Differential roles for the inositol phosphatase SHIP in the regulation of macrophages and lymphocytes

Immunologic Research

Volumn 43, Issue 1-3, 2009, Pages 243-251

  Leung, Wai Hang ^a   Tarasenko, Tatyana ^a   Bolland, Silvia ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Conditional knockout; Lymphocytes; Macrophages; SHIP; T bet

Indexed keywords

INOSITOL PHOSPHATASE; INTERLEUKIN 17; PHOSPHATASE; UNCLASSIFIED DRUG; INOSITOL 1,4,5 TRISPHOSPHATE 5 PHOSPHATASE; INOSITOL-1,4,5-TRISPHOSPHATE 5-PHOSPHATASE; LYMPHOCYTE ANTIGEN RECEPTOR;

ANTIGEN PRESENTING CELL; B LYMPHOCYTE; CELL LINEAGE; CELL MATURATION; CELL SELECTION; CYTOTOXIC T LYMPHOCYTE; EXPERIMENTAL ANIMAL; HELPER CELL; INFLAMMATION; LYMPHOCYTE; MACROPHAGE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; TH1 CELL; ANIMAL; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; MOUSE MUTANT; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; B-LYMPHOCYTES; LYMPHOCYTES; MACROPHAGES; MICE; MICE, KNOCKOUT; PHOSPHORIC MONOESTER HYDROLASES; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS;

EID: 66449092234     PISSN: 0257277X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12026-008-8078-1     Document Type: Review

References (53)

1. M Ono S Bolland P Tempst JV Ravetch 1996 Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB Nature 383 263 6 8805703 10.1038/383263a0 1:CAS:528:DyaK28Xlsl2ksLg%3D (Pubitemid 26317676)
2. LR Rohrschneider JF Fuller I Wolf Y Liu DM Lucas 2000 Structure, function, and biology of SHIP proteins Genes Dev 14 505 20 10716940 1:CAS:528:DC%2BD3cXitFWrsr8%3D
3. MJ Rauh J Kalesnikoff M Hughes L Sly V Lam G Krystal 2003 Role of Src homology 2-containing-inositol 5'-phosphatase (SHIP) in mast cells and macrophages Biochem Soc Trans 31 286 91 12546703 10.1042/BST0310286 1:CAS:528:DC%2BD3sXptF2qtQ%3D%3D
4. J Kalesnikoff LM Sly MR Hughes T Buchse MJ Rauh LP Cao V Lam A Mui M Huber G Krystal 2003 The role of SHIP in cytokine-induced signaling Rev Physiol Biochem Pharmacol 149 87 103 12692707 10.1007/s10254-003-0016-y 1:CAS:528:DC%2BD2cXitFSlu7w%3D
5. R Parihar R Trotta JM Roda AK Ferketich S Tridandapani MA Caligiuri WE Carson 3rd 2005 Src homology 2-containing inositol 5'-phosphatase 1 negatively regulates IFN-gamma production by natural killer cells stimulated with antibody-coated tumor cells and interleukin-12 Cancer Res 65 9099 107 16204085 10.1158/0008-5472.CAN-04-4424 1:CAS:528:DC%2BD2MXhtVKiu7vL (Pubitemid 41377403)
6. JE Damen L Liu P Rosten RK Humphries AB Jefferson PW Majerus G Krystal 1996 The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3, 4, 5-triphosphate 5-phosphatase Proc Natl Acad Sci USA 93 1689 93 8643691 10.1073/pnas.93.4.1689 1:CAS:528:DyaK28Xht1entLw%3D (Pubitemid 26075186)
7. MN Lioubin PA Algate S Tsai K Carlberg A Aebersold LR Rohrschneider 1996 p150Ship, a signal transduction molecule with inositol polyphosphate-5- phosphatase activity Genes Dev 10 1084 95 8654924 10.1101/gad.10.9.1084 1:CAS:528:DyaK28XjtFajtbk%3D
8. S Bolland RN Pearse T Kurosaki JV Ravetch 1998 SHIP modulates immune receptor responses by regulating membrane association of Btk Immunity 8 509 16 9586640 10.1016/S1074-7613(00)80555-5 1:CAS:528:DyaK1cXjtVygsrg%3D (Pubitemid 28196804)
9. 2+ oscillatory response J Immunol 161 5129 32 9820480 1:CAS:528:DyaK1cXnsVOrtr8%3D
10. Q Liu AJ Oliveira-Dos-Santos S Mariathasan D Bouchard J Jones R Sarao I Kozieradzki PS Ohashi JM Penninger DJ Dumont 1998 The inositol polyphosphate 5-phosphatase ship is a crucial negative regulator of B cell antigen receptor signaling J Exp Med 188 1333 42 9763612 10.1084/jem.188.7.1333 1:CAS:528:DyaK1cXmsFalsrY%3D (Pubitemid 28478021)
11. C Edmunds RV Parry SJ Burgess B Reaves SG Ward 1999 CD28 stimulates tyrosine phosphorylation, cellular redistribution and catalytic activity of the inositol lipid 5-phosphatase SHIP Eur J Immunol 29 3507 15 10556805 10.1002/(SICI)1521-4141(199911)29:11<3507::AID-IMMU3507>3.0.CO;2-9 1:CAS:528:DyaK1MXnt1Ogt7c%3D (Pubitemid 29527798)
12. RW Freeburn KL Wright SJ Burgess E Astoul DA Cantrell SG Ward 2002 Evidence that SHIP-1 contributes to phosphatidylinositol 3, 4, 5-trisphosphate metabolism in T lymphocytes and can regulate novel phosphoinositide 3-kinase effectors J Immunol 169 5441 50 12421919 1:CAS:528:DC%2BD38Xoslyqtb0%3D
13. LM Sly MJ Rauh J Kalesnikoff CH Song G Krystal 2004 LPS-induced upregulation of SHIP is essential for endotoxin tolerance Immunity 21 227 39 15308103 10.1016/j.immuni.2004.07.010 1:CAS:528:DC%2BD2cXnsVKlt7g%3D (Pubitemid 39094052)
14. M Huber CD Helgason JE Damen MP Scheid V Duronio V Lam RK Humphries G Krystal 1999 The role of the SRC homology 2-containing inositol 5'-phosphatase in Fc epsilon R1-induced signaling Curr Top Microbiol Immunol 244 29 41 10453647 1:CAS:528:DyaK1MXls1ens7w%3D
15. T Kimura H Sakamoto E Appella RP Siraganian 1997 The negative signaling molecule SH2 domain-containing inositol-polyphosphate 5-phosphatase (SHIP) binds to the tyrosine-phosphorylated beta subunit of the high affinity IgE receptor J Biol Chem 272 13991 6 9153264 10.1074/jbc.272.21.13991 1:CAS:528: DyaK2sXjsFantL8%3D (Pubitemid 27224846)
16. S Tridandapani M Pradhan JR LaDine S Garber CL Anderson KM Coggeshall 1999 Protein interactions of Src homology 2 (SH2) domain-containing inositol phosphatase (SHIP): association with Shc displaces SHIP from FcgammaRIIb in B cells J Immunol 162 1408 14 9973396 1:CAS:528:DyaK1MXhtVWnu7Y%3D
17. S Tridandapani T Kelley M Pradhan D Cooney LB Justement KM Coggeshall 1997 Recruitment and phosphorylation of SH2-containing inositol phosphatase and Shc to the B-cell Fc gamma immunoreceptor tyrosine-based inhibition motif peptide motif Mol Cell Biol 17 4305 11 9234687 1:CAS:528:DyaK2sXkvVert7w%3D
18. MA Osborne G Zenner M Lubinus X Zhang Z Songyang LC Cantley P Majerus P Burn JP Kochan 1996 The inositol 5'-phosphatase SHIP binds to immunoreceptor signaling motifs and responds to high affinity IgE receptor aggregation J Biol Chem 271 29271 8 8910587 10.1074/jbc.271.51.32689 1:CAS:528:DyaK28XntFKks7s%3D (Pubitemid 27008692)
19. M Huber CD Helgason JE Damen M Scheid V Duronio L Liu MD Ware RK Humphries G Krystal 1999 The role of SHIP in growth factor induced signalling Prog Biophys Mol Biol 71 423 34 10354708 10.1016/S0079-6107(98)00049-2 1:CAS:528:DyaK1MXislaqtb8%3D (Pubitemid 29156311)
20. AM Scharenberg O El-Hillal DA Fruman LO Beitz Z Li S Lin I Gout LC Cantley DJ Rawlings JP Kinet 1998 Phosphatidylinositol-3, 4, 5-trisphosphate (PtdIns-3, 4, 5-P3)/Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals EMBO J 17 1961 72 9524119 10.1093/emboj/17.7. 1961 1:CAS:528:DyaK1cXisV2ktbY%3D (Pubitemid 28154526)
21. DJ Carver MJ Aman KS Ravichandran 2000 SHIP inhibits Akt activation in B cells through regulation of Akt membrane localization Blood 96 1449 56 10942391 1:CAS:528:DC%2BD3cXlvF2iur0%3D
22. R Galandrini I Tassi G Mattia L Lenti M Piccoli L Frati A Santoni 2002 SH2-containing inositol phosphatase (SHIP-1) transiently translocates to raft domains and modulates CD16-mediated cytotoxicity in human NK cells Blood 100 4581 9 12393695 10.1182/blood-2002-04-1058 1:CAS:528:DC%2BD38XpsFCqtrg%3D (Pubitemid 35429701)
23. G Krystal JE Damen CD Helgason M Huber MR Hughes J Kalesnikoff V Lam P Rosten MD Ware S Yew RK Humphries 1999 SHIPs ahoy Int J Biochem Cell Biol 31 1007 10 10582334 10.1016/S1357-2725(99)00072-2 1:CAS:528:DyaK1MXmsVWitro%3D (Pubitemid 29454541)
24. M Ono H Okada S Bolland S Yanagi T Kurosaki JV Ravetch 1997 Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling Cell 90 293 301 9244303 10.1016/S0092-8674(00)80337-2 1:CAS:528:DyaK2sXltVCjt7s%3D (Pubitemid 27329714)
25. 2+ mobilization by Src homology 2 domain-containing inositol 5'-phosphatase (SHIP) J Biol Chem 274 11203 8 10196207 10.1074/jbc.274.16.11203 1:CAS:528:DyaK1MXis1Gmtr8%3D (Pubitemid 29191112)
26. ME March DM Lucas MJ Aman KS Ravichandran 2000 p135 src homology 2 domain-containing inositol 5'-phosphatase (SHIPbeta) isoform can substitute for p145 SHIP in fcgamma RIIB1-mediated inhibitory signaling in B cells J Biol Chem 275 29960 7 10900203 10.1074/jbc.M003714200 1:CAS:528:DC%2BD3cXnt1ahtbo%3D
27. MJ Aman SF Walk ME March HP Su DJ Carver KS Ravichandran 2000 Essential role for the C-terminal noncatalytic region of SHIP in FcgammaRIIB1-mediated inhibitory signaling Mol Cell Biol 20 3576 89 10779347 10.1128/MCB.20.10.3576- 3589.2000 1:CAS:528:DC%2BD3cXivFyhtL8%3D (Pubitemid 30243903)
28. MG Tomlinson VL Heath CW Turck SP Watson A Weiss 2004 SHIP family inositol phosphatases interact with and negatively regulate the Tec tyrosine kinase J Biol Chem 279 55089 96 15492005 10.1074/jbc.M408141200 1:CAS:528:DC%2BD2cXhtFeis77F (Pubitemid 40066501)
29. S Dong B Corre E Foulon E Dufour A Veillette O Acuto F Michel 2006 T cell receptor for antigen induces linker for activation of T cell-dependent activation of a negative signaling complex involving Dok-2, SHIP-1, and Grb-2 J Exp Med 203 2509 18 17043143 10.1084/jem.20060650 1:CAS:528:DC%2BD28XhtFGqtL7L (Pubitemid 44664620)
30. CD Helgason JE Damen P Rosten R Grewal P Sorensen SM Chappel A Borowski F Jirik G Krystal RK Humphries 1998 Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span Genes Dev 12 1610 20 9620849 10.1101/gad.12.11.1610 1:CAS:528:DyaK1cXjslOjsLo%3D
31. K Nakamura A Malykhin KM Coggeshall 2002 The Src homology 2 domain-containing inositol 5-phosphatase negatively regulates Fcgamma receptor-mediated phagocytosis through immunoreceptor tyrosine-based activation motif-bearing phagocytic receptors Blood 100 3374 82 12384440 10.1182/blood-2002-03-0787 1:CAS:528:DC%2BD38XosVSit78%3D (Pubitemid 35217090)
32. M Huber CD Helgason JE Damen L Liu RK Humphries G Krystal 1998 The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation Proc Natl Acad Sci USA 95 11330 5 9736736 10.1073/pnas.95.19. 11330 1:CAS:528:DyaK1cXmt1agurw%3D (Pubitemid 28450128)
33. A Brauweiler I Tamir S Marschner CD Helgason JC Cambier 2001 Partially distinct molecular mechanisms mediate inhibitory FcgammaRIIB signaling in resting and activated B cells J Immunol 167 204 11 11418650 1:CAS:528: DC%2BD3MXkslSqur4%3D
34. L Neill AH Tien J Rey-Ladino CD Helgason 2007 SHIP-deficient mice provide insights into the regulation of dendritic cell development and function Exp Hematol 35 627 39 17379073 10.1016/j.exphem.2007.01.048 1:CAS:528: DC%2BD2sXjsVeksbo%3D (Pubitemid 46427971)
35. JA Wahle KH Paraiso RD Kendig HR Lawrence L Chen J Wu WG Kerr 2007 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 179 8009 15 18056340 1:CAS:528: DC%2BD2sXhtlyitrnM
36. AL Loy CC Goodnow 2002 Novel approaches for identifying genes regulating lymphocyte development and function Curr Opin Immunol 14 260 5 11869902 10.1016/S0952-7915(02)00331-X 1:CAS:528:DC%2BD38XhsFCqs7o%3D (Pubitemid 34188489)
37. MC Karlsson R Guinamard S Bolland M Sankala RM Steinman JV Ravetch 2003 Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone J Exp Med 198 333 40 12874264 10.1084/jem.20030684 1:CAS:528:DC%2BD3sXlvVyjur4%3D (Pubitemid 36987858)
38. PP Lee DR Fitzpatrick C Beard HK Jessup S Lehar KW Makar M Perez-Melgosa MT Sweetser MS Schlissel S Nguyen SR Cherry JH Tsai SM Tucker WM Weaver A Kelso R Jaenisch CB Wilson 2001 A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival Immunity 15 763 74 11728338 10.1016/S1074-7613(01)00227-8 1:CAS:528:DC%2BD3MXptVGgtbw%3D (Pubitemid 34008504)
39. T Tarasenko HK Kole AW Chi MM Mentink-Kane TA Wynn S Bolland 2007 T cell-specific deletion of the inositol phosphatase SHIP reveals its role in regulating Th1/Th2 and cytotoxic responses Proc Natl Acad Sci USA 104 11382 7 17585010 10.1073/pnas.0704853104 1:CAS:528:DC%2BD2sXnvFOms74%3D (Pubitemid 47175149)
40. M Kashiwada G Cattoretti L McKeag T Rouse BM Showalter U Al-Alem M Niki PP Pandolfi EH Field PB Rothman 2006 Downstream of tyrosine kinases-1 and Src homology 2-containing inositol 5'-phosphatase are required for regulation of CD4+CD25+ T cell development J Immunol 176 3958 65 16547230 1:CAS:528: DC%2BD28Xis1ertbw%3D
41. CV Ramana MP Gil RD Schreiber GR Stark 2002 Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling Trends Immunol 23 96 101 11929133 10.1016/S1471-4906(01)02118-4 1:CAS:528:DC%2BD38XivVSlsrg%3D (Pubitemid 34310151)
42. AA Lighvani DM Frucht D Jankovic H Yamane J Aliberti BD Hissong BV Nguyen M Gadina A Sher WE Paul JJ O'Shea 2001 T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells Proc Natl Acad Sci USA 98 15137 42 11752460 10.1073/pnas.261570598 1:CAS:528:DC%2BD38XpsVWl (Pubitemid 34013982)
43. BM Sullivan A Juedes SJ Szabo M von Herrath LH Glimcher 2003 Antigen-driven effector CD8 T cell function regulated by T-bet Proc Natl Acad Sci USA 100 15818 23 14673093 10.1073/pnas.2636938100 1:CAS:528: DC%2BD2cXhtVClsg%3D%3D (Pubitemid 38021073)
44. CD Helgason CP Kalberer JE Damen SM Chappel N Pineault G Krystal RK Humphries 2000 A dual role for Src homology 2 domain-containing inositol-5-phosphatase (SHIP) in immunity: aberrant development and enhanced function of b lymphocytes in ship -/- mice J Exp Med 191 781 94 10704460 10.1084/jem.191.5.781 1:CAS:528:DC%2BD3cXhslygt74%3D (Pubitemid 30690322)
45. RC Rickert J Roes K Rajewsky 1997 B lymphocyte-specific, Cre-mediated mutagenesis in mice Nucleic Acids Res 25 1317 8 9092650 10.1093/nar/25.6.1317 1:CAS:528:DyaK2sXitF2ntro%3D (Pubitemid 27303232)
46. K Nakamura T Kouro PW Kincade A Malykhin K Maeda KM Coggeshall 2004 Src homology 2-containing 5-inositol phosphatase (SHIP) suppresses an early stage of lymphoid cell development through elevated interleukin-6 production by myeloid cells in bone marrow J Exp Med 199 243 54 14718513 10.1084/jem.20031193 1:CAS:528:DC%2BD2cXmsFGrsQ%3D%3D (Pubitemid 38129704)
47. L Nitschke R Carsetti B Ocker G Kohler MC Lamers 1997 CD22 is a negative regulator of B-cell receptor signalling Curr Biol 7 133 43 9016707 10.1016/S0960-9822(06)00057-1 1:CAS:528:DyaK2sXhtlKqurk%3D
48. JC Poe M Fujimoto PJ Jansen AS Miller TF Tedder 2000 CD22 forms a quaternary complex with SHIP, Grb2, and Shc. A pathway for regulation of B lymphocyte antigen receptor-induced calcium flux J Biol Chem 275 17420 7 10748054 10.1074/jbc.M001892200 1:CAS:528:DC%2BD3cXktFaksLw%3D (Pubitemid 30430779)
49. AM Oliver F Martin GL Gartland RH Carter JF Kearney 1997 Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses Eur J Immunol 27 2366 74 9341782 10.1002/eji.1830270935 1:CAS:528:DyaK2sXmt1ensLs%3D (Pubitemid 27404323)
50. C Garcia de Vinuesa P O'Leary DM Sze KM Toellner IC MacLennan 1999 T-independent type 2 antigens induce B cell proliferation in multiple splenic sites, but exponential growth is confined to extrafollicular foci Eur J Immunol 29 1314 23 10229099 10.1002/(SICI)1521-4141(199904)29:04<1314::AID- IMMU1314>3.0.CO;2-4 1:CAS:528:DyaK1MXisVGjurs%3D
51. R Guinamard M Okigaki J Schlessinger JV Ravetch 2000 Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response Nat Immunol 1 31 6 10881171 10.1038/76882 1:CAS:528:DC%2BD3cXls1yqsrc%3D
52. F Martin AM Oliver JF Kearney 2001 Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens Immunity 14 617 29 11371363 10.1016/S1074-7613(01)00129-7 1:CAS:528: DC%2BD3MXktVantLc%3D (Pubitemid 32520872)
53. T Ghansah KHT Paraiso S Highfill C Desponts S May JK McIntosh J-W Wang J Ninos J Brayer F Cheng E Sotomayor WG Kerr 2004 Expansion of myeloid suppressor cells in SHIP-deficient mice represses allogeneic T cell responses J Immunol 173 7324 30 15585856 1:CAS:528:DC%2BD2cXhtVCqurzJ