Genetic predisposition to hemophagocytic lymphohistiocytosis: Report on 500 patients from the Italian registry

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 1, 2016, Pages 188-196.e4

  Cetica, Valentina ^a   Sieni, Elena ^a   Pende, Daniela ^b   Danesino, Cesare ^c   De Fusco, Carmen ^d   Locatelli, Franco ^c   Micalizzi, Concetta ^e   Putti, Maria Caterina ^f   Biondi, Andrea ^g   Fagioli, Franca ^h   Moretta, Lorenzo ^e   Griffiths, Gillian M ⁱ   Luzzatto, Lucio ^j   Aricò, Maurizio ^j,k  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d Ospedale Pausilipon   (Italy)

^e G GASLINI INSTITUTE   (Italy)

^f UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^g SAN GERARDO HOSPITAL   (Italy)

^h REGINA MARGHERITA CHILDREN S HOSPITAL   (Italy)

ⁱ ADDENBROOKE S HOSPITAL   (United Kingdom)

^j ISTITUTO TOSCANO TUMORI   (Italy)

^k Azienda sanitaria provinciale (ASP)   (Italy)

more..

Author keywords

Hemophagocytic lymphohistiocytosis; immunologic tests; PRF1; UNC13D

Indexed keywords

PERFORIN; MEMBRANE PROTEIN; PRF1 PROTEIN, HUMAN; UNC13D PROTEIN, HUMAN;

ADOLESCENT; ADULT; ARTICLE; CHILD; CYTOTOXICITY ASSAY; DEGRANULATION; ERYTHROPHAGOCYTOSIS; FEMALE; GENE; GENE FREQUENCY; GENE MUTATION; GENETIC DISORDER; GENETIC PREDISPOSITION; HEMOPHAGOCYTIC SYNDROME; HOMOZYGOTE; HUMAN; INFANT; ITALIAN (CITIZEN); MAJOR CLINICAL STUDY; MALE; NEWBORN; PRF1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGISTER; SURVIVAL; UNC13D GENE; GENETICS; IMMUNOLOGY; ITALY; MIDDLE AGED; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFANT; INFANT, NEWBORN; ITALY; LYMPHOHISTIOCYTOSIS, HEMOPHAGOCYTIC; MALE; MEMBRANE PROTEINS; MIDDLE AGED; PERFORIN; REGISTRIES; YOUNG ADULT;

EID: 84953635379     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.06.048     Document Type: Article

References (60)

1. R. Bodley-Scott, and A.H.T. Robb-Smith Histiocytic medullary reticulosis Lancet 234 6047 1939 194 198
2. J.W. Farquhar, and A.E. Claireaux Familial haemophagocytic reticulosis Arch Dis Child 27 1952 519 525
3. M. Arico, G. Janka, A. Fischer, J.I. Henter, S. Blanche, G. Elinder, and et al. Haemophagocytic lymphohistiocytosis: report of 122 children from the International Registry Leukemia 10 1996 197 203
4. G. Janka, and U. zur Stadt Familial and acquired hemophagocytic lymphohistiocytosis Hematology Am Soc Hematol Educ Program 2005 82 88
5. S.E. Stepp, R. Dufourcq-Lagelouse, F. Le Deist, S. Bhawan, S. Certain, P.A. Mathew, and et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis Science 286 1999 1957 1959
6. J. Feldmann, I. Callebaut, G. Raposo, S. Certain, D. Bacq, C. Dumont, and et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3) Cell 115 2003 461 473
7. U. Zur Stadt, S. Schmidt, B. Kasper, K. Beutel, A.S. Diler, J.I. Henter, and et al. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type 4 to chromosome 6q24 and identification of mutation in syntaxin 11 Hum Mol Genet 14 2005 827 834
8. U. zur Stadt, J. Rohr, W. Seifert, F. Koch, S. Grieve, J. Pagel, and 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 85 2009 482 492
9. M. Côte, M.M. Ménager, A. Burgess, N. Mahlaoui, C. Picard, C. Schaffner, and et al. Munc18-2 deficiency causes familial hemophagocytic lymphohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells J Clin Invest 119 2009 3765 3773
10. M. Arico, S. Imashuku, R. Clementi, S. Hibi, T. Teramura, C. Danesino, and et al. Hemophagocytic lymphohistiocytosis due to germline mutations in SH2D1A, the X-linked lymphoproliferative disease gene Blood 97 2001 1131 1133
11. C. Griscelli, A. Durandy, D. Guy-Grand, F. Daguillard, C. Herzog, and M. Prunieras A syndrome associating partial albinism and immunodeficiency Am J Med 65 1978 691 702
12. M.M. Chediak New leukocyte anomaly of constitutional and familial character Rev Hematol 7 1952 362 367
13. O. Higashi Congenital gigantism of peroxidase granules; the first case ever reported of qualitative abnormality of peroxidase Tohoku J Exp Med 59 1954 315 332
14. F. Hermansky, and P. Pudlak Albinism associated with hemorrhagic diathesis and unusual pigmented reticular cells in the bone marrow: report of two cases with histochemical studies Blood 14 1959 162 169
15. M. Aricò, C. Danesino, D. Pende, and L. Moretta Pathogenesis of haemophagocytic lymphohistiocytosis Br J Haematol 114 2001 761 769
16. A. Ravelli, A.A. Grom, E.M. Behrens, and R.Q. Cron Macrophage activation syndrome as part of systemic juvenile idiopathic arthritis: diagnosis, genetics, pathophysiology and treatment Genes Immun 13 2012 289 298
17. A. Basheer, S. Padhi, V. Boopathy, S. Mallick, S. Nair, R.G. Varghese, and et al. Hemophagocytic lymphohistiocytosis: an unusual complication of orientia tsutsugamushi disease (scrub typhus) Mediterr J Hematol Infect Dis 7 2015 e2015008
18. J.I. Henter, A. Samuelsson-Horne, M. Aricò, R.M. Egeler, G. Elinder, A.H. Filipovich, et al. Histocyte Society Treatment of hemophagocytic lymphohistiocytosis with HLH-94 immunochemotherapy and bone marrow transplantation Blood 100 2002 2367 2373
19. H. Trottestam, A. Horne, M. Aricò, R.M. Egeler, A.H. Filipovich, H. Gadner, et al. Histiocyte Society Chemoimmunotherapy for hemophagocytic lymphohistiocytosis: long-term results of the HLH-94 treatment protocol Blood 118 2011 4577 4584
20. A. Fischer, N. Cerf-Bensussan, S. Blanche, F. Le Deist, C. Bremard-Oury, G. Leverger, and et al. Allogeneic bone marrow transplantation for erythrophagocytic lymphohistiocytosis J Pediatr 108 1986 267 270
21. S. Cesaro, F. Locatelli, E. Lanino, F. Porta, L. Di Maio, C. Messina, and et al. Hematopoietic stem cell transplantation for hemophagocytic lymphohistiocytosis: a retrospective analysis of data from the Italian Association of Pediatric Hematology Oncology (AIEOP) Haematologica 93 2008 1694 1701
22. N. Cooper, K. Rao, K. Gilmour, L. Hadad, S. Adams, C. Cale, and et al. Stem cell transplantation with reduced-intensity conditioning for hemophagocytic lymphohistiocytosis Blood 107 2006 1233 1236
23. J.I. Henter, A. Horne, M. Aricò, R.M. Egeler, A.H. Filipovich, S. Imashuku, and et al. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis Pediatr Blood Cancer 48 2007 124 131
24. Y.T. Bryceson, D. Pende, A. Maul-Pavicic, K.C. Gilmour, H. Ufheil, T. Vraetz, and et al. A prospective evaluation of degranulation assays in the rapid diagnosis of familial hemophagocytic syndromes Blood 119 2012 2754 2763
25. K. Kogawa, S.M. Lee, J. Villanueva, D. Marmer, J. Sumegi, and A.H. Filipovich Perforin expression in cytotoxic lymphocytes from patients with hemophagocytic lymphohistiocytosis and their family members Blood 99 2002 61 66
26. S. Marcenaro, F. Gallo, S. Martini, A. Santoro, G.M. Griffiths, M. Aricò, and et al. 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 2006 2316 2323
27. R.A. Marsh, J.J. Bleesing, and A.H. Filipovich Using flow cytometry to screen patients for X-linked lymphoproliferative disease due to SAP deficiency and XIAP deficiency J Immunol Methods 362 2010 1 9
28. R. Meazza, C. Tuberosa, V. Cetica, M. Falco, F. Loiacono, S. Parolini, and et al. XLP1 inhibitory effect by 2B4 does not affect DNAM-1 and NKG2D activating pathways in NK cells Eur J Immunol 44 2014 1526 1534
29. R. Meazza, C. Tuberosa, V. Cetica, M. Falco, S. Parolini, S. Grieve, and et al. Diagnosing XLP1 in patients with hemophagocytic lymphohistiocytosis J Allergy Clin Immunol 134 2014 1381 1387.e7
30. C. Trambas, F. Gallo, D. Pende, S. Marcenaro, L. Moretta, C. De Fusco, and et al. A single amino acid change, A91V, leads to conformational changes that can impair processing to the active form of perforin Blood 106 2005 932 937
31. J.I. Henter, G. Elinder, O. Söder, and A. Ost Incidence in Sweden and clinical features of familial hemophagocytic lymphohistiocytosis Acta Paediatr Scand 80 1991 428 435
32. K. Zhang, M.B. Jordan, R.A. Marsh, J.A. Johnson, D. Kissell, J. Meller, and et al. Hypomorphic mutations in PRF1, MUNC13-4, and STXBP2 are associated with adult-onset familial HLH Blood 118 2011 5794 5798
33. E. Sieni, V. Cetica, A. Piccin, F. Gherlinzoni, F.C. Sasso, M. Rabusin, and et al. Familial hemophagocytic lymphohistiocytosis may present during adulthood: clinical and genetic features of a small series PLoS One 7 2012 e44649
34. M. Ramos-Casals, P. Brito-Zerón, A. López-Guillermo, M.A. Khamashta, and X. Bosch Adult haemophagocytic syndrome Lancet 383 2014 1503 1516
35. E. Sieni, V. Cetica, Y. Hackmann, M.L. Coniglio, M. Da Ros, B. Ciambotti, and et al. Familial hemophagocytic lymphohistiocytosis: when rare diseases shed light on immune system functioning Front Immunol 5 2014 167
36. Y. Hackmann, S.C. Graham, S. Ehl, S. Höning, K. Lehmberg, M. Aricò, and et al. Syntaxin binding mechanism and disease-causing mutations in Munc18-2 Proc Natl Acad Sci U S A 110 2013 E4482 E4491
37. J. Pachlopnik Schmid, M. Côte, M.M. Ménager, A. Burgess, N. Nehme, G. Ménasché, and et al. Inherited defects in lymphocyte cytotoxic activity Immunol Rev 235 2010 10 23
38. A. Trizzino, U. zur Stadt, I. Ueda, K. Risma, G. Janka, E. Ishii, and et al. Genoptype-phenotype study of familial haemophagocytic lymphohistiocytosis due to perforin mutations J Med Genet 45 2008 15 21
39. I. Voskoboinik, M.C. Thia, and J.A. Trapani A functional analysis of the putative polymorphisms A91V and N252S and 22 missense perforin mutations associated with familial hemophagocytic lymphohistiocytosis Blood 105 2005 4700 4706
40. A. Santoro, S. Cannella, A. Trizzino, L. Lo Nigro, G. Corsello, and M. Aricò A single amino acid change A91V in perforin: a novel, frequent predisposing factor to childhood acute lymphoblastic leukemia? Haematologica 90 2005 697 698
41. U. Zur Stadt, K. Beutel, B. Weber, H. Kabisch, R. Schneppenheim, and G. Janka A91V is a polymorphism in the perforin gene not causative of an FHLH phenotype Blood 104 2004 1909
42. I. Voskoboinik, and J.A. Trapani Perforinopathy: a spectrum of human immune disease caused by defective perforin delivery or function Front Immunol 4 2013 441
43. A. Santoro, S. Cannella, G. Bossi, F. Gallo, A. Trizzino, D. Pende, and et al. Novel Munc13-4 mutations in children and young adult patients with haemophagocytic lymphohistiocytosis J Med Genet 43 2006 953 960
44. U. Zur Stadt, K. Beutel, S. Kolberg, R. Schneppenheim, H. Kabisch, G. Janka, and et al. Mutation spectrum in children with primary hemophagocytic lymphohistiocytosis: molecular and functional analyses of PRF1, UNC13D, STX11, and RAB27A Hum Mutat 27 2006 62 68
45. A. Santoro, S. Cannella, A. Trizzino, G. Bruno, C. De Fusco, L.D. Notarangelo, and et al. Mutations affecting mRNA splicing are the most common molecular defect in patients with familial hemophagocytic lymphohistiocytosis type 3 Haematologica 93 2008 1086 1090
46. E. Sieni, V. Cetica, A. Santoro, K. Beutel, E. Mastrodicasa, M. Meeths, and et al. Genotype-phenotype study of familial haemophagocytic lymphohistiocytosis type 3 J Med Genet 48 2011 343 352
47. F. Cichocki, H. Schlums, H. Li, V. Stache, T. Holmes, T.R. Lenvik, and et al. Transcriptional regulation of Munc13-4 expression in cytotoxic lymphocytes is disrupted by an intronic mutation associated with a primary immunodeficiency J Exp Med 211 2014 1079 1091
48. Y. Qian, J.A. Johnson, J.A. Connor, C.A. Valencia, N. Barasa, J. Schubert, and et al. The 253-kb inversion and deep intronic mutations in UNC13D are present in North American patients with familial hemophagocytic lymphohistiocytosis 3 Pediatr Blood Cancer 61 2014 1034 1040
49. K. Nagai, K. Yamamoto, H. Fujiwara, J. An, T. Ochi, K. Suemori, and et al. Subtypes of familial hemophagocytic lymphohistiocytosis in Japan based on genetic and functional analyses of cytotoxic T lymphocytes PLoS One 5 2010 e14173
50. J.Y. Seo, J.S. Song, K.O. Lee, H.H. Won, J.W. Kim, S.H. Kim, and et al. Founder effects in two predominant intronic mutations of UNC13D, c.118-308C>T and c.754-1G>C underlie the unusual predominance of type 3 familial hemophagocytic lymphohistiocytosis (FHL3) in Korea Ann Hematol 92 2013 357 364
51. K.M. Kaufman, B. Linghu, J.D. Szustakowski, A. Husami, F. Yang, K. Zhang, and et al. Whole exome sequencing reveals overlap between macrophage activation syndrome in systemic juvenile idiopathic arthritis and familial hemophagocytic lymphohistiocytosis Arthritis Rheumatol 66 2014 3486 3495
52. R. Strippoli, I. Caiello, and F. De Benedetti Reaching the threshold: a multilayer pathogenesis of macrophage activation syndrome J Rheumatol 40 2013 761 767
53. S. Canna, A.A. de Jesus, Z. Deng, S.R. Brooks, B. Marrero, Y. Liu, and et al. Macrophage activation syndrome-like illness due to an activating mutation in NLRC4 Arthritis Rheumatol 66 suppl 11 2014 S203
54. Y.T. Bryceson, D. Pende, A. Maul-Pavicic, K.C. Gilmour, H. Ufheil, T. Vraetz, and et al. A prospective evaluation of degranulation assays in the rapid diagnosis of familial hemophagocytic syndromes Blood 119 2012 2754 2763
55. K. Kogawa, S.M. Lee, J. Villanueva, D. Marmer, J. Sumegi, and A.H. Filipovich Perforin expression in cytotoxic lymphocytes from patients with hemophagocytic lymphohistiocytosis and their family members Blood 99 2002 61 66
56. S. Marcenaro, F. Gallo, S. Martini, A. Santoro, G.M. Griffiths, M. Aricó, and et al. 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 2006 2316 2323
57. R.A. Marsh, J.J. Bleesing, and A.H. Filipovich Using flow cytometry to screen patients for X-linked lymphoproliferative disease due to SAP deficiency and XIAP deficiency J Immunol Methods 362 2010 1 9
58. R. Meazza, C. Tuberosa, V. Cetica, M. Falco, F. Loiacono, S. Parolini, and et al. XLP1 inhibitory effect by 2B4 does not affect DNAM-1 and NKG2D activating pathways in NK cells Eur J Immunol 44 2014 1526 1534
59. R. Meazza, C. Tuberosa, V. Cetica, M. Falco, S. Parolini, S. Grieve, and et al. Diagnosing XLP1 in patients with hemophagocytic lymphohistiocytosis J Allergy Clin Immunol 134 2014 1381 1387.e7
60. J.I. Henter, A. Horne, M. Aricò, R.M. Egeler, A.H. Filipovich, S. Imashuku, and et al. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis Pediatr Blood Cancer 48 2007 124 131