Disruption of HLA class II antigen presentation in Burkitt lymphoma: Implication of a 47 000 MW acid labile protein in CD4+ T-cell recognition

Immunology

Volumn 142, Issue 3, 2014, Pages 492-505

  God, Jason M ^a   Zhao, Dan ^a   Cameron, Christine A ^a   Amria, Shereen ^a   Bethard, Jennifer R ^b   Haque, Azizul ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Antigen presentation; Burkitt lymphoma; Enolase like molecules; HLA class II; Immune escape

Indexed keywords

ACID LABILE PROTEIN; ACID PROTEIN; ENOLASE; HLA ANTIGEN CLASS 2; PEPTIDE; UNCLASSIFIED DRUG;

ACIDITY; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; BURKITT LYMPHOMA; BURKITT LYMPHOMA CELL LINE; CD4+ T LYMPHOCYTE; COMPLEX FORMATION; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOMA CELL; MACROPHAGE; MOLECULAR WEIGHT; MOLECULE; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANTIGEN PRESENTATION; BURKITT LYMPHOMA; ENOLASE-LIKE MOLECULES; HLA CLASS II; IMMUNE ESCAPE;

BURKITT LYMPHOMA; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; HYDROGEN-ION CONCENTRATION; MOLECULAR WEIGHT; PHOSPHOPYRUVATE HYDRATASE;

EID: 84901992716     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12281     Document Type: Article

References (66)

1. Biko DM, Anupindi SA, Hernandez A, Kersun L, Bellah R. Childhood Burkitt lymphoma: abdominal and pelvic imaging findings. AJR Am J Roentgenol 2009; 192:1304-15.
2. Ott G, Rosenwald A, Campo E. Understanding MYC-driven aggressive B-cell lymphomas: pathogenesis and classification. Blood 2013; 122:3884-91.
3. Gromminger S, Mautner J, Bornkamm GW. Burkitt lymphoma: the role of Epstein-Barr virus revisited. Br J Haematol 2012; 156:719-29.
4. Brady G, Macarthur GJ, Farrell PJ. Epstein-Barr virus and Burkitt lymphoma. Postgrad Med J 2008; 84:372-7.
5. Perkins AS, Friedberg JW. Burkitt lymphoma in adults. Hematology Am Soc Hematol Educ Program 2008; 2008:341-8.
6. Molyneux EM, Rochford R, Griffin B et al. Burkitt's lymphoma. Lancet 2012; 379:1234-44.
7. Yustein JT, Dang CV. Biology and treatment of Burkitt's lymphoma. Curr Opin Hematol 2007; 14:375-81.
8. Magrath I. Epidemiology: clues to the pathogenesis of Burkitt lymphoma. Br J Haematol 2012; 156:744-56.
9. Bellan C, Stefano L, Giulia de F, Rogena EA, Lorenzo L. Burkitt lymphoma versus diffuse large B-cell lymphoma: a practical approach. Hematol Oncol 2009; 27:182-5.
10. Liu D, Shimonov J, Primanneni S, Lai Y, Ahmed T, Seiter K. t(8;14;18): a 3-way chromosome translocation in two patients with Burkitt's lymphoma/leukemia. Mol Cancer 2007; 6:35.
11. Gerbitz A, Mautner J, Geltinger C et al. Deregulation of the proto-oncogene c-myc through t(8;22) translocation in Burkitt's lymphoma. Oncogene 1999; 18:1745-53.
12. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-Myc target gene network. Semin Cancer Biol 2006; 16:253-64.
13. Slack GW, Gascoyne RD. MYC and aggressive B-cell lymphomas. Adv Anat Pathol 2011; 18:219-28.
14. Ambinder RF. Epstein-Barr virus and Hodgkin lymphoma. Hematology Am Soc Hematol Educ Program 2007; 2007:204-9.
15. Kawa K. Diagnosis and treatment of Epstein-Barr virus-associated natural killer cell lymphoproliferative disease. Int J Hematol 2003; 78:24-31.
16. Snow AL, Martinez OM. Epstein-Barr virus: evasive maneuvers in the development of PTLD. Am J Transplant 2007; 7:271-7.
17. Ohtsubo H, Arima N, Tei C. Epstein-Barr virus involvement in T-cell malignancy: significance in adult T-cell leukemia. Leuk Lymphoma 1999; 33:451-8.
18. Griskevicius L, Stulpinas R, Vengalyte I, Saulyte-Trakymiene S, Mickys U, Pranys D, Jurgutis M. Favorable outcome with chemo-immunotherapy in Burkitt lymphoma and leukemia. Leuk Res 2009; 33:587-8.
19. Hesseling P, Israels T, Harif M, Chantada G, Molyneux E. Pediatric Oncology in Developing C. Practical recommendations for the management of children with endemic Burkitt lymphoma (BL) in a resource limited setting. Pediatr Blood Cancer 2013; 60:357-62.
20. Sharipo A, Imreh M, Leonchiks A, Imreh S, Masucci MG. A minimal glycine-alanine repeat prevents the interaction of ubiquitinated I κB α with the proteasome: a new mechanism for selective inhibition of proteolysis. Nat Med 1998; 4:939-44.
21. Yin Y, Manoury B, Fahraeus R. Self-inhibition of synthesis and antigen presentation by Epstein-Barr virus-encoded EBNA1. Science 2003; 301:1371-4.
22. Frisan T, Zhang QJ, Levitskaya J, Coram M, Kurilla MG, Masucci MG. Defective presentation of MHC class I-restricted cytotoxic T-cell epitopes in Burkitt's lymphoma cells. Int J Cancer 1996; 68:251-8.
23. Khanolkar A, Badovinac VP, Harty JT. CD8 T cell memory development: CD4 T cell help is appreciated. Immunol Res 2007; 39:94-104.
24. Tel J, Sittig SP, Blom RA, Cruz LJ, Schreibelt G, Figdor CG, de Vries IJ. Targeting uptake receptors on human plasmacytoid dendritic cells triggers antigen cross-presentation and robust type I IFN secretion. J Immunol 2013; 191:5005-12.
25. + T cell to a fully functional tumor killer cell. Cancer Res 2002; 62:6438-41.
26. + T cells play a critical role in the generation of primary and memory antitumor immune responses elicited by SA-4-1BBL and TAA-based vaccines in mouse tumor models. PLoS ONE 2013; 8:e73145.
27. Masucci MG, Torsteindottir S, Colombani J, Brautbar C, Klein E, Klein G. Down-regulation of class I HLA antigens and of the Epstein-Barr virus-encoded latent membrane protein in Burkitt lymphoma lines. Proc Natl Acad Sci U S A 1987; 84:4567-71.
28. Gavioli R, De Campos-Lima PO, Kurilla MG, Kieff E, Klein G, Masucci MG. Recognition of the Epstein-Barr virus-encoded nuclear antigens EBNA-4 and EBNA-6 by HLA-A11-restricted cytotoxic T lymphocytes: implications for down-regulation of HLA-A11 in Burkitt lymphoma. Proc Natl Acad Sci U S A 1992; 89:5862-6.
29. Jilg W, Voltz R, Markert-Hahn C, Mairhofer H, Munz I, Wolf H. Expression of class I major histocompatibility complex antigens in Epstein-Barr virus-carrying lymphoblastoid cell lines and Burkitt lymphoma cells. Cancer Res 1991; 51:27-32.
30. Ressing ME, van Leeuwen D, Verreck FA et al. Epstein-Barr virus gp42 is posttranslationally modified to produce soluble gp42 that mediates HLA class II immune evasion. J Virol 2005; 79:841-52.
31. Ressing ME, van Leeuwen D, Verreck FA et al. Interference with T cell receptor-HLA-DR interactions by Epstein-Barr virus gp42 results in reduced T helper cell recognition. Proc Natl Acad Sci U S A 2003; 100:11583-8.
32. Staege MS, Lee SP, Frisan T et al. MYC overexpression imposes a nonimmunogenic phenotype on Epstein-Barr virus-infected B cells. Proc Natl Acad Sci U S A 2002; 99:4550-5.
33. + T cell recognition of human B-cell lymphoma by resveratrol. Leuk Lymphoma 2012; 53:305-14.
34. Kovats S, Whiteley PE, Concannon P, Rudensky AY, Blum JS. Presentation of abundant endogenous class II DR-restricted antigens by DM-negative B cell lines. Eur J Immunol 1997; 27:1014-21.
35. Kovats S, Nepom GT, Coleman M, Nepom B, Kwok WW, Blum JS. Deficient antigen-presenting cell function in multiple genetic complementation groups of type II bare lymphocyte syndrome. J Clin Invest 1995; 96:217-23.
36. Amria S, Hajiaghamohseni LM, Harbeson C, Zhao D, Goldstein O, Blum JS, Haque A. HLA-DM negatively regulates HLA-DR4-restricted collagen pathogenic peptide presentation and T cell recognition. Eur J Immunol 2008; 38:1961-70.
37. + T-cell recognition. Clin Dev Immunol 2011; 2011:780839.
38. Kovats S, Drover S, Marshall WH, Freed D, Whiteley PE, Nepom GT, Blum JS. Coordinate defects in human histocompatibility leukocyte antigen class II expression and antigen presentation in bare lymphocyte syndrome. J Exp Med 1994; 179:2017-22.
39. Haque MA, Hawes JW, Blum JS. Cysteinylation of MHC class II ligands: peptide endocytosis and reduction within APC influences T cell recognition. J Immunol 2001; 166:4543-51.
40. Hiraiwa A, Yamanaka K, Kwok WW, Mickelson EM, Masewicz S, Hansen JA, Radha SF, Nepom GT. Structural requirements for recognition of the HLA-Dw14 class II epitope: a key HLA determinant associated with rheumatoid arthritis. Proc Natl Acad Sci U S A 1990; 87:8051-5.
41. Haque A, Hajiaghamohseni LM, Li P, Toomy K, Blum JS. Invariant chain modulates HLA class II protein recycling and peptide presentation in nonprofessional antigen presenting cells. Cell Immunol 2007; 249:20-9.
42. Ma C, Whiteley PE, Cameron PM et al. Role of APC in the selection of immunodominant T cell epitopes. J Immunol 1999; 163:6413-23.
43. Pathak SS, Blum JS. Endocytic recycling is required for the presentation of an exogenous peptide via MHC class II molecules. Traffic 2000; 1:561-9.
44. Goldstein OG, Hajiaghamohseni LM, Amria S, Sundaram K, Reddy SV, Haque A. γ-IFN-inducible-lysosomal thiol reductase modulates acidic proteases and HLA class II antigen processing in melanoma. Cancer Immunol Immunother 2008; 57:1461-70.
45. Li P, Haque MA, Blum JS. Role of disulfide bonds in regulating antigen processing and epitope selection. J Immunol 2002; 169:2444-50.
46. Younger AR, Amria S, Jeffrey WA, Mahdy AE, Goldstein OG, Norris JS, Haque A. HLA class II antigen presentation by prostate cancer cells. Prostate Cancer Prostatic Dis 2008; 11:334-41.
47. Hill CM, Liu A, Marshall KW et al. Exploration of requirements for peptide binding to HLA DRB1*0101 and DRB1*0401. J Immunol 1994; 152:2890-8.
48. Haque MA, Li P, Jackson SK et al. Absence of γ-interferon-inducible lysosomal thiol reductase in melanomas disrupts T cell recognition of select immunodominant epitopes. J Exp Med 2002; 195:1267-77.
49. Amria S, Cameron C, Stuart R, Haque A. Defects in HLA class II antigen presentation in B-cell lymphomas. Leuk Lymphoma 2008; 49:353-5.
50. God JM, Haque A. Burkitt lymphoma: pathogenesis and immune evasion. J Oncol 2010; 2010:516047.
51. Khanna R, Burrows SR, Steigerwald-Mullen PM, Moss DJ, Kurilla MG, Cooper L. Targeting Epstein-Barr virus nuclear antigen 1 (EBNA1) through the class II pathway restores immune recognition by EBNA1-specific cytotoxic T lymphocytes: evidence for HLA-DM-independent processing. Int Immunol 1997; 9:1537-43.
52. + cytotoxic T-cell responses during chronic viral infection. J Virol 1994; 68:8056-63.
53. + T clones in a human model of B-cell non-Hodgkin follicular lymphoma. Br J Haematol 2006; 135:324-35.
54. Khalil H, Deshaies F, Bellemare-Pelletier A, Brunet A, Faubert A, Azar GA, Thibodeau J. Class II transactivator-induced expression of HLA-DOβ in HeLa cells. Tissue Antigens 2002; 60:372-82.
55. Lovitch SB, Petzold SJ, Unanue ER. Cutting edge: H-2DM is responsible for the large differences in presentation among peptides selected by I-Ak during antigen processing. J Immunol 2003; 171:2183-6.
56. Pouyez J, Mayard A, Vandamme AM, Roussel G, Perpete EA, Wouters J, Housen I, Michaux C. First crystal structure of an endo-inulinase, INU2, from Aspergillus ficuum: discovery of an extra-pocket in the catalytic domain responsible for its endo-activity. Biochimie 2012; 94:2423-30.
57. Anders AK, Call MJ, Schulze MS, Fowler KD, Schubert DA, Seth NP, Sundberg EJ, Wucherpfennig KW. HLA-DM captures partially empty HLA-DR molecules for catalyzed removal of peptide. Nat Immunol 2011; 12:54-61.
58. Feo S, Arcuri D, Piddini E, Passantino R, Giallongo A. ENO1 gene product binds to the c-myc promoter and acts as a transcriptional repressor: relationship with Myc promoter-binding protein 1 (MBP-1). FEBS Lett 2000; 473:47-52.
59. Subramanian A, Miller DM. Structural analysis of α-enolase. Mapping the functional domains involved in down-regulation of the c-myc protooncogene. J Biol Chem 2000; 275:5958-65.
60. Roozendaal C, Zhao MH, Horst G, Lockwood CM, Kleibeuker JH, Limburg PC, Nelis GF, Kallenberg CG. Catalase and α-enolase: two novel granulocyte autoantigens in inflammatory bowel disease (IBD). Clin Exp Immunol 1998; 112:10-6.
61. Vermeulen N, Arijs I, Joossens S et al. Anti-α-enolase antibodies in patients with inflammatory Bowel disease. Clin Chem 2008; 54:534-41.
62. Ballot E, Bruneel A, Labas V, Johanet C. Identification of rat targets of anti-soluble liver antigen autoantibodies by serologic proteome analysis. Clin Chem 2003; 49:634-43.
63. Bruschi M, Carnevali ML, Murtas C et al. Direct characterization of target podocyte antigens and auto-antibodies in human membranous glomerulonephritis: α-enolase and borderline antigens. J Proteomics 2011; 74:2008-17.
64. Aldoss IT, Weisenburger DD, Fu K, Chan WC, Vose JM, Bierman PJ, Bociek RG, Armitage JO. Adult Burkitt lymphoma: advances in diagnosis and treatment. Oncology (Williston Park) 2008; 22:1508-17.
65. Thomas DA, Faderl S, O'Brien S et al. Chemoimmunotherapy with hyper-CVAD plus rituximab for the treatment of adult Burkitt and Burkitt-type lymphoma or acute lymphoblastic leukemia. Cancer 2006; 106:1569-80.
66. Oriol A, Ribera JM, Bergua J et al. High-dose chemotherapy and immunotherapy in adult Burkitt lymphoma: comparison of results in human immunodeficiency virus-infected and noninfected patients. Cancer 2008; 113:117-25.