High avidity CD8+ T cells efficiently eliminate motile HIV-infected targets and execute a locally focused program of anti-viral function

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Foley, Maria Hottelet ^a,b,c   Forcier, Talitha ^a,b   McAndrew, Elizabeth ^b   Gonzalez, Michael ^d   Chen, Huabiao ^b   Juelg, Boris ^b   Walker, Bruce D ^b   Irvine, Darrell J ^a,b,c,d  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b HARVARD UNIVERSITY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; T LYMPHOCYTE RECEPTOR;

ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; ARTICLE; CALCIUM SIGNALING; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL KILLING; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; NONHUMAN; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS;

ANTIGENS, CD4; ANTIGENS, CD58; ANTIGENS, VIRAL; CALCIUM; CD4-POSITIVE T-LYMPHOCYTES; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CYTOTOXICITY, IMMUNOLOGIC; GENE EXPRESSION; HIV; HIV INFECTIONS; HUMANS; IMMUNITY, CELLULAR; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84895783498     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087873     Document Type: Article

References (63)

1. Zhang Z, Schuler T, Zupancic M, Wietgrefe S, Staskus KA, et al. (1999) Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286: 1353-1357.
2. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-1038.
3. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, et al. (2012) HIV-infected T cells are migratory vehicles for viral dissemination. Nature 490: 283-287.
4. Li Q, Skinner PJ, Ha SJ, Duan L, Mattila TL, et al. (2009) Visualizing antigen-specific and infected cells in situ predicts outcomes in early viral infection. Science 323: 1726-1729.
5. Reynolds MR, Rakasz E, Skinner PJ, White C, Abel K, et al. (2005) CD8+ T-lymphocyte response to major immunodominant epitopes after vaginal exposure to simian immunodeficiency virus: too late and too little. J Virol 79: 9228-9235. (Pubitemid 40934834)
6. Miller CJ, Li Q, Abel K, Kim EY, Ma ZM, et al. (2005) Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J Virol 79: 9217-9227. (Pubitemid 40934833)
7. Freel SA, Lamoreaux L, Chattopadhyay PK, Saunders K, Zarkowsky D, et al. (2010) Phenotypic and Functional Profile of HIV-Inhibitory CD8 T Cells Elicited by Natural Infection and Heterologous Prime/Boost Vaccination. Journal of Virology 84: 4998-5006.
8. Genesca M, Skinner PJ, Bost KM, Lu D, Wang Y, et al. (2008) Protective attenuated lentivirus immunization induces SIV-specific T cells in the genital tract of rhesus monkeys. Mucosal Immunol 1: 219-228. (Pubitemid 351541307)
9. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, et al. (2011) Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473: 523-527.
10. Hansen SG, Sacha JB, Hughes CM, Ford JC, Burwitz BJ, et al. (2013) Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms. Science 340: 1237874.
11. Faroudi M, Utzny C, Salio M, Cerundolo V, Guiraud M, et al. (2003) Lytic versus stimulatory synapse in cytotoxic T lymphocyte/target cell interaction: manifestation of a dual activation threshold. Proc Natl Acad Sci U S A 100: 14145-14150. (Pubitemid 37499205)
12. Purbhoo MA, Boulter JM, Price DA, Vuidepot AL, Hourigan CS, et al. (2001) The human CD8 coreceptor effects cytotoxic T cell activation and antigen sensitivity primarily by mediating complete phosphorylation of the T cell receptor zeta chain. Journal of Biological Chemistry 276: 32786-32792.
13. Stinchcombe JC, Bossi G, Booth S, Griffiths GM (2001) The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15: 751-761. (Pubitemid 34008503)
14. Yang OO, Kalams SA, Trocha A, Cao HY, Luster A, et al. (1997) Suppression of human immunodeficiency virus type 1 replication by CD8(+) cells: Evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. Journal of Virology 71: 3120-3128. (Pubitemid 27119959)
15. Genesca M, Rourke T, Li J, Bost K, Chohan B, et al. (2007) Live attenuated lentivirus infection elicits polyfunctional simian immunodeficiency virus Gagspecific CD8+ T cells with reduced apoptotic susceptibility in rhesus macaques that control virus replication after challenge with pathogenic SIVmac239. J Immunol 179: 4732-4740.
16. Migueles SA, Laborico AC, Shupert WL, Sabbaghian MS, Rabin R, et al. (2002) HIV-specific CD8(+) T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nature Immunology 3: 1061-1068. (Pubitemid 35363659)
17. Yang H, Wu H, Hancock G, Clutton G, Sande N, et al. (2012) Antiviral inhibitory capacity of CD8+ T cells predicts the rate of CD4+ T-cell decline in HIV-1 infection. J Infect Dis 206: 552-561.
18. Mempel TR, Pittet MJ, Khazaie K, Weninger W, Weissleder R, et al. (2006) Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 25: 129-141. (Pubitemid 44066829)
19. Kawakami N, Nagerl UV, Odoardi F, Bonhoeffer T, Wekerle H, et al. (2005) Live imaging of effector cell trafficking and autoantigen recognition within the unfolding autoimmune encephalomyelitis lesion. J Exp Med 201: 1805-1814. (Pubitemid 41002899)
20. Kang SS, Herz J, Kim JV, Nayak D, Stewart-Hutchinson P, et al. (2011) Migration of cytotoxic lymphocytes in cell cycle permits local MHC I-dependent control of division at sites of viral infection. Journal of Experimental Medicine 208: 747-759.
21. Coppieters K, Amirian N, von Herrath M (2011) Intravital imaging of CTLs killing islet cells in diabetic mice. J Clin Invest.
22. McGavern DB, Christen U, Oldstone MBA (2002) Molecular anatomy of antigen-specific CD8(+) T cell engagement and synapse formation in vivo. Nature Immunology 3: 918-925. (Pubitemid 35154004)
23. Purbhoo MA, Irvine DJ, Huppa JB, Davis MM (2004) T cell killing does not require the formation of a stable mature immunological synapse. Nature Immunology 5: 524-530. (Pubitemid 38660465)
24. Isaaz S, Baetz K, Olsen K, Podack E, Griffiths GM (1995) Serial Killing by Cytotoxic T-Lymphocytes - T-Cell Receptor Triggers Degranulation, Re-Filling of the Lytic Granules and Secretion of Lytic Proteins Via a Non-Granule Pathway. European Journal of Immunology 25: 1071-1079.
25. Jenkins MR, La Gruta NL, Doherty PC, Trapani JA, Turner SJ, et al. (2009) Visualizing CTL activity for different CD8(+) effector T cells supports the idea that lower TCR/epitope avidity may be advantageous for target cell killing. Cell Death and Differentiation 16: 537-542.
26. Petrovas C, Mueller YM, Katsikis PD (2004) HIV-specific CD8+ T cells: serial killers condemned to die? Curr HIV Res 2: 153-162. (Pubitemid 38854927)
27. Lieberman J, Shankar P, Manjunath N, Andersson J (2001) Dressed to kill? A review of why antiviral CD8 T lymphocytes fail to prevent progressive immunodeficiency in HIV-1 infection. Blood 98: 1667-1677.
28. Beal AM, Anikeeva N, Varma R, Cameron TO, Vasiliver-Shamis G, et al. (2009) Kinetics of early T cell receptor signaling regulate the pathway of lytic granule delivery to the secretory domain. Immunity 31: 632-642.
29. Wagner L, Yang OO, Garcia-Zepeda EA, Ge YM, Kalams SA, et al. (1998) beta-chemokines are released from HIV-1-specific cytolytic T-cell granules complexed to proteoglycans. Nature 391: 908-911. (Pubitemid 28157670)
30. Faroudi M, Zaru R, Paulet P, Muller S, Valitutti S (2003) Cutting edge: T lymphocyte activation by repeated immunological synapse formation and intermittent signaling. J Immunol 171: 1128-1132. (Pubitemid 36900039)
31. Wiedemann A, Depoil D, Faroudi M, Valitutti S (2006) Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses. Proceedings of the National Academy of Sciences of the United States of America 103: 10985-10990. (Pubitemid 44148405)
32. Almeida JR, Sauce D, Price DA, Papagno L, Shin SY, et al. (2009) Antigen sensitivity is a major determinant of CD8(+) T-cell polyfunctionality and HIV-suppressive activity. Blood 113: 6351-6360.
33. Friedl P, Brocker EB (2004) Reconstructing leukocyte migration in 3D extracellular matrix by time-lapse videomicroscopy and computer-assisted tracking. Methods Mol Biol 239: 77-90.
34. Weigelin B, Friedl P (2010) A three-dimensional organotypic assay to measure target cell killing by cytotoxic T lymphocytes. Biochem Pharmacol 80: 2087-2091.
35. Wolf K, Alexander S, Schacht V, Coussens LM, von Andrian UH, et al. (2009) Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol 20: 931-941.
36. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, et al. (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283: 857-860.
37. Genesca M, Skinner PJ, Hong JJ, Li J, Lu D, et al. (2008) With minimal systemic T-cell expansion, CD8+ T Cells mediate protection of rhesus macaques immunized with attenuated simian-human immunodeficiency virus SHIV89.6 from vaginal challenge with simian immunodeficiency virus. J Virol 82: 11181-11196.
38. Bennett MS, Ng HL, Dagarag M, Ali A, Yang OO (2007) Epitope-dependent avidity thresholds for cytotoxic T-lymphocyte clearance of virus-infected cells. Journal of Virology 81: 4973-4980. (Pubitemid 46744409)
39. Iversen AKN, Stewart-Jones G, Learn GH, Christie N, Sylvester-Hviid C, et al. (2006) Conflicting selective forces affect T cell receptor contacts in an immunodominant human immunodeficiency virus epitope. Nature Immunology 7: 179-189. (Pubitemid 43135884)
40. Dustin ML, Bromley SK, Kan ZY, Peterson DA, Unanue ER (1997) Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proceedings of the National Academy of Sciences of the United States of America 94: 3909-3913. (Pubitemid 27180472)
41. Breart B, Lemaitre F, Celli S, Bousso P (2008) Two-photon imaging of intratumoral CD8(+) T cell cytotoxic activity during adoptive T cell therapy in mice. Journal of Clinical Investigation 118: 1390-1397. (Pubitemid 351500432)
42. Mrass P, Takano H, Ng LG, Daxini S, Lasaro MO, et al. (2006) Random migration precedes stable target cell interactions of tumor-infiltrating T cells. Journal of Experimental Medicine 203: 2749-2761. (Pubitemid 44833350)
43. Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S (2007) In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. Journal of Experimental Medicine 204: 345-356. (Pubitemid 46294550)
44. Tsomides TJ, Aldovini A, Johnson RP, Walker BD, Young RA, et al. (1994) Naturally processed viral peptides recognized by cytotoxic T lymphocytes on cells chronically infected by human immunodeficiency virus type 1. J Exp Med 180: 1283-1293. (Pubitemid 24289602)
45. Tenzer S, Wee E, Burgevin A, Stewart-Jones G, Friis L, et al. (2009) Antigen processing influences HIV-specific cytotoxic T lymphocyte immunodominance. Nature Immunology 10: 636-U109.
46. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, et al. (2006) HIV nonprogressors preferentially maintain highly functional HIV-specific CD8(+) T cells. Blood 107: 4781-4789. (Pubitemid 43882629)
47. Chen H, Ndhlovu ZM, Liu D, Porter LC, Fang JW, et al. (2012) TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat Immunol 13: 691-700.
48. Migueles SA, Osborne CM, Royce C, Compton AA, Joshi RP, et al. (2008) Lytic Granule Loading of CD8(+) T Cells Is Required for HIV-Infected Cell Elimination Associated with Immune Control. Immunity 29: 1009-1021.
49. Barouch DH, O'Brien KL, Simmons NL, King SL, Abbink P, et al. (2010) Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat Med 16: 319-323.
50. Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, et al. (2007) Superior control of HIV-1 replication by CD8(+) T cells is reflected by their avidity, polyfunctionality, and clonal turnover. Journal of Experimental Medicine 204: 2473-2485. (Pubitemid 47529331)
51. Cocchi F, DeVico AL, Yarchoan R, Redfield R, Cleghorn F, et al. (2000) Higher macrophage inflammatory protein (MIP)-1alpha and MIP-1beta levels from CD8+ T cells are associated with asymptomatic HIV-1 infection. Proc Natl Acad Sci U S A 97: 13812-13817.
52. Dolan MJ, Kulkarni H, Camargo JF, He W, Smith A, et al. (2007) CCL3L1 and CCR5 influence cell-mediated immunity and affect HIV-AIDS pathogenesis via viral entry-independent mechanisms. Nat Immunol 8: 1324-1336. (Pubitemid 350131170)
53. Shaw S, Luce GE, Quinones R, Gress RE, Springer TA, et al. (1986) Two antigen-independent adhesion pathways used by human cytotoxic T-cell clones. Nature 323: 262-264. (Pubitemid 16054312)
54. Anikeeva N, Somersalo K, Sims TN, Thomas VK, Dustin ML, et al. (2005) Distinct role of lymphocyte function-associated antigen-1 in mediating effective cytolytic activity by cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 102: 6437-6442. (Pubitemid 40617461)
55. Celli S, Garcia Z, Bousso P (2005) CD4 T cells integrate signals delivered during successive DC encounters in vivo. J Exp Med 202: 1271-1278. (Pubitemid 41586957)
56. Valitutti S, Muller S, Dessing M, Lanzavecchia A (1996) Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J Exp Med 183: 1917-1921. (Pubitemid 26134333)
57. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF (2010) The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 10: 11-23.
58. Cerottini JC, Brunner KT (1974) Cell-mediated cytotoxicity, allograft rejection, and tumor immunity. Adv Immunol 18: 67-132.
59. Rothstein TL, Mage M, Jones G, McHugh LL (1978) Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J Immunol 121: 1652-1656. (Pubitemid 9050239)
60. Zagury D, Bernard J, Thierness N, Feldman M, Berke G (1975) Isolation and Characterization of Individual Functionally Reactive Cytotoxic T-Lymphocytes - Conjugation, Killing and Recycling at Single Cell Level. European Journal of Immunology 5: 818-822.
61. Brown A, Gartner S, Kawano T, Benoit N, Cheng-Mayer C (2005) HLA-A2 down-regulation on primary human macrophages infected with an M-tropic EGFP-tagged HIV-1 reporter virus. J Leukoc Biol 78: 675-685. (Pubitemid 41292090)
62. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D (1998) HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391: 397-401. (Pubitemid 28093515)
63. Schneidewind A, Brockman MA, Yang R, Adam RI, Li B, et al. (2007) Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J Virol 81: 12382-12393. (Pubitemid 350085852)