z. Structure, function, and regulation of leukotriene A4 hydrolase. Am. J. Respir. Crit. Care Med. 161 (2000) S25-S31
49. Jung N.H., Kim H.P., Kim B.R., Cha S.H., Kim G.A., Ha H., Na Y.E., and Cha Y.N. Evidence for heme oxygenase-1 association with caveolin-1 and -2 in mouse mesangial cells. IUBMB Life 55 (2003) 525-532
50. Kopitar-Jerala N. The role of cystatins in cells of the immune system. FEBS Lett. 580 (2006) 6295-6301
51. Pines A., Perrone L., Bivi N., Romanello M., Damante G., Gulisano M., Kelley M.R., Quadrifoglio F., and Tell G. Activation of APE1/Ref-1 is dependent on reactive oxygen species generated after purinergic receptor stimulation by ATP. Nucleic Acids Res. 33 (2005) 4379-4394
52. Aquaro S., Svicher V., Schols D., Pollicita M., Antinori A., Balzarini J., and Perno C.F. Mechanisms underlying activity of antiretroviral drugs in HIV-1-infected macrophages: new therapeutic strategies. J. Leukoc. Biol. 80 (2006) 1103-1110
53. Choi J., Liu R.M., Kundu R.K., Sangiorgi F., Wu W., Maxson R., and Forman H.J. Molecular mechanism of decreased glutathione content in human immunodeficiency virus type 1 Tat-transgenic mice. J. Biol. Chem. 275 (2000) 3693-3698
54. Mollace V., Salvemini D., Riley D.P., Muscoli C., Iannone M., Granato T., Masuelli L., Modesti A., Rotiroti D., Nistico R., Bertoli A., Perno C.F., and Aquaro S. The contribution of oxidative stress in apoptosis of human-cultured astroglial cells induced by supernatants of HIV-1-infected macrophages. J. Leukoc. Biol. 71 (2002) 65-72
55. Setsukinai K., Urano Y., Kakinuma K., Majima H.J., and Nagano T. Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278 (2003) 3170-3175
56. Brigelius-Flohe R., Kelly F.J., Salonen J.T., Neuzil J., Zingg J.M., and Azzi A. The European perspective on vitamin E: current knowledge and future research. Am. J. Clin. Nutr. 76 (2002) 703-716
57. Wu D., Hayek M.G., and Meydani S. Vitamin E and macrophage cyclooxygenase regulation in the aged. J. Nutr. 131 (2001) 382S-388S
58. Droga-Mazovec G., Bojic L., Petelin A., Ivanova S., Romih R., Repnik U., Salvesen G.S., Stoka V., Turk V., and Turk B. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J. Biol. Chem. 283 (2008) 19140-19150
59. Foghsgaard L., Wissing D., Mauch D., Lademann U., Bastholm L., Boes M., Elling F., Leist M., and Jaattela M. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 153 (2001) 999-1010
60. Leist M., and Jaattela M. Triggering of apoptosis by cathepsins. Cell Death Differ. 8 (2001) 324-326
61. Sloane B.F., Rozhin J., Johnson K., Taylor H., Crissman J.D., and Honn K.V. Cathepsin B: association with plasma membrane in metastatic tumors. Proc. Natl. Acad. Sci. USA 83 (1986) 2483-2487
62. Babior B.M. Oxidants from phagocytes: agents of defense and destruction. Blood 64 (1984) 959-966
63. Verdot L., Lalmanach G., Vercruysse V., Hartmann S., Lucius R., Hoebeke J., Gauthier F., and Vray B. Cystatins up-regulate nitric oxide release from interferon-gamma-activated mouse peritoneal macrophages. J. Biol. Chem. 271 (1996) 28077-28081
64. Neil S., Martin F., Ikeda Y., and Collins M. Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J. Virol. 75 (2001) 5448-5456
65. Triques K., and Stevenson M. Characterization of restrictions to human immunodeficiency virus type 1 infection of monocytes. J. Virol. 78 (2004) 5523-5527
66. Colton C.A., and Gilbert D.L. Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett. 223 (1987) 284-288
67. Babior B.M. NADPH oxidase: an update. Blood 93 (1999) 1464-1476
68. Babior B.M. NADPH oxidase. Curr. Opin. Immunol. 16 (2004) 42-47
69. Elbim C., Hakim J., and Gougerot-Pocidalo M.A. Heterogeneity in Lewis-X and sialyl Lewis-X antigen expression on monocytes in whole blood: relation to stimulus-induced oxidative burst. Am. J. Pathol. 152 (1998) 1081-1090
70. Gut J., Goldman D.W., Jamieson G.C., and Trudell J.R. Conversion of leukotriene A4 to leukotriene B4: catalysis by human liver microsomes under anaerobic conditions. Arch. Biochem. Biophys. 259 (1987) 497-509
71. Bivik C., Rosdahl I., and Ollinger K. Hsp70 protects against UVB induced apoptosis by preventing release of cathepsins and cytochrome c in human melanocytes. Carcinogenesis 28 (2007) 537-544
72. Nylandsted J., Gyrd-Hansen M., Danielewicz A., Fehrenbacher N., Lademann U., Hoyer-Hansen M., Weber E., Multhoff G., Rohde M., and Jaattela M. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J. Exp. Med. 200 (2004) 425-435
73. Iordanskiy S., Zhao Y., Dubrovsky L., Iordanskaya T., Chen M., Liang D., and Bukrinsky M. Heat shock protein 70 protects cells from cell cycle arrest and apoptosis induced by human immunodeficiency virus type 1 viral protein R. J. Virol. 78 (2004) 9697-9704
74. Deiss L.P., Galinka H., Berissi H., Cohen O., and Kimchi A. Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J. 15 (1996) 3861-3870
75. Yamashima T., Kohda Y., Tsuchiya K., Ueno T., Yamashita J., Yoshioka T., and Kominami E. Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis. Eur. J. Neurosci. 10 (1998) 1723-1733
76. Kalter D.C., Nakamura M., Turpin J.A., Baca L.M., Hoover D.L., Dieffenbach C., Ralph P., Gendelman H.E., and Meltzer M.S. Enhanced HIV replication in macrophage colony-stimulating factor-treated monocytes. J. Immunol. 146 (1991) 298-306