Microparticle-Mediated Transfer of the Viral Receptors CAR and CD46, and the CFTR Channel in a CHO Cell Model Confers New Functions to Target Cells

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Gonzalez, Gaëlle ^a   Vituret, Cyrielle ^a,b   Di Pietro, Attilio ^b   Chanson, Marc ^c   Boulanger, Pierre ^a   Hong, Saw See ^a,d  

^a UNIVERSITÉ LYON 1   (France)

^b INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE CHANNEL; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GREEN FLUORESCENT PROTEIN; MEMBRANE COFACTOR PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CHO CELL; CONTROLLED STUDY; CYSTIC FIBROSIS; FEMALE; HUMAN; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS 35; HUMAN ADENOVIRUS 5; HUMAN CELL; INCUBATION TIME; INTRACELLULAR TRANSPORT; MEMBRANE MICROPARTICLE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SEROTYPE; TARGET CELL;

ANIMALS; ANTIGENS, CD46; BIOLOGICAL TRANSPORT; CELL-DERIVED MICROPARTICLES; CHO CELLS; COXSACKIE AND ADENOVIRUS RECEPTOR-LIKE MEMBRANE PROTEIN; CRICETINAE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; MICROSCOPY, ELECTRON;

ADENOVIRIDAE; HUMAN ADENOVIRUS;

EID: 84871405261     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052326     Document Type: Article

References (82)

1. György B, Szabó TG, Pásztói M, Pál Z, Misják P, et al. (2011) Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 68: 2667-2688.
2. Mathivanan S, Ji H, Simpson RJ, (2010) Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73: 1907-1920.
3. Mause SF, Weber C, (2010) Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res 107: 1047-1057.
4. Meckes DGJ, Raab-Traub N, (2011) Microvesicles and viral infection. J Virol 85: 12844-12854.
5. Ste{ogonek}pień E, Kabłak-Ziembicka A, Czyż J, Przewłocki T, Małecki M, (2012) Microparticles, not only markers but also a therapeutic target in the early stage of diabetic retinopathy and vascular aging. Expert Opin Ther Targets 16: 677-688.
6. Dainiak N, Riordan MA, Strauss PR, Feldman L, Kreczko S, (1988) Contractile proteins participate in release of erythroid growth regulators from mononuclear cells. Blood 72: 165-171.
7. Eldh M, Ekström K, Valadi H, Sjöstrand M, Olsson B, et al. (2010) Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA. PLoS ONE 5: e15353.
8. Beyer C, Pisetsky DS, (2010) The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol 6: 21-29.
9. Boulanger CM, Amabile N, Tedgui A, (2006) Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension 48: 180-186.
10. Boulanger CM, (2010) Microparticles, vascular function and hypertension. Curr Opin Nephrol Hypertens 19: 177-180.
11. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659.
12. Pap E, Pállinger E, Pásztói M, Falus A, (2009) Highlights of a new type of intercellular communication: microvesicle-based information transfer. Inflamm Res 58: 1-8.
13. Shet AS, (2008) Characterizing blood microparticles: technical aspects and challenges. Vasc Health Risk Manag 4: 769-774.
14. Diamant M, Tushuizen ME, Sturk A, R N, (2004) Cellular microparticles: new players in the field of vascular disease? Eur J Clin Invest 34: 392-401.
15. Baj-Krzyworzeka M, Majka M, Pratico D, Ratajczak J, Vilaire G, et al. (2002) Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells. Exp Hematol 30: 450-459.
16. Thomas GM, Panicot-Dubois L, Lacroix R, Dignat-George F, Lombardo D, et al. (2009) Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J Exp Med 206: 1913-1927.
17. Mack M, Kleinschmidt A, Brühl H, Klier C, Nelson PJ, et al. (2000) Transfert of the chemokin receptor CCR5 between cells by membrane derived microparticles: a mechanism for cellular human immunodeficiency virus infection. Nature Med 6: 769-775.
18. Chaput N, Taïeb J, Schartz N, Flament C, Novault S, et al. (2005) The potential of exosomes in immunotherapy of cancer. Blood Cells Mol Dis 35: 111-115.
19. Ahn YS, Jy W, Horstman LL, Jimenez JJ, (2008) Cell-derived microparticles: a mediator of inflammation in aortic valve stenosis? Thromb Haemost 99: 657-658.
20. Taïeb J, Chaput N, Zitvogel L, (2005) Dendritic cell-derived exosomes as cell-free peptide-based vaccines. Crit Rev Immunol 25: 215-223.
21. Baj-Krzyworzeka M, Szatanek R, Weglarczyk K, Baran J, Zembala M, (2007) Tumour-derived microvesicles modulate biological activity of human monocytes. Immunol Lett 113: 76-82.
22. Hugel B, Martinez MC, Kunzelmann C, Freyssinet J-M, (2005) Membrane microparticles: two sides of the coin. Physiology 20: 22-27.
23. Köppler B, Cohen C, Schlöndorff D, Mack M, (2006) Differential mechanisms of microparticle transfer to B cells and monocytes: anti-inflammatory properties of microparticles. Eur J Immunol 36: 648-660.
24. Hudrisier D, Bongrand P, (2002) Intercellular transfer of antigen-presenting cell determinants onto T cells: molecular mechanisms and biological significance. FASEB J 16: 477-486.
25. Joly E, Hudrisier D, (2003) What is trogocytosis and what is its purpose? Nature Immunol 4: 815.
26. Jimenez JJ, Jy W, Mauro LM, Horstman LL, Bidot CJ, et al. (2005) Endothelial microparticles (EMP) as vascular disease markers. Adv Clin Chem 39: 131-157.
27. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, et al. (2008) Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3: e3694.
28. Kesimer M, Scull M, Brighton B, DeMaria G, Burns K, et al. (2009) Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: a possible role in innate defense. FASEB J 23: 1858-1868.
29. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, et al. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476.
30. Vickers KC, Remaley AT, (2012) Lipid-based carriers of microRNAs and intercellular communication. Curr Opin Lipidol 23: 91-97.
31. Bebawy M, Combes V, Lee E, Jaiswal R, Gong J, et al. (2009) Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia 23: 1643-1649.
32. Lenassi M, Cagney G, Liao M, Vaupotic T, Bartholomeeusen K, et al. (2010) HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic 11: 110-122.
33. Liu R, Klich I, Ratajczak J, Ratajczak MZ, Zuba-Surma EK, (2009) Erythrocyte-derived microvesicles may transfer phosphatidylserine to the surface of nucleated cells and falsely 'mark' them as apoptotic. Eur J Haematol 83: 220-229.
34. Muratori C, Cavallin LE, Krätzel K, Tinari A, De Milito A, et al. (2009) Massive secretion by T cells is caused by HIV Nef in infected cells and by Nef transfer to bystander cells. Cell Host Microbe 6: 218-230.
35. Farley DC, Iqball S, Smith JC, Miskin JE, Kingsman SM, et al. (2007) Factors that influence VSV-G pseudotyping and transduction efficiency of lentiviral vectors - in vitro and in vivo implications. J Gene Med 9: 345-356.
36. Granio O, Porcherot M, Corjon S, Kitidee K, Henning P, et al. (2009) Improved adenovirus type 5 vector-mediated transduction of resistant cells by piggybacking on Coxsackie B-adenovirus receptor-pseudotyped baculovirus. J Virol 83: 6048-6066.
37. Guibinga GH, Friedmann T, (2005) Baculovirus GP64-pseudotyped HIV-based lentivirus vectors are stabilized against complement inactivation by codisplay of decay accelerating factor (DAF) or of a GP64-DAF fusion protein. Mol Ther 11: 645-651.
38. Guibinga GH, Miyanohara A, Esko JD, Friedmann T, (2002) Cell surface heparan sulfate is a receptor for attachment of envelope protein-free retrovirus-like particles and VSV-G pseudotyped MLV-derived retrovirus vectors to target cells. Mol Ther 5: 538-546.
39. Okimoto T, Friedmann T, Miyanohara A, (2001) VSV-G envelope glycoprotein forms complexes with plasmid DNA and MLV retrovirus-like particles in cell-free conditions and enhances DNA transfection. Mol Ther 4: 232-238.
40. Sandrin V, Boulanger P, Penin F, Granier C, Cosset F-L, et al. (2005) Assembly of functional hepatitis C virus glycoproteins on infectious pseudoparticles occurs intracellularly and requires concomitant incorporation of E1 and E2 glycoproteins. J Gen Virol 86: 3189-3199.
41. D'Souza-Schorey C, Clancy JW, (2012) Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev 26: 1287-1299.
42. Benameur T, Andriantsitohaina R, Martinez MC, (2009) Therapeutic potential of plasma membrane-derived microparticles. Pharmacol Reports 61: 49-57.
43. Arnberg N, (2009) Adenovirus receptors: implications for tropism, treatment and targeting. Rev Med Virol 19: 165-178.
44. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, et al. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275: 1320-1323.
45. Law LK, Davidson BL, (2005) What does it take to bind CAR? Mol Ther 12: 599-609.
46. Tomko RP, Xu R, Philipson L, (1997) HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B Coxsackieviruses. Proc Natl Acad Sci USA 94: 3352-3356.
47. Gerlier D, Valentin H, (2009) Measles virus interaction with host cells and impact on innate immunity. Curr Top Microbiol Immunol 329: 163-191.
48. Gaggar A, Shayakhmetov DM, Lieber A, (2003) CD46 is a cellular receptor for group B adenoviruses. Nature Med 8: 746-755.
49. Segerman A, Atkinson JP, Marttila M, Dennerquist V, Wadell G, et al. (2003) Adenovirus type 11 uses CD46 as a cellular receptor. J Virol 77: 9183-9191.
50. Riley-Vargas RC, Gill DB, Kemper C, Liszewski MK, Atkinson JP, (2004) CD46: expanding beyond complement regulation. Trends Immunol 25: 496-503.
51. Grumelli S, Lu B, Peterson L, Maeno T, Gerard C, (2011) CD46 protects against chronic obstructive pulmonary disease. PLoS One 6: e18785.
52. Walters RW, Grunst T, Bergelson JM, Finberg RW, Welsh MJ, et al. (1999) Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J Biol Chem 274: 10219-10226.
53. Bradbury NA, (1999) Intracellular CFTR: localization and function. Physiol Rev 79: S175-S191.
54. Chow YH, Plumb J, Wen Y, Steer BM, Lu Z, et al. (2000) Targeting Transgene Expression to Airway Epithelia and Submucosal Glands, Prominent Sites of Human CFTR Expression. Mol Ther 2: 359-367.
55. Granio O, Norez C, Ashbourne Excoffon KJ, Karp PH, Lusky M, et al. (2007) Cellular localization and activity of Ad-delivered GFP-CFTR in airway epithelial and tracheal cells. Am J Respir Cell Mol Biol 37: 631-639.
56. Mohamed A, Ferguson D, Seibert FS, Cai HM, Kartner N, et al. (1997) Functional expression and apical localization of the cystic fibrosis transmembrane conductance regulator in MDCK I cells. Biochem J 322: 259-265.
57. Sheppard DN, Welsh MJ, (1999) Structure and function of the CFTR chloride channel. Physiol Rev 79: S23-45.
58. Guo Y, Su M, McNutt MA, Jiang Gu J, (2009) Expression and distribution of cystic fibrosis transmembrane conductance regulator in neurons of the human brain. J Histochem Cytochem 57: 1113-1120.
59. Yanagi Y, Takeda M, Ohno S, (2006) Measles virus: cellular receptors, tropism and pathogenesis. J Gen Virol 87: 2767-2779.
60. Kowalski MP, Pier GB, (2004) Localization of cystic fibrosis transmembrane conductance regulator to lipid rafts of epithelial cells is required for Pseudomonas aeruginosa-Induced cellular activation. J Immunol 172: 418-425.
61. Buchholz CJ, Koller D, Devaux P, Mumenthaler C, Schneider-Schaulies J, et al. (1997) Mapping of the primary binding site of measles virus to its receptor CD46. J Biol Chem 272: 22072-22079.
62. Christiansen D, Devaux P, Réveil B, Evlashev A, Horvat B, et al. (2000) Octamerization enables soluble CD46 receptor to neutralize measles virus in vitro and in vivo. J Virol 74: 4672-4678.
63. Devaux P, Loveland B, Christiansen D, Milland J, Gerlier D (1996) Interactions between the ectodomains of haemagglutinin and CD46 as a primary step in measles virus entry. J Gen Virol 1477-1481.
64. Corjon S, Gonzalez G, Henning P, Grichine A, Lindholm L, et al. (2011) Cell entry and trafficking of human adenovirus bound to blood factor X is determined by the fiber serotype and not hexon:heparan sulfate interaction. PLoS ONE 6: e18205.
65. Coclet-Ninin J, Rochat T, Poitry S, Chanson M, (2002) Discrimination between cystic fibrosis and CFTR-corrected epithelial cells by a membrane potential-sensitive probe. Exp Lung Res 28: 181-199.
66. Granio O, Ashbourne Excoffon KJD, Henning P, Melin P, Gonzalez G, et al. (2010) Adenovirus 5-fiber 35 chimeric vector mediates efficient apical correction of the cystic fibrosis transmembrane conductance regulator defect in cystic fibrosis primary airway epithelia. Hum Gene Ther 21: 1-19.
67. DaFonseca S, Blommaert A, Coric P, Hong SS, Bouaziz S, et al. (2007) The 3-O-(3′,3′-dimethylsuccinyl) derivative of betulinic acid (DSB) inhibits the assembly of virus-like particles in HIV-1 Gag precursor-expressing cells. Antiviral Ther 12: 1185-1203.
68. Tabcharani JA, Chang XB, Riordan JR, Hanrahan JW, (1991) Phosphorylation-regulated Cl- channel in CHO cells stably expressing the cystic fibrosis gene. Nature 352: 628-631.
69. Abe A, Miyanohara A, Friedmann T, (1998) Enhanced gene transfer with fusogenic liposomes containing vesicular stomatitis virus G glycoprotein. J Virol 72: 6159-6163.
70. Roche S, Albertini AA, Lepault J, Bressanelli S, Gaudin Y, (2008) Structures of vesicular stomatitis virus glycoprotein: membrane fusion revisited. Cell Mol Life Sci 65: 1716-1728.
71. Roche S, Rey FA, Gaudin Y, Bressanelli S, (2007) Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science. 315: 843-848.
72. Hudrisier D, Clemenceau B, Balor S, Daubeuf S, Magdeleine E, et al. (2009) Ligand binding but undetected functional response of FcR after their capture by T cells via trogocytosis. J Immunol 183: 6102-6113.
73. D'Halluin JC, Milleville M, Boulanger P, (1980) Effects of novobiocin on adenovirus DNA synthesis and encapsidation. Nucl Acids Res 8: 1625-1641.
74. Benharouga M, Haardt M, Kartner N, Lukacs GL, (2001) COOH-terminal truncations promote proteasome-dependent degradation of mature cystic fibrosis transmembrane conductance regulator from post-Golgi compartments. J Cell Biol 153: 957-970.
75. Heda GD, Tanwani M, Marino CR, (2001) The Delta F508 mutation shortens the biochemical half-life of plasma membrane CFTR in polarized epithelial cells. Am J Physiol Cell Physiol 280: C166-174.
76. Bartoszewski R, Rab A, Twitty G, Stevenson L, Fortenberry J, et al. (2008) The mechanism of cystic fibrosis transmembrane conductance regulator transcriptional repression during the unfolded protein response. J Biol Chem 283: 12154-12165.
77. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, et al. (2010) Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One 5: e11803.
78. Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, et al. (2007) Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110: 2440-2448.
79. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, et al. (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20: 847-856.
80. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, et al. (2009) Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4: e4722.
81. Combes V, Simon AC, Grau GE, Arnoux D, Camoin L, et al. (1999) In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J Clin Invest 104: 93-102.
82. Franqueville L, Henning P, Magnusson MK, Vigne E, Schoehn G, et al. (2008) Protein crystals in adenovirus type 5-infected cells: requirements for intranuclear crystallogenesis, structural and functional analysis. PLoS One 3: e2894.