Super Resolution Microscopy Reveals that Caveolin-1 Is Required for Spatial Organization of CRFB1 and Subsequent Antiviral Signaling in Zebrafish

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Gabor, Kristin A ^a,b   Stevens, Chad R ^a,e   Pietraszewski, Matthew J ^a,f   Gould, Travis J ^b,g   Shim, Juyoung ^a   Yoder, Jeffrey A ^d   Lam, Siew Hong ^c   Gong, Zhiyuan ^c   Hess, Samuel T ^a,b   Kim, Carol H ^a  

^a UNIVERSITY OF MAINE   (United States)

^b National University of Singapore ^*  (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e ORGANOGENESIS INC   (United States)

^f Lohmann Animal Health International   (United States)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CAVEOLIN 1B; CYTOKINE RECEPTOR; CYTOKINE RECEPTOR FAMILY MEMBER 1; INTERFERON RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DOWN REGULATION; HOST RESISTANCE; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MICROSCOPY; MORTALITY; NONHUMAN; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SUPER RESOLUTION MICROSCOPY; VIRUS INFECTION; VIRUS LOAD; VIRUS VIRULENCE; ZEBRA FISH;

ANIMALS; CAVEOLIN 1; CELL MEMBRANE; DISEASE RESISTANCE; FISH DISEASES; IMMUNITY, INNATE; INTERFERONS; PROTEIN BINDING; RECEPTORS, INTERFERON; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84879899037     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068759     Document Type: Article

References (75)

1. Okamoto T, Schlegel A, Scherer PE, Lisanti MP, (1998) Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273: 5419-5422.
2. Fang PK, Solomon KR, Zhuang L, Qi M, McKee M, et al. (2006) Caveolin-1alpha and-1beta perform nonredundant roles in early vertebrate development. Am J Pathol 169: 2209-2222.
3. Lisanti MP, Scherer PE, Tang Z, Sargiacomo M, (1994) Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis. Trends Cell Biol 4: 231-235.
4. Williams TM, Lisanti MP, (2004) The caveolin proteins. Genome Biol 5: 214.
5. Medina FA, de Almeida CJ, Dew E, Li J, Bonuccelli G, et al. (2006) Caveolin-1-deficient mice show defects in innate immunity and inflammatory immune response during Salmonella enterica serovar Typhimurium infection. Infect Immun 74: 6665-6674.
6. Parton RG, Simons K, (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8: 185-194.
7. Simons K, Vaz WL, (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33: 269-295.
8. Schlegel A, Volonte D, Engelman JA, Galbiati F, Mehta P, et al. (1998) Crowded little caves: structure and function of caveolae. Cell Signal 10: 457-463.
9. Couet J, Sargiacomo M, Lisanti MP, (1997) Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem 272: 30429-30438.
10. Abulrob A, Lu Z, Baumann E, Vobornik D, Taylor R, et al. (2009) Nanoscale imaging of epidermal growth factor receptor clustering: Effects of inhibitors. J Biol Chem.
11. Pelkmans L, Kartenbeck J, Helenius A, (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3: 473-483.
12. Galbiati F, Razani B, Lisanti MP, (2001) Emerging themes in lipid rafts and caveolae. Cell 106: 403-411.
13. Rust MJ, Lakadamyali M, Zhang F, Zhuang X, (2004) Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat Struct Mol Biol 11: 567-573.
14. Simmons G, Rennekamp AJ, Chai N, Vandenberghe LH, Riley JL, et al. (2003) Folate receptor alpha and caveolae are not required for Ebola virus glycoprotein-mediated viral infection. J Virol 77: 13433-13438.
15. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, et al. (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168: 477-488.
16. Wang H, Yang P, Liu K, Guo F, Zhang Y, et al. (2008) SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway. Cell Res 18: 290-301.
17. Sanchez-San Martin C, Lopez T, Arias CF, Lopez S, (2004) Characterization of rotavirus cell entry. J Virol 78: 2310-2318.
18. Ewers H, Romer W, Smith AE, Bacia K, Dmitrieff S, et al. (2010) GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 12: 11-18; sup 11-12.
19. van den Broek MF, Muller U, Huang S, Aguet M, Zinkernagel RM, (1995) Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. J Virol 69: 4792-4796.
20. Steinhoff U, Muller U, Schertler A, Hengartner H, Aguet M, et al. (1995) Antiviral protection by vesicular stomatitis virus-specific antibodies in alpha/beta interferon receptor-deficient mice. J Virol 69: 2153-2158.
21. Takaoka A, Mitani Y, Suemori H, Sato M, Yokochi T, et al. (2000) Cross talk between interferon-gamma and-alpha/beta signaling components in caveolar membrane domains. Science 288: 2357-2360.
22. Altmann SM, Mellon MT, Distel DL, Kim CH, (2003) Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J Virol 77: 1992-2002.
23. Altmann SM, Mellon MT, Johnson MC, Paw BH, Trede NS, et al. (2004) Cloning and characterization of an Mx gene and its corresponding promoter from the zebrafish, Danio rerio. Dev Comp Immunol 28: 295-306.
24. Aggad D, Mazel M, Boudinot P, Mogensen KE, Hamming OJ, et al. (2009) The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J Immunol 183: 3924-3931.
25. Levraud JP, Boudinot P, Colin I, Benmansour A, Peyrieras N, et al. (2007) Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system. J Immunol 178: 4385-4394.
26. Kisseleva T, Bhattacharya S, Braunstein J, Schindler CW, (2002) Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene 285: 1-24.
27. Meeker ND, Trede NS, (2008) Immunology and zebrafish: spawning new models of human disease. Dev Comp Immunol 32: 745-757.
28. Traver D, Herbomel P, Patton EE, Murphey RD, Yoder JA, et al. (2003) The zebrafish as a model organism to study development of the immune system. Adv Immunol 81: 253-330.
29. Shogomori H, Brown DA, (2003) Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol Chem 384: 1259-1263.
30. Brown DA, (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21: 430-439.
31. Hess ST, Girirajan TP, Mason MD, (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91: 4258-4272.
32. Gould TJ, Verkhusha VV, Hess ST, (2009) Imaging biological structures with fluorescence photoactivation localization microscopy. Nat Protoc 4: 291-308.
33. Hess ST, Gould TJ, Gudheti MV, Maas SA, Mills KD, et al. (2007) Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc Natl Acad Sci U S A 104: 17370-17375.
34. Juette MF, Gould TJ, Lessard MD, Mlodzianoski MJ, Nagpure BS, et al. (2008) Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat Methods 5: 527-529.
35. Ogi M, Yokomori H, Oda M, Yoshimura K, Nomura M, et al. (2003) Distribution and localization of caveolin-1 in sinusoidal cells in rat liver. Med Electron Microsc 36: 33-40.
36. Kwok W, Lee SH, Culberson C, Korneszczuk K, Clemens MG, (2009) Caveolin-1 mediates endotoxin inhibition of endothelin-1-induced endothelial nitric oxide synthase activity in liver sinusoidal endothelial cells. Am J Physiol Gastrointest Liver Physiol 297: G930-939.
37. Balbis A, Baquiran G, Mounier C, Posner BI, (2004) Effect of insulin on caveolin-enriched membrane domains in rat liver. J Biol Chem 279: 39348-39357.
38. Phelan PE, Pressley ME, Witten PE, Mellon MT, Blake S, et al. (2005) Characterization of snakehead rhabdovirus infection in zebrafish (Danio rerio). J Virol 79: 1842-1852.
39. McCurley AT, Callard GV, (2008) Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol 9: 102.
40. Nixon SJ, Carter A, Wegner J, Ferguson C, Floetenmeyer M, et al. (2007) Caveolin-1 is required for lateral line neuromast and notochord development. J Cell Sci 120: 2151-2161.
41. Swaim LE, Connolly LE, Volkman HE, Humbert O, Born DE, et al. (2006) Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect Immun 74: 6108-6117.
42. Sullivan C, Kim CH, (2008) Zebrafish as a model for infectious disease and immune function. Fish Shellfish Immunol 25: 341-350.
43. Lam SH, Chua HL, Gong Z, Lam TJ, Sin YM, (2004) Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev Comp Immunol 28: 9-28.
44. Sullivan C, Postlethwait JH, Lage CR, Millard PJ, Kim CH, (2007) Evidence for evolving Toll-IL-1 receptor-containing adaptor molecule function in vertebrates. J Immunol 178: 4517-4527.
45. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA, (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
46. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
47. Akira S, Takeda K, (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
48. Honda K, Yanai H, Takaoka A, Taniguchi T, (2005) Regulation of the type I IFN induction: a current view. Int Immunol 17: 1367-1378.
49. Kawai T, Akira S, (2006) Innate immune recognition of viral infection. Nat Immunol 7: 131-137.
50. Uematsu S, Akira S, (2007) Toll-like receptors and Type I interferons. J Biol Chem 282: 15319-15323.
51. de Weerd NA, Samarajiwa SA, Hertzog PJ, (2007) Type I interferon receptors: biochemistry and biological functions. J Biol Chem 282: 20053-20057.
52. Hou SX, Zheng Z, Chen X, Perrimon N, (2002) The Jak/STAT pathway in model organisms: emerging roles in cell movement. Dev Cell 3: 765-778.
53. Gough DJ, Messina NL, Hii L, Gould JA, Sabapathy K,et al. Functional crosstalk between type I and II interferon through the regulated expression of STAT1. PLoS Biol 8: e1000361.
54. Claudinon J, Monier MN, Lamaze C, (2007) Interfering with interferon receptor sorting and trafficking: impact on signaling. Biochimie 89: 735-743.
55. Pelkmans L, Helenius A, (2002) Endocytosis via caveolae. Traffic 3: 311-320.
56. Werling D, Hope JC, Chaplin P, Collins RA, Taylor G, et al. (1999) Involvement of caveolae in the uptake of respiratory syncytial virus antigen by dendritic cells. J Leukoc Biol 66: 50-58.
57. Marjomaki V, Pietiainen V, Matilainen H, Upla P, Ivaska J, et al. (2002) Internalization of echovirus 1 in caveolae. J Virol 76: 1856-1865.
58. Pichlmair A, Reis e Sousa C, (2007) Innate recognition of viruses. Immunity 27: 370-383.
59. Garcia-Sastre A, (2002) Mechanisms of inhibition of the host interferon alpha/beta-mediated antiviral responses by viruses. Microbes Infect 4: 647-655.
60. Garcia-Sastre A, (2001) Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279: 375-384.
61. Lieschke GJ, Currie PD, (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8: 353-367.
62. Fijan N (1983) Some properties of the Epithelioma Papulosum Cyprini (EPC) cell line from carp Cyprinus carpio. Ann Virol 134 E: 207-220.
63. Ghosh C, Zhou YL, Collodi P, (1994) Derivation and characterization of a zebrafish liver cell line. Cell Biol Toxicol 10: 167-176.
64. Subach FV, Patterson GH, Manley S, Gillette JM, Lippincott-Schwartz J, et al. (2009) Photoactivatable mCherry for high-resolution two-color fluorescence microscopy. Nat Methods 6: 153-159.
65. Gould TJ, Gunewardene MS, Gudheti MV, Verkhusha VV, Yin SR, et al. (2008) Nanoscale imaging of molecular positions and anisotropies. Nat Methods 5: 1027-1030.
66. Reed LJ, Muench H, (1938) A simple method of estimating fifty percent end points. Am J Hyg 27: 493-497.
67. Yoder JA, Orcutt TM, Traver D, Litman GW, (2007) Structural characteristics of zebrafish orthologs of adaptor molecules that associate with transmembrane immune receptors. Gene 401: 154-164.
68. Traver D, Paw BH, Poss KD, Penberthy WT, Lin S, et al. (2003) Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat Immunol 4: 1238-1246.
69. Yoder JA, Turner PM, Wright PD, Wittamer V, Bertrand JY, et al. (2010) Developmental and tissue-specific expression of NITRs. Immunogenetics 62: 117-122.
70. Picker A, Roellig D, Pourquie O, Oates AC, Brand M, (2009) Tissue micromanipulation in zebrafish embryos. Methods Mol Biol 546: 153-172.
71. Thompson RE, Larson DR, Webb WW, (2002) Precise nanometer localization analysis for individual fluorescent probes. Biophys J 82: 2775-2783.
72. Gould TJ, Gunewardene MS, Gudheti MV, Verkhusha VV, Yin S, et al. (2008) Nanoscale imaging of molecular positions and anisotropies. Nat Methods 5: 1027-1030.
73. Gunewardene MS, Subach FV, Gould TJ, Penoncello GP, Gudheti MV,et al. Superresolution imaging of multiple fluorescent proteins with highly overlapping emission spectra in living cells. Biophys J 101: 1522-1528.
74. Folling J, Belov V, Kunetsky R, Medda R, Schonle A, et al. (2007) Photochromic Rhodamines Provide Nanoscopy with Optical Sectioning. Angew Chem Int Ed Engl 46: 6266-6270.
75. Yeomans JM (2002) Statistical Mechanics of Phase Transitions. Oxford: Oxford University Press.