Elevated granzyme B in cytotoxic lymphocytes is a signature of immune activation in hemophagocytic lymphohistiocytosis

Frontiers in Immunology

Volumn 4, Issue MAR, 2013, Pages

  Mellor Heineke, Sabine ^a   Villanueva, Joyce ^a   Jordan, Michael B ^a,b   Marsh, Rebecca ^a,b   Zhang, Kejian ^a,b   Bleesing, Jack J ^a,b   Filipovich, Alexandra H ^a,b   Risma, Kimberly A ^a,b  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Clinical immunology; Granzyme B; Hemophagocytic lymphohistiocytosis; Natural killer cells

Indexed keywords

GRANZYME B; INTERLEUKIN 2 RECEPTOR;

ADOLESCENT; ARTICLE; CD8+ T LYMPHOCYTE; CHILD; CONTROLLED STUDY; CYTOTOXIC LYMPHOCYTE; DISEASE COURSE; FLOW CYTOMETRY; FOLLOW UP; GENE MUTATION; HEMOPHAGOCYTIC SYNDROME; HUMAN; INFANT; MACROPHAGE ACTIVATION; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; NEWBORN; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; SCHOOL CHILD;

EID: 84883781078     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00072     Document Type: Article

References (38)

1. Altimari, A., Gruppioni, E., Capizzi, E., Bagni, A., Corti, B., Fiorentino, M., et al. (2008). Blood monitoring of granzyme B and perforin expression after intestinal transplantation: considerations on clinical relevance. Transplantation 85, 1778-1783.
2. Bem, R. A., Bos, A. P., Bots, M., Wolbink, A. M., van Ham, S. M., Medema, J. P., et al. (2008). Activation of the granzyme pathway in children with severe respiratory syncytial virus infection. Pediatr. Res. 63, 650-655.
3. Bien, E., and Balcerska, A. (2008). Serum soluble interleukin 2 receptor alpha in human cancer of adults and children: a review. Biomarkers 13, 1-26.
4. Bleesing, J., Prada, A., Siegel, D. M., Villanueva, J., Olson, J., Ilowite, N. T., et al. (2007). The diagnostic significance of soluble CD163 and soluble interleukin-2 receptor alpha-chain in macrophage activation syndrome and untreated new-onset systemic juvenile idiopathic arthritis. Arthritis Rheum. 56, 965-971.
5. Boivin, W. A., Cooper, D. M., Hiebert, P. R., and Granville, D. J. (2009). Intracellular versus extracellular granzyme B in immunity and disease: challenging the dogma. Lab. Invest. 89, 1195-1220.
6. Buzza, M. S., and Bird, P. I. (2006). Extracellular granzymes: current perspectives. Biol. Chem. 387, 827-837.
7. Cannons, J. L., Tangye, S. G., and Schwartzberg, P. L. (2011). SLAM family receptors and SAP adaptors in immunity. Annu. Rev. Immunol. 29, 665-705.
8. Crozat, K., Hoebe, K., Ugolini, S., Hong, N. A., Janssen, E., Rutschmann, S., et al. (2007). Jinx, an MCMV susceptibility phenotype caused by disruption of Unc13d: a mouse model of type 3 familial hemophagocytic lymphohistiocytosis. J. Exp. Med. 204, 853-863.
9. de Saint Basile, G., Menasche, G., and Latour, S. (2011) Inherited defects causing hemophagocytic lymphohistiocytic syndrome. Ann. N. Y. Acad. Sci. 1246, 64-76.
10. Filipovich, A. H. (2009). Hemophagocytic lymphohistiocytosis (HLH) and related disorders. Hematology Am. Soc. Hematol. Educ. Program 2009, 127-131.
11. Goldbach-Mansky, R., Suson, S., Wesley, R., Hack, C. E., El-Gabalawy, H. S., and Tak, P. P. (2005). Raised granzyme B levels are associated with erosions in patients with early rheumatoid factor positive rheumatoid arthritis. Ann. Rheum. Dis. 64, 715-721.
12. Grom, A. A., Villanueva, J., Lee, S., Goldmuntz, E. A., Passo, M. H., and Filipovich, A. (2003). Natural killer cell dysfunction in patients with systemic-onset juvenile rheumatoid arthritis and macrophage activation syndrome. J. Pediatr. 142, 292-296.
13. Grossman, W. J., Verbsky, J. W., Tollefsen, B. L., Kemper, C., Atkinson, J. P., and Ley, T. J. (2004). Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 104, 2840-2848.
14. Imashuku, S., Hibi, S., Sako, M., Ishida, Y., Mugishima, H., Chen, J., et al. (1995). Soluble interleukin-2 receptor: a useful prognostic factor for patients with hemophagocytic lymphohistiocytosis. Blood 86, 4706-4707.
15. Johnson, T. S., Villanueva, J., Filipovich, A. H., Marsh, R. A., and Bleesing, J. J. (2011). Contemporary diagnostic methods for hemophagocytic lymphohistiocytic disorders. J. Immunol. Methods 364, 1-13.
16. Jordan, M. B., and Filipovich, A. H. (2008). Hematopoietic cell transplantation for hemophagocytic lymphohistiocytosis: a journey of a thousand miles begins with a single (big) step. Bone Marrow Transplant. 42, 433-437.
17. Jordan, M. B., Hildeman, D., Kappler, J., and Marrack, P. (2004). An animal model of hemophagocytic lymphohistiocytosis (HLH): CD8+ T cells and interferon gamma are essential for the disorder. Blood 104, 735-743.
18. Kim, T. D., Lee, S. U., Yun, S., Sun, H. N., Lee, S. H., Kim, J. W., et al. (2011). Human microRNA-27a* targets Prf1 and GzmB expression to regulate NK-cell cytotoxicity. Blood 118, 5476-5486.
19. Kogawa, K., Lee, S. M., Villanueva, J., Marmer, D., Sumegi, J., and Filipovich, A. H. (2002). Perforin expression in cytotoxic lymphocytes from patients with hemophagocytic lymphohistiocytosis and their family members. Blood 99, 61-66.
20. Komp, D. M., McNamara, J., and Buckley, P. (1989). Elevated soluble interleukin-2 receptor in childhood hemophagocytic histiocytic syndromes. Blood 73, 2128-2132.
21. Lieberman, J. (2010). Anatomy of a murder: how cytotoxic T cells and NK cells are activated, develop, and eliminate their targets. Immunol. Rev. 235, 5-9.
22. Lykens, J. E., Terrell, C. E., Zoller, E. E., Risma, K., and Jordan, M. B. (2011). Perforin is a critical physiologic regulator of T-cell activation. Blood 118, 618-626.
23. Marsh, R. A., and Filipovich, A. H. (2011). Familial hemophagocytic lymphohistiocytosis and X-linked lymphoproliferative disease. Ann. N. Y. Acad. Sci. 1238, 106-121.
24. Marsh, R. A., Madden, L., Kitchen, B. J., Mody, R., McClimon, B., Jordan, M. B., et al. (2010). XIAP deficiency: a unique primary immunodeficiency best classified as X-linked familial hemophagocytic lymphohistiocytosis and not as X-linked lymphoproliferative disease. Blood 116, 1079-1082.
25. Molleran Lee, S., Villanueva, J., Sumegi, J., Zhang, K., Kogawa, K., Davis, J., et al. (2004). Characterisation of diverse PRF1 mutations leading to decreased natural killer cell activity in North American families with haemophagocytic lymphohistiocytosis. J. Med. Genet. 41, 137-144.
26. Pachlopnik Schmid, J., Canioni, D., Moshous, D., Touzot, F., Mahlaoui, N., Hauck, F., et al. (2011). Clinical similarities and differences of patients with X-linked lymphoproliferative syndrome type 1 (XLP-1/SAP deficiency) versus type 2 (XLP-2/XIAP deficiency). Blood 117, 1522-1529.
27. Risma, K., and Jordan, M. B. (2012). Hemophagocytic lymphohistiocytosis: updates and evolving concepts. Curr. Opin. Pediatr. 24, 9-15.
28. Russell, J. H., and Ley, T. J. (2002). Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20, 323-370.
29. Salcedo, T. W., Azzoni, L., Wolf, S. F., and Perussia, B. (1993). Modulation of perforin and granzyme messenger RNA expression in human natural killer cells. J. Immunol. 151, 2511-2520.
30. Sedelies, K. A., Sayers, T. J., Edwards, K. M., Chen, W., Pellicci, D. G., Godfrey, D. I., et al. (2004). Discordant regulation of granzyme H and granzyme B expression in human lymphocytes. J. Biol. Chem. 279, 26581-26587.
31. Skak, K., Frederiksen, K. S., and Lundsgaard, D. (2008). Interleukin-21 activates human natural killer cells and modulates their surface receptor expression. Immunology 123, 575-583.
32. Spaeny-Dekking, E. H., Hanna, W. L., Wolbink, A. M., Wever, P. C., Kummer, J. A., Swaak, A. J., et al. (1998). Extracellular granzymes A and B in humans: detection of native species during CTL responses in vitro and in vivo. J. Immunol. 160, 3610-3616.
33. Tak, P. P., Spaeny-Dekking, L., Kraan, M. C., Breedveld, F. C., Froelich, C. J., and Hack, C. E. (1999). The levels of soluble granzyme A and B are elevated in plasma and synovial fluid of patients with rheumatoid arthritis (RA). Clin. Exp. Immunol. 116, 366-370.
34. Trotta, R., Ciarlariello, D., Dal Col, J., Mao, H., Chen, L., Briercheck, E., et al. (2011). The PP2A inhibitor SET regulates granzyme B expression in human natural killer cells. Blood 117, 2378-2384.
35. Trottestam, H., Horne, A., Arico, M., Egeler, R. M., Filipovich, A. H., Gadner, H., et al. (2011). Chemoimmunotherapy for hemophagocytic lymphohistiocytosis: long-term results of the HLH-94 treatment protocol. Blood 118, 4577-4584.
36. Truong, D. Q., Cornet, A., Wieers, G., Robert, A., Reding, R., and Latinne, D. (2008). Pre- and post-transplant monitoring of granzyme B enzyme-linked immunosorbent spot assay in pediatric liver recipients. Transpl. Immunol. 19, 215-219.
37. Voskoboinik, I., Smyth, M. J., and Trapani, J. A. (2006). Perforin-mediated target-cell death and immune homeostasis. Nat. Rev. Immunol. 6, 940-952.
38. Wang, P., Gu, Y., Zhang, Q., Han, Y., Hou, J., Lin, L., et al. (2012). Identification of resting and type I IFN-activated human NK cell miRNomes reveals microRNA-378 and microRNA-30e as negative regulators of NK cell cytotoxicity. J. Immunol. 189, 211-221.