An N-terminal missense mutation in STX11 causative of FHL4 abrogates syntaxin-11 binding to Munc18-2

Frontiers in Immunology

Volumn 4, Issue JAN, 2014, Pages

  Müller, Martha Lena ^a   Chiang, Samuel C C ^a   Meeths, Marie ^a   Tesi, Bianca ^a   Entesarian, Miriam ^a   Nilsson, Daniel ^a,b   Wood, Stephanie M ^a   Nordenskjöld, Magnus ^a   Henter, Jan Inge ^a   Naqvi, Ahmed ^c   Bryceson, Yenan T ^a,d  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

Familial hemophagocytic lymphohistiocytosis; Munc18 2; N peptide; Syntaxin 11

Indexed keywords

MUNC18 PROTEIN; SHIGA TOXIN; SYNTAXIN;

ARTICLE; BIOCHEMICAL ANALYSIS; CHILD; CONTROLLED STUDY; DEGRANULATION; FLOW CYTOMETRY; GENE EXPRESSION; GENE MUTATION; HEMOPHAGOCYTIC SYNDROME; HUMAN; HUMAN CELL; INFANT; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYLOGENETIC TREE; PLASMID; PRESCHOOL CHILD; PROTEIN BINDING; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS;

EID: 84987800370     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00515     Document Type: Article

References (27)

1. Henter JI, Horne A, Arico M, Egeler RM, Filipovich AH, Imashuku S, et al. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer (2007) 48:124-31. doi: 10.1002/pbc.21039
2. Filipovich AH. The expanding spectrum of hemophagocytic lymphohistiocytosis. Curr Opin Allergy Clin Immunol (2011) 11:512-6. doi:10.1097/ACI.0b013e32834c22f5
3. Janka GE. Familial and acquired hemophagocytic lymphohistiocytosis. Annu Rev Med (2012) 63:233-46. doi:10.1146/annurev-med-041610-134208
4. Henter JI, Elinder G, Soder O, Ost A. Incidence in Sweden and clinical features of familial hemophagocytic lymphohistiocytosis. Acta Paediatr Scand (1991) 80:428-35. doi:10.1111/j.1651-2227.1991.tb11878.x
5. Janka GE. Familial and acquired hemophagocytic lymphohistiocytosis. Eur J Pediatr (2007) 166:95-109. doi:10.1007/s00431-006-0258-1
6. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, Bhawan S, Certain S, Mathew PA, et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science (1999) 286:1957-9. doi:10.1126/science.286.5446.1957
7. Feldmann J, Callebaut I, Raposo G, Certain S, Bacq D, Dumont C, et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell (2003) 115:461-73. doi:10.1016/S0092-8674(03)00855-9
8. Zur Stadt U, Schmidt S, Kasper B, Beutel K, Diler AS, Henter JI, et al. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type-4 to chromosome 6q24 and identification of mutations in syntaxin 11. Hum Mol Genet (2005) 14:827-34. doi:10.1093/hmg/ddi076
9. Cote M, Menager MM, Burgess A, Mahlaoui N, Picard C, Schaffner C, et al. Munc18-2 deficiency causes familial hemophagocytic lymphohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells. J Clin Invest (2009) 119:3765-73. doi:10.1172/JCI40732
10. Zur Stadt U, Rohr J, Seifert W, Koch F, Grieve S, Pagel J, et al. Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11. Am J Hum Genet (2009) 85:482-92. doi:10.1016/j.ajhg.2009.09.005
11. de Saint Basile G, Menasche G, Fischer A. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat Rev Immunol (2010) 10:568-79. doi:10.1038/nri2803
12. Kogl T, Muller J, Jessen B, Schmitt-Graeff A, Janka G, Ehl S, et al. Hemophagocytic lymphohistiocytosis in syntaxin-11-deficient mice: T-cell exhaustion limits fatal disease. Blood (2013) 121:604-13. doi:10.1182/blood-2012-07-441139
13. Sepulveda FE, Debeurme F, Menasche G, Kurowska M, Cote M, Pachlopnik Schmid J, et al. Distinct severity of HLH in both human and murine mutants with complete loss of cytotoxic effector PRF1, RAB27A, and STX11. Blood (2013) 121:595-603. doi:10.1182/blood-2012-07-440339
14. Bryceson YT, Rudd E, Zheng C, Edner J, Ma D, Wood SM, et al. Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood (2007) 110:1906-15. doi:10.1182/blood-2007-02-074468
15. Chiang SC, Theorell J, Entesarian M, Meeths M, Mastafa M, Al-Herz W, et al. Comparison of primary human cytotoxic T-cell and natural killer cell responses reveal similar molecular requirements for lytic granule exocytosis but differences in cytokine production. Blood (2013) 121:1345-56. doi:10.1182/blood-2012-07-442558
16. Valdez AC, Cabaniols JP, Brown MJ, Roche PA. Syntaxin 11 is associated with SNAP-23 on late endosomes and the trans-Golgi network. J Cell Sci (1999) 112(Pt 6):845-54.
17. Offenhauser C, Lei N, Roy S, Collins BM, Stow JL, Murray RZ. Syntaxin 11 binds Vti1b and regulates late endosome to lysosome fusion in macrophages. Traffic (2011) 12:762-73. doi:10.1111/j.1600-0854.2011.01189.x
18. Marsh RA, Satake N, Biroschak J, Jacobs T, Johnson J, Jordan MB, et al. STX11 mutations and clinical phenotypes of familial hemophagocytic lymphohistiocytosis in North America. Pediatr Blood Cancer (2010) 55:134-40. doi:10.1002/pbc.22499
19. Bryceson YT, March ME, Ljunggren HG, Long EO. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood (2006) 107:159-66. doi:10.1182/blood-2005-04-1351
20. Fernandez I, Ubach J, Dulubova I, Zhang X, Sudhof TC, Rizo J. Three-dimensional structure of an evolutionarily conserved N-terminal domain of syntaxin 1A. Cell (1998) 94:841-9. doi:10.1016/S0092-8674(00)81742-0
21. Dulubova I, Khvotchev M, Liu S, Huryeva I, Sudhof TC, Rizo J. Munc18-1 binds directly to the neuronal SNARE complex. Proc Natl Acad Sci U S A (2007) 104:2697-702. doi:10.1073/pnas.0611318104
22. Rickman C, Medine CN, Bergmann A, Duncan RR. Functionally and spatially distinct modes of munc18-syntaxin 1 interaction. J Biol Chem (2007) 282:12097-103. doi:10.1074/jbc.M700227200
23. Bryceson YT, Pende D, Maul-Pavicic A, Gilmour KC, Ufheil H, Vraetz T, et al. A prospective evaluation of degranulation assays in the rapid diagnosis of familial hemophagocytic syndromes. Blood (2012) 119:2754-63. doi:10.1182/blood-2011-08-374199
24. Bin NR, Jung CH, Piggott C, Sugita S. Crucial role of the hydrophobic pocket region of Munc18 protein in mast cell degranulation. Proc Natl Acad Sci U S A (2013) 110:4610-5. doi:10.1073/pnas.1214887110
25. Hackmann Y, Graham SC, Ehl S, Honing S, Lehmberg K, Arico M, et al. Syntaxin binding mechanism and disease-causing mutations in Munc18-2. Proc Natl Acad Sci U S A (2013) 110:E4482-91. doi:10.1073/pnas.1313474110
26. Zhou P, Pang ZP, Yang X, Zhang Y, Rosenmund C, Bacaj T, et al. Syntaxin-1 N-peptide and Habc-domain perform distinct essential functions in synaptic vesicle fusion. EMBO J (2013) 32:159-71. doi:10.1038/emboj.2012.307
27. Boswell KL, James DJ, Esquibel JM, Bruinsma S, Shirakawa R, Horiuchi H, et al. Munc13-4 reconstitutes calcium-dependent SNARE-mediated membrane fusion. J Cell Biol (2012) 197:301-12. doi:10.1083/jcb.201109132