Identification and characterization of a unique role for EDB fibronectin in phagocytosis

Journal of Molecular Medicine

Volumn 94, Issue 5, 2016, Pages 567-581

  Kraft, Sabrina ^a,b   Klemis, Verena ^a,b   Sens, Carla ^a,b   Lenhard, Thorsten ^b   Jacobi, Christian ^b,c   Samstag, Yvonne ^b   Wabnitz, Guido ^b   Kirschfink, Michael ^b   Wallich, Reinhard ^b   Hänsch, G Maria ^b   Nakchbandi, Inaam A ^a,b  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c KRANKENHAUS NORDWEST   (Germany)

Author keywords

Bacterial infection; Circulation; EDB; EIIIB; Fibronectin; Innate immunity; Phagocytosis; Plasma fibronectin; v 3 integrin

Indexed keywords

BETA3 INTEGRIN; EXTRA DOMAIN B; FIBRONECTIN; MESSENGER RNA; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR; ACTIN; PROTEIN BINDING;

ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL MENINGITIS; CEREBROSPINAL FLUID; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTRACELLULAR SIGNALING; LISTERIA MONOCYTOGENES; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; PHAGOCYTOSIS; PROTEIN ANALYSIS; RNA ANALYSIS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; ANIMAL; CASE CONTROL STUDY; CHEMISTRY; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSGENIC MOUSE;

ACTINS; ANIMALS; CASE-CONTROL STUDIES; FIBRONECTINS; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; INTEGRIN BETA3; MENINGITIS, BACTERIAL; MICE; MICE, TRANSGENIC; PHAGOCYTOSIS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84949493578     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-015-1373-0     Document Type: Article

References (57)

1. Johansson S, Svineng G, Wennerberg K, Armulik A, Lohikangas L (1997) Fibronectin-integrin interactions. Front Biosci 2:d126–146
2. Bentmann A, Kawelke N, Moss D, Zentgraf H, Bala Y, Berger I, Gasser JA, Nakchbandi IA (2010) Circulating fibronectin affects bone matrix, whereas osteoblast fibronectin modulates osteoblast function. J Bone Miner Res 25:706–715
3. von Au A, Vasel M, Kraft S, Sens C, Hackl N, Marx A, Stroebel P, Hennenlotter J, Todenhofer T, Stenzl A et al (2013) Circulating fibronectin controls tumor growth. Neoplasia 15:925–938
4. Astrof S, Crowley D, George EL, Fukuda T, Sekiguchi K, Hanahan D, Hynes RO (2004) Direct test of potential roles of EIIIA and EIIIB alternatively spliced segments of fibronectin in physiological and tumor angiogenesis. Mol Cell Biol 24:8662–8670
5. Astrof S, Crowley D, Hynes RO (2007) Multiple cardiovascular defects caused by the absence of alternatively spliced segments of fibronectin. Dev Biol 311:11–24
6. Villa A, Trachsel E, Kaspar M, Schliemann C, Sommavilla R, Rybak JN, Rosli C, Borsi L, Neri D (2008) A high-affinity human monoclonal antibody specific to the alternatively spliced EDA domain of fibronectin efficiently targets tumor neo-vasculature in vivo. Int J Cancer 122:2405–2413
7. Sauer S, Erba PA, Petrini M, Menrad A, Giovannoni L, Grana C, Hirsch B, Zardi L, Paganelli G, Mariani G et al (2009) Expression of the oncofetal ED-B-containing fibronectin isoform in hematologic tumors enables ED-B-targeted 131I-L19SIP radioimmunotherapy in Hodgkin lymphoma patients. Blood 113:2265–2274
8. Olsen AL, Sackey BK, Marcinkiewicz C, Boettiger D, Wells RG (2012) Fibronectin extra domain-A promotes hepatic stellate cell motility but not differentiation into myofibroblasts. Gastroenterology 142(928–937), e923
9. Kanters SD, Banga JD, Algra A, Frijns RC, Beutler JJ, Fijnheer R (2001) Plasma levels of cellular fibronectin in diabetes. Diabetes Care 24:323–327
10. Leiss M, Beckmann K, Giros A, Costell M, Fassler R (2008) The role of integrin binding sites in fibronectin matrix assembly in vivo. Curr Opin Cell Biol 20:502–507
11. Henderson B, Nair S, Pallas J, Williams MA (2011) Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol Rev 35:147–200
12. Jett BD, Gilmore MS (2002) Internalization of Staphylococcus aureus by human corneal epithelial cells: role of bacterial fibronectin-binding protein and host cell factors. Infect Immun 70:4697–4700
13. Sheen TR, Ebrahimi CM, Hiemstra IH, Barlow SB, Peschel A, Doran KS (2010) Penetration of the blood–brain barrier by Staphylococcus aureus: contribution of membrane-anchored lipoteichoic acid. J Mol Med 88:633–639
14. Shinji H, Seki K, Tajima A, Uchida A, Masuda S (2003) Fibronectin bound to the surface of Staphylococcus aureus induces association of very late antigen 5 and intracellular signaling factors with macrophage cytoskeleton. Infect Immun 71:140–146
15. Virtanen I, Tervo K, Korhonen M, Paallysaho T, Tervo T (1992) Integrins as receptors for extracellular matrix proteins in human cornea. Acta Ophthalmol Suppl: 18–21
16. Proctor RA (1987) Fibronectin: an enhancer of phagocyte function. Rev Infect Dis 9(Suppl 4):S412–419
17. Pommier CG, Inada S, Fries LF, Takahashi T, Frank MM, Brown EJ (1983) Plasma fibronectin enhances phagocytosis of opsonized particles by human peripheral blood monocytes. J Exp Med 157:1844–1854
18. Jones HE, Strid J, Osman M, Uronen-Hansson H, Dixon G, Klein N, Wong SY, Callard RE (2008) The role of beta2 integrins and lipopolysaccharide-binding protein in the phagocytosis of dead Neisseria meningitidis. Cell Microbiol 10:1634–1645
19. Schymeinsky J, Gerstl R, Mannigel I, Niedung K, Frommhold D, Panthel K, Heesemann J, Sixt M, Quast T, Kolanus W et al (2009) A fundamental role of mAbp1 in neutrophils: impact on beta(2) integrin-mediated phagocytosis and adhesion in vivo. Blood 114:4209–4220
20. Williams MA, Solomkin JS (1999) Integrin-mediated signaling in human neutrophil functioning. J Leukoc Biol 65:725–736
21. Garcia-Garcia E, Rosales C (2002) Signal transduction during Fc receptor-mediated phagocytosis. J Leukoc Biol 72:1092–1108
22. Foukas LC, Katsoulas HL, Paraskevopoulou N, Metheniti A, Lambropoulou M, Marmaras VJ (1998) Phagocytosis of Escherichia coli by insect hemocytes requires both activation of the Ras/mitogen-activated protein kinase signal transduction pathway for attachment and beta3 integrin for internalization. J Biol Chem 273:14813–14818
23. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S (2002) Identification of a factor that links apoptotic cells to phagocytes. Nature 417:182–187
24. Blystone SD, Slater SE, Williams MP, Crow MT, Brown EJ (1999) A molecular mechanism of integrin crosstalk: alphavbeta3 suppression of calcium/calmodulin-dependent protein kinase II regulates alpha5beta1 function. J Cell Biol 145:889–897
25. Kawelke N, Vasel M, Sens C, von Au A, Dooley S, Nakchbandi IA (2011) Fibronectin protects from excessive liver fibrosis by modulating the availability of and responsiveness of stellate cells to active TGF-beta. PLoS One 6, e28181
26. Bungartz G, Stiller S, Bauer M, Muller W, Schippers A, Wagner N, Fassler R, Brakebusch C (2006) Adult murine hematopoiesis can proceed without beta1 and beta7 integrins. Blood 108:1857–1864
27. Kawelke N, Bentmann A, Hackl N, Hager HD, Feick P, Geursen A, Singer MV, Nakchbandi IA (2008) Isoform of fibronectin mediates bone loss in patients with primary biliary cirrhosis by suppressing bone formation. J Bone Miner Res 23:1278–1286
28. Hodivala-Dilke KM, McHugh KP, Tsakiris DA, Rayburn H, Crowley D, Ullman-Cullere M, Ross FP, Coller BS, Teitelbaum S, Hynes RO (1999) Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest 103:229–238
29. Wagner C, Kaksa A, Muller W, Denefleh B, Heppert V, Wentzensen A, Hansch GM (2004) Polymorphonuclear neutrophils in posttraumatic osteomyelitis: cells recovered from the inflamed site lack chemotactic activity but generate superoxides. Shock 22:108–115
30. Schiller HB, Friedel CC, Boulegue C, Fassler R (2011) Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep 12:259–266
31. Hackl NJ, Bersch C, Feick P, Antoni C, Franke A, Singer MV, Nakchbandi IA (2010) Circulating fibronectin isoforms predict the degree of fibrosis in chronic hepatitis C. Scand J Gastroenterol 45:349–356
32. Goos M, Lange P, Hanisch UK, Prinz M, Scheffel J, Bergmann R, Ebert S, Nau R (2007) Fibronectin is elevated in the cerebrospinal fluid of patients suffering from bacterial meningitis and enhances inflammation caused by bacterial products in primary mouse microglial cell cultures. J Neurochem 102:2049–2060
33. Gervais A, Schuller E (1991) Fibronectin in plasma and CSF: evidence for its intrathecal synthesis. J Neurol Sci 105:200–205
34. Bruno A, Shah N, Lin C, Close B, Hess DC, Davis K, Baute V, Switzer JA, Waller JL, Nichols FT (2010) Improving modified Rankin Scale assessment with a simplified questionnaire. Stroke 41:1048–1050
35. Bonsu BK, Ortega HW, Marcon MJ, Harper MB (2008) A decision rule for predicting bacterial meningitis in children with cerebrospinal fluid pleocytosis when gram stain is negative or unavailable. Acad Emerg Med 15:437–444
36. Wagner C, Pioch M, Meyer C, Iking-Konert C, Andrassy K, Hansch GM (2000) Differentiation of polymorphonuclear neutrophils in patients with systemic infections and chronic inflammatory diseases: evidence of prolonged life span and de novo synthesis of fibronectin. J Mol Med 78:337–345
37. Borregaard N, Lollike K, Kjeldsen L, Sengelov H, Bastholm L, Nielsen MH, Bainton DF (1993) Human neutrophil granules and secretory vesicles. Eur J Haematol 51:187–198
38. Cramer E, Pryzwansky KB, Villeval JL, Testa U, Breton-Gorius J (1985) Ultrastructural localization of lactoferrin and myeloperoxidase in human neutrophils by immunogold. Blood 65:423–432
39. Wagner C, Burger A, Radsak M, Blum S, Hug F, Hansch GM (2000) Fibronectin synthesis by activated T lymphocytes: up-regulation of a surface-associated isoform with signalling function. Immunology 99:532–539
40. Adair BD, Xiong JP, Maddock C, Goodman SL, Arnaout MA, Yeager M (2005) Three-dimensional EM structure of the ectodomain of integrin {alpha}V{beta}3 in a complex with fibronectin. J Cell Biol 168:1109–1118
41. Reyes-Reyes M, Mora N, Gonzalez G, Rosales C (2002) beta1 and beta2 integrins activate different signalling pathways in monocytes. Biochem J 363:273–280
42. Mendoza MC, Vilela M, Juarez JE, Blenis J, Danuser G (2015) ERK reinforces actin polymerization to power persistent edge protrusion during motility. Sci Signal 8: ra47
43. Lefort CT, Hyun YM, Schultz JB, Law FY, Waugh RE, Knauf PA, Kim M (2009) Outside-in signal transmission by conformational changes in integrin Mac-1. J Immunol 183:6460–6468
44. Torre D, Zeroli C, Issi M, Fiori GP, Ferraro G, Speranza F (1991) Cerebrospinal fluid concentration of fibronectin in meningitis. J Clin Pathol 44:783–784
45. Pupek M, Jasonek J, Katnik-Prastowska I (2013) EDA-containing fibronectin levels in the cerebrospinal fluid of children with meningitis. Ann Clin Lab Sci 43:257–266
46. Verbrugh HA, Peterson PK, Smith DE, Nguyen BY, Hoidal JR, Wilkinson BJ, Verhoef J, Furcht LT (1981) Human fibronectin binding to staphylococcal surface protein and its relative inefficiency in promoting phagocytosis by human polymorphonuclear leukocytes, monocytes, and alveolar macrophages. Infect Immun 33:811–819
47. Manabe R, Ohe N, Maeda T, Fukuda T, Sekiguchi K (1997) Modulation of cell-adhesive activity of fibronectin by the alternatively spliced EDA segment. J Cell Biol 139:295–307
48. Datta A, Huber F, Boettiger D (2002) Phosphorylation of beta3 integrin controls ligand binding strength. J Biol Chem 277:3943–3949
49. Dogic D, Rousselle P, Aumailley M (1998) Cell adhesion to laminin 1 or 5 induces isoform-specific clustering of integrins and other focal adhesion components. J Cell Sci 111(Pt 6):793–802
50. Gao B, Curtis TM, Blumenstock FA, Minnear FL, Saba TM (2000) Increased recycling of (alpha)5(beta)1 integrins by lung endothelial cells in response to tumor necrosis factor. J Cell Sci 113(Pt 2):247–257
51. Bridgewater RE, Norman JC, Caswell PT (2012) Integrin trafficking at a glance. J Cell Sci 125:3695–3701
52. Caswell PT, Chan M, Lindsay AJ, McCaffrey MW, Boettiger D, Norman JC (2008) Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J Cell Biol 183:143–155
53. Muller PA, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S, Lukashchuk N, Gillespie DA, Ludwig RL, Gosselin P et al (2009) Mutant p53 drives invasion by promoting integrin recycling. Cell 139:1327–1341
54. Vaudaux PE, Waldvogel FA, Morgenthaler JJ, Nydegger UE (1984) Adsorption of fibronectin onto polymethylmethacrylate and promotion of Staphylococcus aureus adherence. Infect Immun 45:768–774
55. Vaudaux P, Pittet D, Haeberli A, Huggler E, Nydegger UE, Lew DP, Waldvogel FA (1989) Host factors selectively increase staphylococcal adherence on inserted catheters: a role for fibronectin and fibrinogen or fibrin. J Infect Dis 160:865–875
56. Stuart LM, Ezekowitz RA (2005) Phagocytosis: elegant complexity. Immunity 22:539–550
57. Ortiz-Stern A, Rosales C (2003) Cross-talk between Fc receptors and integrins. Immunol Lett 90:137–143