Membrane nanotubes in myeloid cells in the adult mouse cornea represent a novel mode of immune cell interaction

Immunology and Cell Biology

Volumn 91, Issue 1, 2013, Pages 89-95

  Seyed Razavi, Yashar ^a   Hickey, Michael J ^a   Kuffová, Lucia ^b   McMenamin, Paul G ^a   Chinnery, Holly R ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c DEAKIN UNIVERSITY   (Australia)

Author keywords

CD11c; corneal inflammation; Cx3cr1; dendritic cells; intercellular communication; macrophages

Indexed keywords

MEMBRANE NANOTUBE; NANOTUBE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL CONTACT; CELL INTERACTION; CELL STRESS; CONTROLLED STUDY; EX VIVO STUDY; EXPLANT; HERPES SIMPLEX; HERPES SIMPLEX KERATITIS; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 1 INFECTION; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; STARVATION;

ANIMALS; ANTIGENS, CD11C; CELL COMMUNICATION; CELL MEMBRANE STRUCTURES; CORNEA; EYE INFECTIONS, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HISTOCOMPATIBILITY ANTIGENS CLASS II; INFLAMMATION; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MYELOID CELLS; RECEPTORS, CHEMOKINE;

HUMAN HERPESVIRUS 1; MAMMALIA; MURINAE; MUS MUSCULUS;

EID: 84872137228     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2012.52     Document Type: Article

References (43)

1. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science 2004; 303: 1007-1010. (Pubitemid 38209703)
2. Hurtig J, Chiu DT, Onfelt B. Intercellular nanotubes: Insights from imaging studies and beyond. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2010; 2: 260-276.
3. Onfelt B, Nedvetzki S, Benninger RK, Purbhoo MA, Sowinski S, Hume AN et al. Structurally distinct membrane nanotubes between human macrophages support longdistance vesicular traffic or surfing of bacteria. J Immunol 2006; 177: 8476-8483. (Pubitemid 44893810)
4. Onfelt B, Davis DM. Can membrane nanotubes facilitate communication between immune cells? Biochem Soc Trans 2004; 32(Part 5): 676-678. (Pubitemid 39524350)
5. Chauveau A, Aucher A, Eissmann P, Vivier E, Davis DM. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proc Natl Acad Sci USA 2010; 107: 5545-5550.
6. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, Kohler K et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 2008; 10: 211-219. (Pubitemid 351194051)
7. He K, Shi X, Zhang X, Dang S, Ma X, Liu F et al. Long-distance intercellular connectivity between cardiomyocytes and cardiofibroblasts mediated by membrane nanotubes. Cardiovasc Res 2011; 92: 39-47.
8. Davis DM, Sowinski S. Membrane nanotubes: Dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol 2008; 9: 431-436. (Pubitemid 351733399)
9. Wang MJ, Pei DS, Qian GW, Yin XX, Cheng Q, Li LT et al. p53 regulates Ki-67 promoter activity through p53-and Sp1-dependent manner in HeLa cells. Tumour Biol 2011; 32: 905-912.
10. Plotnikov EY, Khryapenkova TG, Galkina SI, Sukhikh GT, Zorov DB. Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture. Exp Cell Res 2010; 316: 2447-2455.
11. Domhan S, Ma L, Tai A, Anaya Z, Beheshti A, Zeier M et al. Intercellular communication by exchange of cytoplasmic material via tunneling nano-tube like structures in primary human renal epithelial cells. PLoS One 2011; 6: E21283.
12. Pyrgaki C, Trainor P, Hadjantonakis AK, Niswander L. Dynamic imaging of mammalian neural tube closure. Dev Biol 2010; 344: 941-947.
13. Eugenin EA, Gaskill PJ, Berman JW. Tunneling nanotubes (TNT) are induced by HIVinfection of macrophages: A potential mechanism for intercellular HIV trafficking. Cell Immunol 2009; 254: 142-148.
14. Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A, Browman DT et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat Cell Biol 2009; 11: 328-336.
15. Quah BJ, Barlow VP, McPhun V, Matthaei KI, Hulett MD, Parish CR. Bystander B cells rapidly acquire antigen receptors from activated B cells by membrane transfer. Proc Natl Acad Sci USA 2008; 105: 4259-4264. (Pubitemid 351754368)
16. Ramirez-Weber FA, Kornberg TB. Cytonemes: Cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 1999; 97: 599-607. (Pubitemid 29256963)
17. Miller J, Fraser SE, McClay D. Dynamics of thin filopodia during sea urchin gastrulation. Development 1995; 121: 2501-2511.
18. Chinnery HR, Pearlman E, McMenamin PG. Cutting edge: Membrane nanotubes in vivo: A feature of MHC class II+ cells in the mouse cornea. J Immunol 2008; 180: 5779-5783.
19. Gerdes HH, Bukoreshtliev NV, Barroso JF. Tunneling nanotubes: A new route for the exchange of components between animal cells. FEBS Lett 2007; 581: 2194-2201. (Pubitemid 46709910)
20. Lindquist RL, Shakhar G, Dudziak D, Wardemann H, Eisenreich T, Dustin ML et al. Visualizing dendritic cell networks in vivo. Nat Immunol 2004; 5: 1243-1250. (Pubitemid 41057739)
21. Knickelbein JE, Watkins SC, McMenamin PG, Hendricks RL. Stratification of antigen-presenting cells within the normal cornea. Ophthalmol Eye Dis 2009; 1: 45-54.
22. Bulloch K, Miller MM, Gal-Toth J, Milner TA, Gottfried-Blackmore A, Waters EM et al. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J Comp Neurol 2008; 508: 687-710. (Pubitemid 351693557)
23. McMenamin PG. Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. J Comp Neurol 1999; 405: 553-562. (Pubitemid 29124070)
24. Chinnery HR, Ruitenberg MJ, McMenamin PG. Novel characterization of monocytederived cell populations in the meninges and choroid plexus and their rates of replenishment in bone marrow chimeric mice. J Neuropathol Exp Neurol 2010; 69: 896-909.
25. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, Mothes W. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nature Cell Biol 2007; 9: 310-U106.
26. Watkins SC, Salter RD. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 2005; 23: 309-318. (Pubitemid 41317798)
27. Hell SW, Wichmann J. Breaking the diffraction resolution limit by stimulated emission: Stimulated-emission-depletion fluorescence microscopy. Opt Lett 1994; 19: 780-782.
28. Willig KI, Kellner RR, Medda R, Hein B, Jakobs S, Hell SW. Nanoscale resolution in GFP-based microscopy. Nat Methods 2006; 3: 721-723. (Pubitemid 44275740)
29. Zhu D, Tan KS, Zhang X, Sun AY, Sun GY, Lee JC. Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J Cell Sci 2005; 118(Part 16): 3695-3703. (Pubitemid 41309416)
30. Ramachandran S, Knickelbein JE, Ferko C, Hendricks RL, Kinchington PR. Development and pathogenic evaluation of recombinant herpes simplex virus type 1 expressing two fluorescent reporter genes from different lytic promoters. Virology 2008; 378: 254-264.
31. Chinnery HR, Carlson EC, Sun Y, Lin M, Burnett SH, Perez VL et al. Bone marrow chimeras and c-fms conditional ablation (Mafia) mice reveal an essential role for resident myeloid cells in lipopolysaccharide/TLR4-induced corneal inflammation. J Immunol 2009; 182: 2738-2744.
32. Onfelt B, Nedvetzki S, Yanagi K, Davis DM. Cutting edge: Membrane nanotubes connect immune cells. J Immunol 2004; 173: 1511-1513. (Pubitemid 38971579)
33. Nishibu A, Ward BR, Jester JV, Ploegh HL, Boes M, Takashima A. Behavioral responses of epidermal Langerhans cells in situ to local pathological stimuli. J Invest Dermatol 2006; 126: 787-796.
34. Ward BR, Jester JV, Nishibu A, Vishwanath M, Shalhevet D, Kumamoto T et al. Local thermal injury elicits immediate dynamic behavioural responses by corneal Langerhans cells. Immunology 2007; 120: 556-572. (Pubitemid 46365015)
35. Koyanagi M, Brandes RP, Haendeler J, Zeiher AM, Dimmeler S. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: A novel mechanism for cell fate changes? Circ Res 2005; 96: 1039-1041. (Pubitemid 40791375)
36. Brown K, Fidanboylu M, Wong W. Intercellular exchange of surface molecules and its physiological relevance. Arch Immunol Ther Exp 2010; 58: 263-272.
37. Feng Y, Santoriello C, Mione M, Hurlstone A, Martin P. Live imaging of innate immune cell sensing of transformed cells in zebrafish larvae: Parallels between tumor initiation and wound inflammation. PLoS Biol 2010; 8: E1000562.
38. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 2000; 20: 4106-4114. (Pubitemid 30314508)
39. Boes M, Cerny J, Massol R, Op den Brouw M, Kirchhausen T, Chen J et al. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 2002; 418: 983-988. (Pubitemid 34976034)
40. Johnson AC, Heinzel FP, Diaconu E, Sun Y, Hise AG, Golenbock D et al. Activation of toll-like receptor (TLR)2, TLR4, and TLR9 in the mammalian cornea induces MyD88-dependent corneal inflammation. Invest Ophthalmol Vis Sci 2005; 46: 589-595. (Pubitemid 40270339)
41. Chinnery HR, Ruitenberg MJ, Plant GW, Pearlman E, Jung S, McMenamin PG. The chemokine receptor CX3CR1 mediates homing of MHC class II-positive cells to the normal mouse corneal epithelium. Invest Ophthalmol Vis Sci 2007; 48: 1568-1574. (Pubitemid 351261340)
42. McMenamin PG. Optimal methods for preparation and immunostaining of iris, ciliary body, and choroidal wholemounts. Invest Ophthalmol Vis Sci 2000; 41: 3043-3048.
43. Kaczara P, Sarna T, Burke JM. Dynamics of H2O2 availability to ARPE-19 cultures in models of oxidative stress. Free Radic Biol Med 2010; 48: 1064-1070.