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Review

Membrane tubulovesicular extensions (cytonemes)

Secretory and adhesive cellular organelles

, , &
Pages 174-186 | Received 13 Aug 2012, Accepted 05 Dec 2012, Published online: 03 Jan 2013

References

  • Gustafson T, Wolpert L. Cellular movement and contact in sea urchin morphogenesis. Biol Rev Camb Philos Soc 1967; 42:442 - 98; http://dx.doi.org/10.1111/j.1469-185X.1967.tb01482.x; PMID: 4864367
  • Solursh M, Lane MC. Extracellular matrix triggers a directed cell migratory response in sea urchin primary mesenchyme cells. Dev Biol 1988; 130:397 - 401; http://dx.doi.org/10.1016/0012-1606(88)90445-9; PMID: 3181638
  • Miller J, Fraser SE, McClay D. Dynamics of thin filopodia during sea urchin gastrulation. Development 1995; 121:2501 - 11; PMID: 7671814
  • Ramírez-Weber FA, Kornberg TB. Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 1999; 97:599 - 607; PMID: 10367889
  • Shao JY, Hochmuth RM. Micropipette suction for measuring piconewton forces of adhesion and tether formation from neutrophil membranes. Biophys J 1996; 71:2892 - 901; http://dx.doi.org/10.1016/S0006-3495(96)79486-9; PMID: 8913626
  • Shao JY, Ting-Beall HP, Hochmuth RM. Static and dynamic lengths of neutrophil microvilli. Proc Natl Acad Sci U S A 1998; 95:6797 - 802; http://dx.doi.org/10.1073/pnas.95.12.6797; PMID: 9618492
  • Schmidtke DW, Diamond SL. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J Cell Biol 2000; 149:719 - 30; http://dx.doi.org/10.1083/jcb.149.3.719; PMID: 10791984
  • Galkina SI, Sud’ina GF, Ullrich V. Inhibition of neutrophil spreading during adhesion to fibronectin reveals formation of long tubulovesicular cell extensions (cytonemes). Exp Cell Res 2001; 266:222 - 8; http://dx.doi.org/10.1006/excr.2001.5227; PMID: 11399050
  • Marcus WD, Hochmuth RM. Experimental studies of membrane tethers formed from human neutrophils. Ann Biomed Eng 2002; 30:1273 - 80; http://dx.doi.org/10.1114/1.1528614; PMID: 12540203
  • Park EY, Smith MJ, Stropp ES, Snapp KR, DiVietro JA, Walker WF, et al. Comparison of PSGL-1 microbead and neutrophil rolling: microvillus elongation stabilizes P-selectin bond clusters. Biophys J 2002; 82:1835 - 47; http://dx.doi.org/10.1016/S0006-3495(02)75534-3; PMID: 11916843
  • Gupta N, DeFranco AL. Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation. Mol Biol Cell 2003; 14:432 - 44; http://dx.doi.org/10.1091/mbc.02-05-0078; PMID: 12589045
  • Marcus WD, McEver RP, Zhu C. Forces required to initiate membrane tether extrusion from cell surface depend on cell type but not on the surface molecule. Mech Chem Biosyst 2004; 1:245 - 51; PMID: 16783921
  • Ramachandran V, Williams M, Yago T, Schmidtke DW, McEver RP. Dynamic alterations of membrane tethers stabilize leukocyte rolling on P-selectin. Proc Natl Acad Sci U S A 2004; 101:13519 - 24; http://dx.doi.org/10.1073/pnas.0403608101; PMID: 15353601
  • Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science 2004; 303:1007 - 10; http://dx.doi.org/10.1126/science.1093133; PMID: 14963329
  • Onfelt B, Nedvetzki S, Yanagi K, Davis DM. Cutting edge: Membrane nanotubes connect immune cells. J Immunol 2004; 173:1511 - 3; PMID: 15265877
  • Onfelt B, Nedvetzki S, Benninger RK, Purbhoo MA, Sowinski S, Hume AN, et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J Immunol 2006; 177:8476 - 83; PMID: 17142745
  • Wittig D, Wang X, Walter C, Gerdes HH, Funk RH, Roehlecke C. Multi-level communication of human retinal pigment epithelial cells via tunneling nanotubes. PLoS One 2012; 7:e33195; http://dx.doi.org/10.1371/journal.pone.0033195; PMID: 22457742
  • Watkins SC, Salter RD. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 2005; 23:309 - 18; http://dx.doi.org/10.1016/j.immuni.2005.08.009; PMID: 16169503
  • Veranic P, Lokar M, Schütz GJ, Weghuber J, Wieser S, Hägerstrand H, et al. Different types of cell-to-cell connections mediated by nanotubular structures. Biophys J 2008; 95:4416 - 25; http://dx.doi.org/10.1529/biophysj.108.131375; PMID: 18658210
  • Hurtig J, Chiu DT, Onfelt B. Intercellular nanotubes: insights from imaging studies and beyond. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2010; 2:260 - 76; http://dx.doi.org/10.1002/wnan.80; PMID: 20166114
  • Xu G, Shao JY. Human neutrophil surface protrusion under a point load: location independence and viscoelasticity. Am J Physiol Cell Physiol 2008; 295:C1434 - 44; http://dx.doi.org/10.1152/ajpcell.00136.2008; PMID: 18815230
  • Liu B, Goergen CJ, Shao JY. Effect of temperature on tether extraction, surface protrusion, and cortical tension of human neutrophils. Biophys J 2007; 93:2923 - 33; http://dx.doi.org/10.1529/biophysj.107.105346; PMID: 17586566
  • Edmondson KE, Denney WS, Diamond SL. Neutrophil-bead collision assay: pharmacologically induced changes in membrane mechanics regulate the PSGL-1/P-selectin adhesion lifetime. Biophys J 2005; 89:3603 - 14; http://dx.doi.org/10.1529/biophysj.105.066134; PMID: 16100264
  • Oh H, Diamond SL. Ethanol enhances neutrophil membrane tether growth and slows rolling on P-selectin but reduces capture from flow and firm arrest on IL-1-treated endothelium. J Immunol 2008; 181:2472 - 82; PMID: 18684938
  • Oh H, Mohler ER 3rd, Tian A, Baumgart T, Diamond SL. Membrane cholesterol is a biomechanical regulator of neutrophil adhesion. Arterioscler Thromb Vasc Biol 2009; 29:1290 - 7; http://dx.doi.org/10.1161/ATVBAHA.109.189571; PMID: 19667108
  • Galkina SI, Molotkovsky JG, Ullrich V, Sud’ina GF. Scanning electron microscopy study of neutrophil membrane tubulovesicular extensions (cytonemes) and their role in anchoring, aggregation and phagocytosis. The effect of nitric oxide. Exp Cell Res 2005; 304:620 - 9; http://dx.doi.org/10.1016/j.yexcr.2004.12.005; PMID: 15748905
  • Galkina SI, Romanova JM, Stadnichuk VI, Molotkovsky JG, Sud’ina GF, Klein T. Nitric oxide-induced membrane tubulovesicular extensions (cytonemes) of human neutrophils catch and hold Salmonella enterica serovar Typhimurium at a distance from the cell surface. FEMS Immunol Med Microbiol 2009; 56:162 - 71; http://dx.doi.org/10.1111/j.1574-695X.2009.00560.x; PMID: 19453754
  • Galkina SI, Stadnichuk VI, Molotkovsky JG, Romanova JM, Sud’ina GF, Klein T. Microbial alkaloid staurosporine induces formation of nanometer-wide membrane tubular extensions (cytonemes, membrane tethers) in human neutrophils. Cell Adh Migr 2010; 4:32 - 8; http://dx.doi.org/10.4161/cam.4.1.10314; PMID: 20009568
  • Galkina SI, Fedorova NV, Serebryakova MV, Romanova JM, Golyshev SA, Stadnichuk VI, et al. Proteome analysis identified human neutrophil membrane tubulovesicular extensions (cytonemes, membrane tethers) as bactericide trafficking. Biochim Biophys Acta 2012; 1820:1705 - 14; http://dx.doi.org/10.1016/j.bbagen.2012.06.016; PMID: 22766193
  • Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532 - 5; http://dx.doi.org/10.1126/science.1092385; PMID: 15001782
  • Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 176:231 - 41; http://dx.doi.org/10.1083/jcb.200606027; PMID: 17210947
  • Nauseef WM. Editorial: Nyet to NETs? A pause for healthy skepticism. J Leukoc Biol 2012; 91:353 - 5; http://dx.doi.org/10.1189/jlb.1011495; PMID: 22379074
  • Rupp I, Sologub L, Williamson KC, Scheuermayer M, Reininger L, Doerig C, et al. Malaria parasites form filamentous cell-to-cell connections during reproduction in the mosquito midgut. Cell Res 2011; 21:683 - 96; http://dx.doi.org/10.1038/cr.2010.176; PMID: 21173797
  • Galkina SI, Romanova JM, Bragina EE, Tiganova IG, Stadnichuk VI, Alekseeva NV, et al. Membrane tubules attach Salmonella Typhimurium to eukaryotic cells and bacteria. FEMS Immunol Med Microbiol 2011; 61:114 - 24; http://dx.doi.org/10.1111/j.1574-695X.2010.00754.x; PMID: 21054581
  • Evans E, Heinrich V, Leung A, Kinoshita K. Nano- to microscale dynamics of P-selectin detachment from leukocyte interfaces. I. Membrane separation from the cytoskeleton. Biophys J 2005; 88:2288 - 98; http://dx.doi.org/10.1529/biophysj.104.051698; PMID: 15653718
  • Galkina SI, Sud’ina GF, Klein T. Metabolic regulation of neutrophil spreading, membrane tubulovesicular extensions (cytonemes) formation and intracellular pH upon adhesion to fibronectin. Exp Cell Res 2006; 312:2568 - 79; http://dx.doi.org/10.1016/j.yexcr.2006.04.011; PMID: 16740258
  • Biswas S, Ray M, Misra S, Dutta DP, Ray S. Is absence of pyruvate dehydrogenase complex in mitochondria a possible explanation of significant aerobic glycolysis by normal human leukocytes?. FEBS Lett 1998; 425:411 - 4; http://dx.doi.org/10.1016/S0014-5793(98)00273-7; PMID: 9563504
  • Nelson N. Structure and pharmacology of the proton-ATPases. Trends Pharmacol Sci 1991; 12:71 - 5; http://dx.doi.org/10.1016/0165-6147(91)90501-I; PMID: 1827218
  • Nishi T, Forgac M. The vacuolar (H+)-ATPases--nature’s most versatile proton pumps. Nat Rev Mol Cell Biol 2002; 3:94 - 103; http://dx.doi.org/10.1038/nrm729; PMID: 11836511
  • Parra KJ, Kane PM. Reversible association between the V1 and V0 domains of yeast vacuolar H+-ATPase is an unconventional glucose-induced effect. Mol Cell Biol 1998; 18:7064 - 74; PMID: 9819393
  • Su Y, Zhou A, Al-Lamki RS, Karet FE. The a-subunit of the V-type H+-ATPase interacts with phosphofructokinase-1 in humans. J Biol Chem 2003; 278:20013 - 8; http://dx.doi.org/10.1074/jbc.M210077200; PMID: 12649290
  • Lu M, Holliday LS, Zhang L, Dunn WA Jr., Gluck SL. Interaction between aldolase and vacuolar H+-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J Biol Chem 2001; 276:30407 - 13; http://dx.doi.org/10.1074/jbc.M008768200; PMID: 11399750
  • Lu M, Sautin YY, Holliday LS, Gluck SL. The glycolytic enzyme aldolase mediates assembly, expression, and activity of vacuolar H+-ATPase. J Biol Chem 2004; 279:8732 - 9; http://dx.doi.org/10.1074/jbc.M303871200; PMID: 14672945
  • Peters C, Bayer MJ, Bühler S, Andersen JS, Mann M, Mayer A. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 2001; 409:581 - 8; http://dx.doi.org/10.1038/35054500; PMID: 11214310
  • Bayer MJ, Reese C, Buhler S, Peters C, Mayer A. Vacuole membrane fusion: V0 functions after trans-SNARE pairing and is coupled to the Ca2+-releasing channel. J Cell Biol 2003; 162:211 - 22; http://dx.doi.org/10.1083/jcb.200212004; PMID: 12876274
  • Hiesinger PR, Fayyazuddin A, Mehta SQ, Rosenmund T, Schulze KL, Zhai RG, et al. The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 2005; 121:607 - 20; http://dx.doi.org/10.1016/j.cell.2005.03.012; PMID: 15907473
  • Liégeois S, Benedetto A, Garnier JM, Schwab Y, Labouesse M. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J Cell Biol 2006; 173:949 - 61; http://dx.doi.org/10.1083/jcb.200511072; PMID: 16785323
  • Liégeois S, Benedetto A, Michaux G, Belliard G, Labouesse M. Genes required for osmoregulation and apical secretion in Caenorhabditis elegans. Genetics 2007; 175:709 - 24; http://dx.doi.org/10.1534/genetics.106.066035; PMID: 17179093
  • Sun-Wada GH, Toyomura T, Murata Y, Yamamoto A, Futai M, Wada Y. The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J Cell Sci 2006; 119:4531 - 40; http://dx.doi.org/10.1242/jcs.03234; PMID: 17046993
  • Baars TL, Petri S, Peters C, Mayer A. Role of the V-ATPase in regulation of the vacuolar fission-fusion equilibrium. Mol Biol Cell 2007; 18:3873 - 82; http://dx.doi.org/10.1091/mbc.E07-03-0205; PMID: 17652457
  • Zhang W, Wang D, Volk E, Bellen HJ, Hiesinger PR, Quiocho FA. V-ATPase V0 sector subunit a1 in neurons is a target of calmodulin. J Biol Chem 2008; 283:294 - 300; http://dx.doi.org/10.1074/jbc.M708058200; PMID: 17933871
  • Glaser PE, Gross RW. Rapid plasmenylethanolamine-selective fusion of membrane bilayers catalyzed by an isoform of glyceraldehyde-3-phosphate dehydrogenase: discrimination between glycolytic and fusogenic roles of individual isoforms. Biochemistry 1995; 34:12193 - 203; http://dx.doi.org/10.1021/bi00038a013; PMID: 7547960
  • Hessler RJ, Blackwood RA, Brock TG, Francis JW, Harsh DM, Smolen JE. Identification of glyceraldehyde-3-phosphate dehydrogenase as a Ca2+-dependent fusogen in human neutrophil cytosol. J Leukoc Biol 1998; 63:331 - 6; PMID: 9500520
  • Glaser PE, Han X, Gross RW. Tubulin is the endogenous inhibitor of the glyceraldehyde 3-phosphate dehydrogenase isoform that catalyzes membrane fusion: Implications for the coordinated regulation of glycolysis and membrane fusion. Proc Natl Acad Sci U S A 2002; 99:14104 - 9; http://dx.doi.org/10.1073/pnas.222542999; PMID: 12381782
  • Nakagawa T, Hirano Y, Inomata A, Yokota S, Miyachi K, Kaneda M, et al. Participation of a fusogenic protein, glyceraldehyde-3-phosphate dehydrogenase, in nuclear membrane assembly. J Biol Chem 2003; 278:20395 - 404; http://dx.doi.org/10.1074/jbc.M210824200; PMID: 12651855
  • Decker BL, Wickner WT. Enolase activates homotypic vacuole fusion and protein transport to the vacuole in yeast. J Biol Chem 2006; 281:14523 - 8; http://dx.doi.org/10.1074/jbc.M600911200; PMID: 16565073
  • Forgac M. The vacuolar H+-ATPase of clathrin-coated vesicles is reversibly inhibited by S-nitrosoglutathione. J Biol Chem 1999; 274:1301 - 5; http://dx.doi.org/10.1074/jbc.274.3.1301; PMID: 9880499
  • Wu K, Aoki C, Elste A, Rogalski-Wilk AA, Siekevitz P. The synthesis of ATP by glycolytic enzymes in the postsynaptic density and the effect of endogenously generated nitric oxide. Proc Natl Acad Sci U S A 1997; 94:13273 - 8; http://dx.doi.org/10.1073/pnas.94.24.13273; PMID: 9371836
  • Mohr S, Hallak H, de Boitte A, Lapetina EG, Brüne B. Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 1999; 274:9427 - 30; http://dx.doi.org/10.1074/jbc.274.14.9427; PMID: 10092623
  • Holliday LS, Lu M, Lee BS, Nelson RD, Solivan S, Zhang L, et al. The amino-terminal domain of the B subunit of vacuolar H+-ATPase contains a filamentous actin binding site. J Biol Chem 2000; 275:32331 - 7; http://dx.doi.org/10.1074/jbc.M004795200; PMID: 10915794
  • Chen SH, Bubb MR, Yarmola EG, Zuo J, Jiang J, Lee BS, et al. Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J Biol Chem 2004; 279:7988 - 98; http://dx.doi.org/10.1074/jbc.M305351200; PMID: 14662773
  • Vitavska O, Merzendorfer H, Wieczorek H. The V-ATPase subunit C binds to polymeric F-actin as well as to monomeric G-actin and induces cross-linking of actin filaments. J Biol Chem 2005; 280:1070 - 6; http://dx.doi.org/10.1074/jbc.M406797200; PMID: 15525650
  • Arnold H, Pette D. Binding of aldolase and triosephosphate dehydrogenase to F-actin and modification of catalytic properties of aldolase. Eur J Biochem 1970; 15:360 - 6; http://dx.doi.org/10.1111/j.1432-1033.1970.tb01016.x; PMID: 5502667
  • Karp GC, Solursh M. Dynamic activity of the filopodia of sea urchin embryonic cells and their role in directed migration of the primary mesenchyme in vitro. Dev Biol 1985; 112:276 - 83; http://dx.doi.org/10.1016/0012-1606(85)90398-7; PMID: 4076544
  • Raghunathan A, Sivakamasundari R, Wolenski J, Poddar R, Weissman SM. Functional analysis of B144/LST1: a gene in the tumor necrosis factor cluster that induces formation of long filopodia in eukaryotic cells. Exp Cell Res 2001; 268:230 - 44; http://dx.doi.org/10.1006/excr.2001.5290; PMID: 11478849
  • Schwan C, Stecher B, Tzivelekidis T, van Ham M, Rohde M, Hardt WD, et al. Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria. PLoS Pathog 2009; 5:e1000626; http://dx.doi.org/10.1371/journal.ppat.1000626; PMID: 19834554
  • Aktories K, Lang AE, Schwan C, Mannherz HG. Actin as target for modification by bacterial protein toxins. FEBS J 2011; 278:4526 - 43; http://dx.doi.org/10.1111/j.1742-4658.2011.08113.x; PMID: 21466657
  • Whipple RA, Cheung AM, Martin SS. Detyrosinated microtubule protrusions in suspended mammary epithelial cells promote reattachment. Exp Cell Res 2007; 313:1326 - 36; http://dx.doi.org/10.1016/j.yexcr.2007.02.001; PMID: 17359970
  • Lian JP, Marks PG, Wang JY, Falls DL, Badwey JA. A protein kinase from neutrophils that specifically recognizes Ser-3 in cofilin. J Biol Chem 2000; 275:2869 - 76; http://dx.doi.org/10.1074/jbc.275.4.2869; PMID: 10644754
  • Messier JM, Shaw LM, Chafel M, Matsudaira P, Mercurio AM. Fimbrin localized to an insoluble cytoskeletal fraction is constitutively phosphorylated on its headpiece domain in adherent macrophages. Cell Motil Cytoskeleton 1993; 25:223 - 33; http://dx.doi.org/10.1002/cm.970250303; PMID: 8221900
  • Jones SL, Brown EJ. FcgammaRII-mediated adhesion and phagocytosis induce L-plastin phosphorylation in human neutrophils. J Biol Chem 1996; 271:14623 - 30; http://dx.doi.org/10.1074/jbc.271.24.14623; PMID: 8663066
  • Shibata M, Ohoka T, Mizuno S, Suzuki K. Characterization of a 64-kd protein phosphorylated during chemotactic activation with IL-8 and fMLP of human polymorphonuclear leukocytes. I. Phosphorylation of a 64-kd protein and other proteins. J Leukoc Biol 1993; 54:1 - 9; PMID: 8393062
  • Paclet MH, Davis C, Kotsonis P, Godovac-Zimmermann J, Segal AW, Dekker LV. N-Formyl peptide receptor subtypes in human neutrophils activate L-plastin phosphorylation through different signal transduction intermediates. Biochem J 2004; 377:469 - 77; http://dx.doi.org/10.1042/BJ20031114; PMID: 14556648
  • Rosales C, Jones SL, McCourt D, Brown EJ. Bromophenacyl bromide binding to the actin-bundling protein l-plastin inhibits inositol trisphosphate-independent increase in Ca2+ in human neutrophils. Proc Natl Acad Sci U S A 1994; 91:3534 - 8; http://dx.doi.org/10.1073/pnas.91.9.3534; PMID: 8170942
  • Gao C, Guo H, Wei J, Mi Z, Wai PY, Kuo PC. Identification of S-nitrosylated proteins in endotoxin-stimulated RAW264.7 murine macrophages. Nitric Oxide 2005; 12:121 - 6; http://dx.doi.org/10.1016/j.niox.2004.11.006; PMID: 15740986
  • Zhang Y, Keszler A, Broniowska KA, Hogg N. Characterization and application of the biotin-switch assay for the identification of S-nitrosated proteins. Free Radic Biol Med 2005; 38:874 - 81; http://dx.doi.org/10.1016/j.freeradbiomed.2004.12.012; PMID: 15749383
  • Clancy R, Leszczynska J, Amin A, Levartovsky D, Abramson SB. Nitric oxide stimulates ADP ribosylation of actin in association with the inhibition of actin polymerization in human neutrophils. J Leukoc Biol 1995; 58:196 - 202; PMID: 7643014
  • Jog NR, Rane MJ, Lominadze G, Luerman GC, Ward RA, McLeish KR. The actin cytoskeleton regulates exocytosis of all neutrophil granule subsets. Am J Physiol Cell Physiol 2007; 292:C1690 - 700; http://dx.doi.org/10.1152/ajpcell.00384.2006; PMID: 17202227
  • Muallem S, Kwiatkowska K, Xu X, Yin HL. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol 1995; 128:589 - 98; http://dx.doi.org/10.1083/jcb.128.4.589; PMID: 7860632
  • Mitchell T, Lo A, Logan MR, Lacy P, Eitzen G. Primary granule exocytosis in human neutrophils is regulated by Rac-dependent actin remodeling. Am J Physiol Cell Physiol 2008; 295:C1354 - 65; http://dx.doi.org/10.1152/ajpcell.00239.2008; PMID: 18799653
  • Jena BP. Discovery of the Porosome: revealing the molecular mechanism of secretion and membrane fusion in cells. J Cell Mol Med 2004; 8:1 - 21; http://dx.doi.org/10.1111/j.1582-4934.2004.tb00255.x; PMID: 15090256
  • Faurschou M, Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 2003; 5:1317 - 27; http://dx.doi.org/10.1016/j.micinf.2003.09.008; PMID: 14613775
  • Lominadze G, Powell DW, Luerman GC, Link AJ, Ward RA, McLeish KR. Proteomic analysis of human neutrophil granules. Mol Cell Proteomics 2005; 4:1503 - 21; http://dx.doi.org/10.1074/mcp.M500143-MCP200; PMID: 15985654
  • Creutz CE. The annexins and exocytosis. Science 1992; 258:924 - 31; http://dx.doi.org/10.1126/science.1439804; PMID: 1439804
  • Francis JW, Balazovich KJ, Smolen JE, Margolis DI, Boxer LA. Human neutrophil annexin I promotes granule aggregation and modulates Ca(2+)-dependent membrane fusion. J Clin Invest 1992; 90:537 - 44; http://dx.doi.org/10.1172/JCI115892; PMID: 1386611
  • Meers P, Mealy T, Tauber AI. Annexin I interactions with human neutrophil specific granules: fusogenicity and coaggregation with plasma membrane vesicles. Biochim Biophys Acta 1993; 1147:177 - 84; http://dx.doi.org/10.1016/0005-2736(93)90002-H; PMID: 8476911
  • Kerkhoff C, Klempt M, Kaever V, Sorg C. The two calcium-binding proteins, S100A8 and S100A9, are involved in the metabolism of arachidonic acid in human neutrophils. J Biol Chem 1999; 274:32672 - 9; http://dx.doi.org/10.1074/jbc.274.46.32672; PMID: 10551823
  • Creutz CE. cis-Unsaturated fatty acids induce the fusion of chromaffin granules aggregated by synexin. J Cell Biol 1981; 91:247 - 56; http://dx.doi.org/10.1083/jcb.91.1.247; PMID: 6457840
  • MacLaren A, Attias M, de Souza W. Aspects of the early moments of interaction between tachyzoites of Toxoplasma gondii with neutrophils. Vet Parasitol 2004; 125:301 - 12; http://dx.doi.org/10.1016/j.vetpar.2004.07.006; PMID: 15482886
  • Ryu JS, Kang JH, Jung SY, Shin MH, Kim JM, Park H, et al. Production of interleukin-8 by human neutrophils stimulated with Trichomonas vaginalis. Infect Immun 2004; 72:1326 - 32; http://dx.doi.org/10.1128/IAI.72.3.1326-1332.2004; PMID: 14977935
  • Frasson AP, De Carli GA, Bonan CD, Tasca T. Involvement of purinergic signaling on nitric oxide production by neutrophils stimulated with Trichomonas vaginalis. Purinergic Signal 2012; 8:1 - 9; http://dx.doi.org/10.1007/s11302-011-9254-7; PMID: 21833696
  • Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007; 87:315 - 424; http://dx.doi.org/10.1152/physrev.00029.2006; PMID: 17237348
  • Jordan JE, Zhao ZQ, Vinten-Johansen J. The role of neutrophils in myocardial ischemia-reperfusion injury. Cardiovasc Res 1999; 43:860 - 78; http://dx.doi.org/10.1016/S0008-6363(99)00187-X; PMID: 10615413
  • Gilcrease MZ, Hoover RL. Neutrophil adhesion to endothelium following hyperosmolar insult. Diabetes Res 1991; 16:149 - 57; PMID: 1802480
  • Kim SY, Johnson MA, McLeod DS, Alexander T, Hansen BC, Lutty GA. Neutrophils are associated with capillary closure in spontaneously diabetic monkey retinas. Diabetes 2005; 54:1534 - 42; http://dx.doi.org/10.2337/diabetes.54.5.1534; PMID: 15855343
  • Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991; 43:109 - 42; PMID: 1852778
  • Sessa WC. The nitric oxide synthase family of proteins. J Vasc Res 1994; 31:131 - 43; http://dx.doi.org/10.1159/000159039; PMID: 7511942
  • Wallerath T, Gath I, Aulitzky WE, Pollock JS, Kleinert H, Förstermann U. Identification of the NO synthase isoforms expressed in human neutrophil granulocytes, megakaryocytes and platelets. Thromb Haemost 1997; 77:163 - 7; PMID: 9031468
  • Greenberg SS, Ouyang J, Zhao X, Giles TD. Human and rat neutrophils constitutively express neural nitric oxide synthase mRNA. Nitric Oxide 1998; 2:203 - 12; http://dx.doi.org/10.1006/niox.1998.0176; PMID: 9731638
  • Lefer DJ, Jones SP, Girod WG, Baines A, Grisham MB, Cockrell AS, et al. Leukocyte-endothelial cell interactions in nitric oxide synthase-deficient mice. Am J Physiol 1999; 276:H1943 - 50; PMID: 10362674
  • Carey C, Siegfried MR, Ma XL, Weyrich AS, Lefer AM. Antishock and endothelial protective actions of a NO donor in mesenteric ischemia and reperfusion. Circ Shock 1992; 38:209 - 16; PMID: 1292885
  • Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A 1991; 88:4651 - 5; http://dx.doi.org/10.1073/pnas.88.11.4651; PMID: 1675786
  • Mitchell DJ, Yu J, Tyml K. Local L-NAME decreases blood flow and increases leukocyte adhesion via CD18. Am J Physiol 1998; 274:H1264 - 8; PMID: 9575930
  • Banick PD, Chen Q, Xu YA, Thom SR. Nitric oxide inhibits neutrophil beta 2 integrin function by inhibiting membrane-associated cyclic GMP synthesis. J Cell Physiol 1997; 172:12 - 24; http://dx.doi.org/10.1002/(SICI)1097-4652(199707)172:1<12::AID-JCP2>3.0.CO;2-G; PMID: 9207921
  • Kubes P, Kurose I, Granger DN. NO donors prevent integrin-induced leukocyte adhesion but not P-selectin-dependent rolling in postischemic venules. Am J Physiol 1994; 267:H931 - 7; PMID: 7522408
  • Kosonen O, Kankaanranta H, Malo-Ranta U, Moilanen E. Nitric oxide-releasing compounds inhibit neutrophil adhesion to endothelial cells. Eur J Pharmacol 1999; 382:111 - 7; http://dx.doi.org/10.1016/S0014-2999(99)00581-6; PMID: 10528145
  • Alam MS, Akaike T, Okamoto S, Kubota T, Yoshitake J, Sawa T, et al. Role of nitric oxide in host defense in murine salmonellosis as a function of its antibacterial and antiapoptotic activities. Infect Immun 2002; 70:3130 - 42; http://dx.doi.org/10.1128/IAI.70.6.3130-3142.2002; PMID: 12011007
  • MacFarlane AS, Schwacha MG, Eisenstein TK. In vivo blockage of nitric oxide with aminoguanidine inhibits immunosuppression induced by an attenuated strain of Salmonella typhimurium, potentiates Salmonella infection, and inhibits macrophage and polymorphonuclear leukocyte influx into the spleen. Infect Immun 1999; 67:891 - 8; PMID: 9916105
  • Vazquez-Torres A, Jones-Carson J, Mastroeni P, Ischiropoulos H, Fang FC. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J Exp Med 2000; 192:227 - 36; http://dx.doi.org/10.1084/jem.192.2.227; PMID: 10899909
  • Klink M, Cedzyński M, St Swierzko A, Tchórzewski H, Sulowska Z. Involvement of nitric oxide donor compounds in the bactericidal activity of human neutrophils in vitro. J Med Microbiol 2003; 52:303 - 8; http://dx.doi.org/10.1099/jmm.0.04974-0; PMID: 12676868
  • McCollister BD, Bourret TJ, Gill R, Jones-Carson J, Vázquez-Torres A. Repression of SPI2 transcription by nitric oxide-producing, IFNgamma-activated macrophages promotes maturation of Salmonella phagosomes. J Exp Med 2005; 202:625 - 35; http://dx.doi.org/10.1084/jem.20050246; PMID: 16129704
  • Stevanin TM, Poole RK, Demoncheaux EA, Read RC. Flavohemoglobin Hmp protects Salmonella enterica serovar typhimurium from nitric oxide-related killing by human macrophages. Infect Immun 2002; 70:4399 - 405; http://dx.doi.org/10.1128/IAI.70.8.4399-4405.2002; PMID: 12117950
  • Bang IS, Liu L, Vazquez-Torres A, Crouch ML, Stamler JS, Fang FC. Maintenance of nitric oxide and redox homeostasis by the salmonella flavohemoglobin hmp. J Biol Chem 2006; 281:28039 - 47; http://dx.doi.org/10.1074/jbc.M605174200; PMID: 16873371
  • Klink M, Bednarska K, Jastrzembska K, Banasik M, Sulowska Z. Signal transduction pathways affected by nitric oxide donors during neutrophil functional response in vitro. Inflamm Res 2007; 56:282 - 90; http://dx.doi.org/10.1007/s00011-007-6205-4; PMID: 17659433
  • Machado JD, Segura F, Brioso MA, Borges R. Nitric oxide modulates a late step of exocytosis. J Biol Chem 2000; 275:20274 - 9; http://dx.doi.org/10.1074/jbc.M000930200; PMID: 10747967
  • Lowenstein CJ. Nitric oxide regulation of protein trafficking in the cardiovascular system. Cardiovasc Res 2007; 75:240 - 6; http://dx.doi.org/10.1016/j.cardiores.2007.03.024; PMID: 17490627
  • Ginocchio CC, Olmsted SB, Wells CL, Galán JE. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 1994; 76:717 - 24; http://dx.doi.org/10.1016/0092-8674(94)90510-X; PMID: 8124710
  • Reed KA, Clark MA, Booth TA, Hueck CJ, Miller SI, Hirst BH, et al. Cell-contact-stimulated formation of filamentous appendages by Salmonella typhimurium does not depend on the type III secretion system encoded by Salmonella pathogenicity island 1. Infect Immun 1998; 66:2007 - 17; PMID: 9573083
  • Follett EA, Gordon J. An Electron Microscope Study of Vibrio Flagella. J Gen Microbiol 1963; 32:235 - 9; http://dx.doi.org/10.1099/00221287-32-2-235; PMID: 14053270
  • Seidler RJ, Starr MP. Structure of the flagellum of Bdellovibrio bacteriovorus. J Bacteriol 1968; 95:1952 - 5; PMID: 5650092
  • Geis G, Suerbaum S, Forsthoff B, Leying H, Opferkuch W. Ultrastructure and biochemical studies of the flagellar sheath of Helicobacter pylori. J Med Microbiol 1993; 38:371 - 7; http://dx.doi.org/10.1099/00222615-38-5-371; PMID: 8487294
  • Allen RD, Baumann P. Structure and arrangement of flagella in species of the genus Beneckea and Photobacterium fischeri. J Bacteriol 1971; 107:295 - 302; PMID: 4105030
  • Sjoblad RD, Emala CW, Doetsch RN. Invited review: bacterial flagellar sheaths: structures in search of a function. Cell Motil 1983; 3:93 - 103; http://dx.doi.org/10.1002/cm.970030108; PMID: 6850813
  • McCarter LL. Polar flagellar motility of the Vibrionaceae. [table of contents.] Microbiol Mol Biol Rev 2001; 65:445 - 62; http://dx.doi.org/10.1128/MMBR.65.3.445-462.2001; PMID: 11528005
  • Jauffred L, Callisen TH, Oddershede LB. Visco-elastic membrane tethers extracted from Escherichia coli by optical tweezers. Biophys J 2007; 93:4068 - 75; http://dx.doi.org/10.1529/biophysj.107.103861; PMID: 17704145
  • Low HH, Löwe J. A bacterial dynamin-like protein. Nature 2006; 444:766 - 9; http://dx.doi.org/10.1038/nature05312; PMID: 17122778
  • Low HH, Sachse C, Amos LA, Löwe J. Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving. Cell 2009; 139:1342 - 52; http://dx.doi.org/10.1016/j.cell.2009.11.003; PMID: 20064379
  • Lanzer M, Wickert H, Krohne G, Vincensini L, Braun Breton C. Maurer’s clefts: a novel multi-functional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes. Int J Parasitol 2006; 36:23 - 36; http://dx.doi.org/10.1016/j.ijpara.2005.10.001; PMID: 16337634
  • Mota LJ, Ramsden AE, Liu M, Castle JD, Holden DW. SCAMP3 is a component of the Salmonella-induced tubular network and reveals an interaction between bacterial effectors and post-Golgi trafficking. Cell Microbiol 2009; 11:1236 - 53; http://dx.doi.org/10.1111/j.1462-5822.2009.01329.x; PMID: 19438519
  • Gagnon E, Duclos S, Rondeau C, Chevet E, Cameron PH, Steele-Mortimer O, et al. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002; 110:119 - 31; http://dx.doi.org/10.1016/S0092-8674(02)00797-3; PMID: 12151002
  • Burlak C, Whitney AR, Mead DJ, Hackstadt T, Deleo FR. Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Mol Cell Proteomics 2006; 5:620 - 34; http://dx.doi.org/10.1074/mcp.M500336-MCP200; PMID: 16415295

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