Unique physicochemical properties of human enteric Ad41 responsible for its survival and replication in the gastrointestinal tract

Virology

Volumn 322, Issue 1, 2004, Pages 93-104

  Favier, Anne Laure ^a,c   Burmeister, Wilhelm P ^b   Chroboczek, Jadwiga ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^c CENTRE DE RECHERCHES   (France)

Author keywords

Acid shock; AD; Ad41; Adenovirus; Basic charge; Dipalmitoyl phosphatidylcholine; Dipalmitoyl phosphatidylglycerol; DPPC; DPPG; Enteric adenovirus; FFU; Focus forming units; Gut tropism; Mucus layer; PE; Sphingolipids; Virus lipid interactions

Indexed keywords

ACID; LIPID; PHOSPHOLIPID; SPHINGOLIPID; VIRUS PROTEIN;

ADENOVIRUS; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EMBRYO; ENTERIC VIRUS; EXPOSURE; GASTROINTESTINAL TRACT; HUMAN; HUMAN CELL; INTESTINE MUCOSA; NONHUMAN; NUCLEOTIDE SEQUENCE; PH MEASUREMENT; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN INTERACTION; RESPIRATORY SYSTEM; STOMACH MUCOSA; VIRION; VIRUS ADSORPTION; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS SURVIVAL;

ADENOVIRUSES, HUMAN; CELL LINE; CELLS, CULTURED; ELECTROSTATICS; GASTROINTESTINAL TRACT; HUMANS; HYDROGEN-ION CONCENTRATION; INTESTINAL MUCOSA; LIPID METABOLISM; MODELS, MOLECULAR; PHOSPHOLIPIDS; VIRAL PROTEINS; VIRUS REPLICATION;

ADENOVIRIDAE;

EID: 1942518221     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.01.020     Document Type: Article

References (68)

1. Albinsson B., Kidd A.H. Adenovirus type 41 lacks an RGD alpha(v) integrin binding motif on the penton base and undergoes delayed uptake in A549 cells. Virus Res. 64:1999;125-136.
2. Bai M., Campisi L., Freimuth P. Vitronectin receptor antibodies inhibit infection of HeLa and A549 cells by adenovirus type 12 but not by adenovirus type 2. J. Virol. 68:1994;5925-5932.
3. Balakireva L., Schoehn G., Thouvenin E., Chroboczek J. Binding of adenovirus capsid to dipalmitoylphosphatidylcholine provides a novel pathway for virus entry. J. Virol. 77:2002;4858-4866.
4. Bergelson J.M., Cunningham G.D., Kurt-jones E.A., Krithivas A., Hong A., Horwitz M.S., Crowell R.L., Finberg R.W. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science. 275:1997;1320-1323.
5. Bernhard W., Postle A.D., Linck M., Sewing K.F. Composition of phospholipid classes and phosphatidylcholine molecular species of gastric mucosa and mucus. Biochim. Biophys. Acta. 1255:1995;99-104.
6. Bewley M.C., Springer K., Zhang Y.B., Freimuth P., Flanagan J.M. Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science. 286:1999;1579-1583.
7. Bhat S., Mettus R.V., Reddy E.P., Ugen K.E., Srikanthan V., Williams W.V., Weiner D.B. The galactosyl ceramide/sulfatide receptor binding region of HIV-1 gp120 maps to amino acids 206-275. AIDS Res. Hum. Retroviruses. 9:1993;175-181.
8. Boot H.J., Kolen C.P., van Noort J.M., Pouwels P.H. S-layer protein of Lactobacillus acidophilus ATCC 4356: purification, expression in Escherichia coli, and nucleotide sequence of the corresponding gene. J. Bacteriol. 175:1993;6089-6096.
9. Chroboczek J., Gout E., Favier A.L., Galinier R. Novel partner proteins of adenovirus penton. Curr. Top. Microbiol. Immunol. 272:2003;37-55.
10. Cook D.G., Fantini J., Spitalnik S.L., Gonzalez-Scarano F. Binding of human immunodeficiency virus type I (HIV-1) gp120 to galactosylceramide (GalCer): relationship to the V3 loop. Virology. 201:1994;206-214.
11. Corbo D.C., Liu J.C., Chien W.Y. Characterization of the barrier properties of mucosal membranes. J. Pharm. Sci. 79:1990;202-206.
12. Croyle M.A., Stone M., Amidon G.L., Roessler B.J. In vitro and in vivo assessment of adenovirus 41 as a vector for gene delivery to the intestine. Gene Ther. 5:1998;645-654.
13. Croyle M.A., Roessler B.J., Hsu C.P., Sun R., Amidon G.L. Beta cyclodextrins enhance adenoviral-mediated gene delivery to the intestine. Pharm Res. 15:1998;1348-1355.
14. Czajkowsky D.M., Iwamoto H., Cover T.L., Shao Z. The vacuolating toxin from Helicobacter pylori forms hexameric pores in lipid bilayers at low pH. Proc. Natl. Acad. Sci. U.S.A. 96:1999;2001-2006.
15. Davison A.J., Telford E.A., Watson M.S., McBride K., Mautner V. The DNA sequence of adenovirus type 40. J. Mol. Biol. 234:1993;1308-1316.
16. de Jong J.C., Wigand R., Kidd A.H., Wadell G., Kapsenberg J.G., Muzerie C.J., Wermenbol A.G., Firtzlaff R.G. Candidate adenoviruses 40 and 41: fastidious adenoviruses from human infant stool. J. Med. Virol. 11:1983;215-231.
17. Devaux C., Caillet-Boudin M.L., Jacrot B., Boulanger P. Crystallization, enzymatic cleavage, and the polarity of the adenovirus type 2 fibre. Virology. 161:1987;121-128.
18. Dowler S., Currie R.A., Downes C.P., Alessi D.R. DAPP1: a dual adaptor for phosphotyrosine and 3-phosphoinositides. Biochem. J. 342:1999;7-12.
19. Durmort C., Stehlin C., Schoehn G., Mitraki A., Drouet E., Cusack S., Burmeister W.P. Structure of the fiber head of Ad3, a non-CAR-binding serotype of adenovirus. Virology. 285:2001;302-312.
20. Estes M.K., Graham D.Y., Mason B.B. Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J. Virol. 39:1981;879-888.
21. Favier, A.L., Ph.D. Dissertation, Interactions moléculaí res entre I'adénovirus enterique de sérotype 41 et la cellule hóle. Grenoble, UJF-2002.
22. Favier A.L., Schoehn G., Jaquinod M., Harsi C., Chroboczek J. Structural studies of human enteric adenovirus type 41. Virology. 293:2002;75-85.
23. Fender P., Ruigrok R.W., Gout E., Buffet S., Chroboczek J. Adenovirus dodecahedron, a new vector for human gene transfer. Nat. Biotechnol. 15:1997;52-56.
24. Foreman P.K., Wainwright M.J., Alicke B., Kovesdi I., Wickham T.J., Smith J.G., Meier-Davis S., Fix J.A., Daddona P., Gardner P., Huang M.T. Adenovirus-mediated transduction of intestinal cells in vivo. Hum. Gene Ther. 9:1998;1313-1321.
25. Ganz T., Lehrer R.I. Defensins. Curr. Opin. Immunol. 6:1994;584-589.
26. Gary G.W. Jr., Hierholzer J.C., Black R.E. Characteristics of noncultivable adenoviruses associated with diarrhea in infants: a new subgroup of human adenoviruses. J. Clin. Microbiol. 10:1979;96-103.
27. Greber U.F., Willetts M., Webster P., Helenius A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell. 5:1993;477-486.
28. Green M., Pina M. Biochemical studies on adenovirus multiplication: IV. Isolation, purification and chemical analysis of adenovirus. Virology. 20:1963;199-207.
29. Gryboski J., Walker W.A. Gastrointestinal Problems in the Infant. 1983;Saunders, Philadelphia.
30. Hakomori S. Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. J. Biol. Chem. 265:1990;18713-18716.
31. Heideman D.A., van Beusechem V.W., Offerhaus J.G., Wickham T.J., Roelvink P.W., Craanen M.E., Pinedo H.M., Meijer C.J., Gerritsen W.R. Selective gene transfer into primary human gastric tumors using epithelial cell adhesion molecule-targeted adenoviral vectors with ablated native tropism. Hum. Gene Ther. 13:2002;1677-1685.
32. Hong J.S., Engler J.A. The amino terminus of the adenovirus fibre protein encodes the nuclear localization signal. Virology. 185:1991;758-767.
33. Jacobsson P.A., Johansson M.E., Wadell G. Identification of an enteric adenovirus by immunoelectroosmophoresis (IEOP) technique. J. Med. Virol. 3:1979;307-312.
34. Jones E.Y., Miller A. Analysis of structural design features in collagen. J. Mol. Biol. 218:1991;209-219.
35. Kagnoff M.F., Paterson Y.J., Kumar P.J., Kasarda D.D., Carbone F.R., Unsworth D.J., Austin R.K. Evidence for the role of a human intestinal adenovirus in the pathogenesis of coeliac disease. Gut. 28:1987;995-1001.
36. Kanegae Y., Makimura M., Saito I. A simple and efficient method for purification of infectious recombinant adenovirus. Jpn. J. Med. Sci. Biol. 47:1994;157-166.
37. Kidd A.H., Chroboczek J., Cusack S., Ruigrok R.W. Adenovirus type 40 virions contain two distinct fibres. Virology. 192:1993;73-84.
38. Larhed A.W., Artursson P., Bjork E. The influence of intestinal mucus components on the diffusion of drugs. Pharm. Res. 15:1998;66-71.
39. Lehr C.M., Poelma F.G.J., Junginger H.E., Tukker J.J. An estimate of turnover time of intestinal mucus gel layer in the rat in situ loop. Int. J. Pharm. 70:1991;235-240.
40. Lichtenberger L.M. The hydrophobic barrier properties of gastrointestinal mucus. Annu. Rev. Physiol. 57:1995;565-583.
41. Lingwood C.A. Glycolipid receptors for verotoxin and Helicobacter pylori: role in pathology. Biochim. Biophys. Acta. 1455:1999;375-386.
42. Mahdavi J., Sonden B., Hurtig M., Olfat F.-O., Forsberg L., Roche N., Angstrom J., Larsson T., Teneberg S., Karlsson K.A., Altraja T., Wadstrom T., Kersulyte D., Berg D.E., Dubois A., Petersson C., Magnusson K.E., Norberg T., Lindh F., Lundskog B.B., Arnqvist A., Hammarstrom L., Boren T. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science. 297:2002;573-578.
43. Mathias P., Wickham T., Moore M., Nemerow G. Multiple adenovirus serotypes use alpha v integrins for infection. J. Virol. 168:1994;6811-6814.
44. Mitraki A., Barge A., Chroboczek J., Andrieu J.P., Gagnon J., Ruigrok R.W. Unfolding studies of human adenovirus type 2 fibre trimers. Evidence for a stable domain. Eur. J. Biochem. 264:1999;599-606.
45. Nakamura T., Sato K., Hamada H. Reduction of natural adenovirus tropism to the liver by both ablation of fiber-coxsackievirus and adenovirus receptor interaction and use of replaceable short fiber. J. Virol. 77:2003;2512-2521.
46. Nardone G., Laccetti P., Civiletti C., Budillon G. Phospholipid composition of human gastric mucosa: a study of endoscopic biopsy specimens. Gut. 34:1993;456-460.
47. Nicolls A., Sharp K., Horning B. Protein folding and association: insights from the interfacial and thermodynamics properties. Proteins: Struct., Funct., Genet. 11:1991;281-296.
48. Pereira H.G., Wrigley N.G. In vitro reconstitution, hexon bonding and handedness of incomplete adenovirus capsid. J. Mol. Biol. 85:1974;617-630.
49. Pieniazek N.J., Slemenda S.B., Pieniazek D., Velarde J., Luftig R.B. Human enteric adenovirus type 41 (Tak) contains a second fibre protein gene. Nucleic Acids Res. 18:1990;1901.
50. Roberts J.R., O'Neill K.E., Clifford T.Y. DNA sequences from the adenovirus 2 genome. J. Biol. Chem. 259:1984;13968-13975.
51. Roelvink P.W., Lizonova A., Lee J.G., Li Y., Bergelson J.M., Finberg R.W., Brough D.E., Kovesdi I., Wickham T.J. The coxsackievirus-adenovirus receptor protein can function as protein can function as a cellular protein for adenovirus serotypes from groups A, C, D, E and F. J. Virol. 72:1998;7909-7915.
52. Rousset E., Harel J., Dubreuil J.D. Sulfatide from the pig jejunum brush border epithelial cell surface is involved in binding of Escherichia coli enterotoxin b. Infect. Immun. 66:1998;5650-5658.
53. Ruiz M.C., Alonso-Torre S.R., Charpilienne A., Vasseur M., Michelangeli F., Cohen J., Alvarado F. Rotavirus interaction with isolated membrane vesicles. J. Virol. 68:1994;4009-4016.
54. Schmitz G., Muller G. Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J. Lipid Res. 32:1991;1539-1570.
55. Simons K., van Meer G. Lipid sorting in epithelial cells. Biochemistry. 27:1988;6197-6202.
56. Svensson M., Frendeus B., Butters T., Platt F., Dwek R., Svanborg C. Glycolipid depletion in antimicrobial therapy. Mol. Microbiol. 47:2003;453-461.
57. Thomas C.C., Dowler S., Deak M., Alessi D.R., van Aalten D.M. Crystal structure of the phosphatidylinositol 3,4-bisphosphate-binding pleckstrin homology (PH) domain of tandem PH-domain-containing protein 1 (TAPP1): molecular basis of lipid specificity. Biochem. J. 358:2001;287-294.
58. Thomas C.C., Deak M., Alessi D.R., van Aalten D.M. High-resolution structure of the pleckstrin homology domain of protein kinase b/akt bound to phosphatidylinositol (3,4,5)-trisphosphate. Curr. Biol. 12:2002;1256-1262.
59. Uhnoo I., Wadell G., Svensson L., Johansson M.E. Two new serotypes of enteric adenovirus causing infantile diarrhoea. Dev. Biol. Stand. 53:1983;311-318.
60. Uhnoo I., Wadell G., Svensson L., Johansson M.E. Importance of enteric adenovirus 40 and 41 in acute gastroenteritis in infants and young children. J. Clin. Microbiol. 20:1984;365-372.
61. van Oostrum J., Burnett R.M. Molecular composition of the adenovirus type 2 virion. J. Virol. 56:1985;439-448.
62. van Raaij M.J., Louis N., Chroboczek J., Cusack S. Structure of the human adenovirus serotype 2 fiber head domain at 1.5 A resolution. Virology. 262:1999;333-343.
63. Weiss C., Clark H.F. Rapid inactivation of rotaviruses by exposure to acid buffer or acidic gastric juice. J. Gen. Virol. 66:1985;2725-2730.
64. Wickham T.J., Mathias P., Cheresh D.A., Nemerow G. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell. 73:1993;309-319.
65. Willoughby R.E., Yolken R.H., Schnaar R.L. Rotaviruses specifically bind to the neutral glycosphingolipid asialo-GM1. J. Virol. 64:1990;4830-4835.
66. Xia D., Henry L., Gerard R.D., Deisenhofer J. Structure of the receptor binding domain of adenovirus type 5 fiber protein. Curr. Top. Microbiol. Immunol. 199:1995;39-46.
67. Yeh H.Y., Pieniazek N., Pieniazek D., Gelderblom H., Luftig R.B. Human adenovirus type 41 contains two fibres. Virus Res. 33:1994;179-198.
68. Zhou X.H., Li Wan Po A. Stability and in vitro absorption of captopril, enalapril and lisinopril across the rat intestine. Biochem. Pharmacol. 47:1994;1121-1126.