Severe impairment of IFN-γ and IFN-α responses in cells of a patient with a novel STAT1 splicing mutation

Blood

Volumn 118, Issue 7, 2011, Pages 1806-1817

  Vairo, Donatella ^a   Tassone, Laura ^a   Tabellini, Giovanna ^b   Tamassia, Nicola ^c   Gasperini, Sara ^c   Bazzoni, Flavia ^c   Plebani, Alessandro ^a   Porta, Fulvio ^d   Notarangelo, Luigi D ^e   Parolini, Silvia ^b   Giliani, Silvia ^a   Badolato, Raffaele ^a  

^a Laboratory of Genetic Disorders of Childhood   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

^d SPEDALI CIVILI   (Italy)

^e BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIMYCOBACTERIAL AGENT; CD56 ANTIGEN; CHEMOKINE RECEPTOR CXCR1; CYSTEINE; FUNGUS ANTIGEN; GAMMA INTERFERON; GANCICLOVIR; GLYCINE; ISOPROTEIN; MESSENGER RNA; SIGNAL TRANSDUCER AND ACTIVATOR OF TRANSCRIPTION ALPHA ISOFORM; SIGNAL TRANSDUCER AND ACTIVATOR OF TRANSCRIPTION BETA ISOFORM; STAT1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS FUMIGATUS; ATYPICAL MYCOBACTERIOSIS; BONE MARROW TRANSPLANTATION; CASE REPORT; CHILD; CONTROLLED STUDY; CYTOLYSIS; CYTOMEGALOVIRUS INFECTION; DISEASE SEVERITY; DNA BINDING; EXON SKIPPING; GENE EXPRESSION; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTERFERON PRODUCTION; INTERSTITIAL PNEUMONIA; LUNG INFECTION; MALE; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RESPIRATORY DISTRESS; RESPIRATORY FAILURE; SIGNAL TRANSDUCTION; SPLICING DEFECT; T LYMPHOCYTE; VIRAL SKIN DISEASE; WILD TYPE;

EID: 80051876588     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-01-330571     Document Type: Article

References (38)

1. van de Vosse, van Dissel JT, Ottenhoff TH. Genetic deficiencies of innate immune signalling in human infectious disease. Lancet Infect Dis. 2009;9(11):688-698.
2. Al Muhsen S., Casanova J.L. The genetic heterogeneity of mendelian susceptibility to mycobacterial diseases. J Allergy Clin Immunol. 2008;122(6):1043-1051.
3. Dupuis S., Jouanguy E., Al Hajjar S., et al. Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat Genet. 2003;33(3):388-391. (Pubitemid 36278855)
4. Chapgier A.,Wynn R.F., Jouanguy E., et al. Human complete Stat-1 deficiency is associated with defective type I and II IFN responses in vitro but immunity to some low virulence viruses in vivo. J Immunol. 2006;176(8):5078- 5083.
5. Averbuch D., Chapgier A., Boisson-Dupuis S., Casanova J.L., Engelhard D. The clinical spectrum of patients with deficiency of Signal Transducer and Activator of Transcription-1. Pediatr Infect Dis J. 2011;30(4):352-355.
6. Jankowski M., Kopinski P., Goc A. Interleukin-27: Biological properties and clinical application. Arch Immunol Ther Exp (Warsz). 2010;58(6):417-425.
7. Strengell M., Matikainen S., Siren J., et al. IL-21 in synergy with IL-15 or IL-18 enhances IFN-gamma production in human NK and T cells. J Immunol. 2003;170(11):5464-5469. (Pubitemid 36617833)
8. Zhang C., Zhang J., Niu J., Zhang J., Tian Z. Interleukin-15 improves cytotoxicity of natural killer cells via up-regulating NKG2D and cytotoxic effector molecule expression as well as STAT1 and ERK1/2 phosphorylation. Cytokine. 2008;42(1):128-136.
9. Platanias L.C. Mechanisms of type-I- and type- II-interferon-mediated signalling. Nat Rev Immunol. 2005;5(5):375-386. (Pubitemid 40685987)
10. Banninger G., Reich N.C. STAT2 nuclear trafficking. J Biol Chem. 2004;279(38):39199-39206. (Pubitemid 39258180)
11. Mao X., Ren Z., Parker G.N., et al. Structural bases of unphosphorylated STAT1 association and receptor binding. Mol Cell. 2005;17(6):761-771. (Pubitemid 40386938)
12. Zhong M., Henriksen M.A., Takeuchi K., et al. Implications of an antiparallel dimeric structure of non-phosphorylated STAT1 for the activation-inactivation cycle. Proc Natl Acad Sci U S A. 2005; 102(11):3966-3971. (Pubitemid 40388539)
13. Dupuis S., Dargemont C., Fieschi C., et al. Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation. Science. 2001;293(5528):300-303. (Pubitemid 32694746)
14. Chapgier A., Kong X.F., Boisson-Dupuis S., et al. A partial form of recessive STAT1 deficiency in humans. J Clin Invest. 2009;119(6):1502-1514.
15. Chapgier A., Boisson-Dupuis S., Jouanguy E., et al. Novel STAT1 alleles in otherwise healthy patients with mycobacterial disease. PLoS Genet. 2006;2(8):e131.
16. Kong X.F., Ciancanelli M., Al Hajjar S., et al. A novel form of human STAT1 deficiency impairing early but not late responses to interferons. Blood. 2010;116(26):5895-5906.
17. Kristensen I.A., Veirum J.E., Moller B.K., Christiansen M. Novel STAT1 alleles in a patient with impaired resistance to Mycobacteria. J Clin Immunol. 2011;31(2):265-271.
18. Parolini S., Bottino C., Falco M., et al. 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. 2000;192(3):337-346. (Pubitemid 30629159)
19. Moretta A., Vitale M., Bottino C., et al. P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells: Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J Exp Med. 1993;178(2):597-604. (Pubitemid 23218208)
20. Gulino A.V., Moratto D., Sozzani S., et al. Altered leukocyte response to CXCL12 in patients with warts hypogammaglobulinemia, infections, myelokathexis (WHIM) syndrome. Blood. 2004;104(2):444-452. (Pubitemid 38900027)
21. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983;11(5):1475-1489.
22. McDonald P.P., Bald A., Cassatella M.A. Activation of the NF-kappaB pathway by inflammatory stimuli in human neutrophils. Blood. 1997;89(9):3421-3433.
23. Holzinger D., Jorns C., Stertz S., et al. Induction of MxA gene expression by influenza A virus requires type I or type III interferon signaling. J Virol. 2007;81(14):7776-7785. (Pubitemid 47047864)
24. Carlin J.M., Borden E.C., Sondel P.M., Byrne G.I. Interferon-induced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. J Leukoc Biol. 1989;45(1):29-34. (Pubitemid 19043368)
25. Costa P., Sivori S., Bozzano F., et al. IFN-alphamediated increase in cytolytic activity of maturing NK cell upon exposure to HSV-infected myelomonocytes. Eur J Immunol. 2009;39(1):147-158.
26. Nguyen K.B., Salazar-Mather T.P., Dalod M.Y., et al. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol. 2002;169(8):4279-4287. (Pubitemid 35178200)
27. Moretta A., Marcenaro E., Parolini S., Ferlazzo G., Moretta L. NK cells at the interface between innate and adaptive immunity. Cell Death Differ. 2008;15(2):226-233.
28. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P., Salazar-Mather T.P. Natural killer cells in antiviral defense: Function and regulation by innate cytokines. Annu Rev Immunol. 1999;17:189-220. (Pubitemid 29241123)
29. Biassoni R., Cantoni C., Pende D., et al. Human natural killer cell receptors and co-receptors. Immunol Rev. 2001;181:203-214. (Pubitemid 32703408)
30. Miyagi T., Gil M.P., Wang X., Louten J., Chu W.M., Biron C.A. High basal STAT4 balanced by STAT1 induction to control type 1 interferon effects in natural killer cells. J Exp Med. 2007;204(10):2383-2396. (Pubitemid 47529324)
31. Miyagi T., Lee S.H., Biron C.A. Intracellular staining for analysis of the expression and phosphorylation of signal transducers and activators of transcription (STATs) in NK cells. Methods Mol Biol. 2010;612:159-175.
32. Vinkemeier U., Moarefi I., Darnell J.E. Jr, Kuriyan J. Structure of the amino-terminal protein interaction domain of STAT-4. Science. 1998;279(5353):1048-1052. (Pubitemid 28113309)
33. Strehlow I., Schindler C. Amino-terminal signal transducer and activator of transcription (STAT) domains regulate nuclear translocation and STAT deactivation. J Biol Chem. 1998;273(43):28049-28056. (Pubitemid 28496098)
34. Xu X., Sun Y.L., Hoey T. Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain. Science. 1996; 273(5276):794-797. (Pubitemid 26271524)
35. Zhang J.J., Vinkemeier U., Gu W., Chakravarti D., Horvath C.M., Darnell J.E. Jr. Two contact regions between Stat1 and CBP/p300 in interferon gamma signaling. Proc Natl Acad Sci U S A. 1996;93(26):15092-15096. (Pubitemid 127606373)
36. Vinkemeier U., Cohen S.L., Moarefi I., Chait B.T., Kuriyan J., Darnell J.E. Jr. DNA binding of in vitro activated Stat1 alpha, Stat1 beta and truncated Stat1: Interaction between NH2-terminal domains stabilizes binding of two dimers to tandem DNA sites. EMBO J. 1996;15(20):5616-5626. (Pubitemid 26385621)
37. Mertens C., Zhong M., Krishnaraj R., Zou W., Chen X., Darnell J.E. Jr. Dephosphorylation of phosphotyrosine on STAT1 dimers requires extensive spatial reorientation of the monomers facilitated by the N-terminal domain. Genes Dev. 2006;20(24):3372-3381. (Pubitemid 44969156)
38. Wenta N., Strauss H., Meyer S., Vinkemeier U. Tyrosine phosphorylation regulates the partitioning of STAT1 between different dimer conformations. Proc Natl Acad Sci U S A. 2008;105(27):9238-9243.