Monoallelic mutations of the perforin gene may represent a predisposing factor to childhood anaplastic large cell lymphoma

Journal of Pediatric Hematology/Oncology

Volumn 36, Issue 6, 2014, Pages

  Ciambotti, Benedetta ^a,b   Mussolin, Lara ^c,d   D'Amore, Emanuele S G ^e   Pillon, Marta ^d   Sieni, Elena ^a   Coniglio, Maria L ^a,b   Ros, Martina D ^a,b   Cetica, Valentina ^a,b   Aricò, Maurizio ^a,b   Rosolen, Angelo ^a,f  

^a UNIVERSITY OF FLORENCE   (Italy)

^b ISTITUTO TOSCANO TUMORI   (Italy)

^c Istituto di Ricerca Pediatrico Fondazione Città della Speranza   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e SAN BORTOLO HOSPITAL   (Italy)

^f UNIVERSITY OF UDINE   (Italy)

Author keywords

anaplastic large cell lymphoma; monoallelic mutation; pediatric; PRF1; UNC13D

Indexed keywords

PERFORIN; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN;

ADOLESCENT; ARTICLE; CANCER CELL CULTURE; CHILD; CHILDHOOD CANCER; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC SCREENING; GERMLINE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFANT; LARGE CELL LYMPHOMA; MALE; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; PRF1 GENE; PRIORITY JOURNAL; SCHOOL CHILD; SH2D1A GENE; TUMOR GENE; UNC13D GENE;

ADOLESCENT; ADULT; ALLELES; ANIMALS; CERCOPITHECUS AETHIOPS; CHILD; COMPUTER SIMULATION; COS CELLS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GERM-LINE MUTATION; HUMANS; LYMPHOMA, LARGE-CELL, ANAPLASTIC; MALE; MEMBRANE PROTEINS; MUTATION, MISSENSE; PORE FORMING CYTOTOXIC PROTEINS; YOUNG ADULT;

EID: 84905113173     PISSN: 10774114     EISSN: 15363678     Source Type: Journal    
DOI: 10.1097/MPH.0000000000000073     Document Type: Article

References (55)

1. Stein H, Mason DY, Gerdes J, et al. The expression of the Hodgkin disease associated antigen Ki-1 in reactive and neoplastic lymphoid tissue: Evidence that Reed-Sternberg cells and histiocytic malignancies are derived from activated lymphoid cells. Blood. 1985;66:848-858.
2. Delsol G, Al Saati T, Gatter C, et al. Coexpression of epithelial membrane antigen (EMA), Ki-1 and interleukin-2 receptor by anaplastic large cell lymphomas: Diagnostic value in so-called malignant histiocytosis. Am J Pathol. 1988;130:59-70.
3. Egeler RM, Schmitz L, Sonneveld P, et al. Malignant histiocytosis: A reassessment of cases formerly classified as histiocytic neoplasms and review of the literature. Med Pediatr Oncol. 1995;25:1-7.
4. Stein H, Foss HD, Durkop H, et al. CD30(1) anaplastic large cell lymphoma: A review of its histopathologic, genetic, and clinical features. Blood. 2000;96:3681-3695.
5. Jaffe SE, Harris SNL, Stein H, et al. Pathology and genetics of tumours of haematopoietic and lymphoid tissues. World Health Organization Classification of Tumours. Lyon, France: IARC Press; 2001:352.
6. Rimokh R, Magaud JP, Berger F, et al. A translocation involving a specific breakpoint
7. Morris SW, Kirstein MN, Valentine MB, et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma [letter]. Science. 1994;263:1281-1284.
8. Wright D, McKeever P, Carter R. Childhood non-Hodgkin lymphomas in the United Kingdom: Findings from the UK Children's Cancer Study Group. J Clin Pathol. 1997;50: 128-134.
9. Gudgin E, Rashbass J, Pulford KJ, et al. Primary and isolated anaplastic large cell lymphoma of the bone marrow. Leuk Lymphoma. 2005;46:461-463.
10. Bhagwati NS, Oiseth SJ, Abebe LS, et al. Intravascular lymphoma associated with hemophagocytic syndrome: A rare but aggressive clinical entity. Ann Hematol. 2004;83:247-250.
11. Wong KF, Chan JK, Ng CS, et al. Anaplastic large cell Ki-1 lymphoma involving bone marrow: Marrow findings and association with reactive hemophagocytosis. Am J Hematol. 1991;37:112-119.
12. Invernizzi R, Paulli M, Rosso R, et al. Reactive hemophagocytosis in Ki-1 positive large cell lymphoma: A case study. Haematologica. 1989;74:155-159.
13. Burnet FM. The concept of immunological surveillance. Progr Exp Tumor Res. 1970;13:1-27.
14. Imai K, Matsuyama S, Miyake S, et al. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: An 11-year follow-up study of a general population. Lancet. 2000;356:1795-1799.
15. Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol. 2002; 2:735-747.
16. Lowin B, Peitsch MC, Tschopp J. Perforin and granzymes: Crucial effector molecules in cytolytic T lymphocyte and natural killer cell-mediated cytotoxicity. Curr Top Microbiol Immunol. 1995;198:1-24.
17. Trambas CM, Griffiths GM. Delivering the kiss of death. Nat Immunol. 2003;4:399-403.
18. Uellner R, Zvelebil MJ, Hopkins J, et al. Perforin is activated by a proteolytic cleavage during biosynthesis which reveals a phospholipid-binding C2 domain. EMBO J. 1997;16: 7287-7296.
19. Masson D, Peters PJ, Geuze HJ, et al. Interaction of chondroitin sulfate with perforin and granzymes of cytolytic T-cells is dependent on pH. Biochemistry. 1990;29: 11229-11235.
20. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science. 1999;286:1957-1959.
21. Arico M, Janka G, Fischer A, et al. Hemophagocytic lymphohistiocytosis. Report of 122 children from the International Registry. FHL Study Group of the Histiocyte Society. Leukemia. 1996;10:197-203.
22. Burnham JM, Kreiger PA, Paessler M, et al. Picture of the month: Anaplastic large cell lymphoma with hemophagocytic lymphohistiocytosis. Arch Pediatr Adolesc Med. 2006;160: 1177-1179.
23. Trizzino A, zur Stadt U, Ueda I, et al. Histiocyte Society HLH Study group. Genotype-phenotype study of familial haemophagocytic lymphohistiocytosis due to perforin mutations. J Med Genet. 2008;45:15-21.
24. Falini B, Pileri S, De Solas I, et al. Peripheral T-cell lymphoma associated with hemophagocytic syndrome. Blood. 1990; 75:434-444.
25. Arico M. Peripheral T-cell lymphoma associated with hemophagocytic syndrome and hemophagocytic lymphohistiocytosis of children: Do they share something?. Blood. 1990; 76:2163-2164.
26. Clementi R, Locatelli F, Dupre L, et al. A proportion of patients with lymphoma may harbor mutations of the perforin gene. Blood. 2005;105:4424-4428.
27. Clementi R, Chiocchetti A, Cappellano G, et al. Variations of the perforin gene in patients with autoimmunity/lymphoproliferation and defective Fas function. Blood. 2006;108: 3079-3084.
28. Cappellano G, Orilieri E, Comi C, et al. Variations of the perforin gene in patients with multiple sclerosis. Genes Immun. 2008;9:438-444.
29. Cannella S, Santoro A, Bruno G, et al. Germline mutations of the perforin gene are a frequent occurrence in childhood anaplastic large cell lymphoma. Cancer. 2007;109:2566-2571.
30. Feldmann J, Callebaut I, Raposo G, et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell. 2003;115:461-473.
31. Booth C, Gilmour KC, Veys P, et al. X-linked lymphoproliferative disease due to SAP/SH2D1A deficiency: A multicenter study on the manifestations, management and outcome of the disease. Blood. 2011;117:53-62.
32. Arico M, Imashuku S, Clementi R, et al. Hemophagocytic lymphohistiocytosis due to germline mutations in SH2D1A, the X-linked lymphoproliferative disease gene. Blood. 2001;97:1131-1133.
33. Le Deley MC, Rosolen A, Williams DM, et al. Brugieres Vinblastine in children and adolescents with high-risk anaplastic large-cell lymphoma: Results of the randomized ALCL99-vinblastine trial. J Clin Oncol. 2010;28:3987-3993.
34. Ferrer-Costa C, Gelpi JL, Zamakola L, et al. PMUT: A webbased tool for the annotation of pathological mutations on proteins. Bioinformatics. 2005;21:3176-3178.
35. Pulford K, Lamant L, Morris SW, et al. Detection of ALK and NPM-ALK proteins in normal and neoplastic cells with the monoclonal antibody ALK-1. Blood. 1997;89:1394-1404.
36. Santoro A, Cannella S, Bossi G, et al. Novel Munc13-4 mutations in children and young adult patients with haemophagocytic lymphohistiocytosis. J Med Genet. 2006;43: 953-960.
37. van Montfrans JM, Rudd E, van de Corput L, et al. Fatal hemophagocytic lymphohistiocytosis in X-linked chronic granulomatous disease associated with a perforin gene variant. Pediatr Blood Cancer. 2009;52:527-529.
38. Zhizhuo H, Junmei X, Yuelin S, et al. Screening the PRF1, UNC13D, STX11, SH2D1A, XIAP, and ITK gene mutations in Chinese children with Epstein-Barr virus-Associated hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer. 2012;58:410-414.
39. Ueda I, Kurokawa Y, Koike K, et al. Late-onset cases of familial hemophagocytic lymphohistiocytosis with missense perforin gene mutations. Am J Hematol. 2007;82:427-432.
40. zur Stadt U, Beutel K, Kolberg S, et al. Mutation spectrum in children with primary hemophagocytic lymphohistiocytosis: Molecular and functional analyses of PRF1, UNC13D, STX11, and RAB27A. Hum Mutat. 2006;27:62-68.
41. Chia J, Yeo KP, Whisstock JC, et al. Temperature sensitivity of human perforin mutants unmasks subtotal loss of cytotoxicity, delayed FHL, and a predisposition to cancer. Proc Natl Acad Sci USA. 2009;106:9809-9814.
42. Sieni E, Cetica V, Mastrodicasa E, et al. Familial hemophagocytic lymphohistiocytosis: A model for understanding the human machinery of cellular cytotoxicity. Cell Mol Life Sci. 2012;69:29-40.
43. Sieni E, Cetica V, Santoro A, et al. Genotype-phenotype study of familial haemophagocytic lymphohistiocytosis type 3.JMed Genet. 2011;48:343-352.
44. Cetica V, Pende D, Griffiths GM, et al. Molecular basis of familial hemophagocytic lymphohistiocytosis. Haematologica. 2010;95:538-541.
45. Cetica V, Santoro A, Gilmour KC, et al. STXBP2 mutations in children with familial haemophagocytic lymphohistiocytosis type 5. J Med Genet. 2010;47:595-600.
46. Trapani JA, Thia KY, Andrews M, et al. Human perforin mutations and susceptibility to multiple primary cancers. Oncoimmunology. 2013;2:e24185.
47. Voskoboinik I, Thia MC, Trapani JA. A functional analysis of the putative polymorphisms A91V and N252S, and 22 missense perforin mutations associated with hemophagocytic lymphohistiocytosis. Blood. 2005;105:4700-4706.
48. Trambas C, Gallo F, Pende D, et al. A single amino acid change, A91V, lead to conformational changes which can impair processing to the active form of perforin. Blood. 2005;106:932-937.
49. Yu CR, Ortaldo JR, Curiel RE, et al. Role of a STAT binding site in the regulation of the human perforin promoter. J Immunol. 1999;162:2785-2790.
50. Marzec M, Zhang Q, Goradia A, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci USA. 2008;105:20852-20857.
51. Rimsza LM, Roberts RA, Miller TP, et al. Loss of MHC class II gene and protein expression in diffuse large B-cell lymphoma is related to decreased tumor immunosurveillance and poor patient survival regardless of other prognostic factors: A follow-up study from the Leukemia and LymphomaMolecular Profiling Project. Blood. 2004;103:4251-4258.
52. Pulford K, Falini B, Banham AH, et al. Immune response to the ALK oncogenic tyrosine kinase in patients with anaplastic large-cell lymphoma. Blood. 2000;96:1605-1607.
53. Mussolin L, Bonvini P, Ait-Tahar K, et al. Kinetics of humoral response to ALK and its relationship with minimal residual disease in pediatric ALCL. Leukemia. 2009;23:400-402.
54. Ait-Tahar K, Barnardo MC, Pulford K, et al. CD4 T-helper responses to the anaplastic lymphoma kinase (ALK) protein in patients with ALK-positive anaplastic large-cell lymphoma. Cancer Res. 2007;67:1898-1901.
55. Ait-Tahar K, Cerundolo V, Banham AH, et al. B and CTL responses to the ALK protein in patients with ALKpositive ALCL. Int J Cancer. 2006;118:688-695.