Spreading by snail (Lymnaea stagnalis) defence cells is regulated through integrated PKC, FAK and Src signalling

Cell and Tissue Research

Volumn 341, Issue 1, 2010, Pages 131-145

  Walker, Anthony J ^a   Lacchini, Audrey H ^a   Sealey, Katie L ^a   MacKintosh, David ^a   Davies, Angela J ^a  

^a KINGSTON UNIVERSITY   (United Kingdom)

Author keywords

Focal adhesion kinase; Hemocyte haemocyte; Innate immunity; Integrin mediated cell adhesion; Lymnaea stagnalis (Mollusca); Protein kinase C

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; FIBRONECTIN; FOCAL ADHESION KINASE; HERBIMYCIN A; INTEGRIN; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; ARGINYL-GLYCYL-ASPARTYL-SERINE; OLIGOPEPTIDE; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; BLOOD CELL; CELL ADHESION; CELL SPREADING; CELL SUSPENSION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; FILOPODIUM; FOCAL ADHESION; IMMUNE SYSTEM; LAMELLIPODIUM; LYMNAEA; LYMNAEA STAGNALIS; MEMBRANE STRUCTURE; MOLLUSC; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; SNAIL; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL MOTION; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT;

ANIMALS; CELL ADHESION; CELL MOVEMENT; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; HEMOCYTES; LYMNAEA; MODELS, BIOLOGICAL; OLIGOPEPTIDES; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

GASTROPODA; LYMNAEA STAGNALIS; MOLLUSCA;

EID: 77954387304     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-010-0986-4     Document Type: Article

References (58)

1. CM Adema EC van Deutekom-Mulder WPW van der Knapp T Sminia 1994 Schistosomicidal activities of Lymnaea stagnalis haemocytes: the role of oxygen radicals Parasitology 109 479 485 10.1017/S0031182000080732 7800416
2. DT Babcock AR Brock GS Fish Y Wang L Perrin MA Krasnow MJ Galko 2008 Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae Proc Natl Acad Sci USA 105 10017 10022 10.1073/pnas.0709951105 1:CAS:528:DC%2BD1cXptFGksbc%3D 18632567
3. A Besson TL Wilson VW Yong 2002 The anchoring protein RACK1 links protein kinase Cε to integrin β chains - requirement for adhesion and motility J Biol Chem 277 22073 22084 10.1074/jbc.M111644200 1:CAS:528: DC%2BD38Xksl2jtrY%3D 11934885 (Pubitemid 34952362)
4. CS Buensuceso D Woodside JL Huff GE Plopper TE O'Toole 2001 The Wd protein RACK1 mediates protein kinase C and integrin-dependent cell migration J Cell Sci 114 1691 1698 1:CAS:528:DC%2BD3MXjslyqurg%3D 11309199
5. CS Buensuceso A Obergfell A Soriani K Eto WB Kiosses EG Arias-Salgado T Kawakami SJ Shattil 2005 Regulation of outside-in signaling in platelets by integrin-associated protein kinase Cβ J Biol Chem 280 644 653 1:CAS:528:DC%2BD2cXhtFGgu7fL 15536078
6. L Canesi M Betti C Ciacci LC Lorusso G Gallo C Pruzzo 2005 Interactions between Mytilus haemocytes and different strains of Escherichia coli and Vibrio cholerae 01 E1 Tor: role of kinase-mediated signalling Cell Microbiol 7 667 674 10.1111/j.1462-5822.2005.00499.x 1:CAS:528:DC%2BD2MXjvFaktL8%3D 15839896 (Pubitemid 40585008)
7. Caswell PT, Norman JC (2006) Integrin trafficking and the control of cell migration. Traffic 14:14-21
8. BY Chang M Chiang CA Cartwright 2001 The interaction of Src and RACK1 is enhanced by activation of protein kinase C and tyrosine phosphorylation of RACK1 J Biol Chem 276 20346 20356 10.1074/jbc.M101375200 1:CAS:528: DC%2BD3MXktlKnt7w%3D 11279199
9. BS Cobb MD Schaller TH Leu JT Parsons 1994 Stable association of pp 60src and pp59fyn with focal adhesion-associated protein tyrosine kinase, pp125FAK Mol Cell Biol 14 147 155 1:CAS:528:DyaK2cXhtVeiur4%3D 7505391
10. EA Cox D Bennin AT Doan T O'Toole A Huttenlocher 2003 RACK1 regulates integrin-mediated adhesion, protrusion, and chemotactic cell migration via its Src-binding site Mol Biol Cell 14 658 669 10.1091/mbc.E02-03-0142 1:CAS:528:DC%2BD3sXitFWmu74%3D 12589061 (Pubitemid 36237023)
11. BJ Davids TP Yoshino 1998 Integrin-like RGD-dependent binding mechanism involved in the spreading response of circulating molluscan phagocytes Dev Comp Immunol 22 39 53 10.1016/S0145-305X(97)00039-6 1:CAS:528:DyaK1cXktVSisbg%3D 9617582 (Pubitemid 28221678)
12. BJ Davids XJ Wu TP Yoshino 1999 Cloning of a β integrin subunit cDNA from an embryonic cell line derived from the freshwater mollusc, Biomphalaria glabrata Gene 228 213 223 10.1016/S0378-1119(99)00008-6 1:CAS:528: DyaK1MXitFSmtL8%3D 10072774 (Pubitemid 29136702)
13. P Defilippi C Olivio M Venturino L Dolce L Silengo G Tarone 1999 Actin cytoskeleton organization in response to integrin-mediated adhesion Microsc Res Tech 47 67 78 10.1002/(SICI)1097-0029(19991001)47:1<67::AID-JEMT7>3.0. CO;2-P 1:CAS:528:DyaK1MXmvFaksLY%3D 10506763 (Pubitemid 29474836)
14. G DeGaffe ES Loker 1998 Susceptibility of Biomphalaria glabrata to infection with Echinostoma paraensei: Correlation with the effect of parasite secretory-excretory products on host hemocyte spreading J Invert Path 71 64 72 10.1006/jipa.1997.4710 1:STN:280:DyaK1c7htVejsg%3D%3D (Pubitemid 128352151)
15. MH Disatnik TA Rando 1999 Integrin-mediated muscle cell spreading - the role of protein kinase C in outside-in and inside-out signaling and evidence of integrin cross-talk J Biol Chem 274 32486 32492 10.1074/jbc.274.45.32486 1:CAS:528:DyaK1MXnt12isrY%3D 10542294 (Pubitemid 29522998)
16. MH Disatnik SB Boutet CH Lee D Mochly-Rosen TA Rando 2002 Sequential activation of individual PKC isozymes in integrin-mediated muscle cell spreading: a role for MARCKS in an integrin signaling pathway J Cell Sci 115 2151 2163 1:CAS:528:DC%2BD38Xks1yktr8%3D 11973356
17. 3 integrin for internalization J Biol Chem 273 14813 14818 10.1074/jbc.273.24.14813 1:CAS:528:DyaK1cXktVeis70%3D 9614082 (Pubitemid 28272768)
18. J Furuhjelm J Peränen 2003 The C-terminal end of R-Ras contains a focal adhesion targeting signal J Cell Sci 116 3729 3738 10.1242/jcs.00689 1:CAS:528:DC%2BD3sXnvVWhu7s%3D 12890755 (Pubitemid 37185302)
19. Garcia MG, Toney SJ, Hille MB (2004) Focal adhesion kinase (FAK) expression and phosphorylation in sea urchin embryos. Gene Expr Patterns 4:223-234
20. B Haimovich N Kaneshiki P Li 1996 Protein kinase C regulates tyrosine phosphorylation of pp 125FAK in platelets adherent to fibrinogen Blood 87 152 161 1:CAS:528:DyaK28Xit1Sjtw%3D%3D 8547637
21. H Haller C Lindschau C Maasch H Olthoff D Kurscheid FC Luft 1998 Integrin-induced protein kinase Cα and Cε translocation to focal adhesions mediates vascular smooth muscle cell spreading Circ Res 82 157 165 1:CAS:528:DyaK1cXptlOmtQ%3D%3D 9468186
22. DS Harburger DA Calderwood 2009 Integrin signalling at a glance J Cell Sci 122 159 163 10.1242/jcs.018093 1:CAS:528:DC%2BD1MXit1GqtLw%3D 19118207
23. MC Heidkamp AL Bayer BT Scully DM Eble AM Samarel 2003 Activation of focal adhesion kinase by protein kinase C epsilon in neonatal rat ventricular myocytes Am J Physiol Heart Lung Physiol 285 H1684 H1696 1:CAS:528: DC%2BD3sXosVKjtbw%3D
24. JE Humphries E Elizondo TP Yoshino 2001 Protein kinase C regulation of cell spreading in the molluscan Biomphalaria glabrata embryonic (Bge) cell line Biochim Biophys Acta 1540 243 252 10.1016/S0167-4889(01)00136-7 1:CAS:528:DC%2BD3MXnt1Shtrc%3D 11583819 (Pubitemid 32913633)
25. P Irving JM Ubeda D Doucet L Troxler D Zachary JA Hoffman C Hetru M Meister 2005 New insights into Drosophila larval haemocyte functions through genome-wide analysis Cell Microbiol 7 335 350 10.1111/j.1462-5822.2004.00462.x 1:CAS:528:DC%2BD2MXhs1Knsbg%3D 15679837 (Pubitemid 40277914)
26. 2 production and downstream ERK activation J Exp Biol 209 4829 4840 10.1242/jeb.02561 1:CAS:528:DC%2BD2sXhvVGjurg%3D 17142672 (Pubitemid 46166711)
27. I Lamprou I Mamali K Dallas V Fertakis M Lampropoulou VJ Marmaras 2007 Distinct signalling pathways promote phagocytosis of bacteria, latex beads and lipopolysaccharide in medfly haemocytes Immunology 121 314 327 10.1111/j.1365-2567.2007.02576.x 1:CAS:528:DC%2BD2sXntV2ksrw%3D 17376199 (Pubitemid 46817353)
28. V Lardans E Serra A Capron C Dissous 1998 Characterization of an intracellular receptor for activated protein kinase C (RACK) from the mollusc Biomphalaria glabrata, the intermediate host for Schistosoma mansoni Exp Parasitol 88 194 199 10.1006/expr.1998.4236 1:CAS:528:DyaK1cXislersL0%3D 9562422 (Pubitemid 28375786)
29. C Larsson 2006 Protein kinase C and the regulation of the actin cytoskeleton Cell Signal 18 276 284 10.1016/j.cellsig.2005.07.010 1:CAS:528:DC%2BD2MXht1GhsL7P 16109477 (Pubitemid 41661343)
30. MD Lavine MR Strand 2003 Haemocytes from Pseudoplusia includens express multiple α and β integrin subunits Insect Mol Biol 12 441 452 10.1046/j.1365-2583.2003.00428.x 1:CAS:528:DC%2BD3sXotVSqsrg%3D 12974949 (Pubitemid 37207551)
31. MS Lee YB Kim SY Lee JG Kim SH Kim SK Ye JW Lee 2006 Integrin signaling and cell spreading mediated by phorbol 12-myristate 13-acetate treatment J Cell Biochem 99 88 95 10.1002/jcb.20830 1:CAS:528:DC%2BD28XovVKqsLg%3D 16598791 (Pubitemid 44297952)
32. J Liliental DD Chang 1998 RACK1, a receptor for activated protein kinase, interacts with integrin β subunits J Biol Chem 273 2379 2383 10.1074/jbc.273.4.2379 1:CAS:528:DyaK1cXnsVKktw%3D%3D 9442085 (Pubitemid 28069294)
33. V Mahairaki G Lycett C Blass C Louis 2001 Beta-integrin of Anopheles gambiae: mRNA cloning and analysis of structure and expression Insect Mol Biol 10 217 223 10.1046/j.1365-2583.2001.00259.x 1:CAS:528:DC%2BD3MXlt1ahur4%3D 11437913 (Pubitemid 32602226)
34. G Martiny-Baron MG Kazanietz H Mischak PM Blumberg G Kochs H Hug D Marmé C Schächtele 1993 Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976 J Biol Chem 268 9194 9197 1:CAS:528:DyaK3sXkvV2ktrs%3D 8486620
35. SK Mitra DD Schlaepfer 2006 Integrin-regulated FAK-Src signaling in normal and cancer cells Curr Opin Cell Biol 18 516 523 10.1016/j.ceb.2006.08.011 1:CAS:528:DC%2BD28XpsVOjtL8%3D 16919435 (Pubitemid 44332916)
36. D Mochly-Rosen AS Gordon 1998 Anchoring proteins for protein kinase: a means of isozyme selectivity FASEB J 12 35 42 1:CAS:528:DyaK1cXktFKgtw%3D%3D 9438408
37. Z Mostafavi-Pour JA Askari SJ Parkinson PJ Parker TTC Ng MJ Humphries 2003 Integrin-specific signaling pathways controlling focal adhesion formation and cell migration J Cell Biol 161 155 167 10.1083/jcb.200210176 1:CAS:528:DC%2BD3sXjtVait7Y%3D 12695503 (Pubitemid 36459088)
38. ED Motley SM Kabir CD Gardner K Eguchi GD Frank T Kuroki M Ohba T Yamakawa S Eguchi 2002 Lysophosphatidylcholine inhibits insulin-induced Akt activation through protein kinase C-α in vascular smooth muscle cells Hypertension 39 508 512 10.1161/hy02t2.102907 1:CAS:528:DC%2BD38Xhs1Wltbw%3D 11882599 (Pubitemid 34165174)
39. Myat MM, Anderson S, Allen LA, Aderem A (1997) MARCKS regulates membrane ruffling and cell spreading. Curr Biol 7:611-614
40. LD Plows RT Cook AJ Davies AJ Walker 2005 Carbohydrates that mimic schistosome surface coat components affect ERK and PKC signalling in Lymnaea stagnalis haemocytes Int J Parasitol 35 293 302 10.1016/j.ijpara.2004.11.012 1:CAS:528:DC%2BD2MXhslCisLk%3D 15722081 (Pubitemid 40250213)
41. LD Plows RT Cook AJ Davies AJ Walker 2006 Phagocytosis by Lymnaea stagnalis haemocytes: a potential role for phosphatidylinositol 3-kinase but not protein kinase A J Invert Pathol 91 74 77 10.1016/j.jip.2005.10.011 1:CAS:528:DC%2BD28XkvFak (Pubitemid 43003835)
42. LD Plows RT Cook AJ Davies AJ Walker 2006 Integrin engagement modulates the phosphorylation of focal adhesion kinase, phagocytosis, and cell spreading in molluscan defence cells Biochim Biophys Acta 1763 779 786 10.1016/j.bbamcr.2006.04.008 1:CAS:528:DC%2BD28XotlWhs7c%3D 16766054 (Pubitemid 44205271)
43. A Richardson JT Parsons 1996 A mechanism for regulation of the adhesion-associated protein tyrosine kinase pp 125FAK Nature 380 538 540 10.1038/380538a0 1:CAS:528:DyaK28Xit1OlsLw%3D 8606775 (Pubitemid 26110644)
44. N Rucci C DiGiacinto L Orrù D Millimaggi R Baron A Teti 2005 A novel protein kinase C α-dependent signal to ERK1/2 activated by αvβ3 integrin in osteoclasts and in Chinese hamster ovary (CHO) cells J Cell Sci 118 3263 3275 10.1242/jcs.02436 1:CAS:528:DC%2BD2MXpvFKmtr0%3D 16014375 (Pubitemid 41246084)
45. DD Schlaepfer SK Hanks T Hunter P Vandergeer 1994 Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase Nature 372 786 791 1:CAS:528:DyaK2MXivVSjsrg%3D 7997267
46. Y Shimizu DM Rose MH Grinsberg 1999 Integrins in the immune system Adv Immunol 72 325 380 10.1016/S0065-2776(08)60024-3 1:CAS:528:DyaK1MXlsFGktr8%3D 10361579
47. A Siah R Masson B Loup F Bultelle J Pellerin F Leboulenger JM Danger 2007 Receptor activated C kinase is down-regulated in the male gonad of the marine bivalve mollusc Mya arenaria exposed to tributyltin (TBT) Aquat Toxicol 83 295 305 10.1016/j.aquatox.2007.05.003 1:CAS:528:DC%2BD2sXnsFKnsLc%3D 17582516 (Pubitemid 47016692)
48. T Sminia 1972 Structure and function of blood and connective tissue cells of the freshwater pulmonate Lymnaea stagnalis studies by electron microscopy and enzyme histochemistry Z Zellforsch Mikrosk Anat 130 497 526 10.1007/BF00307004 1:STN:280:DyaE3s%2FivFCmtQ%3D%3D 4117131
49. K Terahara KG Takahashi K Mori 2005 Pacific oyster haemocytes undergo apoptosis following cell adhesion mediated by integrin-like molecules Comp Biochem Physiol A 141 215 222 10.1016/j.cbpb.2005.05.040 (Pubitemid 40965755)
50. CN Torgler M Narasimha AL Knox CG Zervas MC Vernon NH Brown 2004 Tensin stabilizes integrin adhesive contacts in Drosophila Dev Cell 6 357 369 10.1016/S1534-5807(04)00055-3 1:CAS:528:DC%2BD2cXis1Kms7Y%3D 15030759 (Pubitemid 38364568)
51. I Vlisidou AJ Dowling IR Evans N Waterfield RH Ffrench-Constant W Wood 2009 Drosophila embryos as model systems for monitoring bacterial infection in real time PLoS Path 5 e1000518 10.1371/journal.ppat.1000518
52. AJ Walker 2006 Do trematode parasites disrupt defence-cell signalling in their snail hosts? Trends Parasitol 22 154 159 10.1016/j.pt.2006.02.003 1:CAS:528:DC%2BD28XivVartrk%3D 16488192
53. AJ Walker LD Plows 2003 Bacterial lipopolysaccharide modulates protein kinase C signalling in Lymnaea stagnalis haemocytes Biol Cell 95 527 533 10.1016/j.biolcel.2003.09.001 1:CAS:528:DC%2BD3sXptVGqs74%3D 14630390 (Pubitemid 37461483)
54. W Wood C Faria A Jacinto 2006 Distinct mechanisms regulate haemocyte chemotaxis during development and wound healing in Drosophila melanogaster J Cell Biol 173 405 416 10.1083/jcb.200508161 1:CAS:528:DC%2BD28Xks1OjsLg%3D 16651377
55. B Wright AH Lacchini AJ Davies AJ Walker 2006 Regulation of nitric oxide production in snail (Lymnaea stagnalis) defence cells: a role for PKC and ERK signalling pathways Biol Cell 98 265 278 10.1042/BC20050066 1:CAS:528: DC%2BD28XjsFGls7g%3D 16293103
56. Z Zahoor AJ Davies RS Kirk D Rollinson AJ Walker 2008 Disruption of ERK signalling in Biomphalaria glabrata defence cells by Schistosoma mansoni: Implications for parasite survival in the snail host Dev Comp Immunol 32 1561 1571 10.1016/j.dci.2008.05.014 1:CAS:528:DC%2BD1cXhtVejtrjF 18619674
57. Z Zahoor AJ Davies RS Kirk D Rollinson AJ Walker 2009 Nitric oxide production by Biomphalaria glabrata haemocytes: effects of Schistosoma mansoni ESPs and regulation through the extracellular signal-regulated kinase pathway Parasites Vectors 2 18 10.1186/1756-3305-2-18 19386102
58. S Zhuang L Kelo JB Nardi MR Kanost 2008 Multiple α subunits of integrin are involved in cell-mediated responses of the Manduca immune system Dev Comp Immunol 32 365 379 10.1016/j.dci.2007.07.007 1:CAS:528: DC%2BD2sXhsVOrurzM 17868866 (Pubitemid 350296328)