IL-2 induces a WAVE2-dependent pathway for actin reorganization that enables WASp-independent human NK cell function

Journal of Clinical Investigation

Volumn 121, Issue 4, 2011, Pages 1535-1548

  Orange, Jordan S ^a,b   Roy Ghanta, Sumita ^a   Mace, Emily M ^a   Maru, Saumya ^a   Rak, Gregory D ^a   Sanborn, Keri B ^a   Fasth, Anders ^c   Saltzman, Rushani ^a   Paisley, Allison ^a   Monaco Shawver, Linda ^a   Banerjee, Pinaki P ^a   Pandey, Rahul ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; F ACTIN; INTERLEUKIN 2; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN FAMILY VERPROLIN HOMOLOGOUS 2;

ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; NATURAL KILLER CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE; WISKOTT ALDRICH SYNDROME;

ACTINS; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; INTERLEUKIN-2; KILLER CELLS, NATURAL; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME; WISKOTT-ALDRICH SYNDROME PROTEIN; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 79953331939     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI44862     Document Type: Article

References (44)

1. Nolz JC, et al. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr Biol. 2006;16(1):24-34. (Pubitemid 43049883)
2. Nolz JC, et al. The WAVE2 complex regulates T cell receptor signaling to integrins via Abl- and CrkL-C3G-mediated activation of Rap1. J Cell Biol. 2008;182(6):1231-1244.
3. Zhang J, et al. Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J Exp Med. 1999;190(9):1329-1342.
4. Cannon JL, Burkhardt JK. Differential roles for Wiskott-Aldrich syndrome protein in immune synapse formation and IL-2 production. J Immunol. 2004;173(3):1658-1662. (Pubitemid 38971596)
5. Kenney D, Cairns L, Remold-O'Donnell E, Peterson J, Rosen FS, Parkman R. Morphological abnormalities in the lymphocytes of patients with the Wiskott-Aldrich syndrome. Blood. 1986;68(6):1329-1332. (Pubitemid 17228811)
6. Trifari S, et al. Defective Th1 cytokine gene transcription in CD4+ and CD8+ T cells from Wiskott-Aldrich syndrome patients. J Immunol. 2006;177(10):7451-7461. (Pubitemid 44715116)
7. Molina IJ, Sancho J, Terhorst C, Rosen FS, Remold-O'Donnell E. T cells of patients with the Wiskott-Aldrich syndrome have a restricted defect in proliferative responses. J Immunol. 1993;151(8):4383-4390. (Pubitemid 23298772)
8. Strom TS, Gabbard W, Kelly PF, Cunningham JM, Nienhuis AW. Functional correction of T cells derived from patients with the Wiskott-Aldrich syndrome (WAS) by transduction with an oncoretroviral vector encoding the WAS protein. Gene Ther. 2003;10(9):803-809. (Pubitemid 36621825)
9. Lopez-Botet M, Fontan G, Garcia Rodriguez MC, de Landazuri MO. Relationship between IL 2 synthesis and the proliferative response to PHA in different primary immunodeficiencies. J Immunol. 1982;128(2):679-683. (Pubitemid 12168422)
10. Sullivan KE, Mullen CA, Blaese RM, Winkelstein JA. A multiinstitutional survey of the Wiskott-Aldrich syndrome. J Pediatr. 1994;125(6 pt 1):876-885. (Pubitemid 24379120)
11. Orange JS. Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect. 2002;4(15):1545-1558. (Pubitemid 36050824)
12. Kuijpers TW, Baars PA, Dantin C, van den Burg M, van Lier RA, Roosnek E. Human NK cells can control CMV infection in the absence of T cells. Blood. 2008;112(3):914-915.
13. Waldhauer I, Steinle A. NK cells and cancer immunosurveillance. Oncogene. 2008;27(45):5932-5943.
14. Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol. 2008;8(9):713-725.
15. Orange JS, Harris KE, Andzelm MM, Valter MM, Geha RS, Strominger JL. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc Natl Acad Sci U S A. 2003;100(24):14151-14156. (Pubitemid 37499206)
16. Orange JS, et al. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc Natl Acad Sci U S A. 2002;99(17):11351-11356. (Pubitemid 34920929)
17. Gismondi A, et al. Impaired natural and CD16- mediated NK cell cytotoxicity in patients with WAS and XLT: ability of IL-2 to correct NK cell functional defect. Blood. 2004;104(2):436-443. (Pubitemid 38900026)
18. Albert MH, et al. X-linked thrombocytopenia (XLT) due to WAS mutations: clinical characteristics, long-term outcome, and treatment options. Blood. 2010;115(16):3231-3238.
19. De Meester J, Calvez R, Valitutti S, Dupre L. The Wiskott-Aldrich syndrome protein regulates CTL cytotoxicity and is required for efficient killing of B cell lymphoma targets. J Leukoc Biol. 2010;88(5):1031-1040.
20. Yodoi J, et al. TCGF (IL 2)-receptor inducing factor(s). I. Regulation of IL 2 receptor on a natural killer-like cell line (YT cells). J Immunol. 1985;134(3):1623-1630.
21. Gong JH, Maki G, Klingemann HG. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia. 1994;8(4):652-658. (Pubitemid 24133034)
22. Lutskiy MI, Rosen FS, Remold-O'Donnell E. Genotype-proteotype linkage in the Wiskott-Aldrich syndrome. J Immunol. 2005;175(2):1329-1336. (Pubitemid 41095023)
23. Banerjee PP, Orange JS. Quantitative measurement of F-actin accumulation at the NK cell immunological synapse. J Immunol Methods. 2010;355(1-2):1-13.
24. Peterson JR, et al. Chemical inhibition of N-WASP by stabilization of a native autoinhibited conformation. Nat Struct Mol Biol. 2004;11(8):747-755. (Pubitemid 39014500)
25. Gross ER, Hsu AK, Gross GJ. The JAK/STAT pathway is essential for opioid-induced cardioprotection: JAK2 as a mediator of STAT3, Akt, and GSK-3 beta. Am J Physiol Heart Circ Physiol. 2006;291(2):H827-H834. (Pubitemid 44175091)
26. Piscitelli SC, Wells MJ, Metcalf JA, Baseler M, Stevens R, Davey RT Jr. Pharmacokinetics and pharmacodynamics of subcutaneous interleukin-2 in HIV-infected patients. Pharmacotherapy. 1996;16(5):754-759. (Pubitemid 26322179)
27. Baume DM, Robertson MJ, Levine H, Manley TJ, Schow PW, Ritz J. Differential responses to interleukin 2 define functionally distinct subsets of human natural killer cells. Eur J Immunol. 1992;22(1):1-6.
28. Lebensohn AM, Kirschner MW. Activation of the WAVE complex by coincident signals controls actin assembly. Mol Cell. 2009;36(3):512-524.
29. Danson CM, Pocha SM, Bloomberg GB, Cory GO. Phosphorylation of WAVE2 by MAP kinases regulates persistent cell migration and polarity. J Cell Sci. 2007;120(pt 23):4144-4154.
30. Nolz JC, et al. WAVE2 regulates high-affinity integrin binding by recruiting vinculin and talin to the immunological synapse. Mol Cell Biol. 2007;27(17):5986-6000. (Pubitemid 47326689)
31. Huang Y, Comiskey EO, Dupree RS, Li S, Koleske AJ, Burkhardt JK. The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood. 2008;112(1):111-119.
32. Gallego MD, Santamaria M, Pena J, Molina IJ. Defective actin reorganization and polymerization of Wiskott-Aldrich T cells in response to CD3-mediated stimulation. Blood. 1997;90(8):3089-3097. (Pubitemid 27444203)
33. Cianferoni A, et al. Defective nuclear translocation of nuclear factor of activated T cells and extracellular signal-regulated kinase underlies deficient IL-2 gene expression in Wiskott-Aldrich syndrome. J Allergy Clin Immunol. 2005;116(6):1364-1371. (Pubitemid 41740950)
34. Azuma H, Sakata H, Saijyou M, Okuno A. Effect of interleukin 2 on intractable herpes virus infection and chronic eczematoid dermatitis in a patient with Wiskott-Aldrich syndrome. Eur J Pediatr. 1993;152(12):998-1000. (Pubitemid 23361975)
35. Starr SE, et al. Phase I/II trial of intravenous recombinant interleukin-2 in HIV-infected children. Aids. 2003;17(15):2181-2189. (Pubitemid 37345162)
36. Azuma H, et al. Impaired interleukin-2 production in T-cells from a patient with Wiskott-Aldrich syndrome: basis of clinical effect of interleukin-2 replacement therapy. Eur J Pediatr. 2000;159(8):633-634. (Pubitemid 30469458)
37. Banerjee PP, Pandey R, Zheng R, Suhoski MM, Monaco-Shawver L, Orange JS. Cdc42-interacting protein-4 functionally links actin and microtubule networks at the cytolytic NK cell immunological synapse. J Exp Med. 2007;204(10):2305-2320. (Pubitemid 47529318)
38. Sanborn KB, et al. Myosin IIA associates with NK cell lytic granules to enable their interaction with F-actin and function at the immunological synapse. J Immunol. 2009;182(11):6969-6984.
39. Carrizosa E, et al. Hematopoietic lineage cell-specific protein 1 is recruited to the immunological synapse by IL-2-inducible T cell kinase and regulates phospholipase Cgamma1 Microcluster dynamics during T cell spreading. J Immunol. 2009;183(11):7352-7361.
40. Svitkina T. Electron microscopic analysis of the leading edge in migrating cells. Methods Cell Biol. 2007;79:295-319.
41. Zhu Q, et al. Wiskott-Aldrich syndrome/X-linked thrombocytopenia: WASP gene mutations, protein expression, and phenotype. Blood. 1997;90(7):2680-2689. (Pubitemid 27413478)
42. Caligiuri MA, et al. Selective modulation of human natural killer cells in vivo after prolonged infusion of low dose recombinant interleukin 2. J Clin Invest. 1993;91(1):123-132. (Pubitemid 23037263)
43. Hornef MW, Wagner HJ, Kruse A, Kirchner H. Cytokine production in a whole-blood assay after Epstein-Barr virus infection in vivo. Clin Diagn Lab Immunol. 1995;2(2):209-213.
44. Wright-Browne V, et al. Serum cytokine levels in infectious mononucleosis at diagnosis and convalescence. Leuk Lymphoma. 1998;30(5-6):583-589. (Pubitemid 28393692)