Adenoviral transduction of enterocytes and M-cells using in vitro models based on caco-2 cells: The coxsackievirus and adenovirus receptor (CAR) mediates both apical and basolateral transduction

Molecular Pharmaceutics

Volumn 7, Issue 3, 2010, Pages 619-629

  Kesisoglou, Filippos ^a,b   Schmiedlin Ren, Phyllissa ^b   Fleisher, David ^a   Zimmermann, Ellen M ^b  

^a Department of Pharmacology and Toxicology   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Adenovirus; Caco 2 cells; Cell culture; Coculture; Coxsackievirus and adenovirus receptor; Enterocytes; M cells; Vector

Indexed keywords

COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; HEPARIN; INTEGRIN;

ADENOVIRUS; ANIMAL EXPERIMENT; ARTICLE; CARCINOMA CELL; CELL DIFFERENTIATION; CELL INTERACTION; CELL STRAIN CACO 2; COCULTURE; COLON ADENOCARCINOMA; CONTROLLED STUDY; COXSACKIE VIRUS; DOSE RESPONSE; GENE DELIVERY SYSTEM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; IN VITRO STUDY; INTESTINE CELL; LYMPHOCYTE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAJI CELL; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; ALKALINE PHOSPHATASE; ANIMALS; CACO-2 CELLS; CELL LINE; CELLS, CULTURED; COCULTURE TECHNIQUES; ENTEROCYTES; HUMANS; LYMPHOCYTES; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, TRANSMISSION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSDUCTION, GENETIC;

EID: 77953252401     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp9001377     Document Type: Article

References (40)

1. Hidalgo, I. J.; Raub, T. J.; Borchardt, R. T. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability Gastroenterology 1989, 96, 736-749
2. Walter, E.; Croyle, M. A.; Davidson, B. L.; Roessler, B. J.; Hilfinger, J. M.; Amidon, G. L. Adenovirus mediated gene transfer to intestinal epithelial cells as a potential approach for oral delivery of peptides and proteins J. Controlled Release 1997, 46, 75-87
3. Walter, E.; Croyle, M. A.; Roessler, B. J.; Amidon, G. L. The absence of accessible vitronectin receptors in differentiated tissue hinders adenoviral-mediated gene transfer to the intestinal epithelium in vitro Pharm. Res. 1997, 14, 1216-1222
4. Croyle, M. A.; Walter, E.; Janich, S.; Roessler, B. J.; Amidon, G. L. Role of integrin expression in adenovirus-mediated gene delivery to the intestinal epithelium Hum. Gene Ther. 1998, 9, 561-573
5. Bergelson, J. M.; Cunningham, J. A.; Droguett, G.; Kurt-Jones, E. A.; Krithivas, A.; Hong, J. S.; Horwitz, M. S.; Crowell, R. L.; Finberg, R. W. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5 Science 1997, 275, 1320-1323
6. Walters, R. W.; Grunst, T.; Bergelson, J. M.; Finberg, R. W.; Welsh, M. J.; Zabner, J. Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia J. Biol. Chem. 1999, 274, 10219-10226
7. Dechecchi, M. C.; Tamanini, A.; Bonizzato, A.; Cabrini, G. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions Virology 2000, 268, 382-390
8. Dechecchi, M. C.; Melotti, P.; Bonizzato, A.; Santacatterina, M.; Chilos, M.; Cabrini, G. Heparan sulfate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5 J. Virol. 2001, 75, 8772-8780
9. Neutra, M. R.; Pringault, E.; Kraehenbuhl, J. P. Antigen sampling across epithelial barriers and induction of mucosal immune responses Annu. Rev. Immunol. 1996, 14, 275-300
10. Wittig, B. M.; Zeitz, M. The gut as an organ of immunology Int. J. Colorectal Dis. 2003, 18, 181-187
11. Spahn, T. W.; Kucharzik, T. Modulating the intestinal immune system: the role of lymphotoxin and GALT organs Gut 2004, 53, 456-65
12. Kernéis, S.; Bogdanova, A.; Kraehenbuhl, J. P.; Pringault, E. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria Science 1997, 277, 949-952
13. Gullberg, E.; Leonard, M.; Karlsson, J.; Hopkins, A. M.; Brayden, D.; Baird, A. W.; Artursson, P. Expression of specific markers and particle transport in a new human intestinal M-cell model Biochem. Biophys. Res. Commun. 2000, 279, 808-813
14. Hsu, K. H.; Lonberg-Holm, K.; Alstein, B.; Crowell, R. L. A monoclonal antibody specific for the cellular receptor for the group B coxsackieviruses J. Virol. 1988, 62, 1647-1652
15. Gerard, R. D.; Meidell, R. S. Adenovirus Vectors. In DNA Cloning 4: A Practical Approach-Mammalian Systems, 2nd ed.; Glover, D. M.; Hames, B. D., Eds.; Oxford University Press: Oxford, U.K., 1995; pp 285 - 305.
16. Croyle, M. A.; Anderson, D. J.; Roessler, B. J.; Amidon, G. L. Development of a Highly Efficient Purification Process for Recombinant Adenoviral Vectors for Oral Gene Delivery Pharm. Dev. Technol. 1998, 3, 365-372
17. Calhau, C.; Martel, F.; Pinheiro-Silva, S.; Pinheiro, H.; Soares-da-Silva, P.; Hip-lito-Reis, C.; Azevedo, I. Modulation of Insulin Transport in Rat Brain Microvessel Endothelial Cells by an Ecto-Phosphatase Activity J. Cell. Biochem. 2002, 84, 389-400
18. Kesisoglou, F.; Schmiedlin-Ren, P.; Fleisher, D.; Roessler, B.; Zimmermann, E. M. Restituting intestinal epithelial cells exhibit increased transducibility by adenoviral vectors J. Gene Med. 2006, 8, 1379-1392
19. Bergelson, J. M. Receptors mediating adenovirus attachment and internalization Biochem. Pharmacol. 1999, 5, 975-979
20. Russell, W. C. Update on adenovirus and its vectors J. Gen. Virol. 2000, 81 (11) 2573-2604
21. Nemerow, G. R.; Stewart, P. L. Role of alpha(v) integrins in adenovirus cell entry and gene delivery Microbiol. Mol. Biol. Rev. 1999, 63, 725-734
22. Wickham, T. J.; Mathias, P.; Cheresh, D. A.; Nemerow, G. R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment Cell 1993, 73, 309-319
23. Pickles, R. J.; Fahrner, J. A.; Petrella, J. M.; Boucher, R. C.; Bergelson, J. M. Retargeting the coxsackievirus and adenovirus receptor to the apical surface of polarized epithelial cells reveals the glycocalyx as a barrier to adenovirus-mediated gene transfer J. Virol. 2000, 74, 6050-6057
24. Zabner, J.; Zeiher, B. G.; Friedman, E.; Welsh, M. J. Adenovirus-mediated gene transfer to ciliated airway epithelia requires prolonged incubation time J. Virol. 1996, 70, 6994-7003 (Pubitemid 26307414)
25. Zabner, J.; Freimuth, P.; Puga, A.; Fabrega, A.; Welsh, M. J. Lack of high affinity fiber receptor activity explains the resistance of ciliated airway epithelia to adenovirus infection J. Clin. Invest. 1997, 100, 1144-1149
26. Cohen, C. J.; Shieh, J. T.; Pickles, R. J.; Okegawa, T.; Hsieh, J. T.; Bergelson, J. M. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 15191-15196
27. Walters, R. W.; Freimuth, P.; Moninger, T.; Ganske, I.; Zabner, J.; Welsh, M. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape Cell 2002, 110, 789-799
28. Vachon, P. H.; Durand, J.; Beaulieu, J. F. Basement membrane formation and re-distribution of the beta 1 integrins in a human intestinal co-culture system Anat. Rec. 1993, 235, 567-576
29. Coconnier, M. H.; Bernet-Camard, M. F.; Servin, A. L. How intestinal epithelial cell differentiation inhibits the cell-entry of Yersinia pseudotuberculosis in colon carcinoma Caco-2 cell line in culture Differentiation 2000, 58, 87-94
30. Esclatine, A.; Bellon, A.; Michelson, S.; Servin, A. L.; Quero, A. M.; Geniteau-Legendre, M. Differentiation-dependent redistribution of heparan sulfate in epithelial intestinal Caco-2 cells leads to basolateral entry of cytomegalovirus Virology 2001, 289, 23-33
31. Mertens, G.; Van der Schueren, B.; van den Berghe, H.; David, G. Heparan sulfate expression in polarized epithelial cells: the apical sorting of glypican (GPI-anchored proteoglycan), is inversely related to its heparan sulfate content J. Cell Biol. 1996, 132, 487-497
32. Salmivirta, M.; Safaiyan, F.; Prydz, K.; Andresen, M. S.; Aryan, M.; Kolset, S. O. Differentiation-associated modulation of heparan sulfate structure and function in CaCo-2 colon carcinoma cells Glycobiology 1998, 8, 1029-1036
33. Cheng, X.; Ming, X.; Croyle, M. A. PEGylated adenoviruses for gene delivery to the intestinal epithelium by the oral route Pharm. Res. 2003, 20, 1444-1451
34. 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. 1998, 9, 1313-1321
35. Kernéis, S.; Caliot, E.; Stubbe, H.; Bogdanova, A.; Kraehenbuhl, J.; Pringault, E. Molecular studies of the intestinal mucosal barrier physiopathology using cocultures of epithelial and immune cells: a technical update Microbes Infect. 2000, 2, 1119-1124
36. Caliot, E.; Libon, C.; Kernéis, S.; Pringault, E. Translocation of ribosomal immunostimulant through an in vitro-reconstituted digestive barrier containing M-like cells Scand. J. Immunol. 2000, 52, 588-594
37. Liang, E.; Kabcenell, A. K.; Coleman, J. R.; Robson, J.; Ruffles, R.; Yazdanian, M. Permeability measurement of macromolecules and assessment of mucosal antigen sampling using in vitro converted M cells J. Pharmacol. Toxicol. Methods 2001, 46, 93-101
38. van der Lubben, I. M.; van Opdorp, F. A.; Hengeveld, M. R.; Onderwater, J. J.; Koerten, H. K.; Verhoef, J. C.; Borchard, G.; Junginger, H. E. Transport of chitosan microparticles for mucosal vaccine delivery in a human intestinal M-cell model J. Drug Targeting 2002, 10, 449-456
39. Lo, D.; Tynan, W.; Dickerson, J.; Scharf, M.; Cooper, J.; Byrne, D.; Brayden, D.; Higgins, L.; Evans, C.; O'Mahony, D. J. Cell culture modeling of specialized tissue: identification of genes expressed specifically by follicle-associated epithelium of Peyer's patch by expression profiling of Caco-2/Raji co-cultures Int. Immunol. 2004, 16, 91-99
40. Leon, R. P.; Hedlund, T.; Meech, S. J.; Li, S.; Schaack, J.; Hunger, S. P.; Duke, R. C.; DeGregori, J. Adenoviral-mediated gene transfer in lymphocytes Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 13159-13164