Loss-of-function mutations within the IL-2 inducible kinase ITK in patients with EBV-associated lymphoproliferative diseases

Leukemia

Volumn 26, Issue 5, 2012, Pages 963-971

  Linka, R M ^a   Risse, S L ^b   Bienemann, K ^a   Werner, M ^c   Linka, Y ^a   Krux, F ^a   Synaeve, C ^d,e   Deenen, R ^a   Ginzel, S ^a   Dvorsky, R ^b   Gombert, M ^a   Halenius, A ^a   Hartig, R ^f   Helminen, M ^g   Fischer, A ^d,e   Stepensky, P ^h   Vettenranta, K ^g   Kohrer K ^a   Ahmadian, M R ^b   Laws, H J ^a   Fleckenstein, B ⁱ   Jumaa, H ^c   Latour, S ^d,e   Schraven, B ^f   Borkhardt, A ^a   more..

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b Department of Orthopedic Surgery   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f OTTO VON GUERICKE UNIVERSITY   (Germany)

^g TAMPERE UNIVERSITY HOSPITAL   (Finland)

^h HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

ⁱ UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

EBV; ITK; Kinase; loss of function; lymphoma; primary immunodeficiency

Indexed keywords

BRUTON TYROSINE KINASE; INTERLEUKIN 2 INDUCIBLE T CELL KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PLECKSTRIN; PROTEIN KINASE; UNCLASSIFIED DRUG;

ADOLESCENT; ARTICLE; CALCIUM TRANSPORT; CHILD; CLINICAL ARTICLE; EPSTEIN BARR VIRUS INFECTION; FEMALE; GENE MUTATION; HEPATOSPLENOMEGALY; HUMAN; INDEL MUTATION; LYMPHADENOPATHY; LYMPHOPROLIFERATIVE DISEASE; MALE; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN METABOLISM; SCHOOL CHILD; T LYMPHOCYTE;

EID: 84860772152     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.371     Document Type: Article

References (49)

1. Tanaka N, Asao H, Ohtani K, Nakamura M, Sugamura K. A novel human tyrosine kinase gene inducible in T cells by interleukin 2. FEBS Lett 1993; 324: 1-5.
2. Siliciano JD, Morrow TA, Desiderio SV. Itk, a T-cell-specific tyrosine kinase gene inducible by interleukin 2. Proc Natl Acad Sci USA 1992; 89: 11194-11198.
3. Gibson S, Leung B, Squire JA, Hill M, Arima N, Goss P et al. Identification, cloning, and characterization of a novel human T-cell-specific tyrosine kinase located at the hematopoietin complex on chromosome 5q. Blood 1993; 82: 1561-1572.
4. Greenman C, Stephens P, Smith R, Dalgliesh GL, Hunter C, Bignell G et al. Patterns of somatic mutation in human cancer genomes. Nature 2007; 446: 153-158.
5. Väliaho J, Smith CIE, Vihinen M. Btkbase: the mutation database for X-linked agammaglobulinemia. Hum Mutat 2006; 27: 1209-1217.
6. Lindvall JM, Blomberg KEM, Väliaho J, Vargas L, Heinonen JE, Berglöf A et al. Bruton's tyrosine kinase: cell biology, sequence conservation, mutation spectrum, siRNA modifications, and expression profiling. Immunol Rev 2005; 203: 200-215.
7. Huck K, Feyen O, Niehues T, Rüschendorf F, Hü bner N, Laws H et al. Girls homozygous for an Il-2-inducible T cell kinase mutation that leads to protein deficiency develop fatal EBV-associated lymphoproliferation. J Clin Invest 2009; 119: 1350-1358.
8. Sahu N, Venegas AM, Jankovic D, Mitzner W, Gomez-Rodriguez J, Cannons JL et al. Selective expression rather than specific function of Txk and Itk regulate Th1 and Th2 responses. J Immunol 2008; 181: 6125-6131.
9. Hu J, Sahu N, Walsh E, August A. Memory phenotype CD8+ T cells with innate function selectively develop in the absence of active Itk. Eur J Immunol 2007; 37: 2892-2899.
10. Au-Yeung BB, Katzman SD, Fowell DJ. Cutting edge: Itk-dependent signals required for CD4+ T cells to exert, but not gain, Th2 effector function. J Immunol 2006; 176: 3895-3899.
11. Andreotti AH, Schwartzberg PL, Joseph RE, Berg LJ. T-cell signaling regulated by the Tec family kinase, Itk. Cold Spring Harb Perspect Biol 2010; 2: a002287.
12. Schaeffer EM, Yap GS, Lewis CM, Czar MJ, McVicar DW, Cheever AW et al. Mutation of Tec family kinases alters T helper cell differentiation. Nat Immunol 2001; 2: 1183-1188.
13. Schaeffer EM, Debnath J, Yap G, McVicar D, Liao XC, Littman DR et al. Requirement for Tec kinases Rlk and Itk in T cell receptor signaling and immunity. Science 1999; 284: 638-641.
14. Edgar R, Domrachev M, Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002; 30: 207-210.
15. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989; 77: 51-59.
16. Mielke C, Tümmler M, Schü beler D, von Hoegen I, Hauser H. Stabilized, long-term expression of heterodimeric proteins from tricistronic mRNA. Gene 2000; 254: 1-8.
17. Linka RM, Porter ACG, Volkov A, Mielke C, Boege F, Christensen MO. C-terminal regions of topoisomerase IIalpha and IIbeta determine isoform-specific functioning of the enzymes in vivo. Nucleic Acids Res 2007; 35: 3810-3822.
18. Hu C, Chinenov Y, Kerppola TK. Visualization of interactions among bZip and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 2002; 9: 789-798.
19. Waibler Z, Sender LY, Merten C, Hartig R, Kliche S, Gunzer M et al. Signaling signatures and functional properties of anti-human CD28 superagonistic antibodies. PLoS ONE 2008; 3: e1708.
20. Liao XC, Littman DR. Altered T cell receptor signaling and disrupted T cell development in mice lacking Itk. Immunity 1995; 3: 757-769.
21. Stepensky P, Weintraub M, Yanir A, Revel-Vilk S, Krux F, Huck K et al. Il-2-inducible T-cell kinase deficiency: clinical presentation and therapeutic approach. Haematologica 2011; 96: 472-476.
22. Biesinger B, Mü ller-Fleckenstein I, Simmer B, Lang G, Wittmann S, Platzer E et al. Stable growth transformation of human T lymphocytes by Herpesvirus saimiri. Proc Natl Acad Sci USA 1992; 89: 3116-3119.
23. Blomberg KEM, Boucheron N, Lindvall JM, Yu L, Raberger J, Berglöf A et al. Transcriptional signatures of Itk-deficient CD3+, CD4+ and CD8+ T-cells. BMC Genomics 2009; 10: 233.
24. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 2010; 38 (Database issue): D355-D360.
25. Liu KQ, Bunnell SC, Gurniak CB, Berg LJ. T cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itk-deficient T cells. J Exp Med 1998; 187: 1721-1727.
26. Nagy E, Maquat LE. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci 1998; 23: 198-199.
27. Readinger JA, Mueller KL, Venegas AM, Horai R, Schwartzberg PL. Tec kinases regulate T-lymphocyte development and function: new insights into the roles of Itk and Rlk/Txk. Immunol Rev 2009; 228: 93-114.
28. Lemmon MA, Ferguson KM. Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 2000; 350 (Part 1): 1-18.
29. Baraldi E, Djinovic Carugo K, Hyvönen M, Surdo PL, Riley AM, Potter BV et al. Structure of the PH domain from Bruton's tyrosine kinase in complex with inositol 1,3,4,5-tetrakisphosphate. Structure 1999; 7: 449-460.
30. Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 2008; 9: 99-111.
31. Woods ML, Kivens WJ, Adelsman MA, Qiu Y, August A, Shimizu Y. A novel function for the Tec family tyrosine kinase Itk in activation of beta 1 integrins by the T-cell receptor. EMBO J 2001; 20: 1232-1244.
32. Qi Q, Sahu N, August A. Tec kinase Itk forms membrane clusters specifically in the vicinity of recruiting receptors. J Biol Chem 2006; 281: 38529-38534.
33. Raberger J, Schebesta A, Sakaguchi S, Boucheron N, Blomberg KEM, Berglöf A et al. The transcriptional regulator Plzf induces the development of CD44 high memory phenotype T cells. Proc Natl Acad Sci USA 2008; 105: 17919-17924.
34. Hu J, August A. Naive and innate memory phenotype CD4+ T cells have different requirements for active Itk for their development. J Immunol 2008; 180: 6544-6552.
35. Horai R, Mueller KL, Handon RA, Cannons JL, Anderson SM, Kirby MR et al. Requirements for selection of conventional and innate T lymphocyte lineages. Immunity 2007; 27: 775-785.
36. Berg LJ, Finkelstein LD, Lucas JA, Schwartzberg PL. Tec family kinases in T lymphocyte development and function. Annu Rev Immunol 2005; 23: 549-600.
37. Pachlopnik Schmid J, Canioni D, Moshous D, Touzot F, Mahlaoui N, Hauck F et al. 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 2011; 117: 1522-1529.
38. Latour S, Gish G, Helgason CD, Humphries RK, Pawson T, Veillette A. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat Immunol 2001; 2: 681-690.
39. Mohaamed AJ, Yu L, Bäckesjö C, Vargas L, Faryal R, Aints A et al. Bruton's tyrosine kinase (Btk): function, regulation, and transformation with special emphasis on the PH domain. Immunol Rev 2009; 228: 58-73.
40. Brown K, Long JM, Vial SCM, Dedi N, Dunster NJ, Renwick SB et al. Crystal structures of interleukin-2 tyrosine kinase and their implications for the design of selective inhibitors. J Biol Chem 2004; 279: 18727-18732.
41. Heyeck SD, Wilcox HM, Bunnell SC, Berg LJ. Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J Biol Chem 1997; 272: 25401-25408.
42. Cho N, Feng P, Lee S, Lee B, Liang X, Chang H et al. Inhibition of T cell receptor signal transduction by tyrosine kinase-interacting protein of Herpesvirus saimiri. J Exp Med 2004; 200: 681-687.
43. Pearson H. Surviving a knockout blow. Nature 2002; 415: 8-9.
44. Rameh LE, Arvidsson AK, Carraway KL, Couvillon AD, Rathbun G, Crompton A et al. A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J Biol Chem 1997; 272: 22059-22066.
45. Huang YH, Grasis JA, Miller AT, Xu R, Soonthornvacharin S, Andreotti AH et al. Positive regulation of Itk PH domain function by soluble Ip4. Science 2007; 316: 886-889.
46. Qi Q, August A. The Tec family kinase Itk exists as a folded monomer in vivo. J Biol Chem 2009; 284: 29882-29892.
47. Nomura K, Kanegane H, Karasuyama H, Tsukada S, Agematsu K, Murakami G et al. Genetic defect in human x-linked agammaglobulinemia impedes a maturational evolution of pro-B cells into a later stage of pre-B cells in the B-cell differentiation pathway. Blood 2000; 96: 610-617.
48. Bienemann K, Iouannidou K, Schoenberg K, Krux F, Reuther S, Feyen O et al. INKT cell frequency in peripheral blood of caucasian children and adolescent: the absolute iNKT cell count is stable from birth to adulthood. Scand J Immunol 2011; 74: 406-411.
49. Shearer WT, Rosenblatt HM, Gelman RS, Oyomopito R, Plaeger S, Stiehm ER et al. Lymphocyte subsets in healthy children from birth through 18 years of age: the pediatric aids clinical trials group p1009 study. J Allergy Clin Immunol 2003; 112: 973-980.