Leukotrienes inhibit early stages of HIV-1 infection in monocyte-derived microglia-like cells

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Bertin, Jonathan ^a   Barat, Corinne ^a   Bélanger, Dave ^a   Tremblay, Michel J ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Central nervous system; HIV 1; Leukotrienes; Microglia

Indexed keywords

CHEMOKINE RECEPTOR CCR5; LEUKOTRIENE B4; LEUKOTRIENE C4; PROTEIN KINASE C; SUBSTANCE P; VIRUS DNA;

ARTICLE; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MICROGLIA; MONOCYTE; MONOCYTE DERIVED MICROGLIA LIKE CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VIRUS EXPRESSION; VIRUS PARTICLE; VIRUS REPLICATION; BRAIN; CELL CULTURE; CYTOLOGY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; PATHOLOGY; VIROLOGY;

BRAIN; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; LEUKOTRIENE B4; MICROGLIA; SUBSTANCE P; TRANSFECTION;

EID: 84858235582     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-55     Document Type: Article

References (80)

1. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslen M, Grant I, Heaton RK, Joseph J, Marder K, Marra CM, McArthur JC, Nunn M, Price RW, Pulliam L, Robertson KR, Sacktor N, Valcour V, Wojna VE. Updated research nosology for HIV-associated neurocognitive disorders. Neurology 2007, 69:1789-1799. 10.1212/01.WNL.0000287431.88658.8b, 17914061.
2. Ghafouri M, Amini S, Khalili K, Sawaya BE. HIV-1 associated dementia: symptoms and causes. Retrovirology 2006, 3:28. 10.1186/1742-4690-3-28, 1513597, 16712719.
3. Canestri A, Lescure FX, Jaureguiberry S, Moulignier A, Amiel C, Marcelin AG, Peytavin G, Tubiana R, Pialoux G, Katlama C. Discordance between cerebral spinal fluid and plasma HIV replication in patients with neurological symptoms who are receiving suppressive antiretroviral therapy. Clin Infect Dis 2010, 50:773-778. 10.1086/650538, 20100092.
4. Christo PP, Greco DB, Aleixo AW, Livramento JA. HIV-1 RNA levels in cerebrospinal fluid and plasma and their correlation with opportunistic neurological diseases in a Brazilian AIDS reference hospital. Arq Neuropsiquiatr 2005, 63:907-913.
5. De Luca A, Ciancio BC, Larussa D, Murri R, Cingolani A, Rizzo MG, Giancola ML, Ammassari A, Ortona L. Correlates of independent HIV-1 replication in the CNS and of its control by antiretrovirals. Neurology 2002, 59:342-347.
6. Schnell G, Spudich S, Harrington P, Price RW, Swanstrom R. Compartmentalized human immunodeficiency virus type 1 originates from long-lived cells in some subjects with HIV-1-associated dementia. PLoS Pathog 2009, 5:e1000395. 10.1371/journal.ppat.1000395, 2668697, 19390619.
7. Peters PJ, Bhattacharya J, Hibbitts S, Dittmar MT, Simmons G, Bell J, Simmonds P, Clapham PR. Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J Virol 2004, 78:6915-6926. 10.1128/JVI.78.13.6915-6926.2004, 421670, 15194768.
8. Evers S, Rahmann A, Schwaag S, Frese A, Reichelt D, Husstedt IW. Prevention of AIDS dementia by HAART does not depend on cerebrospinal fluid drug penetrance. AIDS Res Hum Retroviruses 2004, 20:483-491. 10.1089/088922204323087723, 15186522.
9. Letendre S, Marquie-Beck J, Capparelli E, Best B, Clifford D, Collier AC, Gelman BB, McArthur JC, McCutchan JA, Morgello S, Simpson D, Grant I, Ellis RJ, . CHARTER Group Validation of the CNS Penetration-Effectiveness rank for quantifying antiretroviral penetration into the central nervous system. Arch Neurol 2008, 65:65-70. 10.1001/archneurol.2007.31, 2763187, 18195140, CHARTER Group.
10. Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, Merlin TL, Young SA, Mills RG, Wachsman W, Wiley CA. Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 1992, 42:1736-1739.
11. Hult B, Chana G, Masliah E, Everall I. Neurobiology of HIV. Int Rev Psychiatry 2008, 20:3-13. 10.1080/09540260701862086, 18240058.
12. Nottet HS, Persidsky Y, Sasseville VG, Nukuna AN, Bock P, Zhai QH, Sharer LR, McComb RD, Swindells S, Soderland C, Gendelman HE. Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J Immunol 1996, 156:1284-1295.
13. Buckner CM, Calderon TM, Willams DW, Belbin TJ, Berman JW. Characterization of monocyte maturation/differentiation that facilitates their transmigration across the blood-brain barrier and infection by HIV: implications for NeuroAIDS. Cell Immunol 2011, 267:109-123. 10.1016/j.cellimm.2010.12.004, 21292246.
14. Wang H, Sun J, Goldstein H. Human immunodeficiency virus type 1 infection increases the in vivo capacity of peripheral monocytes to cross the blood-brain barrier into the brain and the in vivo sensitivity of the blood-brain barrier to disruption by lipopolysaccharide. J Virol 2008, 82:7591-7600. 10.1128/JVI.00768-08, 2493310, 18508884.
15. Pu H, Hayashi K, Andras IE, Eum SY, Hennig B, Toborek M. Limited role of COX-2 in HIV Tat-induced alterations of tight junction protein expression and disruption of the blood-brain barrier. Brain Res 2007, 1184:333-344.
16. Kaul M, Garden GA, Lipton SA. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 2001, 410:988-994. 10.1038/35073667, 11309629.
17. Koenig S, Gendelman HE, Orenstein JM, Dal Canto MC, Pezeshkpour GH, Yungbluth M, Janotta F, Aksamit A, Martin MA, Fauci AS. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 1986, 233:1089-1093. 10.1126/science.3016903, 3016903.
18. Gorry PR, Bristol G, Zack JA, Ritola K, Swanstrom R, Birch CJ, Bell JE, Bannert N, Crawford K, Wang H, Schols D, De Clercq E, Kunstman K, Wolinsky SM, Gabuzda D. Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J Virol 2001, 75:10073-10089. 10.1128/JVI.75.21.10073-10089.2001, 114582, 11581376.
19. Churchill MJ, Wesselingh SL, Cowley D, Pardo CA, McArthur JC, Brew BJ, Gorry PR. Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 2009, 66:253-258. 10.1002/ana.21697, 19743454.
20. Wang T, Gong N, Liu J, Kadiu I, Kraft-Terry SD, Schlautman JD, Ciborowski P, Volsky DJ, Gendelman HE. HIV-1-infected astrocytes and the microglial proteome. J Neuroimmune Pharmacol 2008, 3:173-186. 10.1007/s11481-008-9110-x, 2579774, 18587649.
21. Singh RK, Gupta S, Dastidar S, Ray A. Cysteinyl leukotrienes and their receptors: molecular and functional characteristics. Pharmacology 2010, 85:336-349. 10.1159/000312669, 20516735.
22. Ciana P, Fumagalli M, Trincavelli ML, Verderio C, Rosa P, Lecca D, Ferrario S, Parravicini C, Capra V, Gelosa P, Guerrini U, Belcredito S, Cimino M, Sironi L, Tremoli E, Rovati GE, Martini C, Abbracchio MP. The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J 2006, 25:4615-4627. 10.1038/sj.emboj.7601341, 1589991, 16990797.
23. Kato K, Yokomizo T, Izumi T, Shimizu T. Cell-specific transcriptional regulation of human leukotriene B(4) receptor gene. J Exp Med 2000, 192:413-420. 10.1084/jem.192.3.413, 2193224, 10934229.
24. Yokomizo T, Kato K, Terawaki K, Izumi T, Shimizu T. A second leukotriene B(4) receptor, BLT2. A new therapeutic target in inflammation and immunological disorders. J Exp Med 2000, 192:421-432. 10.1084/jem.192.3.421, 2193217, 10934230.
25. Kanaoka Y, Boyce JA. Cysteinyl leukotrienes and their receptors: cellular distribution and function in immune and inflammatory responses. J Immunol 2004, 173:1503-1510.
26. Ballerini P, Di Iorio P, Ciccarelli R, Caciagli F, Poli A, Beraudi A, Buccella S, D'Alimonte I, D'Auro M, Nargi E, Patricelli P, Visini D, Traversa U. P2Y1 and cysteinyl leukotriene receptors mediate purine and cysteinyl leukotriene co-release in primary cultures of rat microglia. Int J Immunopathol Pharmacol 2005, 18:255-268.
27. Okubo M, Yamanaka H, Kobayashi K, Noguchi K. Leukotriene synthases and the receptors induced by peripheral nerve injury in the spinal cord contribute to the generation of neuropathic pain. Glia 2010, 58:599-610.
28. Lammers CH, Schweitzer P, Facchinetti P, Arrang JM, Madamba SG, Siggins GR, Piomelli D. Arachidonate 5-lipoxygenase and its activating protein: prominent hippocampal expression and role in somatostatin signaling. J Neurochem 1996, 66:147-152.
29. Matsuo M, Hamasaki Y, Fujiyama F, Miyazaki S. Eicosanoids are produced by microglia, not by astrocytes, in rat glial cell cultures. Brain Res 1995, 685:201-204. 10.1016/0006-8993(95)00490-H, 7583247.
30. Hui Y, Funk CD. Cysteinyl leukotriene receptors. Biochem Pharmacol 2002, 64:1549-1557. 10.1016/S0006-2952(02)01357-6, 12429344.
31. Zhang WP, Hu H, Zhang L, Ding W, Yao HT, Chen KD, Sheng WW, Chen Z, Wei EQ. Expression of cysteinyl leukotriene receptor 1 in human traumatic brain injury and brain tumors. Neurosci Lett 2004, 363:247-251. 10.1016/j.neulet.2004.03.088, 15182953.
32. Mayatepek E. Leukotriene C4 synthesis deficiency: a member of a probably underdiagnosed new group of neurometabolic diseases. Eur J Pediatr 2000, 159:811-818. 10.1007/s004310000601, 11079193.
33. Heise CE, O'Dowd BF, Figueroa DJ, Sawyer N, Nguyen T, Im DS, Stocco R, Bellefeuille JN, Abramovitz M, Cheng R, Williams DL, Zeng Z, Liu Q, Ma L, Clements MK, Coulombe N, Liu Y, Austin CP, George SR, O''Neill GP, Metters KM, Lynch KR, Evans JF. Characterization of the human cysteinyl leukotriene 2 receptor. J Biol Chem 2000, 275:30531-30536.
34. Hu H, Chen G, Zhang JM, Zhang WP, Zhang L, Ge QF, Yao HT, Ding W, Chen Z, Wei EQ. Distribution of cysteinyl leukotriene receptor 2 in human traumatic brain injury and brain tumors. Acta Pharmacol Sin 2005, 26:685-690. 10.1111/j.1745-7254.2005.00092.x, 15916734.
35. Lecca D, Trincavelli ML, Gelosa P, Sironi L, Ciana P, Fumagalli M, Villa G, Verderio C, Grumelli C, Guerrini U, Tremoli E, Rosa P, Cuboni S, Martini C, Buffo A, Cimino M, Abbracchio M. The recently identified P2Y-like receptor GPR17 is a sensor of brain damage and a new target for brain repair. PLoS One 2008, 3:e3579. 10.1371/journal.pone.0003579, 2570486, 18974869.
36. Genis P, Jett M, Bernton EW, Boyle T, Gelbard HA, Dzenko K, Keane RW, Resnick L, Mizrachi Y, Volsky DJ, Epstein LG, Gendelman HE. Cytokines and arachidonic metabolites produced during human immunodeficiency virus (HIV)-infected macrophage-astroglia interactions: implications for the neuropathogenesis of HIV disease. J Exp Med 1992, 176:1703-1718. 10.1084/jem.176.6.1703, 2119464, 1460427.
37. Froldi M, Castagna A, Parma M, Piona A, Tedeschi A, Miadonna A, Lorini M, Orazio EN, Lazzarin A. Mediator release in cerebrospinal fluid of human immunodeficiency virus-positive patients with central nervous system involvement. J Neuroimmunol 1992, 38:155-161. 10.1016/0165-5728(92)90100-Y, 1315794.
38. Basselin M, Ramadan E, Igarashi M, Chang L, Chen M, Kraft AD, Harry GJ, Rapoport SI. Imaging upregulated brain arachidonic acid metabolism in HIV-1 transgenic rats. J Cereb Blood Flow Metab 2011, 31:486-493. 10.1038/jcbfm.2010.111, 2992106,2992106, 20664612.
39. Rao JS, Kim HW, Kellom M, Greenstein D, Chen M, Kraft AD, Harry GJ, Rapoport SI, Basselin M. Increased neuroinflammatory and arachidonic acid cascade markers, and reduced synaptic proteins, in brain of HIV-1 transgenic rats. J Neuroinflammation 2011, 8:101. 10.1186/1742-2094-8-101, 3175175, 21846384.
40. Albright AV, Gonzalez-Scarano F. Microarray analysis of activated mixed glial (microglia) and monocyte-derived macrophage gene expression. J Neuroimmunol 2004, 157:27-38. 10.1016/j.jneuroim.2004.09.007, 15579277.
41. Aloisi F. Immune function of microglia. Glia 2001, 36:165-179. 10.1002/glia.1106, 11596125.
42. Ghorpade A, Persidsky Y, Swindells S, Borgmann K, Persidsky R, Holter S, Cotter R, Gendelman HE. Neuroinflammatory responses from microglia recovered from HIV-1-infected and seronegative subjects. J Neuroimmunol 2005, 163:145-156. 10.1016/j.jneuroim.2005.01.022, 15869805.
43. Wu DT, Woodman SE, Weiss JM, McManus CM, D'Aversa TG, Hesselgesser J, Major EO, Nath A, Berman JW. Mechanisms of leukocyte trafficking into the CNS. J Neurovirol 2000, 6(Suppl 1):S82-S85.
44. Flamand L, Borgeat P, Lalonde R, Gosselin J. Release of anti-HIV mediators after administration of leukotriene B4 to humans. J Infect Dis 2004, 189:2001-2009. 10.1086/386374, 15143466.
45. Flamand L, Tremblay MJ, Borgeat P. Leukotriene B4 triggers the in vitro and in vivo release of potent antimicrobial agents. J Immunol 2007, 178:8036-8045.
46. Li Y, Hui H, Burgess CJ, Price RW, Sharp PM, Hahn BH, Shaw GM. Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectiveness and complementation. J Virol 1992, 66:6587-6600. 240154, 1404605.
47. Li Y, Kappes JC, Conway JA, Price RW, Shaw GM, Hahn BH. Molecular characterization of human immunodeficiency virus type 1 cloned directly from uncultured human brain tissue: identification of replication-competent and -defective viral genomes. J Virol 1991, 65:3973-3985. 248827, 1830110.
48. Dornadula G, Zhang H, Shetty S, Pomerantz RJ. HIV-1 virions produced from replicating peripheral blood lymphocytes are more infectious than those from nonproliferating macrophages due to higher levels of intravirion reverse transcripts: implications for pathogenesis and transmission. Virology 1999, 253:10-16. 10.1006/viro.1998.9465, 9887314.
49. Fortin JF, Cantin R, Lamontagne G, Tremblay M. Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity. J Virol 1997, 71:3588-3596. 191506, 9094631.
50. Bounou S, Leclerc JE, Tremblay MJ. Presence of host ICAM-1 in laboratory and clinical strains of human immunodeficiency virus type 1 increases virus infectivity and CD4(+)-T-cell depletion in human lymphoid tissue, a major site of replication in vivo. J Virol 2002, 76:1004-1014. 10.1128/JVI.76.3.1004-1014.2002, 135853, 11773376.
51. Steckbeck JD, Orlov I, Chow A, Grieser H, Miller K, Bruno J, Robinson JE, Montelaro RC, Cole KS. Kinetic rates of antibody binding correlate with neutralization sensitivity of variant simian immunodeficiency virus strains. J Virol 2005, 79:12311-12320. 10.1128/JVI.79.19.12311-12320.2005, 1211559, 16160158.
52. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, Chen IS. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 1990, 61:213-222. 10.1016/0092-8674(90)90802-L, 2331748.
53. Suzuki Y, Misawa N, Sato C, Ebina H, Masuda T, Yamamoto N, Koyanagi Y. Quantitative analysis of human immunodeficiency virus type 1 DNA dynamics by real-time PCR: integration efficiency in stimulated and unstimulated peripheral blood mononuclear cells. Virus Genes 2003, 27:177-188. 10.1023/A:1025732728195, 14501196.
54. Chun TW, Stuyver L, Mizell SB, Ehler LA, Mican JA, Baseler M, Lloyd AL, Nowak MA, Fauci AS. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci USA 1997, 94:13193-13197. 10.1073/pnas.94.24.13193, 24285, 9371822.
55. Leone C, Le Pavec G, Meme W, Porcheray F, Samah B, Dormont D, Gras G. Characterization of human monocyte-derived microglia-like cells. Glia 2006, 54:183-192. 10.1002/glia.20372, 16807899.
56. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 2007, 10:1544-1553. 10.1038/nn2015, 18026096.
57. Noto D, Takahashi K, Miyake S, Yamada M. In vitro differentiation of lineage-negative bone marrow cells into microglia-like cells. Eur J Neurosci 2010, 31:1155-1163. 10.1111/j.1460-9568.2010.07152.x, 20345919.
58. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 1998, 57:1-9.
59. Bailie MB, Standiford TJ, Laichalk LL, Coffey MJ, Strieter R, Peters-Golden M. Leukotriene-deficient mice manifest enhanced lethality from Klebsiella pneumonia in association with decreased alveolar macrophage phagocytic and bactericidal activities. J Immunol 1996, 157:5221-5224.
60. Feinmark SJ, Lindgren JA, Claesson HE, Malmsten C, Samuelsson B. Stimulation of human leukocyte degranulation by leukotriene B4 and its omega-oxidized metabolites. FEBS Lett 1981, 136:141-144. 10.1016/0014-5793(81)81233-1, 6274698.
61. Foster A, Fitzsimmons B, Letts LG. The synthesis of N-acetyl-leukotriene E4 and its effects on cardiovascular and respiratory function of the anesthetized pig. Prostaglandins 1986, 31:1077-1086. 10.1016/0090-6980(86)90211-X, 3763939.
62. Warrilow D, Gardner J, Darnell GA, Suhrbier A, Harrich D. HIV type 1 inhibition by protein kinase C modulatory compounds. AIDS Res Hum Retroviruses 2006, 22:854-864. 10.1089/aid.2006.22.854, 16989610.
63. Thivierge M, Le Gouill C, Tremblay MJ, Stankova J, Rola-Pleszczynski M. Prostaglandin E2 induces resistance to human immunodeficiency virus-1 infection in monocyte-derived macrophages: downregulation of CCR5 expression by cyclic adenosine monophosphate. Blood 1998, 92:40-45.
64. Hayes MM, Lane BR, King SR, Markovitz DM, Coffey MJ. Prostaglandin E(2) inhibits replication of HIV-1 in macrophages through activation of protein kinase A. Cell Immunol 2002, 215:61-71. 10.1016/S0008-8749(02)00017-5, 12142037.
65. Boisvert M, Cote S, Vargas A, Pasvanis S, Bounou S, Barbeau B, Dumais N. PGJ2 antagonizes NF-kappaB-induced HIV-1 LTR activation in colonic epithelial cells. Virology 2008, 380:1-11. 10.1016/j.virol.2008.07.023, 18755491.
66. Kalantari P, Narayan V, Henderson AJ, Prabhu KS. 15-Deoxy-Delta12,14-prostaglandin J2 inhibits HIV-1 transactivating protein, Tat, through covalent modification. FASEB J 2009, 23:2366-2373. 10.1096/fj.08-124982, 2717765, 19299483.
67. Malaviya R, Abraham SN. Role of mast cell leukotrienes in neutrophil recruitment and bacterial clearance in infectious peritonitis. J Leukoc Biol 2000, 67:841-846.
68. Demitsu T, Katayama H, Saito-Taki T, Yaoita H, Nakano M. Phagocytosis and bactericidal action of mouse peritoneal macrophages treated with leukotriene B4. Int J Immunopharmacol 1989, 11:801-808. 10.1016/0192-0561(89)90134-3, 2557289.
69. Medeiros AI, Sa-Nunes A, Soares EG, Peres CM, Silva CL, Faccioli LH. Blockade of endogenous leukotrienes exacerbates pulmonary histoplasmosis. Infect Immun 2004, 72:1637-1644. 10.1128/IAI.72.3.1637-1644.2004, 355884, 14977971.
70. Chen N, Restivo A, Reiss CS. Leukotrienes play protective roles early during experimental VSV encephalitis. J Neuroimmunol 2001, 120:94-102. 10.1016/S0165-5728(01)00415-5, 11694324.
71. Cherrier T, Suzanne S, Redel L, Calao M, Marban C, Samah B, Mukerjee R, Schwartz C, Gras G, Sawaya BE, Zeichner SL, Aunis D, Van Lint C, Rohr O. p21(WAF1) gene promoter is epigenetically silenced by CTIP2 and SUV39H1. Oncogene 2009, 28:3380-3389. 10.1038/onc.2009.193, 19581932.
72. Owman C, Garzino-Demo A, Cocchi F, Popovic M, Sabirsh A, Gallo RC. The leukotriene B4 receptor functions as a novel type of coreceptor mediating entry of primary HIV-1 isolates into CD4-positive cells. Proc Natl Acad Sci USA 1998, 95:9530-9534. 10.1073/pnas.95.16.9530, 21372, 9689114.
73. Martin V, Ronde P, Unett D, Wong A, Hoffman TL, Edinger AL, Doms RW, Funk CD. Leukotriene binding, signaling, and analysis of HIV coreceptor function in mouse and human leukotriene B4 receptor-transfected cells. J Biol Chem 1999, 274:8597-8603. 10.1074/jbc.274.13.8597, 10085095.
74. Lehmann-Che J, Saib A. Early stages of HIV replication: how to hijack cellular functions for a successful infection. AIDS Rev 2004, 6:199-207.
75. Sherman MP, Greene WC. Slipping through the door: HIV entry into the nucleus. Microbes Infect 2002, 4:67-73. 10.1016/S1286-4579(01)01511-8, 11825777.
76. Arhel NJ, Souquere-Besse S, Munier S, Souque P, Guadagnini S, Rutherford S, Prevost MC, Allen TD, Charneau P. HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO J 2007, 26:3025-3037. 10.1038/sj.emboj.7601740, 1894778, 17557080.
77. Krishnan L, Matreyek KA, Oztop I, Lee K, Tipper CH, Li X, Dar MJ, Kewalramani VN, Engelman A. The requirement for cellular transportin 3 (TNPO3 or TRN-SR2) during infection maps to human immunodeficiency virus type 1 capsid and not integrase. J Virol 2010, 84:397-406. 10.1128/JVI.01899-09, 2798409, 19846519.
78. Christ F, Thys W, De Rijck J, Gijsbers R, Albanese A, Arosio D, Emiliani S, Rain JC, Benarous R, Cereseto A, Debyser Z. Transportin-SR2 imports HIV into the nucleus. Curr Biol 2008, 18:1192-1202. 10.1016/j.cub.2008.07.079, 18722123.
79. Thys W, De Houwer S, Demeulemeester J, Taltynov O, Vancraenenbroeck R, Gerard M, De Rijck J, Gijsbers R, Christ F, Debyser Z. Interplay between HIV entry and transportin-SR2 dependency. Retrovirology 2011, 8:7. 10.1186/1742-4690-8-7, 3041740, 21276267.
80. Kehlenbach RH, Gerace L. Phosphorylation of the nuclear transport machinery down-regulates nuclear protein import in vitro. J Biol Chem 2000, 275:17848-17856. 10.1074/jbc.M001455200, 10749866.