Inherited defects causing hemophagocytic lymphohistiocytic syndrome

Annals of the New York Academy of Sciences

Volumn 1246, Issue 1, 2011, Pages 64-76

  de Saint Basile, Geneviève ^a,b,c   Ménasché, Gaël ^a,b   Latour, Sylvain ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

Apoptosis; Cytotoxicity; Hemophagocytic; Immune regulation; Syndrome; interferon

Indexed keywords

GAMMA INTERFERON; GRANZYME; PERFORIN;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL INFILTRATION; CELL MEMBRANE; CELL POLARITY; CYTOKINE PRODUCTION; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; EXOCYTOSIS; HEMOPHAGOCYTIC LYMPHOHISTIOCYTOSIS; HEMOPHAGOCYTIC SYNDROME; HOMEOSTASIS; HUMAN; IMMUNOREGULATION; MACROPHAGE ACTIVATION; NONHUMAN; T LYMPHOCYTE ACTIVATION; TARGET CELL;

EID: 84855300076     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2011.06307.x     Document Type: Article

References (96)

1. Henter, J.I., G. Elinder & A. Ost. 1991. Diagnostic guidelines for hemophagocytic lymphohistiocytosis. The FHL Study Group of the Histiocyte Society. Semin. Oncol. 18: 29-33.
2. Henter, J.I., G. Elinder, O. Soder, et al. 1991. Hypercytokinemia in familial hemophagocytic lymphohistiocytosis. Blood 78: 2918-2922.
3. Billiau, A.D., T. Roskams, R. Van Damme-Lombaerts, et al. 2005. Macrophage activation syndrome: characteristic findings on liver biopsy illustrating the key role of activated, IFN-gamma-producing lymphocytes and IL-6- and TNF-alpha-producing macrophages. Blood 105: 1648-1651.
4. Henter, J.I., M. Arico, G. Elinder, et al. 1998. Familial hemophagocytic lymphohistiocytosis: primary hemophagocytic lymphohistiocytosis. Hematol. Oncol. Clin. N. Am. 12: 417-433.
5. Farquhar, J. & A. Claireaux. 1952. Familial haemophagocytic reticulosis. Arch. Dis. Child 27: 519-525.
6. Osugi, Y., J. Hara, S. Tagawa, et al. 1997. Cytokine production regulating Th1 and Th2 cytokines in hemophagocytic lymphohistiocytosis. Blood 89: 4100-4103.
7. Voskoboinik, I., M.J. Smyth & J.A. Trapani. 2006. Perforin-mediated target-cell death and immune homeostasis. Nat. Rev. Immunol. 6: 940-952.
8. Henter, J.I., G. Elinder, O. Soder & A. Ost. 1991. Incidence in Sweden and clinical features of familial hemophagocytic lymphohistiocytosis diagnostic guidelines for hemophagocytic lymphohistiocytosis. The FHL Study Group of the Histiocyte Society. Acta. Paediatr. Scand. 80: 428-435.
9. Bechara, E., F. Dijoud, G. de Saint Basile, et al. 2011. Hemophagocytic lymphohistiocytosis with Munc13-4 mutation: a cause of recurrent fatal hydrops fetalis. Pediatrics 128: e251-e254.
10. Lipton, J.M., S. Westra, C.E. Haverty, et al. 2004. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises: case 28-2004. Newborn twins with thrombocytopenia, coagulation defects, and hepatosplenomegaly. N. Engl. J. Med. 351: 1120-1130.
11. Chia, J., K.P. Yeo, J.C. Whisstock, et al. 2009. Temperature sensitivity of human perforin mutants unmasks subtotal loss of cytotoxicity, delayed FHL, and a predisposition to cancer. Proc. Natl. Acad. Sci. USA 106: 9809-9814.
12. Rohr, J., K. Beutel, A. Maul-Pavicic, et al. 2010. Atypical familial hemophagocytic lymphohistiocytosis due to mutations in UNC13D and STXBP2 overlaps with primary immunodeficiency diseases. Haematologica 95: 2080-2087.
13. Schneider, E.M., I. Lorenz, M. Muller-Rosenberger, et al. 2002. Hemophagocytic lymphohistiocytosis is associated with deficiencies of cellular cytolysis but normal expression of transcripts relevant to killer-cell-induced apoptosis. Blood 100: 2891-2898.
14. Stepp, S., R. Dufourcq-Lagelouse, F. Le Deist, et al. 1999. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science 286: 1957-1959.
15. Feldmann, J., F. Le Deist, M. Ouachee-Chardin, et al. 2002. Functional consequences of perforin gene mutations in 22 patients with familial haemophagocytic lymphohistiocytosis. Br. J. Haematol. 117: 965-972.
16. Voskoboinik, I., M.C. Thia, A. De Bono, et al. 2004. The functional basis for hemophagocytic lymphohistiocytosis in a patient with co-inherited missense mutations in the perforin (PFN1) gene. J. Exp. Med. 200: 811-816.
17. Feldmann, J., G. Menasche, I. Callebaut, et al. 2005. Severe and progressive encephalitis as a presenting manifestation of a novel missense perforin mutation and impaired cytolytic activity. Blood 105: 2658-2663.
18. Zur Stadt, U., K. Beutel, B. Weber, et al. 2004. A91V is a polymorphism in the perforin gene not causative of an FHLH phenotype. Blood 104: 1909; author reply 1910.
19. Trambas, C., F. Gallo, D. Pende, et al. 2005. A single amino acid change, A91V, leads to conformational changes that can impair processing to the active form of perforin. Blood 106: 932-937.
20. Santoro, A., S. Cannella, A. Trizzino, et al. 2005. A single amino acid change A91V in perforin: a novel, frequent predisposing factor to childhood acute lymphoblastic leukemia? Haematologica 90: 697-698.
21. Voskoboinik, I., V.R. Sutton, A. Ciccone, et al. 2007. Perforin activity and immune homeostasis: the common A91V polymorphism in perforin results in both presynaptic and postsynaptic defects in function. Blood 110: 1184-1190.
22. Feldmann, J., I. Callebaut, G. Raposo, et al. 2003. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115: 461-473.
23. Ueda, I., E. Ishii, A. Morimoto, et al. 2006. Correlation between phenotypic heterogeneity and gene mutational characteristics in familial hemophagocytic lymphohistiocytosis (FHL). Pediatr. Blood Can. 46: 482-488.
24. Marcenaro, S., F. Gallo, S. Martini, et al. 2006. Analysis of natural killer-cell function in familial hemophagocytic lymphohistiocytosis (FHL): defective CD107a surface expression heralds Munc13-4 defect and discriminates between genetic subtypes of the disease. Blood 108: 2316-2323.
25. Hong, W. 2005. Cytotoxic T lymphocyte exocytosis: bring on the SNAREs! Trends Cell Biol. 15: 644-650.
26. Brose, N., K. Hofmann, Y. Hata & T.C. Sudhof. 1995. Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J. Biol. Chem. 270: 25273-25280.
27. Brose, N., C. Rosenmund & J. Rettig. 2000. Regulation of transmitter release by Unc-13 and its homologues. Curr. Opin. Neurobiol. 10: 303-311.
28. zur Stadt, U., S. Schmidt, B. Kasper, et al. 2005. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type-4 to chromosome 6q24 and identification of mutations in syntaxin 11. Hum. Mol. Genet. 14: 827-834.
29. Prekeris, R., J. Klumperman & R.H. Scheller. 2000. Syntaxin 11 is an atypical SNARE abundant in the immune system. Eur. J. Cell. Biol. 79: 771-780.
30. Jahn, R. & R.H. Scheller. 2006. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell. Biol. 7: 631-643.
31. Zur Stadt, U., K. Beutel, S. Kolberg, et al. 2006. Mutation spectrum in children with primary hemophagocytic lymphohistiocytosis: molecular and functional analyses of PRF1, UNC13D, STX11, and RAB27A. Hum. Mutat. 27: 62-68.
32. Bryceson, Y.T., E. Rudd, C. Zheng, et al. 2007. Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood 110: 1906-1915.
33. Cote, M., M.M. Menager, A. Burgess, et al. 2009. Munc18-2 deficiency causes familial hemophagocytic lymphohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells. J. Clin. Invest. 119: 3765-3773.
34. Zhang, S., D. Ma, X. Wang, et al. 2008. Syntaxin-11 is expressed in primary human monocytes/macrophages and acts as a negative regulator of macrophage engulfment of apoptotic cells and IgG-opsonized target cells. Br. J. Haematol. 142: 469-479.
35. Arneson, L.N., A. Brickshawana, C.M. Segovis, et al. 2007. Cutting edge: syntaxin 11 regulates lymphocyte-mediated secretion and cytotoxicity. J. Immunol. 179: 3397-3401.
36. zur Stadt, U., J. Rohr, W. Seifert, et al. 2009. Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11. Am. J. Hum. Genet. 85: 482-492.
37. Toonen, R.F. & M. Verhage. 2003. Vesicle trafficking: pleasure and pain from SM genes. Trends Cell. Biol. 13: 177-186.
38. Sudhof, T.C. & J.E. Rothman. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-477.
39. Verhage, M., A.S. Maia, J.J. Plomp, et al. 2000. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287: 864-869.
40. Toonen, R.F. & M. Verhage. 2007. Munc18-1 in secretion: lonely Munc joins SNARE team and takes control. Trends Neurosci. 30: 564-572.
41. Ménasché, G., E. Pastural, J. Feldmann, et al. 2000. Mutations in RAB27A cause Griscelli syndrome associated with hemophagocytic syndrome. Nat. Genet. 25: 173-176.
42. Stinchcombe, J.C., D.C. Barral, E.H. Mules, et al. 2001. Rab27a is required for regulated secretion in cytotoxic t lymphocytes. J. Cell. Biol. 152: 825-834.
43. Menager, M.M., G. Menasche, M. Romao, et al. 2007. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8: 257-267.
44. Wu, X.S., K. Rao, H. Zhang, et al. 2002. Identification of an organelle receptor for myosin-Va. Nat. Cell. Biol. 4: 271-278.
45. Menasche, G., J. Feldmann, A. Fischer & G. de Saint Basile. 2005. Primary hemophagocytic syndromes point to a direct link between lymphocyte cytotoxicity and homeostasis. Immunol. Rev. 203: 165-179.
46. Stinchcombe, J., G. Bossi & G.M. Griffiths. 2004. Linking albinism and immunity: the secrets of secretory lysosomes. Science 305: 55-59.
47. Tardieu, M., C. Lacroix, B. Neven, et al. 2005. Progressive neurologic dysfunctions 20 years after allogeneic bone marrow transplantation for Chediak-Higashi syndrome. Blood 106: 40-42.
48. Nagle, D.L., A.M. Karim, E.A. Woolf, et al. 1996. Identification and mutation analysis of the complete gene for Chediak-Higashi syndrome. Nat. Genet. 14: 307-311.
49. Barbosa, M.D.F.S., Q.A. Nguyen, V.T. Tchernev, et al. 1996. Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 382: 262-265.
50. Gebauer, D., J. Li, G. Jogl, et al. 2004. Crystal structure of the PH-BEACH domains of human LRBA/BGL. Biochemistry 43: 14873-14880.
51. Jogl, G., Y. Shen, D. Gebauer, et al. 2002. Crystal structure of the BEACH domain reveals an unusual fold and extensive association with a novel PH domain. EMBO J. 21: 4785-4795.
52. Purtilo, D.T., C.K. Cassel, J.P. Yang & R. Harper. 1975. X-linked recessive progressive combined variable immunodeficiency (Duncan's disease). Lancet 1: 935-940.
53. Coffey, A.J., R.A. Brooksbank, O. Brandau, et al. 1998. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene [see comments]. Nat. Genet. 20: 129-135.
54. Nichols, K.E., D.P. Harkin, S. Levitz, et al. 1998. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl. Acad. Sci. USA 95: 13765-13770.
55. Sayos, J., C. Wu, M. Morra, et al. 1998. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395: 462-469.
56. Rigaud, S., M.C. Fondaneche, N. Lambert, et al. 2006. XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 444: 110-114.
57. Seemayer, T.A., T.G. Gross, R.M. Egeler, et al. 1995. X-linked lymphoproliferative disease: twenty-five years after the discovery. Pediatr. Res. 38: 471-478.
58. Gaspar, H.B., R. Sharifi, K.C. Gilmour & A.J. Thrasher. 2002. X-linked lymphoproliferative disease: clinical, diagnostic and molecular perspective. Br. J. Haematol. 119: 585-595.
59. Pachlopnik Schmid, J., D. Canioni, D. Moshous, 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.
60. Horn, P.C., B.H. Belohradsky, C. Urban, et al. 2011. Two new families with X-linked inhibitor of apoptosis deficiency and a review of all 26 published cases. J. Allergy. Clin. Immunol. 127: 544-546.
61. Marsh, R.A., L. Madden, B.J. Kitchen, 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 7: 1079-1082.
62. Schwartzberg, P.L., K.L. Mueller, H. Qi & J.L. Cannons. 2009. SLAM receptors and SAP influence lymphocyte interactions, development and function. Nat. Rev. Immunol. 9: 39-46.
63. Veillette, A., Z. Dong, L.A. Perez-Quintero, et al. 2009. Importance and mechanism of 'switch' function of SAP family adapters. Immunol. Rev. 232: 229-239.
64. Latour, S., G. Gish, C.D. Helgason, et al. 2001. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat. Immunol. 2: 681-690.
65. Dong, Z., M.E. Cruz-Munoz, M.C. Zhong, et al. 2009. Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat. Immunol. 10: 973-980.
66. Bottino, C., M. Falco, S. Parolini, et al. 2001. NTB-A [correction of GNTB-A], a novel SH2D1A-associated surface molecule contributing to the inability of natural killer cells to kill Epstein-Barr virus-infected B cells in X-linked lymphoproliferative disease. J. Exp. Med. 194: 235-246.
67. Parolini, S., C. Bottino, M. Falco, et al. 2000. X-linked lymphoproliferative disease. 2B4 molecules displaying inhibitory rather than activating function are responsible for the inability of natural killer cells to kill Epstein-Barr virus-infected cells. J. Exp. Med. 192: 337-346.
68. Dupre, L., G. Andolfi, S.G. Tangye, et al. 2005. SAP controls the cytolytic activity of CD8+ T cells against EBV-infected cells. Blood 105: 4383-4389.
69. Sharifi, R., J.C. Sinclair, K.C. Gilmour, et al. 2004. SAP mediates specific cytotoxic T-cell functions in X-linked lymphoproliferative disease. Blood 103: 3821-3827.
70. Hislop, A.D., U. Palendira, A.M. Leese, et al. 2010. Impaired Epstein-Barr virus-specific CD8+ T cell function in X-linked lymphoproliferative disease is restricted to SLAM family-positive B cell targets. Blood 116: 3249-3257.
71. Bloch-Queyrat, C., M.C. Fondaneche, R. Chen, et al. 2005. Regulation of natural cytotoxicity by the adaptor SAP and the Src-related kinase Fyn. J. Exp. Med. 202: 181-192.
72. Yin, L., U. Al-Alem, J. Liang, et al. 2003. Mice deficient in the X-linked lymphoproliferative disease gene sap exhibit increased susceptibility to murine gammaherpesvirus-68 and hypo-gammaglobulinemia. J. Med. Virol. 71: 446-455.
73. Snow, A.L., R.A. Marsh, S.M. Krummey, et al. 2009. Restimulation-induced apoptosis of T cells is impaired in patients with X-linked lymphoproliferative disease caused by SAP deficiency. J. Clin. Invest. 119: 2976-2989.
74. Pasquier, B., L. Yin, M.C. Fondaneche, et al. 2005. Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J. Exp. Med. 201: 695-701.
75. Nichols, K.E., J. Hom, S.Y. Gong, et al. 2005. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat. Med. 11: 340-345.
76. Latour, S. 2007. Natural killer T cells and X-linked lymphoproliferative syndrome. Curr. Opin. Allergy Clin. Immunol. 7: 510-514.
77. Bendelac, A., P.B. Savage & L. Teyton. 2007. The biology of NKT cells. Annu. Rev. Immunol. 25: 297-336.
78. Eckelman, B.P., G.S. Salvesen & F.L. Scott. 2006. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep. 7: 988-994.
79. Paulsen, M., S. Ussat, M. Jakob, et al. 2008. Interaction with XIAP prevents full caspase-3/-7 activation in proliferating human T lymphocytes. Eur. J. Immunol. 38: 1979-1987.
80. Dubrez-Daloz, L., A. Dupoux, & J. Cartier. 2008. IAPs: more than just inhibitors of apoptosis proteins. Cell Cycle 7: 1036-1046.
81. Krieg, A., R.G. Correa, J.B. Garrison, et al. 2009. XIAP mediates NOD signaling via interaction with RIP2. Proc. Natl. Acad. Sci. USA 106: 14524-14529.
82. Harlin, H., S.B. Reffey, C.S. Duckett, et al. 2001. Characterization of XIAP-deficient mice. Mol. Cell. Biol. 21: 3604-3608.
83. Olayioye, M.A., H. Kaufmann, M. Pakusch, et al. 2005. XIAP-deficiency leads to delayed lobuloalveolar development in the mammary gland. Cell Death Differ. 12: 87-90.
84. Badovinac, V.P., S.E. Hamilton & J.T. Harty. 2003. Viral infection results in massive CD8+ T cell expansion and mortality in vaccinated perforin-deficient mice. Immunity 18: 463-474.
85. Jordan, M.B., D. Hildeman, J. Kappler & P. Marrack. 2004. An animal model of hemophagocytic lymphohistiocytosis (HLH): CD8+ T cells and interferon gamma are essential for the disorder. Blood 104: 735-743.
86. Crozat, K., K. Hoebe, S. Ugolini, 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.
87. Pachlopnik Schmid, J., C.H. Ho, J. Diana, et al. 2008. A Griscelli syndrome type 2 murine model of hemophagocytic lymphohistiocytosis (HLH). Eur. J. Immunol. 38: 3219-3225.
88. Mazodier, K., V. Marin, D. Novick, et al. 2005. Severe imbalance of IL-18/IL-18BP in patients with secondary hemophagocytic syndrome. Blood 106: 3483-3489.
89. Smyth, M.J., K.Y. Thia, S.E. Street, et al. 2000. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J. Exp. Med. 192: 755-760.
90. Bolitho, P., S.E. Street, J.A. Westwood, et al. 2009. Perforin-mediated suppression of B-cell lymphoma. Proc. Natl. Acad. Sci. USA 106: 2723-2728.
91. Cannella, S., A. Santoro, G. Bruno, et al. 2007. Germline mutations of the perforin gene are a frequent occurrence in childhood anaplastic large cell lymphoma. Cancer 109: 2566-2571.
92. Mehta, P.A., S.M. Davies, A. Kumar, et al. 2006. Perforin polymorphism A91V and susceptibility to B-precursor childhood acute lymphoblastic leukemia: a report from the Children's Oncology Group. Leukemia 20: 1539-1541.
93. Clementi, R., F. Locatelli, L. Dupre, et al. 2005. A proportion of patients with lymphoma may harbor mutations of the perforin gene. Blood 105: 4424-4428.
94. Pachlopnik Schmid, J., C.H. Ho, F. Chrétien, et al. 2009. Neutralization of IFNγ defeats hemophagocytosis in LCMV-infected perforin- and Rab27a-deficient mice. EMBO Mol. Med. 1: 112-124.
95. Henter, J.I., A. Horne, M. Arico, et al. 2007. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr. Blood Can. 48: 124-131.
96. Mahlaoui, N., M. Ouachee-Chardin, G. de Saint Basile, et al. 2007. Immunotherapy of familial hemophagocytic lymphohistiocytosis with antithymocyte globulins: a single-center retrospective report of 38 patients. Pediatrics 120: e622-e628.