Abstract
The SH2-containing inositol-5′-phosphatase, SHIP (aka SHIP1) is a hematopoietic-restricted phosphoinositol phosphatase that translocates to the plasma membrane following extracellular stimulation and hydrolyses the phosphatidylinositol-3-kinase (PI3K)-generated second messenger PI-3,4,5-P3 (PIP3) to PI-3,4-P2. As a result, it often acts as a negative regulator of PI3K, reducing the sensitivity of blood cells and blood cell progenitors to extracellular stimulators of proliferation, survival, and activation. However, because SHIP generates the second messenger PI-3,4-P2 and can also act as an adaptor, via its many protein–protein interaction domains, its effects are very cell type and stimulus dependent. In this review, we focus on SHIP’s structure and binding partners, the regulation of its expression and its biological properties, especially in terms of its potential effects on the M1 versus M2 skewing of tumor-associated macrophages.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- ALL:
-
acute lymphocytic leukemia
- BMmφs:
-
bone marrow-derived macrophages
- BMMCs:
-
bone marrow mast cells
- CML:
-
chronic myelogenous leukemia
- COX-2:
-
cyclooxygenase-2
- DCs:
-
dendritic cells
- DLBCL:
-
diffuse large B-cell lymphoma
- Doks:
-
downstream of tyrosine kinases
- ES:
-
embryonic stem
- F.t.:
-
Francisella tularensis
- GvHD:
-
graft-versus-host disease
- HA:
-
hyaluronic acid
- HSCs:
-
hematopoietic stem cells
- iNOS:
-
inducible nitric oxide synthase
- IP4 :
-
inositol-1,3,4,5-tetrakisphosphate
- INPP4B:
-
inositol polyphosphate 4-phosphatase type II
- ITAMs:
-
immunoreceptor tyrosine-based activation motifs
- ITIMs:
-
immunoreceptor tyrosine-based inhibitory motifs
- LPS:
-
lipopolysaccharide
- M-CSF:
-
macrophage colony-stimulating factor
- mφs:
-
macrophages
- MDSCs:
-
myeloid-derived suppressor cells
- mIRs:
-
microRNAs
- NK:
-
natural killer
- NO:
-
nitric oxide
- PGE2 :
-
prostaglandin E2
- PGN:
-
peptidoglycan
- PH:
-
pleckstrin homology
- PIAS1:
-
protein inhibitor of activated STAT1
- PI3K:
-
phosphatidylinositol-3-kinase
- PIP3 :
-
phosphatidylinositol 3,4,5-trisphosphate
- PKB:
-
protein kinase B
- PTB:
-
phosphotyrosine binding
- PTEN:
-
phosphatase and tensin homologue deleted on chromosome ten
- ROS:
-
reactive oxygen species
- SH2:
-
Src homology 2
- SHIP:
-
Src homology 2-containing inositol 5′-phosphatase
- sSHIP:
-
stem cell SHIP
- TLRs:
-
Toll-like receptors
- UTR:
-
untranslated region
References
Allam A, Marshall AJ (2005) Immunol Lett 97:7–17
Aman MJ, Walk SF, March ME et al (2000) Mol Cell Biol 20:3576–3589
Androulidaki A, Iliopoulos D, Arranz A et al (2009) Immunity 31:220–231
Antignano F, Ruschmann J, Hamilton M et al (2009) The Src homology 2 containing inositol 5¢ phosphatases. In: Bradshan RA, Dennis EA (eds) Handbook of cell signalling, Elsevier Inc, San Diego, CA
Antignano F, Ibaraki M, Kim C et al (2010) J Immunol 184:2805–2813
Astle MV, Horan KA, Ooms LM et al (2007) Biochem Soc Symp 74:161–181
Baran CP, Tridandapani S, Helgason CD et al (2003) J Biol Chem 278:38628–38636
Bennett M, Onnebo SM, Azevedo C et al (2006) Cell Mol Life Sci 63:552–564
Bishop JL, Sly LM, Krystal G et al (2008) Infect Immun 76:2913–2922
Bone H, Welham MJ (2000) Cell Signal 12:183–194
Brauweiler A, Tamir I, Marschner S et al (2001) J Immunol 167:204–211
Busche T, Horras N, Lenfert E et al (2011) Mol cell proteomics July 1 [Epub Ahead of Print]
Campbell IG, Russell SE, Choong DY et al (2004) Cancer Res 64:7678–7681
Cantley LC, Neel BG (1999) Proc Natl Acad Sci USA 96:4240–4245
Cao L, Yu K, Banh C et al (2007) J Immunol 179:5864–5876
Coggeshall KM (1998) Curr Opin Immunol 10:306–312
Collazo MM, Wood D, Paraiso KH et al (2009) Blood 113:2934–2944
Costinean S, Sandhu SK, Pedersen IM et al (2009) Blood 114:1374–1382
Cox D, Dale BM, Kashiwada M et al (2001) J Exp Med 193:61–71
Cremer TJ, Ravneberg DH, Clay CD et al (2009) PLoS One 4:e8508
Cuschieri J, Bulger E, Grinsell R et al (2007) Shock 29:285–290
Damen JE, Liu L, Rosten P et al (1996) Proc Natl Acad Sci USA 93:1689–1693
Damen JE, Liu L, Ware MD et al (1998) Blood 92:1199–1205
Damen JE, Ware MD, Kalesnikoff J et al (2001) Blood 97:1343–1351
Downes CP, Leslie NR, Batty IH et al (2007) Biochem Soc Trans 35:188–192
Dybedal I, Bryder D, Fossum A et al (2001) Blood 98:1782–1791
Dyson JM, O’Malley CJ, Becanovic J et al (2001) J Cell Biol 155:1065–1079
Feng Y, Wente SR, Majerus PW (2001) Proc Natl Acad Sci USA 98:875–879
Forestell SP, Bohnlein E, Rigg RJ (1995) Gene Ther 2:723–730
Frimberger AE, McAuliffe CI, Werme KA et al (2001) Br J Haematol 112:644–654
Fry MJ (2001) Breast Cancer Res 3:304–312
Galandrini R, Tassi I, Morrone S et al (2001) Eur J Immunol 31:2016–2025
Galandrini R, Tassi I, Mattia G et al (2002) Blood 100:4581–4589
Geier SJ, Algate PA, Carlberg K et al (1997) Blood 89:1876–1885
Gewinner C, Wang ZC, Richardson A et al (2009) Cancer Cell 16:115–125
Ghansah T, Paraiso KH, Highfill S et al (2004) J Immunol 173:7324–7330
Giallourakis C, Kashiwada M, Pan PY et al (2000) J Biol Chem 275:29275–29282
Giuriato S, Payrastre B, Drayer AL et al (1997) J Biol Chem 272:26857–26863
Gloire G, Charlier E, Rahmouni S et al (2006) Oncogene 25:5485–5494
Gloire G, Erneux C, Piette J (2007) Biochem Soc Trans 35:277–280
Gordon S (2003) Nat Rev Immunol 3:23–35
Gratacap MP, Severin S, Chicanne G et al (2008) Adv Enzyme Regul 48:240–252
Gupta N, Scharenberg AM, Fruman DA et al (1999) J Biol Chem 274:7489–7494
Haddon DJ, Antignano F, Hughes MR et al (2009) J Immunol 183:228–236
Harris SJ, Parry RV, Westwick J et al (2008) J Biol Chem 283:2465–2469
Helgason CD, Damen JE, Rosten P et al (1998) Genes Dev 12:1610–1620
Hennessy BT, Smith DL, Ram PT et al (2005) Nat Rev Drug Discov 4:988–1004
Horn S, Meyer J, Heukeshoven J et al (2001) Leukemia 15:112–120
Huber M, Helgason CD, Scheid MP et al (1998) EMBO J 17:7311–7319
Huber M, Helgason CD, Damen JE et al (1999) The role of SHIP in FcεRI-induced signalling. In: Daeron M, Vivier E (eds) Current topics in microbiology and immunology, vol 244. Springer, Berlin
Ishihara H, Sasaoka T, Hori H et al (1999) Biochem Biophys Res Commun 260:265–272
Jaiswal BS, Janakiraman V, Kljavin NM et al (2009) Cancer Cell 16:463–474
Jiang X, Stuible M, Chalandon Y et al (2003) Blood 102:2976–2984
Kalesnikoff J, Sly LM, Hughes MR et al (2003) The role of SHIP in cytokine-induced signaling. In: Amara SG, Bamberg E, Blaustein MP et al (eds) Reviews of physiology, biochemistry and pharmacology. Springer, Heidelberg
Kamen LA, Levinsohn J, Cadwallader A et al (2008) J Immunol 180:7497–7505
Kashiwada M, Cattoretti G, McKeag L et al (2006) J Immunol 176:3958–3965
Kashiwada M, Lu P, Rothman PB (2007) Immunol Res 39:194–224
Kavanaugh WM, Pot DA, Chin SM et al (1996) Curr Biol 6:438–445
Kim CH, Hangoc G, Cooper S et al (1999) J Clin Invest 104:1751–1759
Kohlhaas S, Garden OA, Scudamore C et al (2009) J Immunol 182:2578–2582
Koncz G, Toth GK, Bokonyi G et al (2001) Eur J Biochem 268:3898–3906
Kowanetz K, Husnjak K, Holler D et al (2004) Mol Biol Cell 15:3155–3166
Krahn AK, Ma K, Hou S et al (2004) J Immunol 172:331–339
Krause M, Leslie JD, Stewart M et al (2004) Dev Cell 7:571–583
Krystal G (2000) Semin Immunol 12:397–403
Kuroda E, Ho V, Ruschmann J et al (2009) J Immunol 183:3652–3660
Kuroda E, Antignano F, Ho VW et al (2011) J Immunol 186:323–332
Leslie NR, Batty IH, Maccario H et al (2008) Oncogene 27:5464–5476
Lesourne R, Fridman WH, Daeron M (2005) J Immunol 174:1365–1373
Leung WH, Tarasenko T, Bolland S (2009) Immunol Res 43:243–251
Lewis CE, Pollard JW (2006) Cancer Res 66:605–612
Liu L, Damen JE, Ware MD et al (1997) J Biol Chem 272:10998–11001
Liu Q, Oliveira-Dos-Santos AJ, Mariathasan S et al (1998a) J Exp Med 188:1333–1342
Liu Q, Shalaby F, Jones J et al (1998b) Blood 91:2753–2759
Lo TC, Barnhill LM, Kim Y et al (2009) Leuk Res 33:1562–1566
Locke NR, Patterson SJ, Hamilton MJ et al (2009) J Immunol 183:975–983
Lu Y, Yu Q, Liu JH et al (2003) J Biol Chem 278:40057–40066
Lucas DM, Rohrschneider LR (1999) Blood 93:1922–1933
Luo HR, Huang YE, Chen JC et al (2003a) Cell 114:559–572
Luo JM, Yoshida H, Komura S et al (2003b) Leukemia 17:1–8
Luo JM, Liu ZL, Hao HL et al (2004) Zhonghua Xue Ye Xue Za Zhi 25:385–388
Ma K, Cheung SM, Marshall AJ et al (2008) Cell Signal 20:684–694
MacDonald SM, Vonakis BM (2001) Mol Immunol 38:1323–1327
MacGlashan DW Jr (2007) J Allergy Clin Immunol 119:626–633
Maeda K, Mehta H, Drevets DA et al (2010) Blood 115:4699–4706
Mantovani A, Sozzani S, Locati M et al (2002) Trends Immunol 23:549–555
Marchetto S, Fournier E, Beslu N et al (1999) Leukemia 13:1374–1382
Maresco DL, Osborne JM, Cooney D et al (1999) J Immunol 162:6458–6465
Marshall AJ, Krahn AK, Ma K et al (2002) Mol Cell Biol 22:5479–5491
Martin-Berenjeno I, Vanhaesebroeck B (2009) Cancer Cell 16:449–450
Martino R, Caballero MD, Canals C et al (2001) Br J Haematol 115:653–659
Mason JM, Halupa A, Hyam D et al (2002) Blood 100:519a.2030
Maxwell MJ, Yuan Y, Anderson KE et al (2004) J Biol Chem 279:32196–32204
Mills CD (2001) Crit Rev Immunol 21:399–425
Nakamura K, Kouro T, Kincade PW et al (2004) J Exp Med 199:243–254
Nishio M, Watanabe K, Sasaki J et al (2007) Nat Cell Biol 9:36–44
O’connell RM, Chaudhuri AA, Rao DS et al (2009) Proc Natl Acad Sci USA 106:7113–7118
Oh SY, Zheng T, Bailey ML et al (2007) J Allergy Clin Immunol 119:123–131
Ong CJ, Ming-Lum A, Nodwell M et al (2007) Blood 110:1942–1949
Ono M, Bolland S, Tempst P et al (1996) Nature 383:263–266
Ooms LM, Horan KA, Rahman P et al (2009) Biochem J 419:29–49
Pearse RN, Kawabe T, Bolland S et al (1999) Immunity 10:753–760
Pedersen IM, Otero D, Kao E et al (2009) EMBO Mol Med 1:288–295
Perez LE, Desponts C, Parquet N et al (2008) PLoS One 3:e3565
Pesesse X, Backers K, Moreau C et al (2006) Adv Enzyme Regul 46:142–153
Phee H, Jacob A, Coggeshall KM (2000) J Biol Chem 275:19090–19097
Phee H, Rodgers W, Coggeshall KM (2001) Mol Cell Biol 21:8615–8625
Prasad NK, Tandon M, Badve S et al (2008a) Carcinogenesis 29:25–34
Prasad NK, Tandon M, Handa A et al (2008b) Tumour Biol 29:330–341
Ramshaw HS, Guthridge MA, Stomski FC et al (2007) Blood 110:3582–3590
Rauh MJ, Ho V, Pereira C et al (2005) Immunity 23:361–374
Robson JD, Davidson D, Veillette A (2004) Mol Cell Biol 24:2332–2343
Rohrschneider LR, Fuller JF, Wolf I et al (2000) Genes Dev 14:505–520
Rohrschneider LR, Custodio JM, Anderson TA et al (2005) Dev Biol 283:503–521
Ruggiero T, Trabucchi M, De Santa F et al (2009) FASEB J 23:2898–2908
Ruschmann J, Ho V, Antignano F et al (2010) Exp Hematol 38:393–402
Saiardi A, Bhandari R, Resnick AC et al (2004) Science 306:2101–2105
Salmeen A, Barford D (2005) Antioxid Redox Signal 7:560–577
Sasaoka T, Wada T, Tsuneki H (2006) Pharmacol Ther 112:799–809
Sattler M, Salgia R, Shrikhande G et al (1997) Oncogene 15:2379–2384
Savage ND, de Boer T, Walburg KV et al (2008) J Immunol 181:2220–2226
Scheid MP, Huber M, Damen JE et al (2002) J Biol Chem 277:9027–9035
Siegel J, Li Y, Whyte P (1999) Oncogene 18:7135–7148
Sinha P, Clements VK, Miller S et al (2005) Cancer Immunol Immunother 54:1137–1142
Sly LM, Rauh MJ, Kalesnikoff J et al (2003) Exp Hematol 31:1170–1181
Sly LM, Rauh MJ, Kalesnikoff J et al (2004) Immunity 21:227–239
Sokol CL, Medzhitov R (2010) Curr Opin Immunol 22:73–77
Song M, Kim MJ, Ha S et al (2005) Exp Mol Med 37:161–168
Sweeney MC, Wavreille AS, Park J et al (2005) Biochemistry 44:14932–14947
Takeshita S, Namba N, Zhao JJ et al (2002) Nat Med 8:943–949
Tanigaki K, Mineo C, Yuhanna IS et al (2009) Circ Res 104:1275–1282
Tarasenko T, Kole HK, Chi AW et al (2007) Proc Natl Acad Sci USA 104:11382–11387
Tomlinson MG, Heath VL, Turck CW et al (2004) J Biol Chem 279:55089–55096
Tridandapani S, Pradhan M, LaDine JR et al (1999) J Immunol 162:1408–1414
Tridandapani S, Wang Y, Marsh CB et al (2002) J Immunol 169:4370–4378
Trotta R, Parihar R, Yu J et al (2005) Blood 105:3011–3018
Tu Z, Ninos JM, Ma Z et al (2001) Blood 98:2028–2038
Valderrama-Carvajal H, Cocolakis E, Lacerte A et al (2002) Nat Cell Biol 4:963–969
Vanderwinden JM, Wang D, Paternotte N et al (2006) Cell Signal 18:661–669
Varin A, Gordon S (2009) Immunobiology 214:630–641
Velazquez L, Gish GD, van der Geer P et al (2000) Blood 96:132–138
Villamon E, Roie P, Gil ML et al (2005) Res Microbiol 156:115–118
Wang JW, Howson JM, Ghansah T et al (2002) Science 295:2094–2097
Wavreille AS, Garaud M, Zhang Y et al (2007) Methods 42:207–219
Wisniewski D, Strife A, Swendeman S et al (1999) Blood 93:2707–2720
Wolf I, Lucas DM, Algate PA et al (2000) Genomics 69:104–112
Yamanaka Y, Tagawa H, Takahashi N et al (2009) Blood 114:3265–3275
Yogo K, Mizutamari M, Mishima K et al (2006) Endocrinology 147:3307–3317
Zhang J, Walk SF, Ravichandran KS et al (2009a) J Biol Chem 284:20070–20078
Zhang TT, Li H, Cheung SM et al (2009b) Immunol Rev 232:255–272
Zhang Y, Wavreille AS, Kunys AR et al (2009c) Biochemistry 48:11075–11083
Zippo A, De Robertis A, Bardelli M et al (2004) Blood 103:4536–4544
Acknowledgments
We thank Christine Kelly for typing the manuscript. This work was supported by the NCI-C, with funds from the Terry Fox Foundation and core support from the BC Cancer Foundation and BC Cancer Agency.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Ho, V.W. et al. (2011). SHIP and Tumour-Associated Macrophages. In: Lawrence, T., Hagemann, T. (eds) Tumour-Associated Macrophages. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0662-4_10
Download citation
DOI: https://doi.org/10.1007/978-1-4614-0662-4_10
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-0661-7
Online ISBN: 978-1-4614-0662-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)