HIV-1 harboring renal tubular epithelial cell interaction with T cells results in T cell trans-infection

Virology

Volumn 385, Issue 1, 2009, Pages 105-114

  Mikulak, Joanna ^a   Teichberg, Saul ^a   Faust, Thomas ^c   Schmidtmayerova, Helena ^d   Singhal, Pravin C ^a,b  

^a NORTH SHORE UNIVERSITY HOSPITAL   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c BURKE MEDICAL RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Endocytosis; HIV 1; Renal proximal tubular epithelial cells; Trans infection

Indexed keywords

DEC 205 PROTEIN; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ARTICLE; CELL ADHESION; CELL INTERACTION; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; KIDNEY DISEASE; KIDNEY TUBULE CELL; KIDNEY TUBULE EPITHELIUM; LYSOSOME; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; T LYMPHOCYTE; VIRUS TRANSMISSION;

ANTIBODIES; ANTIGENS, CD; CELLS, CULTURED; ENDOCYTOSIS; EPITHELIAL CELLS; HIV INFECTIONS; HIV-1; HUMANS; KIDNEY TUBULES; LECTINS, C-TYPE; RECEPTORS, CELL SURFACE; T-LYMPHOCYTES; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 60349103343     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.11.029     Document Type: Article

References (71)

1. Adachi A., Koenig A.S., Gendelman H.E., Daugherty D., Gattoni-Celli S., Fauci A.S., and Martin M.A. Productive, persistent infection of human colorectal cell lines with human immunodeficiency virus. J. Virol. 61 (1987) 209-213
2. Amara A., and Littman D.R. After hrs with HIV. J. Cell. Biol. 162 (2003) 371-375
3. Amigorena S., Salamero J., Davoust J., Fridman W.H., and Bonnerot C. Tyrosine-containing motif that transduces cell activation signal also determinates internalization and antigen presentation via type III receptors for IgG. Nature 358 (1992) 337-341
4. Bonifaz L.C., Bonnyay D.P., Charalambous A., Darguste D.I., Fujii S.-I., Soares H., Brimnes M.K., Moltedo B., Moran T.M., and Steinman R.M. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J. Exp. Med. 199 (2004) 815-824
5. Bourgoignie J.J., and Pardo V. The nephropathology in human immunodeficiency virus (HIV)-infection. Kidney Int. Suppl. 40 (1991) S19-S23
6. Bourinbaiar A.S., and Phillips D.M. Transmission of human immunodeficiency virus from monocytes to epithelia. J. AIDS 4 (1991) 56-63
7. Bruggeman L.A., Dikman S., Meng C., Quaggin S.E., Coffman T.M., and Klotman P.E. Nephropathy in human immunodeficiency virus-1 transgenic mice is due to renal transgene expression. J. Clin. Invest. 100 (1997) 84-92
8. Bruggeman L.A., Ross M.D., Tanji N., Cara A., Dikman S., Gordon R.E., Burns G.C., D'Agati V.D., Winston J.A., Klotman M.E., and Klotman P.E. Renal epithelium is a previously unrecognized site of HIV-1 infection. J. Am. Soc. Nephrol. 11 (2000) 2079-2087
9. Cavrois M., Neidleman J., and Green W.C. The Achilles heel of the Trojan horse of HIV-1 trans-infection. Plos. Pathog. 4 6 (2008) e1000051
10. Chen W.J., Goldstein J.L., and Brown M.S. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265 (1990) 3116-3123
11. Chen Y., Zhang J., Li J., Zhao T., Tang Y., and Wu Y. Expression of B7-H1 in inflammatory renal tubular epithelial cells. Nephron. Exp. Nephrol. 102 (2006) e81-e92
12. Cohen A.H., Sun N.C.J., Shapsak P., and Imagawa D.T. Demonstration of human immunodeficiency virus in renal epithelium in HIV-associated nephropathy. Mod. Pathol. 2 (1989) 125-128
13. Conaldi P.G., Biancone L., Bottelli A., Wade-Evans A., Racusen L.C., Boccellino M., Orlandi V., Serra C., Camussi G., and Toniolo A. HIV-1 kills tubular epithelial cells in vitro by triggering an apoptotic pathway involving caspase activation and Fas upregulation. J. Clin. Invest. 102 (1998) 2041-2049
14. Dalgleish A.G., Beverley P.C., Clapham P.R., Crawford D.H., Greaves M.F., and Weiss R.A. The CD4 (T4) antigen is an essential component of the receptor for AIDS retrovirus. Nature 312 (1984) 763-767
15. de Haij S., Woltman A.M., Trouw L.A., Bakker A.C., Kamerling S.W., van der Kooij S.W., Chen L., Kroczek R.A., Daha M.R., and van Kooten C. Renal tubular epithelial cells modulate T-cell responses via ICOS-L and B7-H1. Kidney Int. 68 (2005) 2091-2102
16. Dezzutti C.S., Guenthner P.C., Cummins Jr. J.E., Cabrera T., Marshall J.H., Dillberger A., and Lal R.B. Cervical and prostate primary epithelial cells are not productively infected but sequester human immunodeficiency virus type 1. J. Infect. Dis. 183 (2001) 1204-1213
17. Douglas G.C., Fry G.N., Thirkill T., Holmes E., Hakim H., Jennings M., and King B.F. Cell-mediated infection of human placental trophoblasts with HIV in vitro. AIDS Res. Hum. Retroviruses 7 (1989) 735-740
18. Eitner F., Cui Y., Hudkins K.L., Stokes M.B., Segerer S., Mack M., Lewis P.L., Abraham A.A., Schlondorff D., Gallo G., Kimmel P.L., and Alpers C.E. Chemokine receptor CCR5 and CXCR4 expression in HIV-associated kidney disease. J. Am. Soc. Nephrol. 11 (2000) 856-867
19. Fantini J., Yahi N., and Chermann J.-C. Human immunodeficiency virus can infect the apical and basolateral surface of human colonic epithaelial cells. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 9297-9301
20. Feinberg H., Park-Snyder S., Kolatkar A.R., Heise C.T., Taylor M.E., and Weis W.I. Structure of a C-type carbohydrate recognition domain from the macrophage mannose receptor. J. Biol. Chem. 275 (2000) 21539-21548
21. Finzi A., Brunet A., Xiao Y., Thibodeau J., and Cohen E.A. Major histocompatibility complex class II promote human immunodeficiency virus type 1 and budding to late endosomal/multivesicular body compartments. J. Virol. 80 (2006) 9789-9797
22. Garcia E., Pion M., Pelchen-Matthews A., Collinson L., Arrighi J.F., Blot G., Leuba F., Escola J.M., Demaurex N., Marsh M., and Piguet V. HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 66 (2005) 488-501
23. Haraouse J.M., Kunsch C., Hartle H.T., Laughlin M.A., Hoxie J.A., Wigdahl B., and Gonzalez-Scarano F. CD4-independent infection of human neural cells by immunodeficiency virus type 1. J. Virol. 63 (1989) 2527-2533
24. Hatsukari I., Singh P., Hitosugi N., Messmer D., Valderrama E., Teichberg S., Chaung W., Gross E., Schmidtmayerova H., and Singhal P.C. DEC-205-mediated internalization of HIV-1 results in the establishment of silent infection in renal tubular cells. J. Am. Soc. Nephrol. 18 (2007) 780-787
25. Howard M.J., and Isacke C.M. The C-type lectin receptor Endo180 displays internalization and recycling properties distinct from other members of the mannose receptor family. J. Biol. Chem. 277 (2002) 32320-32331
26. Huang J.F., Yang Y., Sepulveda H., Shi W., Hwang I., Peterson P.A., Jackson M.R., Sprent J., and Cai Z. TCR-mediated internalization of peptide-MHC complexes acquired by T cells. Science 286 (1999) 952-954
27. Jackman R.M., Stenger S., Lee A., Moody D.B., Rogers R.A., Niazi K.R., Sugita M., Modlin R.L., Peters P.J., and Porcelli S.A. The tyrosine-containing cytoplasmic tail of CD1b is essential for its efficient presentation of bacterial lipid antigens. Immunity 8 (1998) 341-351
28. Jiang W., Swiggard W.J., Heufler C., Peng M., Mirza A., Steinman R.M., and Nussenzweig M.C. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 375 (1995) 151-155
29. Kamya M.R., Kigonya C.N., and McFarland W. HIV infection may adversely affect clinical response to chloroquine therapy for uncomplicated malaria in children. AIDS 15 (2001) 1187-1188
30. Kimmel P.L., Phillips T.M., Ferrira-Centeno A., Farkas-Szlallasi T., Abraham A.A., and Garrett C.T. HIV-associated immune mediated renal disease. Kidney Int. 44 (1993) 1327-1340
31. Kuroiwa T., Schlimgen R., Illei G.G., McInnes I.B., and Boumpas D.T. Distinct T cell/renal tubular epithelial cell interaction define differential chemokine production: implication for tubulointerstitial injury in chronic glomerulonephritides. J. Immunol. 164 (2000) 3323-3329
32. Kwon D.S., Gregorio G., Bitton N., Hendrickson W.A., and Littman D.R. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16 (2002) 135-144
33. Li J., Bentsman G., Potash M.J., and Volsky D.J. Human immunodeficiency virus type 1 efficiently binds to human fetal astrocytes and induce neuroinflammatory responses independent of infection. BMC Neurosci. 8 (2007) 31
34. Li X.L., Moudgil T., Vinters H.V., and Ho D.D. CD4-independent, productive infection of a neuronal cell line by human immunodeficiency virus type 1. J. Virol. 64 (1990) 1383-1387
35. Ludwig I.S., Lekkerkerker A.N., Depla E., Bosman F., Musters R.J.P., Depraetere S., van Kooyk Y., and Geijtenbeek T.B.H. Hepatitis C virus targets DC-SIGN and L-SIGN to escape lysosomal degradation. J. Virol. 78 (2004) 8322-8332
36. Mahnke K., Guo M., Lee S., Sepulveda H., Swain S.L., Nussenzweig M., and Steinman R.M. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J. Cell. Biol. 151 (2000) 673-684
37. Marras D., Bruggeman L.A., Gao F., Tanji N., Mansukhani M.M., Cara A., Ross M.D., Gusella G.L., Benson G., D'Agati V.D., Hahn B.H., Klotman M.E., and Klotman P.E. Replication and compartmentalization of HIV-1 in kidney epithelium of patients with HIV-associated nephropathy. Nat. Med. 8 (2002) 522-526
38. McDonald D., Wu L., Bohks S.M., KewalRamani V.N., Unutmaz D., and Hope T.J. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300 (2003) 1295-1297
39. Meng G., Wei X., Wu X., Sellers M.T., Decker J.M., Moldoveanu Z., Orenstein J.M., Graham M.F., Kappes J.C., Mestecky J., Shaw G.M., and Smith P.D. Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+ cells. Nat. Med. 8 (2003) 114-116
40. Meyers C.M. New insights into the pathogenesis of interstitial nephritis. Curr. Opin. Nephrol. Hypertens. 8 (1999) 287-292
41. Moore J.P., McKeating J.A., Weiss R.A., and Sattentau Q.J. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 250 (1990) 1139-1142
42. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65 (1983) 55-63
43. Naarding M.A., Baan E., Pollakis G., and Paxton M.A. Effect of chloroquine on reducing HIV-1 replication in vitro and the DC-SIGN mediated transfer of virus to CD4-positive T-lymphocytes. Retrovirology 30 (2007) 4-6
44. Pardo V., Aldana M., Colton R.M., Fischl M.A., Jaffe D., Moskowitz L., Hensley G.T., and Bourgoignie J.J. Glomerular lesions in acquired immunodeficiency syndrome. Ann. Inter. Med. 101 (1984) 429-434
45. Pearce-Pratt R., Malamud D., and Phillips D.M. Role of cytoskeleton in cell-to-cell transmission of human immunodeficiency virus. J. Virol. 68 (1994) 2898-2905
46. Pelchen-Matthews A., Kramer B., and Marsh M. Infectious HIV-1 assembles in late endosomes in primary macrophages. J. Cell Biol. 162 (2003) 443-455
47. Phillips D.M., and Bourinbaiar A.S. Mechanism of HIV spread from lymphocytes to epithelia. Virology 186 (1989) 261-273
48. Rayne F., Vendeville A., Bonhoure A., and Beaumelle B. The ability of chloroquine to prevent tat-induce cytokine secretion by monocytes is implicated in it's in-vivo anti-human immunodeficiency virus type 1 activity. J. Virol. 78 (2004) 12054-12057
49. Rao T.K.S., Filppone E.J., Nicastri A.D., Landesman S.H., Frank E., Chen C.K., and Friedman E.A. Associated focal segmental glomerulosclerosis in the acquired immunodeficiency syndrome. N. Engl. J. Med. 310 (1984) 669-673
50. Raposo G., Moore M., Innes D., Leijendekker R., Leigh-Brown A., Benaroch P., and Geuze H. Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic 3 (2002) 718-729
51. Rubin-Kelley V.E., and Jevnikar A.M. Antigen presentation by renal tubular epithelial cells. J. Am. Soc. Nephrol. 2 (1991) 13-26
52. Schoop R., Wahl P., Le Hir M., Heemann U., Wang M., and Wuthrich R.P. Suppressed T-cell activation by IFN-gamma-induced expression of PD-L1 on renal tubular cells. Nephrol. Dial. Transplant 19 (2004) 2713-2720
53. Seth P., Mani H., Singh A.K., Banaudha K.K., Madhavan S., Sidhu G.S., Gaddipati J.P., Vogel S.N., and Maheshwari R.K. Acceleration of viral replication and up-regulation of cytokine levels by antimalarials: implication in malaria-endemic areas. Am. J. Trop. Med. Hyg. 61 (1999) 180-186
54. Sieczkarski S.B., and Whittaker G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 83 (2002) 1535-1545
55. Stahl P.D., and Ezekowitz R.A. The mannose receptor is a pattern recognition receptor involved in host defense. Curr. Opin. Immunol. 10 (1998) 50-55
56. Stantchev T.S., and Broder C.C. Human immunodeficiency virus type-1 and chemokines: beyond competition for common cellular receptors. Cytokine Growth Factor Rev. 12 (2001) 219-243
57. Steinman M. Dendritic cells and immune-based therapies. Exp. Hematol. 24 (1996) 859-862
58. Tanji N., Ross M.D., Tanji K., Bruggeman L.A., Markowitz G.S., Klotman P.E., and D'Agati V.D. Detection and localization of HIV-1 DNA in renal tissues by in situ polymerase chain reaction. Histol. Histopathol. 21 (2006) 393-401
59. Tornatore C., Meyers K., Atwood W., Conant K., and Major E. Temporal patterns of human immunodeficiency virus type 1 transcripts in human fetal astrocytes. J. Virol. 68 (1994) 93-102
60. Vacharaska A., Asrani A.C., Gebhard K.H., Fasching C.E., Giacaman R.A., Janoff E.N., Ross K.F., and Herzberg M.C. Oral keratinocytes support non-replicative infection and transfer of harbored HIV-1 to permissive cells. Retrovirology 5 (2008) 66
61. van Kooten C., Daha M.R., and van Es L.A. Tubular epithelial cells: S critical cell type in the regulation of renal inflammatory processes. Exp. Nephrol. 7 (1999) 429-437
62. Vidricaire G., Imbeault M., and Tremblay M.J. Endocytic host cell machinery plays a dominant role in intracellular trafficking of incoming human immunodeficiency virus type 1 in human placental trophoblasts. J. Virol. 78 (2004) 11904-11915
63. Vidricaire G., Tardif M.R., and Tremblay M.J. The low viral production in trophoblastic cells is due to a high endocytic internalization of the human immunodeficiency virus type 1 and can be overcome by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin-1. J. Biol. Chem. 278 (2003) 15832-15841
64. Vidricaire G., and Tremblay M.J. A clathrin, caveolae, and dynamin-independent endocytic pathway requiring free membrane cholesterol drives HIV-1 internalization and infection in polarized trophoblastic cells. J. Mol. Biol. 368 (2007) 1267-1283
65. Vijaykumar T.S., Nath A., and Chauhan A. Chloroquine mediated molecular tuning of astrocytes for enhanced permissiveness to HIV infection. Virology 381 (2008) 1-5
66. Waeckler-Men Y., Starkem A., Wahl P.R., and Wuthrich R.P. Limited costimulatory molecule expression on renal tubular epithelial cells impairs T cell activation. Kidney Blood Press. Res. 30 (2007) 421-429
67. Wahl P., and Wuthrich R.P. Role of the B7RP-1/ICOS pathway in renal tubular epithelial antigen presentation to CD4 Th1and Th2 cells. Nephron. Exp. Nephrol. 98 (2004) e31-e38
68. Wiley R.D., and Gummuluuru S. Immature dendritic cells-derived exosomes can mediate HIV-1 trans infection. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 738-743
69. Willey R.L., Smith D.H., Lasky L.A., Theodore T.S., Earl P.L., Moss B., Capon D.J., and Martin M.A. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J. Virol. 62 (1988) 139-147
70. Winston J.A., Bruggeman L.A., Ross M.D., D'Agati V.D., Klotman P.E., and Klotman M.E. Nephropathy and establishment of a renal reservoir of HIV type 1 during primary infection. N. Engl. J. Med. 344 (2001) 1979-1984
71. Witmer-Pack M.D., Swiggard W.J., Mirza A., Inaba K., and Steinman R.M. Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. II. Expression in situ in lymphoid and nonlymphoid tissues. Cell Immunol. 163 (1995) 157-162