Mouse natural killer cell development and maturation are differentially regulated by SHIP-1

Blood

Volumn 120, Issue 23, 2012, Pages 4583-4590

  Banh, Cindy ^a,b   Miah, S M Shahjahan ^a   Kerr, William G ^c,d   Brossay, Laurent ^a  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

^d SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; GAMMA INTERFERON; PHOSPHATASE; SH2 CONTAINING INOSITOL PHOSPHATASE 1; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL LOSS; CELL MATURATION; CHIMERA; CONTROLLED STUDY; ENZYME DEFICIENCY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL;

EID: 84870571636     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-04-425009     Document Type: Article

References (50)

1. Di Santo JP. Natural killer cell developmental pathways: a question of balance. Annu Rev Immunol. 2006;24:257-286.
2. Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood. 2009;113(22):5488- 5496.
3. Lodoen MB, Lanier LL. Natural killer cells as an initial defense against pathogens. Curr Opin Immunol. 2006;18(4):391-398. (Pubitemid 43947576)
4. Bottino C, Moretta L, Moretta A. NK cell activating receptors and tumor recognition in humans. Curr Top Microbiol Immunol. 2006;298:175-182.
5. Huntington ND, Tabarias H, Fairfax K, et al. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J Immunol. 2007;178(8):4764-4770. (Pubitemid 46595257)
6. Kim S, Iizuka K, Kang HS, et al. In vivo developmental stages in murine natural killer cell maturation. Nat Immunol. 2002;3(6):523-528. (Pubitemid 34662303)
7. Rosmaraki EE, Douagi I, Roth C, Colucci F, Cumano A, Di Santo JP. Identification of committed NK cell progenitors in adult murine bone marrow. Eur J Immunol. 2001;31(6):1900-1909. (Pubitemid 32547352)
8. Dustin ML, Long EO. Cytotoxic immunological synapses. Immunol Rev. 2010;235(1):24-34.
9. Lanier LL. DAP10- and DAP12-associated receptors in innate immunity. Immunol Rev. 2009;227(1):150-160.
10. Lanier LL. Natural killer cell receptor signaling. Curr Opin Immunol. 2003;15(3):308-314. (Pubitemid 36645107)
11. Ravetch JV, Lanier LL. Immune inhibitory receptors. Science. 2000;290(5489):84-89.
12. Eissmann P, Beauchamp L, Wooters J, Tilton JC, Long EO, Watzl C. Molecular basis for positive and negative signaling by the natural killer cell receptor 2B4 (CD244). Blood. 2005;105(12):4722-4729. (Pubitemid 40807295)
13. Tessmer MS, Fugere C, Stevenaert F, et al. KLRG1 binds cadherins and preferentially associates with SHIP-1. Int Immunol. 2007;19(4):391-400. (Pubitemid 46523387)
14. Wang JW, Howson JM, Ghansah T, et al. Influence of SHIP on the NK repertoire and allogeneic bone marrow transplantation. Science. 2002;295(5562):2094-2097. (Pubitemid 34229475)
15. Ware MD, Rosten P, Damen JE, Liu L, Humphries RK, Krystal G. Cloning and characterization of human SHIP, the 145-kD inositol 5-phosphatase that associates with SHC after cytokine stimulation. Blood. 1996;88(8):2833-2840. (Pubitemid 26357363)
16. Liu Q, Shalaby F, Jones J, Bouchard D, Dumont DJ. The SH2-containing inositol polyphosphate 5-phosphatase, ship, is expressed during hematopoiesis and spermatogenesis. Blood. 1998;91(8):2753-2759. (Pubitemid 28227525)
17. 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(6):1876-1885. (Pubitemid 27132101)
18. Hazen AL, Smith MJ, Desponts C, Winter O, Moser K, Kerr WG. SHIP is required for a functional hematopoietic stem cell niche. Blood. 2009;113(13):2924-2933.
19. Wahle JA, Paraiso KH, Kendig RD, et al. Inappropriate recruitment and activity by the Src homology region 2 domain-containing phosphatase 1 (SHP1) is responsible for receptor dominance in the SHIP-deficient NK cell. J Immunol. 2007;179(12):8009-8015.
20. 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(11):1610-1620. (Pubitemid 28299513)
21. Karlsson MC, Guinamard R, Bolland S, Sankala M, Steinman RM, Ravetch JV. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J Exp Med. 2003;198(2):333-340. (Pubitemid 36987858)
22. Collazo MM, Wood D, Paraiso KH, et al. SHIP limits immunoregulatory capacity in the T-cell compartment. Blood. 2009;113(13):2934-2944.
23. Tarasenko T, Kole HK, Chi AW, Mentink-Kane MM, Wynn TA, Bolland S. T cell-specific deletion of the inositol phosphatase SHIP reveals its role in regulating Th1/Th2 and cytotoxic responses. Proc Natl Acad Sci U S A. 2007;104(27):11382-11387. (Pubitemid 47175149)
24. Fortenbery NR, Paraiso KH, Taniguchi M, Brooks C, Ibrahim L, Kerr WG. SHIP influences signals from CD48 and MHC class I ligands that regulate NK cell homeostasis, effector function, and repertoire formation. J Immunol. 2010;184(9):5065-5074.
25. Wahle JA, Paraiso KH, Costello AL, Goll EL, Sentman CL, Kerr WG. Cutting edge: dominance by an MHC-independent inhibitory receptor compromises NK killing of complex targets. J Immunol. 2006;176(12):7165-7169. (Pubitemid 43849017)
26. Huntington ND, Vosshenrich CA, Di Santo JP. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat Rev Immunol. 2007;7(9):703-714. (Pubitemid 47327395)
27. Robbins SH, Tessmer MS, Mikayama T, Brossay L. Expansion and contraction of the NK cell compartment in response to murine cytomegalovirus infection. J Immunol. 2004;173(1):259-266. (Pubitemid 38797350)
28. Hayakawa Y, Smyth MJ. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol. 2006; 176(3):1517-1524. (Pubitemid 43134295)
29. Fernandez NC, Treiner E, Vance RE, Jamieson AM, Lemieux S, Raulet DH. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood. 2005;105(11):4416-4423. (Pubitemid 40720789)
30. Kim S, Poursine-Laurent J, Truscott SM, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051):709-713. (Pubitemid 41117274)
31. Carotta S, Pang SH, Nutt SL, Belz GT. Identification of the earliest NK-cell precursor in the mouse BM. Blood. 2011;117(20):5449-5452.
32. Fathman JW, Bhattacharya D, Inlay MA, Seita J, Karsunky H, Weissman IL. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood. 2011;118(20):5439-5447.
33. Narni-Mancinelli E, Vivier E. NK cell genesis: a trick of the trail. Immunity. 2012;36(1):1-3.
34. Martín-Fontecha A, Lord GM, Brady HJ. Transcriptional control of natural killer cell differentiation and function. Cell Mol Life Sci. 2011;68(21):3495-3503.
35. Sun JC, Lanier LL. NK cell development, homeostasis and function: parallels with CD8 T cells. Nat Rev Immunol. 2011;11(10):645-657.
36. Elliott JM, Wahle JA, Yokoyama WM. MHC class I-deficient natural killer cells acquire a licensed phenotype after transfer into an MHC class I-sufficient environment. J Exp Med. 2010;207(10):2073-2079.
37. Joncker NT, Shifrin N, Delebecque F, Raulet DH. Mature natural killer cells reset their responsiveness when exposed to an altered MHC environment. J Exp Med. 2010;207(10):2065-2072.
38. Gascoyne DM, Long E, Veiga-Fernandes H, et al. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat Immunol. 2009;10(10):1118-1124.
39. Kamizono S, Duncan GS, Seidel MG, et al. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J Exp Med. 2009;206(13):2977- 2986.
40. Veillette A, Latour S, Davidson D. Negative regulation of immunoreceptor signaling. Annu Rev Immunol. 2002;20:669-707. (Pubitemid 34293437)
41. Kerr WG, Colucci F. Inositol phospholipid signaling and the biology of natural killer cells. J Innate Immun. 2011;3(3):249-257.
42. Trotta R, Parihar R, Yu J, et al. Differential expression of SHIP1 in CD56bright and CD56dim NK cells provides a molecular basis for distinct functional responses to monokine costimulation. Blood. 2005;105(8):3011-3018.
43. Trotta R, Chen L, Ciarlariello D, et al. MiR-155 regulates IFN-gamma production in natural killer cells. Blood. 2012;119(15):3478-3485.
44. Endt J, Eissmann P, Hoffmann SC, Meinke S, Giese T, Watzl C. Modulation of 2B4 (CD244) activity and regulated SAP expression in human NK cells. Eur J Immunol. 2007;37(1):193-198. (Pubitemid 46128799)
45. Dong Z, Cruz-Munoz ME, Zhong MC, Chen R, Latour S, Veillette A. Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat Immunol. 2009;10(9):973-980.
46. Tu Z, Ninos JM, Ma Z, et al. Embryonic and hematopoietic stem cells express a novel SH2-containing inositol 5-phosphatase isoform that partners with the Grb2 adapter protein. Blood. 2001;98(7):2028-2038.
47. Dyson JM, O'Malley CJ, Becanovic J, et al. The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin. J Cell Biol. 2001;155(6):1065-1079. (Pubitemid 34286256)
48. Pesesse X, Moreau C, Drayer AL, Woscholski R, Parker P, Erneux C. The SH2 domain containing inositol 5-phosphatase SHIP2 displays phosphatidylinositol 3,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate 5-phosphatase activity. FEBS Lett. 1998;437(3):301-303. (Pubitemid 28511179)
49. Nguyen NY, Maxwell MJ, Ooms LM, et al. An ENU-induced mouse mutant of SHIP1 reveals a critical role of the stem cell isoform for suppression of macrophage activation. Blood. 2011;117(20):5362-5371.
50. Huntington ND, Xu Y, Nutt SL, Tarlinton DM. A requirement for CD45 distinguishes Ly49Dmediated cytokine and chemokine production from killing in primary natural killer cells. J Exp Med. 2005;201(9):1421-1433. (Pubitemid 40664086)