Preventing acute gut wall damage in infectious diarrhoeas with glycosylated dendrimers

EMBO Molecular Medicine

Volumn 4, Issue 9, 2012, Pages 866-881

  Teo, Ian ^a   Toms, Steve M ^b   Marteyn, Benoit ^c   Barata, Teresa S ^a,d   Simpson, Peter ^e   Johnston, Karen A ^b   Schnupf, Pamela ^c   Puhar, Andrea ^c   Bell, Tracey ^b   Tang, Chris ^f   Zloh, Mire ^d   Matthews, Steve ^e   Rendle, Phillip M ^b   Sansonetti, Philippe J ^c   Shaunak, Sunil ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b CALLAGHAN INNOVATION   (New Zealand)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF LONDON   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Dendrimer; Diarrhoea; Infection; Interleukin 6; Nanobiotechnology

Indexed keywords

BETA DEFENSIN; BETA INTERFERON; CD3 ANTIGEN; DENDRIMER; GASTROINTESTINAL AGENT; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; LIPID A; MESSENGER RNA; POLYAMIDOAMINE DENDRIMER GLUCOSAMINE; POLYPROPYLETHERIMINE DENDRIMER GLUCOSAMINE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG SYNTHESIS; EXPERIMENTAL RABBIT; GENE EXPRESSION; GENE EXPRESSION PROFILING; GLYCOSYLATION; GOBLET CELL; HUMAN; HUMAN CELL; INFECTIOUS DIARRHEA; INTESTINE CRYPT; INTESTINE INJURY; INTESTINE VILLUS; INTESTINE WALL; MATHEMATICAL MODEL; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHIGELLOSIS;

ADMINISTRATION, ORAL; ANIMALS; BACTERIAL TRANSLOCATION; DENDRIMERS; DIARRHEA; DISEASE MODELS, ANIMAL; DYSENTERY, BACILLARY; GASTROINTESTINAL AGENTS; GASTROINTESTINAL TRACT; IMMUNOLOGIC FACTORS; INTERLEUKIN-6; INTERLEUKIN-8; RABBITS; SHIGELLA;

EID: 84865764962     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201201290     Document Type: Article

References (67)

1. Abreu MT (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10: 131-144.
2. Abreu MT, Vora P, Faure E, Thomas LS, Arnold ET, Arditi M (2001) Decreased expression of TLR4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial LPS. J Immunol 167: 1609-1616.
3. Arpia N, Godec J, Lau L, Sivick KE, McLaughlin LM, Jones MB, Dracheva T, Peterson SN, Monack DM, Barton GM (2011) TLR signaling is required for Salmonella typhimurium virulence. Cell 144: 675-688.
4. Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C (2011) Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol 15: 36-45.
5. Atala A, Irvine DJ, Moses M, Shaunak S (2010) Wound healing versus regeneration-role of the tissue environment in regenerative medicine. Mat Res Soc Bull 35: 597-606.
6. Barata TS, Shaunak S, Teo I, Zloh M, Brocchini S (2011a) Structural studies of biologically active glycosylated PAMAM dendrimers. J Mol Model 17: 2051-2060.
7. Barata TS, Teo I, Brocchini S, Zloh M, Shaunak S (2011b) Partially glycosylated dendrimers block MD-2 and prevent TLR4-MD-2-LPS complex mediated cytokine responses. PLoS Comput Biol 7: e1002095.
8. Barata T, Teo I, Lalwani S, Simanek E, Zloh M, Shaunak S (2011c) Computational design principles for bioactive dendrimer based constructs as antagonists of the TLR4-MD-2-LPS complex. Biomaterials 32: 8702-8711.
9. Barreau F, Meinzer U, Chareyre F, Berrebi D, Niwa-Kawakita M, Dussaillant M, Foligne B, Ollendorff V, Heyman M, Bonacorsi S, et al (2007) CARD15/NOD2 is required for Peyer's patches homeostasis in mice. PLoS One 2: e523.
10. Bruckner MMC, Finlay BB (2011) Innate immunity cues virulence. Nature 472: 179-180.
11. Buchholz U, Bernard H, Werber D, Böhmer M, Remschmidt C, Wilking H, Deleré Y, van der Heiden M, Adlhoch C, Dreesman J et al (2011) German outbreak of Escherichia coli O104: H4 associated with sprouts. NEJM 365: 1763-1770.
12. Coron E, Flamant M, Aubert P, Wedel T, Pedron T, Letessier E, Galmiche JP, Sansonetti PJ, Neunlist M (2009) Characterisation of early mucosal and neuronal lesions following Shigella flexneri infection in human colon. PLoS One 4: e4713.
13. Corware K, Harris D, Teo I, Rogers M, Naresh K, Müller I, Shaunak S (2011) Accelerated healing of cutaneous leishmaniasis in non-healing BALB/c mice using water soluble amphotericin B-polymethacrylic acid. Biomaterials 32: 8029-8039.
14. Florence AT, Sakthivel T, Toth I (2000) Oral uptake and translocation of a polylysine dendrimer with a lipid surface. J Controlled Release 65: 253-259.
15. Harendra de Silva DG, Mendis LN, Sheron N, Alexander GJ, Candy DC, Chart H, Rowe B (1993) Concentrations of IL-6 and TNF in serum and stools of children with Shigella dysenteriae 1 infection. Gut 34: 194-198.
16. Hayder M, Poupot M, Baron M, Nigon D, Turrin CO, Caminade AM, Majoral JP, Eisenberg RA, Fournié JJ, Cantagrel A, et al (2011) A phosphorus-based dendrimer targets inflammation and osteoclastogenesis in experimental arthritis. Sci Transl Med 3: 1-11.
17. Hourani R, Kakkar A (2010) Advances in the elegance of chemistry in designing dendrimers. Macromol Rapid Commun 31: 947-974.
18. Inman LR, Cantey JR (1984) Peyer's patch lymphoid follicle epithelial adherence of a rabbit enteropathogenic Escherichia coli. J Clin Invest 74: 90-95.
19. Islam D, Christensson B (2000) Disease-dependent changes in T-cell populations in patients with Shigellosis. APMIS 108: 251-260.
20. Islam MM, Azad AK, Bardhan PK, Raqib R, Islam D (1994) Pathology of shigellosis and its complications. Histopathology 24: 65-71.
21. Islam D, Bandholtz L, Nilsson J, Wigzell H, Christensson B, Agerberth B, Gudmundsson G (2001) Downregulation of bactericidal peptides in enteric infections: a novel immune escape mechanism with bacterial DNA as a potential regulator. Nat Med 7: 180-185.
22. Ismail AS, Behrendt CL, Hooper LV (2009) Reciprocal interactions between commensal bacteria and γδ intraepithelial lymphocytes during mucosal injury. J Immunol 182: 3047-3054.
23. Ismail AS, Severson KM, Vaishnava S, Behrendt CL, Yu X, Benjamin JL, Ruhn KA, Hou B, DeFranco AL, Yarovinsky F, et al (2011) γδ intraepithelial lymphocytes are essential mediators of host-microbial homeostasis at the intestinal mucosal surface. Proc Natl Acad Sci USA 108: 8743-8748.
24. Izcue A, Coombes JL, Powrie F (2009) Regulatory lymphocytes and intestinal inflammation. Ann Rev Immunol 27: 313-338.
25. Jain S, Kaur A, Puri R, Utreja P, Jain A, Bhide M, Ratnam R, Singh V, Patil AS, Jayaraman N, et al (2010) PETIM dendrimer: a novel non-toxic dendrimer for sustained drug delivery. Eur J Med Chem 45: 4997-5005.
26. Jayamurugan G, Jayaraman N (2006) Synthesis of large generation PETIM dendrimers. Tetrahedron 62: 9582-9588.
27. Kannan S, Dai H, Navath RS, Balakrishnan B, Jyoti A, Janisse J, Romero R, Kannan RM (2012) Dendrimer-based postnatal therapy for neuroinflammation and cerebral palsy in a rabbit model. Sci Transl Med 4: 1-11.
28. Konradt C, Frigimelica E, Nothelfer K, Puhar A, Salgado-Pabon W, di Bartolo V, Scott-Algara D, Rodrigues CD, Sansonetti PJ, Phalipon A (2011) The Shigella flexneri type III secretion system effector IpgD inhibits T cell migration by manipulating host phosphoinositide metabolism. Cell Host Microbe 9: 263-272.
29. Kosek M, Yori PP, Olortegui MP (2010) Shigellosis update: advancing antibiotic resistance, investment empowered vaccine development, and green bananas. Curr Opin Infect Dis 23: 475-480.
30. Krishna TR, Jayaraman N (2003) Synthesis of PETIM dendrimers and evaluation of their cytotoxic properties. J Org Chem 68: 9694-9704.
31. Kutuzova GD, Albrecht RM, Erickson CM, Qureshi N (2001) Diphosphoryl lipid A from Rhodobacter sphaeroides blocks the binding and internalization of LPS in RAW 264.7. J Immunol 167: 482-489.
32. Lalwani S, Chouai A, Perez LM, Santiago V, Shaunak S, Simanek EE (2009a) Mimicking PAMAM dendrimers with ampholytic, hybrid triazine dendrimers: a comparison of dispersity and stability. Macromolecules 42: 6723-6732.
33. Lalwani S, Venditto VJ, Chouai A, Rivera GE, Shaunak S, Simanek EE (2009b) Electrophoretic behaviour of anionic triazine & PAMAM dendrimers: methods for improving resolution & assessing purity using capillary electrophoresis. Macromolecules 42: 3152-3161.
34. Lembo-Fazio L, Nigro G, Noël G, Rossi G, Chiara F, Tsilingiri K, Rescigno M, Rasola A, Bernardini ML (2011) Gadd45α activity is the principal effector of Shigella mitochondria-dependent epithelial cell death in vitro and ex vivo. Cell Death Dis 2: e122. DOI:10.1038/cddis.2011.4.
35. Lindberg AA, Karnell A, Weintraub A (1991) The LPS of Shigella bacteria as a virulence factor. Rev Infect Dis 13: S279- S284.
36. 125I-labelled PAMAM dendrimers in vivo. J Controlled Release 65: 133-148.
37. Menjoge AR, Kannan RM, Tomalia DA (2010) Dendrimer-based drug and imaging conjugates: design considerations for nanomedical applications. Drug Discovery Today 15: 171-185.
38. Molinaro A, Silipo A, Castro CD, Sturiale L, Nigro G, Garozzo D, Bernardini ML, Lanzetta R, Parrilli M (2008) Full structural characterization of Shigella flexneri M90T serotype 5 wild-type R-LPS and its δgalU mutant: glycine residue location in the inner core of the LPS. Glycobiology 18: 260-269.
39. Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H, Kronenberg M (2009) IL-10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 10: 1178-1184.
40. Ohto U, Fukase K, Miyake K, Satow Y (2007) Crystal structures of human MD-2 and its complex with antiendotoxic Lipid IVa. Science 316: 1632-1634.
41. Ohto U, Fukase K, Miyake K, Shimizu T (2012) Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Proc Natl Acad Sci USA 109: 7421-7426.
42. O'Neill LAJ (2005) TLRs play good cop, bad cop in the lung. Nat Med 11: 1161-1162.
43. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO (2009) The structural basis of LPS recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195.
44. Perdomo OJ, Cavaillon J, Huerre M, Gounon P, Sansonetti PJ (1994) Acute inflammation causes epithelial invasion and mucosal destruction in experimental Shigellosis. J Exp Med 180: 1307-1319.
45. Rallabhandi P, Awomoyi A, Thomas KE, Phalipon A, Fujimoto Y, Fukase K, Kusumoto S, Qureshi N, Sztein M, Vogel S (2008) Differential activation of human TLR4 by Escherichia coli and Shigella flexneri 2a LPS: combined effects of Lipid A acylation state and TLR4 polymorphisms on signalling. J Immunol 180: 1139-1147.
46. Raqib R, Reinholt FP, Bardhan PK, Karnell A, Lindberg AA (1994) Immunopathological patterns in the rectal mucosa of patients with shigellosis: expression of HLA-DR antigens and T lymphocyte subsets. APMIS 102: 371-380.
47. Raqib R, Lindberg AA, Wretlind B, Bardhan PK, Andersson U, Andersson J (1995) Persistence of local cytokine production in Shigellosis in acute and convalescent stages. Infect Immun 63: 289-296.
48. Raqib R, Ekberg C, Sharkar P, Bardhan PK, Zychlinsky A, Sansonetti PJ, Andersson J (2002) Apoptosis in acute shigellosis is associated with increased production of Fas/Fas ligand, perforin, caspase-1, and caspase-3 but reduced production of Bcl-2 and IL-2. Infect Immun 70: 3199-3207.
49. Rathinam VA, Appledorn DM, Hoag KA, Amalfitano A, Mansfield LS (2009) Campylobacter jejuni induced activation of dendritic cells involves cooperative signaling through TLR4-MyD88 and TLR4-TRIF axes. Infect Immun 77: 2499-2507.
50. Ryan A, Lynch M, Smith SM, Amu S, Nel HJ, McCoy CE, Dowling JK, Draper E, O'Reilly V, McCarthy C et al (2011) A role for TLR4 in Clostridium difficile infection and the recognition of surface layer proteins. PLoS Pathog 7: e1002076.
51. Sabroe I, Jones EC, Usher LR, Whyte MK, Dower SK (2002) TLR2 and TLR4 in human peripheral blood granulocytes: a critical role for monocytes in leukocyte LPS responses. J Immunol 168: 4701-4710.
52. Sakthivel T, Toth I, Florence AT (1999) Distribution of a lipidic 2.5 nm diameter dendrimer carrier after oral administration. Int J Pharm 183: 51-55.
53. Sam S, Touahir L, Andresa JS, Allongue P, Chazalviel JN, Gouget-Laemmel AC, de Villeneuve CH, Moraillon A, Ozanam F, Gabouze N, et al (2010) Semiquantitative study of the EDC/NHS activation of acid terminal groups at modified porous silicon surfaces. Langmuir 26: 809-814.
54. Schnupf P, Sansonetti PJ (2012) Quantitative RT-PCR profiling of the rabbit immune response: assessment of acute Shigella flexneri infection. PLoS One 7: e36446. DOI:10.1371/journal.pone.0036446.
55. Sellge G, Magalhaes JG, Konradt C, Fritz JH, Salgado-Pabon W, Eberl G, Bandeira A, Di Santo JP, Sansonetti PJ, Phalipon A (2010) Th17 cells are the dominant T cell subtype primed by Shigella flexneri mediating protective immunity. J Immunol 184: 2076-2085.
56. Shaunak S, Thomas S, Gianasi E, Godwin A, Jones E, Teo I, Mireskandari K, Luthert P, Duncan R, Patterson S, et al (2004) Polyvalent dendrimer glucosamine conjugates prevent scar tissue formation. Nat Biotechnol 22: 977-985.
57. Singer M, Sansonetti PJ (2004) IL-8 is a key chemokine regulating neutrophils recruitment in a new mouse model of Shigella-induced colitis. J Immunol 173: 4197-4206.
58. Sperandio B, Regnaul B, Guo J, Zhang Z, Stanley SL, Jr, Sansonetti PJ, Pédron T (2008) Virulent Shigella flexneri subverts the host innate immune response through manipulation of antimicrobial peptide gene expression. J Exp Med 205: 1121-1132.
59. Takayama K, Qureshi N, Beutler B, Kirkland TN (1989) Diphosphoryl Lipid A from Rhodopseudomonas sphaeroides ATCC 17023 blocks induction of cachectin in macrophages by LPS. Infect Immun 57: 1336-1338.
60. Takeuchi A (1967) Electron microscope studies of experimental Salmonella infection. Am J Pathol 50: 109-136.
61. Takeuchi A, Formal SB, Sprinz H (1968) Experimental acute colitis in the Rhesus monkey following peroral infection with Shigella flexneri. Am J Pathol 52: 503-529.
62. Takeuchi A, Inman LR, O'Hanley PD, Cantey JR, Lushbaugh WB (1978) Scanning and transmission electron microscopic study of Escherichia coli O15 (RDEC-1) enteric infection in rabbits. Infect Immun 19: 686-694.
63. Unutmaz D, Pulendran B (2009) The gut feeling of Treg cells: IL-10 is the silver lining during colitis. Nat Immunol 10: 1141-1143.
64. Vaisman N, Leibovitz E, Dagan R, Barak V (2003) The involvement of IL-6 and IL-8 in acute invasive gastroenteritis of children. Cytokine 22: 194-197.
65. West NP, Sansonetti P, Mounier J, Exley RM, Parsot C, Guadagnini S, Prevost MC, Prochnicka-Chalufour A, Delepierre M, Tanguy M, et al (2005) Optimization of virulence functions through glucosylation of Shigella LPS. Science 307: 1313-1317.
66. Yu L, Phillips RL, Zhang D, Teghanemt A, Weiss JP, Gioannini TL (2012) Studies of hexaacylated endotoxin bound to wild-type and F126A mutant MD-2 and MD-2-TLR4 ectodomain complexes. J Biol Chem 287: 16346-16355.
67. Zychlinsky A, Thirumalai K, Arondel J, Cantey JR, Aliprantis AO, Sansonetti PJ (1996) In vivo apoptosis in Shigella flexneri infections. Infect Immun 64: 5357-5365.