Selective Loss of Signaling Lymphocytic Activation Molecule Family Member 4-Positive CD8+ T Cells Contributes to the Decreased Cytotoxic Cell Activity in Systemic Lupus Erythematosus

Arthritis and Rheumatology

Volumn 68, Issue 1, 2016, Pages 164-173

  Kis Toth, Katalin ^a   Comte, Denis ^a   Karampetsou, Maria P ^a   Kyttaris, Vasileios C ^a   Kannan, Lakshmi ^a   Terhorst, Cox ^a   Tsokos, George C ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; CD3 ANTIBODY; CD8 ANTIGEN; GRANZYME B; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PERFORIN; SIGNALING LYMPHOCYTIC ACTIVATION MOLECULE FAMILY MEMBER 4; UNCLASSIFIED DRUG; VIRUS PROTEIN; CD244 PROTEIN, HUMAN; CD48 ANTIGEN; CD48 PROTEIN, HUMAN; GRANZYME; IMMUNOGLOBULIN RECEPTOR; LEUKOCYTE ANTIGEN; MESSENGER RNA; SIGNALING LYMPHOCYTIC ACTIVATION MOLECULE; VIRAL PROTEIN;

ARTICLE; CD8+ T LYMPHOCYTE; CELL MEDIATED CYTOTOXICITY; CELL SURFACE; CONTROLLED STUDY; DEGRANULATION; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SYSTEMIC LUPUS ERYTHEMATOSUS; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; CASE CONTROL STUDY; CELL PROLIFERATION; CYTOTOXIC T LYMPHOCYTE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; NATURAL KILLER CELL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANTIGENS, CD; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CD48 ANTIGEN; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FLOW CYTOMETRY; GENE EXPRESSION; GRANZYMES; HUMANS; KILLER CELLS, NATURAL; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; PERFORIN; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, IMMUNOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNALING LYMPHOCYTIC ACTIVATION MOLECULE FAMILY; T-LYMPHOCYTES, CYTOTOXIC; VIRAL PROTEINS;

EID: 84951945399     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39410     Document Type: Article

References (52)

1. Tsokos GC., Systemic lupus erythematosus. N Engl J Med 2011; 365: 2110-21.
2. + T cells from lupus-prone mice are hyperresponsive to T cell receptor engagement with low and high affinity peptide antigens: a model to explain spontaneous T cell activation in lupus. J Exp Med 2001; 193: 329-37.
3. Moulton VR, Tsokos GC., Abnormalities of T cell signaling in systemic lupus erythematosus. Arthritis Res Ther 2011; 13: 207.
4. Tsokos GC, Magrath IT, Balow JE., Epstein-Barr virus induces normal B cell responses but defective suppressor T cell responses in patients with systemic lupus erythematosus. J Immunol 1983; 131: 1797-801.
5. Mok CC, Lau CS., Pathogenesis of systemic lupus erythematosus. J Clin Pathol 2003; 56: 481-90.
6. Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, et al., Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore) 2003; 82: 299-308.
7. Valiante NM, Trinchieri G., Identification of a novel signal transduction surface molecule on human cytotoxic lymphocytes. J Exp Med 1993; 178: 1397-406.
8. + T cells. Mol Immunol 2005; 42: 489-94.
9. Altvater B, Landmeier S, Pscherer S, Temme J, Juergens H, Pule M, et al., 2B4 (CD244) signaling via chimeric receptors costimulates tumor-antigen specific proliferation and in vitro expansion of human T cells. Cancer Immunol Immunother 2009; 58: 1991-2001.
10. Dong Z, Cruz-Munoz ME, Zhong MC, Chen R, Latour S, Veillette A., Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat Immunol 2009; 10: 973-80.
11. Waggoner SN, Kumar V., Evolving role of 2B4/CD244 in T and NK cell responses during virus infection. Front Immunol 2012; 3: 377.
12. + effector αβ T cells. J Immunol 2001; 167: 6165-70.
13. Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, Polley A, et al., Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 2009; 10: 29-37.
14. Petri M., Infection in systemic lupus erythematosus. Rheum Dis Clin North Am 1998; 24: 423-56.
15. Enose-Akahata Y, Matsuura E, Oh U, Jacobson S., High expression of CD244 and SAP regulated CD8 T cell responses of patients with HTLV-I associated neurologic disease. PLoS Pathog 2009; 5: e1000682.
16. Blanco P, Pitard V, Viallard JF, Taupin JL, Pellegrin JL, Moreau JF., Increase in activated CD8+ T lymphocytes expressing perforin and granzyme B correlates with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 2005; 52: 201-11.
17. Fritsch RD, Shen X, Illei GG, Yarboro CH, Prussin C, Hathcock KS, et al., Abnormal differentiation of memory T cells in systemic lupus erythematosus. Arthritis Rheum 2006; 54: 2184-97.
18. Kim JR, Mathew SO, Patel RK, Pertusi RM, Mathew PA., Altered expression of signalling lymphocyte activation molecule (SLAM) family receptors CS1 (CD319) and 2B4 (CD244) in patients with systemic lupus erythematosus. Clin Exp Immunol 2010; 160: 348-58.
19. Ota Y, Kawaguchi Y, Takagi K, Tochimoto A, Kawamoto M, Katsumata Y, et al., Single nucleotide polymorphisms of CD244 gene predispose to renal and neuropsychiatric manifestations with systemic lupus erythematosus. Mod Rheumatol 2010; 20: 427-31.
20. Puxeddu I, Bongiorni F, Chimenti D, Bombardieri S, Moretta A, Bottino C, et al., Cell surface expression of activating receptors and co-receptors on peripheral blood NK cells in systemic autoimmune diseases. Scand J Rheumatol 2012; 41: 298-304.
21. + T cells are significantly elevated in patients with systemic lupus erythematosus. Rheumatology (Oxford) 2012; 51: 1587-94.
22. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al., The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982; 25: 1271-7.
23. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH, and the Committee on Prognosis Studies in SLE. Derivation of the SLEDAI: a disease activity index for lupus patients. Arthritis Rheum 1992; 35: 630-40.
24. Roederer M, Nozzi JL, Nason MC., SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 2011; 79: 167-74.
25. Garni-Wagner BA, Purohit A, Mathew PA, Bennett M, Kumar V., A novel function-associated molecule related to non-MHC-restricted cytotoxicity mediated by activated natural killer cells and T cells. J Immunol 1993; 151: 60-70.
26. + T cells and display an inflammatory effector phenotype. J Immunol 2009; 183: 4675-81.
27. Gravano DM, Hoyer KK., Promotion and prevention of autoimmune disease by CD8+ T cells. J Autoimmun 2013; 45: 68-79.
28. Stohl W, Elliott JE, Li L, Podack ER, Lynch DH, Jacob CO., Impaired nonrestricted cytolytic activity in systemic lupus erythematosus: involvement of a pathway independent of Fas, tumor necrosis factor, and extracellular ATP that is associated with little detectable perforin. Arthritis Rheum 1997; 40: 1130-7.
29. Kang I, Quan T, Nolasco H, Park SH, Hong MS, Crouch J, et al., Defective control of latent Epstein-Barr virus infection in systemic lupus erythematosus. J Immunol 2004; 172: 1287-94.
30. Kang I, Park SH., Infectious complications in SLE after immunosuppressive therapies. Curr Opin Rheumatol 2003; 15: 528-34.
31. Moon UY, Park SJ, Oh ST, Kim WU, Park SH, Lee SH, et al., Patients with systemic lupus erythematosus have abnormally elevated Epstein-Barr virus load in blood. Arthritis Res Ther 2004; 6: R295-302.
32. Lieberman LA, Tsokos GC., Lupus-prone mice fail to raise antigen-specific T cell responses to intracellular infection. PLoS One 2014; 9: e111382.
33. Berner BR, Tary-Lehmann M, Yonkers NL, Askari AD, Lehmann PV, Anthony DD., Phenotypic and functional analysis of EBV-specific memory CD8 cells in SLE. Cell Immunol 2005; 235: 29-38.
34. Larsen M, Sauce D, Deback C, Arnaud L, Mathian A, Miyara M, et al., Exhausted cytotoxic control of Epstein-Barr virus in human lupus. PLoS Pathog 2011; 7: e1002328.
35. Messmer B, Eissmann P, Stark S, Watzl C., CD48 stimulation by 2B4 (CD244)-expressing targets activates human NK cells. J Immunol 2006; 176: 4646-50.
36. Lee KM, Bhawan S, Majima T, Wei H, Nishimura MI, Yagita H, et al., The NK cell receptor 2B4 augments antigen-specific T cell cytotoxicity through CD48 ligation on neighboring T cells. J Immunol 2003; 170: 4881-5.
37. Sivori S, Parolini S, Falco M, Marcenaro E, Biassoni R, Bottino C, et al., 2B4 functions as a co-receptor in human NK cell activation. Eur J Immunol 2000; 30: 787-93.
38. Johnson LA, Goldfarb RH, Mathew PA., Regulation of IFN-γ production following 2B4 activation in human NK cells. In Vivo 2000; 14: 625-9.
39. Dupre L, Andolfi G, Tangye SG, Clementi R, Locatelli F, Arico M, et al., SAP controls the cytolytic activity of CD8+ T cells against EBV-infected cells. Blood 2005; 105: 4383-9.
40. Lee KM, McNerney ME, Stepp SE, Mathew PA, Schatzle JD, Bennett M, et al., 2B4 acts as a non-major histocompatibility complex binding inhibitory receptor on mouse natural killer cells. J Exp Med 2004; 199: 1245-54.
41. Vacca P, Pietra G, Falco M, Romeo E, Bottino C, Bellora F, et al., Analysis of natural killer cells isolated from human decidua: evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK-cell function. Blood 2006; 108: 4078-85.
42. Youngblood B, Wherry EJ, Ahmed R., Acquired transcriptional programming in functional and exhausted virus-specific CD8 T cells. Curr Opin HIV AIDS 2012; 7: 50-7.
43. Ezinne CC, Yoshimitsu M, White Y, Arima N., HTLV-1 specific CD8+ T cell function augmented by blockade of 2B4/CD48 interaction in HTLV-1 infection. PLoS One 2014; 9: e87631.
44. + T cells limits their effectiveness during sustained high viral load. Immunity 2011; 35: 285-98.
45. + T cells that maintains homeostasis in the small intestine. Gastroenterology 2015; 148: 991-1001.e4.
46. Waggoner SN, Taniguchi RT, Mathew PA, Kumar V, Welsh RM., Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis. J Clin Invest 2010; 120: 1925-38.
47. Brown DR, Calpe S, Keszei M, Wang N, McArdel S, Terhorst C, et al., An NK cell-independent role for slamf4 in controlling humoral autoimmunity. J Immunol 2011; 187: 21-5.
48. Moulton VR, Tsokos GC., T cell signaling abnormalities contribute to aberrant immune cell function and autoimmunity. J Clin Invest 2015; 125: 2220-7.
49. Pacheco Y, McLean AP, Rohrbach J, Porichis F, Kaufmann DE, Kavanagh DG., Simultaneous TCR and CD244 signals induce dynamic downmodulation of CD244 on human antiviral T cells. J Immunol 2013; 191: 2072-81.
50. - T cells in health and disease. J Biol Chem 2013; 288: 31880-7.
51. Sandusky MM, Messmer B, Watzl C., Regulation of 2B4 (CD244)-mediated NK cell activation by ligand-induced receptor modulation. Eur J Immunol 2006; 36: 3268-76.
52. Mathew SO, Vaidya SV, Kim JR, Mathew PA., Human natural killer cell receptor 2B4 (CD244) down-regulates its own expression by reduced promoter activity at an Ets element. Biochem Biophys Res Commun 2007; 355: 483-7.