Differential expression of SHIP1 in CD56bright and CD56 dim NK cells provides a molecular basis for distinct functional responses to monokine costimulation

Blood

Volumn 105, Issue 8, 2005, Pages 3011-3018

  Trotta, Rossana ^b   Parihar, Robin ^b   Yu, Jianhua ^b   Becknell, Brian ^b   Allard II, Jeffrey ^b   Wen, Jing ^b   Ding, Wei ^b   Mao, Hsiaoyin ^b   Tridandapani, Susheela ^b   Carson, William E ^b   Caligiuri, Michael A ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD56 ANTIGEN; GAMMA INTERFERON; MUTANT PROTEIN; PROTEIN SH2;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVE SITE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; MOLECULAR BIOLOGY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRAIN DIFFERENCE; WILD TYPE;

EID: 20144389496     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-10-4072     Document Type: Article

References (56)

1. Trinchieri G. Biology of natural killer cells. Adv Immunol. 1989;47:187-376.
2. Perussia B. The cytokine profile of resting and activated NK cells. Methods. 1996;9:370-378.
3. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22:633-640.
4. Cooper MA, Fehniger TA, Turner SC, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood. 2001;97:3146-3151.
5. Lanier LL, Le AM, Civin CI, Loken MR, Phillips JH. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol. 1986;136:4480-4486.
6. Lieberman LA, Hunter CA. Regulatory pathways involved in the infection-induced production of IFN-gamma by NK cells. Microbes Infect. 2002;4:1531-1538.
7. Kaplan DH, Shankaran V, Dighe AS, et al. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci U S A. 1998;95:7556-7561.
8. Shankaran V, Ikeda H, Bruce AT, et al. IFN-gamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410:1107-1111.
9. Fehniger TA, Shah MH, Turner MJ, et al. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J Immunol. 1999;162:4511-4520.
10. Fehniger TA, Caligiuri MA. Interleukin 15: biology and relevance to human disease. Blood. 2001;97:14-32.
11. Akira S. The role of IL-18 in innate immunity. Curr Opin Immunol. 2000;12:59-63,
12. Pignata C, Prasad KV, Hallek M, et al. Phosphorylation of src family lck tyrosine kinase following interleukin-12 activation of human natural killer cells. Cell Immunol. 1995;165:211-216.
13. Adunyah SE, Wheeler BJ, Cooper RS. Evidence for the involvement of LCK and MAP kinase (ERK-1) in the signal transduction mechanism of interleukin-15. Biochem Biophys Res Commun. 1997;232:754-758.
14. Tsuji-Takayama K, Matsumoto S, Koide K, et al. Interleukin-18 induces activation and association of p56(lck) and MAPK in a murine TH1 clone. Biochem Biophys Res Commun. 1997;237:126-130.
15. Kalina U, Kauschat D, Koyama N, et al. IL-18 activates STAT3 in the natural killer cell line 92, augments cytotoxic activity, and mediates IFN-gamma production by the stress kinase p38 and by the extracellular regulated kinases p44erk-1 and p42erk-21. J Immunol. 2000;165:1307-1313.
16. Pignata C, Sanghera JS, Cossette L, Pelech SL, Ritz J. Interleukin-12 induces tyrosine phosphorylation and activation of 44-kD mitogen-activated protein kinase in human T cells. Blood. 1994;83:184-190.
17. Rane SG, Reddy EP. JAKs, STATs and Src kinases in hematopoiesis. Oncogene. 2002;21:3334-3358.
18. Yu CR, Young HA, Ortaldo JR. Characterization of cytokine differential induction of STAT complexes in primary human T and NK cells. J Leukoc Biol. 1998;64:245-258.
19. Kanakaraj P, Ngo K, Wu Y, et al. Defective interleukin (IL)-18-mediated natural killer and T helper cell type 1 responses in IL-1 receptor-associated kinase (IRAK)-deficient mice. J Exp Med. 1999;189:1129-1138.
20. Rohrschneider LR, Fuller JF, Wolf I, Liu Y, Lucas DM. Structure, function, and biology of SHIP proteins. Genes Dev. 2000;14:505-520.
21. Tridandapani S, Kelley T, Cooney D, Pradhan M, Coggeshall KM. Negative signaling in B cells: SHIP Grbs Shc. Immunol Today. 1997;18:424-427.
22. Ono M, Okada H, Bolland S, Yanagi S, Kurosaki T, Ravetch JV. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell. 1997;90:293-301.
23. Vely F, Olivero S, Olcese L, et al. Differential association of phosphatases with hematopoietic co-receptors bearing immunoreceptor tyrosine-based inhibition motifs. Eur J Immunol. 1997;27:1994-2000.
24. Baran CP, Tridandapani S, Helgason CD, Humphries RK, Krystal G, Marsh CB. The inositol 5′-phosphatase SHIP-1 and the Src kinase Lyn negatively regulate macrophage colony-stimulating factor-induced Akt activity. J Biol Chem. 2003;278:38628-38636.
25. Kalesnikoff J, Sly LM, Hughes MR, et al. The role of SHIP in cytokine-induced signaling. Rev Physiol Biochem Pharmacol. 2003;149:87-103.
26. Tridandapani S, Wang Y, Marsh CB, Anderson CL. Src homology 2 domain-containing inositol polyphosphate phosphatase regulates NF-kappa B-mediated gene transcription by phagocytic Fc gamma Rs in human myeloid cells. J Immunol. 2002;169:4370-4378.
27. Galandrini R, Tassi I, Mattia G, et al. SH2-containing inositol phosphatase (SHIP-1) transiently translocates to raft domains and modulates CD16-mediated cytotoxicity in human NK cells. Blood. 2002;100:4581-4589.
28. Galandrini R, Tassi I, Morrone S, et al. The adaptor protein shc is involved in the negative regulation of NK cell-mediated cytotoxicity. Eur J Immunol. 2001;31:2016-2025.
29. Wang JW, Howson JM, Ghansah T, et al. Influence of SHIP on the NK repertoire and allogeneic bone marrow transplantation. Science. 2002;295:2094-2097.
30. Lioubin MN, Algate PA, Tsai S, Carlberg K, Aebersold A, Rohrschneider LR. p150Ship, a signal transduction molecule with inositol polyphosphate-5- phosphatase activity. Genes Dev. 1996;10:1084-1095.
31. Grignani F, Kinsella T, Mencarelli A, et al. High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res. 1998;58:14-19.
32. Sattler M, Verma S, Byrne CH, et al. BCR/ABL directly inhibits expression of SHIP, an SH2-containing polyinositol-5-phosphatase involved in the regulation of hematopoiesis. Mol Cell Biol. 1999;19:7473-7480.
33. Trotta R, Vignudelli T, Candini O, et al. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell. 2003;3:145-160.
34. Helgason CD, Damen JE, Rosten P, et al. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 1998;12:1610-1620.
35. Trotta R, Kanakaraj P, Perussia B. Fc gamma R-dependent mitogen-activated protein kinase activation in leukocytes: a common signal transduction event necessary for expression of TNF-alpha and early activation genes. J Exp Med. 1996;184:1027-1035.
36. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem. 1994;269:5241-5248.
37. Deuter-Reinhard M, Apell G, Pot D, Klippel A, Williams LT, Kavanaugh WM. SIP/SHIP inhibits Xenopus oocyte maturation induced by insulin and phosphatidylinositol 3-kinase. Mol Cell Biol. 1997;17:2559-2565.
38. Jouanguy E, Doffinger R, Dupuis S, Pallier A, Altare F, Casanova JL. IL-12 and IFN-gamma in host defense against mycobacteria and salmonella in mice and men. Curr Opin Immunol. 1999;11:346-351.
39. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21:137-148.
40. Geier SJ, Algate PA, Carlberg K, et al. The human SHIP gene is differentially expressed in cell lineages of the bone marrow and blood. Blood. 1997;89:1876-1885.
41. Sly LM, Rauh MJ, Kalesnikoff J, Buchse T, Krystal G. SHIP, SHIP2, and PTEN activities are regulated in vivo by modulation of their protein levels: SHIP is up-regulated in macrophages and mast cells by lipopolysaccharide. Exp Hematol. 2003;31:1170-1181.
42. Valderrama-Carvajal H, Cocolakis E, Lacerte A, et al. Activin/TGF-beta induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nat Cell Biol. 2002;4:963-969.
43. Sly LM, Rauh MJ, Kalesnikoff J, Song CH, Krystal G. LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity. 2004;21:227-239.
44. Loza MJ, Perussia B. The IL-12 signature: NK cell terminal CD56 high stage and effector functions. J Immunol. 2004;172:88-96.
45. Fehniger TA, Cooper MA, Nuovo GJ, et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood. 2003;101:3052-3057.
46. Cooper MA, Fehniger TA, Fuchs A, Colonna M, Caligiuri MA. NK cell and DC interactions. Trends Immunol. 2004;25:47-52.
47. Freud AG, Becknell B, Roychowdhury S, et al. A novel human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity. In press.
48. Sica A, Dorman L, Viggiano V, et al. Interaction of NF-kappaB and NFAT with the interferon-gamma promoter. J Biol Chem. 1997;272:30412-30420.
49. Kalesnikoff J, Baur N, Leitges M, et al. SHIP negatively regulates IgE + antigen-induced IL-6 production in mast cells by inhibiting NF-kappa B activity. J Immunol. 2002;168:4737-4746.
50. Stokoe D, Stephens LR, Copeland T, et al. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science. 1997;277:567-570.
51. Alessi DR, James SR, Downes CP, et al. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol. 1997;7:261-269.
52. Patra AK, Na SY, Bommhardt U. Active protein kinase B regulates TCR responsiveness by modulating cytoplasmic-nuclear localization of NFATand NF-kappa B proteins. J Immunol. 2004;172:4812-4820.
53. Moody JL, Jirik FR. Compound heterozygosity for Pten and SHIP augments T-dependent humoral immune responses and cytokine production by CD(4+) T cells. Immunology. 2004;112:404-412.
54. Trotta R, Fettucciari K, Azzoni L, et al. Differential role of p38 and c-Jun N-terminal kinase 1 mitogen-activated protein kinases in NK cell cytotoxicity. J Immunol. 2000;165:1782-1789.
55. Trotta R, Puorro KA, Paroli M, et al. Dependence of both spontaneous and antibody-dependent, granule exocytosis-mediated NK cell cytotoxicity on extracellular signal-regulated kinases. J Immunol. 1998;161:6648-6656.
56. Farag SS, VanDeusen JB, Fehniger TA, Caligiuri MA. Biology and clinical impact of human natural killer cells. Int J Hematol. 2003;78:7-17.