3-D intestinal scaffolds for evaluating the therapeutic potential of probiotics

Molecular Pharmaceutics

Volumn 11, Issue 7, 2014, Pages 2030-2039

  Costello, Cait M ^a   Sorna, Rachel M ^a   Goh, Yih Lin ^a   Cengic, Ivana ^a   Jain, Nina K ^a   March, John C ^a  

^a Department of Biological and Environmental Engineering   (United States)

Author keywords

3 D scaffold; intestinal model; probiotics

Indexed keywords

POLYGLACTIN; PROBIOTIC AGENT; TISSUE SCAFFOLD;

ARTICLE; BACTERIUM ADHERENCE; BIOCOMPATIBILITY; BIODEGRADABILITY; CACO 2 CELL LINE; CELL TYPE; COCULTURE; COMMENSAL ESCHERICHIA COLI; ENTEROPATHY; EPITHELIUM CELL; LACTOBACILLUS; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS; SALMONELLA; SMALL INTESTINE; SURFACE TOPOGRAPHY; TOPOGRAPHY; BACTERIUM; BIOMIMETICS; CACO-2 CELL LINE; CELL DIFFERENTIATION; DRUG EFFECTS; DRUG SCREENING; HUMAN; MICROBIOLOGY; PROCEDURES; TISSUE SCAFFOLD;

BACTERIA; BACTERIAL ADHESION; BIOMIMETICS; CACO-2 CELLS; CELL DIFFERENTIATION; DRUG EVALUATION; EPITHELIAL CELLS; HUMANS; INTESTINE, SMALL; PROBIOTICS; TISSUE SCAFFOLDS;

EID: 84903954057     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp5001422     Document Type: Article

References (56)

1. Moon, H. W. Mechanisms in pathogenesis of diarrhea-review J. Am. Vet. Med. Assoc. 1978, 172 (4) 443-448
2. Navaneethan, U.; Giannella, R. A. Mechanisms of infectious diarrhea Nat. Clin. Pract. Gastroenterol. Hepatol. 2008, 5 (11) 637-647
3. Mead, P. S.; Slutsker, L.; Dietz, V.; McCaig, L. F.; Bresee, J. S.; Shapiro, C.; Griffin, P. M.; Tauxe, R. V. Food-related illness and death in the United States Emerging Infect. Dis. 1999, 5 (5) 607-625
4. Palmer, C.; Bik, E. M.; DiGiulio, D. B.; Relman, D. A.; Brown, P. O. Development of the human infant intestinal microbiota PLoS Biol. 2007, 5 (7) 1556-1573
5. Madsen, K.; Cornish, A.; Soper, P.; McKaigney, C.; Jijon, H.; Yachimec, C.; Doyle, J.; Jewell, L.; De Simone, C. Probiotic bacteria enhance murine and human intestinal epithelial barrier function Gastroenterology 2001, 121 (3) 580-591
6. Huang, Y.; Adams, M. C. An in vitro model for investigating intestinal adhesion of potential dairy propionibacteria probiotic strains using cell line C2BBe1 Lett. Appl. Microbiol. 2003, 36 (4) 213-216
7. Servin, A. L.; Coconnier, M. H. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens Best Pract. Res. Clin. Gastroenterol. 2003, 17 (5) 741-754
8. Sartor, R. B. Probiotic therapy of intestinal inflammation and infections Curr. Opin. Gastroenterol. 2005, 21 (1) 44-50
9. Sanchez, B.; Urdaci, M. C.; Margolles, A. Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions Microbiology 2010, 156 (Part 11) 3232-3242
10. Bernardo, D.; Sanchez, B.; Al-Hassi, H. O.; Mann, E. R.; Urdaci, M. C.; Knight, S. C.; Margolles, A. Microbiota/Host Crosstalk Biomarkers: Regulatory Response of Human Intestinal Dendritic Cells Exposed to Lactobacillus Extracellular Encrypted Peptide PLoS One 2012, 7 (5) e36262
11. Shanahan, F. The host-microbe interface within the gut Best Pract. Res. Clin. Gastroenterol. 2002, 16 (6) 915-931
12. Nickerson, C. A.; Richter, E. G.; Ott, C. M. Studying host-pathogen interactions in 3-D: Organotypic models for infectious disease and drug development J. Neuroimmune Pharmacol. 2007, 2 (1) 26-31
13. Marzorati, M.; Van den Abbeele, P.; Possemiers, S.; Benner, J.; Verstraete, W.; Van de Wiele, T. Studying the host-microbiota interaction in the human gastrointestinal tract: basic concepts and in vitro approaches Ann. Microbiol. 2011, 61 (4) 709-715
14. Roeselers, G.; Ponomarenko, M.; Lukovac, S.; Wortelboer, H. M. Ex vivo systems to study host-microbiota interactions in the gastrointestinal tract Best Pract. Res. Clin. Gastroenterol. 2013, 27 (1) 101-113
15. Pfluger, C. A.; McMahon, B. J.; Carrier, R. L.; Burkey, D. D. Precise, biomimetic replication of the multiscale structure of intestinal basement membrane using chemical vapor deposition Tissue Eng., Part A 2013, 19 (5-6) 649-656
16. Wang, L.; Murthy, S. K.; Fowle, W. H.; Barabino, G. A.; Carrier, R. L. Influence of micro-well biomimetic topography on intestinal epithelial Caco-2 cell phenotype Biomaterials 2009, 30 (36) 6825-6834
17. Kim, J.; Hegde, M.; Jayaraman, A. Co-culture of epithelial cells and bacteria for investigating host-pathogen interactions Lab Chip 2010, 10 (1) 43-50
18. Kim, H. J.; Huh, D.; Hamilton, G.; Ingber, D. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow Lab Chip 2012, 12, 2165-2174
19. Barrila, J.; Radtke, A. L.; Crabbe, A.; Sarker, S. F.; Herbst-Kralovetz, M. M.; Ott, C. M.; Nickerson, C. A. Organotypic 3D cell culture models: using the rotating wall vessel to study host-pathogen interactions Nat. Rev. Microbiol. 2010, 8 (11) 791-801
20. Finlay, B. B.; Falkow, S. Salmonella interactions with polarized human intestinal Caco-2 epithelial-cells J. Infect. Dis. 1990, 162 (5) 1096-1106
21. Giannasca, K. T.; Giannasca, P. J.; Neutra, M. R. Adherence of Salmonella typhimurium to Caco-2 cells: Identification of a glycoconjugate receptor Infect. Immun. 1996, 64 (1) 135-145
22. Shah, D. H.; Zhou, X.; Addwebi, T.; Davis, M. A.; Call, D. R. In vitro and in vivo pathogenicity of Salmonella enteritidis clinical strains isolated from North America Arch. Microbiol. 2011, 193 (11) 811-821
23. Gaillard, J. L.; Finlay, B. B. Effect of cell polarization and differentiation on entry of Listeria monocytogenes into the enterocyte-like Caco-2 cell line Infect. Immun. 1996, 64 (4) 1299-1308
24. Carvalho, H. M.; Teel, L. D.; Goping, G.; OBrien, A. D. A three-dimensional tissue culture model for the study of attach and efface lesion formation by enteropathogenic and enterohaemorrhagic Escherichia coli Cellular Microbiology 2005, 7 (12) 1771-1781
25. Gabastou, J. M.; Kerneis, S.; Bernetcamard, M. F.; Barbat, A.; Coconnier, M. H.; Kaper, J. B.; Servin, A. L. Two stages of enteropathogenic Escherichia coli intestinal pathogenicity are up and down-regulated by the epithelial cell differentiation Differentiation 1995, 59 (2) 127-134
26. Coconnier, M. H.; Bernetcamard, 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 1994, 58 (1) 87-94
27. Pereira, S. H. M.; Cervante, M. P.; deBentzmann, S.; Plotkowski, M. C. Pseudomonas aeruginosa entry into Caco-2 cells is enhanced in repairing wounded monolayers Microb. Pathog. 1997, 23 (4) 249-255
28. Finlay, B. B.; Ruschkowski, S.; Dedhar, S. Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells J. Cell Sci. 1991, 99, 283-296
29. Sung, J. H.; Yu, J.; Luo, D.; Shuler, M. L.; March, J. C. Microscale 3-D hydrogel scaffold for biomimetic gastrointestinal (GI) tract model Lab Chip 2011, 11 (3) 389-392
30. Yu, J.; Peng, S.; Luo, D.; March, J. C. In vitro 3D human small intestinal villous model for drug permeability determination Biotechnol. Bioeng. 2012, 109 (9) 2173-2178
31. Esch, M. B.; Sung, J. H.; Yang, J.; Yu, C.; Yu, J.; March, J. C.; Shuler, M. L. On chip porous polymer membranes for integration of gastrointestinal tract epithelium with microfluidic body-on-a-chip devices Biomed. Microdevices 2012, 14 (5) 895-906
32. Costello, C. M.; Hongpeng, J.; Shaffiey, S.; Yu, J.; Jain, N. K.; Hackam, D.; March, J. C. Synthetic Small Intestinal Scaffolds for Improved Studies of Intestinal Differentiation Biotechnol. Bioeng. 2014, 111 (6) 1222-1232
33. Duan, F.; March, J. C. Interrupting Vibrio cholerae infection of human epithelial cells with engineered commensal bacterial signaling Biotechnol. Bioeng. 2008, 101 (1) 128-134
34. Gagnon, M.; Berner, A. Z.; Chervet, N.; Chassard, C.; Lacroix, C. Comparison of the Caco-2, HT-29 and the mucus-secreting HT29-MTX intestinal cell models to investigate Salmonella adhesion and invasion J. Microbiol. Methods 2013, 94 (3) 274-279
35. Steele-Mortimer, O. Infection of epithelial cells with Salmonella enterica Methods Mol. Biol. 2008, 431, 201-211
36. Pinto, M.; Robineleon, S.; Appay, M. D.; Kedinger, M.; Triadou, N.; Dussaulx, E.; Lacroix, B.; Simonassmann, P.; Haffen, K.; Fogh, J.; Zweibaum, A. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture Biol. Cell 1983, 47, 323-330
37. Jumarie, C.; Malo, C. Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro J. Cell. Physiol. 1991, 149 (1) 24-33
38. Basson, M. D.; Turowski, G.; Emenaker, N. J. Regulation of human (Caco-2) intestinal epithelial cell differentiation by extracellular matrix proteins Exp. Cell Res. 1996, 225 (2) 301-305
39. Simon-Assman, P.; Turck, N.; Sidhoum-Jenny, M.; Gradwohl, G.; Kedinger, M. In vitro models of intestinal epithelial cell differentiation Cell Biol. Toxicol. 2007, 23 (4) 241-256
40. Madi, A.; Svinareff, P.; Orange, N.; Feuilloley, M. G. J.; Connil, N. Pseudomonas fluorescens alters epithelial permeability and translocates across Caco-2/TC7 intestinal cells Gut Pathog. 2010, 2 (1) 16
41. Hirakata, Y.; Izumikawa, K.; Yamaguchi, T.; Igimi, S.; Furuya, N.; Maesaki, S.; Tomono, K.; Yamada, Y.; Kohno, S.; Yamaguchi, K.; Kamihira, S. Adherence to and penetration of human intestinal Caco-2 epithelial cell monolayers by Pseudomonas aeruginosa Infect. Immun. 1998, 66 (4) 1748-1751
42. Chauviere, G.; Coconnier, M. H.; Kerneis, S.; Fourniat, J.; Servin, A. L. Adhesion of human Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells J. Gen. Microbiol. 1992, 138 (Part 8) 1689-1696
43. Kerneis, S.; Chauviere, G.; Darfeuille-Michaud, A.; Aubel, D.; Coconnier, M. H.; Joly, B.; Servin, A. L. Expression of receptors for enterotoxigenic Escherichia coli during enterocytic differentiation of human polarized intestinal epithelial cells in culture Infect. Immun. 1992, 60 (7) 2572-2580
44. Grozdanov, L.; Raasch, C.; Schulze, E.; Sonnenborn, U.; Gottschalk, G.; Hacker, J.; Dobrindt, U. Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917 J. Bacteriol. 2004, 186 (16) 5432-5441
45. Bernet, M. F.; Brassart, D.; Neeser, J. R.; Servin, A. L. Lactobacillus acidophilus LA-1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria Gut 1994, 35 (4) 483-489
46. Reid, G.; Burton, J. Use of Lactobacillus to prevent infection by pathogenic bacteria Microbes Infect. 2002, 4 (3) 319-324
47. Lee, Y. K.; Puong, K. Y.; Ouwehand, A. C.; Salminen, S. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli J. Med. Microbiol. 2003, 52 (10) 925-930
48. Jankowska, A.; Laubitz, D.; Antushevich, H.; Zabielski, R.; Grzesiuk, E. Competition of Lactobacillus paracasei with Salmonella enterica for adhesion to Caco-2 cells J. Biomed. Biotechnol. 2008, 10.1155/2008/357964
49. Moussavi, M.; Adams, M. C. An In Vitro Study on Bacterial Growth Interactions and Intestinal Epithelial Cell Adhesion Characteristics of Probiotic Combinations Curr. Microbiol. 2010, 60 (5) 327-335
50. Oelschlaeger, T. A.; Altenhoefer, A.; Hacker, J. Inhibition of Salmonella typhimurium invasion into intestinal cells by the probiotic E. coli strain Nissle 1917 Gastroenterology 2001, 120 (5) A326-A326
51. Altenhoefer, A.; Oswald, S.; Sonnenborn, U.; Enders, C.; Schulze, J.; Hacker, J.; Oelschlaeger, T. A. The probiotic Escherichia coli strain Nissle 1917 interferes with invasion of human intestinal epithelial cells by different enteroinvasive bacterial pathogens FEMS Immunol. Med. Microbiol. 2004, 40 (3) 223-229
52. Schierack, P.; Kleta, S.; Tedin, K.; Babila, J. T.; Oswald, S.; Oelschlaeger, T. A.; Hiemann, R.; Paetzold, S.; Wieler, L. H. E. coli Nissle 1917 Affects Salmonella Adhesion to Porcine Intestinal Epithelial Cells PLoS One 2011, 6 (2) e14712 10.1371/journal.pone.0014712
53. Brown, E. Probiotic Nissle 1917 shown to reduce Salmonella typhimurium intestinal colonization Future Microbiol. 2013, 8 (9) 1060-1060
54. Silva, M.; Jacobus, N. V.; Deneke, C.; Gorbach, S. L. Antimicrobial substance from a human Lactobacillus strain Antimicrob. Agents Chemother. 1987, 31 (8) 1231-1233
55. Coconnier, M. H.; Lievin, V.; BernetCamard, M. F.; Hudault, S.; Servin, A. L. Antibacterial effect of the adhering human Lactobacillus acidophilus strain LB Antimicrob. Agents Chemother. 1997, 41 (5) 1046-1052
56. Storm, D. W.; Koff, S. A.; Horvath, D. J., Jr.; Li, B.; Justice, S. S. In Vitro Analysis of the Bactericidal Activity of Escherichia Coli Nissle 1917 Against Pediatric Uropathogens J. Urol. 2011, 186 (4) 1678-1683