452
Views
41
CrossRef citations to date
0
Altmetric
Review

Carbohydrate-based Clostridium difficile vaccines

, , , , , , , , , & show all
Pages 421-431 | Published online: 09 Jan 2014

References

  • O’Donoghue C, Kyne L. Update on Clostridium difficile infection. Curr. Opin. Gastroenterol. 27(1), 38–47 (2011).
  • Lee BY, Popovich MJ, Tian Y et al. The potential value of Clostridium difficile vaccine: an economic computer simulation model. Vaccine 28(32), 5245–5253 (2010).
  • Kelly CP, LaMont JT. Clostridium difficile–more difficult than ever. N. Engl. J. Med. 359(18), 1932–1940 (2008).
  • Johnson S, Clabots CR, Linn FV, Olson MM, Peterson LR, Gerding DN. Nosocomial Clostridium difficile colonisation and disease. Lancet 336(8707), 97–100 (1990).
  • McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N. Engl. J. Med. 320(4), 204–210 (1989).
  • Kyne L, Warny M, Qamar A, Kelly CP. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N. Engl. J. Med. 342(6), 390–397 (2000).
  • Riggs MM, Sethi AK, Zabarsky TF, Eckstein EC, Jump RL, Donskey CJ. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents. Clin. Infect. Dis. 45(8), 992–998 (2007).
  • Rebeaud F, Bachmann MF. Immunization strategies for Clostridium difficile infections. Expert Rev. Vaccines 11(4), 469–479 (2012).
  • Siddiqui F, O’Connor JR, Nagaro K et al. Vaccination with parenteral toxoid B protects hamsters against lethal challenge with toxin A-negative, toxin B-positive clostridium difficile but does not prevent colonization. J. Infect. Dis. 205(1), 128–133 (2012).
  • Lowy I, Molrine DC, Leav BA et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N. Engl. J. Med. 362(3), 197–205 (2010).
  • Ganeshapillai J, Vinogradov E, Rousseau J, Weese JS, Monteiro MA. Clostridium difficile cell-surface polysaccharides composed of pentaglycosyl and hexaglycosyl phosphate repeating units. Carbohydr. Res. 343(4), 703–710 (2008).
  • Bertolo L, Boncheff AG, Ma Z et al. Clostridium difficile carbohydrates: glucan in spores, PSII common antigen in cells, immunogenicity of PSII in swine and synthesis of a dual C. difficile-ETEC conjugate vaccine. Carbohydr. Res. 354, 79–86 (2012).
  • Reid CW, Vinogradov E, Li J, Jarrell HC, Logan SM, Brisson JR. Structural characterization of surface glycans from Clostridium difficile. Carbohydr. Res. 354, 65–73 (2012).
  • Adamo R, Romano MR, Berti F et al. Phosphorylation of the synthetic hexasaccharide repeating unit is essential for the induction of antibodies to Clostridium difficile PSII cell wall polysaccharide. ACS Chem. Biol. 7(8), 1420–1428 (2012).
  • Danieli E, Lay L, Proietti D, Berti F, Costantino P, Adamo R. First synthesis of C. difficile PS-II cell wall polysaccharide repeating unit. Org. Lett. 13(3), 378–381 (2011).
  • Oberli MA, Hecht ML, Bindschädler P, Adibekian A, Adam T, Seeberger PH. A possible oligosaccharide-conjugate vaccine candidate for Clostridium difficile is antigenic and immunogenic. Chem. Biol. 18(5), 580–588 (2011).
  • Martin CE, Weishaupt MW, Seeberger PH. Progress toward developing a carbohydrate-conjugate vaccine against Clostridium difficile ribotype 027: synthesis of the cell-surface polysaccharide PS-I repeating unit. Chem. Commun. (Camb.) 47(37), 10260–10262 (2011).
  • Jiao Y. An anti-Clostridium difficile vaccine: chemical synthesis of the pentasaccharide repeating unit of polysaccharide PS-I. MSc Thesis. University of Guelph Press, Guelph, ON, Canada (2012).
  • Pfeifer G, Schirmer J, Leemhuis J et al. Cellular uptake of Clostridium difficile toxin B. Translocation of the N-terminal catalytic domain into the cytosol of eukaryotic cells. J. Biol. Chem. 278(45), 44535–44541 (2003).
  • Geurtsen J, Chedammi S, Mesters J et al. Identification of mycobacterial α-glucan as a novel ligand for DC-SIGN: involvement of mycobacterial capsular polysaccharides in host immune modulation. J. Immunol. 183(8), 5221–5231 (2009).
  • Dinadayala P, Lemassu A, Granovski P, Cérantola S, Winter N, Daffé M. Revisiting the structure of the anti-neoplastic glucans of Mycobacterium bovis Bacille Calmette–Guerin. Structural analysis of the extracellular and boiling water extract-derived glucans of the vaccine substrains. J. Biol. Chem. 279(13), 12369–12378 (2004).
  • Papp-Szabó E, Kanipes MI, Guerry P, Monteiro MA. Cell-surface α-glucan in Campylobacter jejuni 81-176. Carbohydr. Res. 340(13), 2218–2221 (2005).
  • Ferreira JA, Pires C, Paulo M et al. Bioaccumulation of amylose-like glycans by Helicobacter pylori. Helicobacter 14(6), 559–570 (2009).
  • Hobson PN, Nasr H. An amylopectin-type polysaccharide synthesized from sucrose by Clostridium butyricum. J. Chem. Soc. 1951, 1855–1857 (1951).
  • Whyte JN, Strasdine GA. An intracellular α-d-glucan from Clostridium botulinum, type E. Carbohydr. Res. 25(2), 435–441 (1972).
  • Strasdine GA. The role of intracellular glucan in endogenous fermentation and spore maturation in Clostridium botulinum type E. Can. J. Microbiol. 18(2), 211–217 (1972).
  • Charnock SJ, Davies GJ. Structure of the nucleotide-diphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed forms. Biochemistry 38(20), 6380–6385 (1999).
  • Dong S, McPherson SA, Wang Y et al. Characterization of the enzymes encoded by the anthrose biosynthetic operon of Bacillus anthracis. J. Bacteriol. 192(19), 5053–5062 (2010).
  • Cappelletti E, Romano MR, Cakici OS et al. Conjugate vaccine against Clostridium difficile. Gycoconj. J. 28(5), 265 (2011).
  • Ma Z, Bertolo L, Arar S, Monteiro MA. TEMPO-mediated glycoconjugation: a scheme for the controlled synthesis of polysaccharide conjugates. Carbohydr. Res. 346(2), 343–347 (2011).
  • Båverud V, Franklin A, Gunnarsson A, Gustafsson A, Hellander-Edman A. Clostridium difficile associated with acute colitis in mares when their foals are treated with erythromycin and rifampicin for Rhodococcus equi pneumonia. Equine Vet. J. 30(6), 482–488 (1998).
  • Songer JG, Post KW, Larson DJ, Jost BH, Glock RD. Infection of neonatal swine with Clostridium difficile. Swine Health Prod. 8(4) 185–189 (2009).
  • Barbut F, Petit JC. Epidemiology of Clostridium difficile-associated infections. Clin. Microbiol. Infect. 7(8), 405–410 (2001).
  • Weese JS, Staempfli HR, Prescott JF. A prospective study of the roles of clostridium difficile and enterotoxigenic Clostridium perfringens in equine diarrhoea. Equine Vet. J. 33(4), 403–409 (2001).
  • Weese JS, Weese HE, Bourdeau TL, Staempfli HR. Suspected Clostridium difficile-associated diarrhea in two cats. J. Am. Vet. Med. Assoc. 218(9), 1436–1439, 1421 (2001).
  • Larson HE, Price AB, Honour P, Borriello SP. Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet 1(8073), 1063–1066 (1978).
  • Jones MA, Hunter D. Isolation of Clostridium difficile from pigs. Vet. Rec. 112(11), 253 (1983).
  • Waters EH, Orr JP, Clark EG, Schaufele CM. Typhlocolitis caused by Clostridium difficile in suckling piglets. J. Vet. Diagn. Invest. 10(1), 104–108 (1998).
  • Songer JG, Anderson MA. Clostridium difficile: an important pathogen of food animals. Anaerobe 12(1), 1–4 (2006).
  • Jones RL, Adney WS, Shideler RK. Isolation of Clostridium difficile and detection of cytotoxin in the feces of diarrheic foals in the absence of antimicrobial treatment. J. Clin. Microbiol. 25(7), 1225–1227 (1987).
  • Perrin J, Cosmetatos I, Gallusser A, Lobsiger L, Straub R, Nicolet J. Clostridium difficile associated with typhlocolitis in an adult horse. J. Vet. Diagn. Invest. 5(1), 99–101 (1993).
  • Magdesian KG, Hirsh DC, Jang SS, Hansen LM, Madigan JE. Characterization of Clostridium difficile isolates from foals with diarrhea: 28 cases (1993–1997). J. Am. Vet. Med. Assoc. 220(1), 67–73 (2002).
  • Arroyo LG, Kruth SA, Willey BM, Staempfli HR, Low DE, Weese JS. PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. J. Med. Microbiol. 54(Pt 2), 163–166 (2005).
  • Jhung MA, Thompson AD, Killgore GE et al. Toxinotype V Clostridium difficile in humans and food animals. Emerging Infect. Dis. 14(7), 1039–1045 (2008).
  • Rodriguez-Palacios A, Stämpfli HR, Duffield T et al. Clostridium difficile PCR ribotypes in calves, Canada. Emerging Infect. Dis. 12(11), 1730–1736 (2006).
  • Keessen EC, Gaastra W, Lipman LJ. Clostridium difficile infection in humans and animals, differences and similarities. Vet. Microbiol. 153(3–4), 205–217 (2011).
  • Hopman NE, Keessen EC, Harmanus C et al. Acquisition of Clostrium difficile by piglets. Vet. Microbiol. 149(1–2), 186–192 (2011).
  • Thean S, Elliott B, Riley TV. Clostridium difficile in horses in Australia – a preliminary study. J. Med. Microbiol. 60(Pt 8), 1188–1192 (2011).
  • Tsuji M, Suzuki K, Kitamura H et al. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29(2), 261–271 (2008).
  • Brandtzaeg P. Role of secretory antibodies in the defence against infections. Int. J. Med. Microbiol. 293(1), 3–15 (2003).
  • Michetti P, Mahan MJ, Slauch JM, Mekalanos JJ, Neutra MR. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60(5), 1786–1792 (1992).
  • Monteiro MA, Baqar S, Hall ER et al. Capsule polysaccharide conjugate vaccine against diarrheal disease caused by Campylobacter jejuni. Infect. Immun. 77(3), 1128–1136 (2009).
  • Gastinel LN, Simister NE, Bjorkman PJ. Expression and crystallization of a soluble and functional form of an Fc receptor related to class I histocompatibility molecules. Proc. Natl Acad. Sci. USA 89(2), 638–642 (1992).
  • Israel EJ, Taylor S, Wu Z et al. Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells. Immunology 92(1), 69–74 (1997).
  • Yoshida M, Claypool SM, Wagner JS et al. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 20(6), 769–783 (2004).
  • Martinoli C, Chiavelli A, Rescigno M. Entry route of Salmonella typhimurium directs the type of induced immune response. Immunity 27(6), 975–984 (2007).
  • Monteiro RC, Van De Winkel JG. IgA Fc receptors. Annu. Rev. Immunol. 21, 177–204 (2003).
  • Kadaoui KA, Corthésy B. Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer’s patches with restriction to mucosal compartment. J. Immunol. 179(11), 7751–7757 (2007).
  • Iwasaki A, Kelsall BL. Freshly isolated Peyer’s patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J. Exp. Med. 190(2), 229–239 (1999).
  • Johal SS, Lambert CP, Hammond J, James PD, Borriello SP, Mahida YR. Colonic IgA producing cells and macrophages are reduced in recurrent and non-recurrent Clostridium difficile associated diarrhoea. J. Clin. Pathol. 57(9), 973–979 (2004).
  • Johnson S, Sypura WD, Gerding DN, Ewing SL, Janoff EN. Selective neutralization of a bacterial enterotoxin by serum immunoglobulin A in response to mucosal disease. Infect. Immun. 63(8), 3166–3173 (1995).
  • Ghose C, Kalsy A, Sheikh A et al. Transcutaneous immunization with Clostridium difficile toxoid A induces systemic and mucosal immune responses and toxin A-neutralizing antibodies in mice. Infect. Immun. 75(6), 2826–2832 (2007).
  • Soloff AC, Barratt-Boyes SM. Enemy at the gates: dendritic cells and immunity to mucosal pathogens. Cell Res. 20(8), 872–885 (2010).
  • Cerutti A. Location, location, location: B-cell differentiation in the gut lamina propria. Mucosal Immunol. 1(1), 8–10 (2008).
  • McDole JR, Wheeler LW, McDonald KG et al. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 483(7389), 345–349 (2012).
  • Jung ES, Kim SM, Cha RH et al. Impact of polymorphisms of the genes encoding angiotensin II-forming enzymes on the progression of IgA nephropathy. Nephron. Clin. Pract. 118(2), c122–c129 (2011).
  • Chang SY, Kweon MN. Langerin-expressing dendritic cells in gut-associated lymphoid tissues. Immunol. Rev. 234(1), 233–246 (2010).
  • Johansson-Lindbom B, Svensson M, Pabst O et al. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202(8), 1063–1073 (2005).
  • Wendland M, Czeloth N, Mach N et al. CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine. Proc. Natl Acad. Sci. USA 104(15), 6347–6352 (2007).
  • Agace WW, Persson EK. How vitamin A metabolizing dendritic cells are generated in the gut mucosa. Trends Immunol. 33(1), 42–48 (2012).
  • Liaudet L, Deb A, Pacher P et al. The flagellin-TLR5 axis: therapeutic opportunities. Drug News Perspect. 15(7), 397–409 (2002).
  • Borsutzky S, Cazac BB, Roes J, Guzmán CA. TGF-β receptor signaling is critical for mucosal IgA responses. J. Immunol. 173(5), 3305–3309 (2004).
  • Cazac BB, Roes J. TGF-β receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 13(4), 443–451 (2000).
  • Hapfelmeier S, Lawson MA, Slack E et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 328(5986), 1705–1709 (2010).
  • Trzasko A, Leeds JA, Praestgaard J, Lamarche MJ, McKenney D. Efficacy of LFF571 in a hamster model of Clostridium difficile infection. Antimicrob. Agents Chemother. 56(8), 4459–4462 (2012).
  • Steele J, Feng H, Parry N, Tzipori S. Piglet models of acute or chronic Clostridium difficile illness. J. Infect. Dis. 201(3), 428–434 (2010).
  • Chen X, Katchar K, Goldsmith JD et al. A mouse model of Clostridium difficile-associated disease. Gastroenterology 135(6), 1984–1992 (2008).
  • Cong Y, Feng T, Fujihashi K, Schoeb TR, Elson CO. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl Acad. Sci. USA 106(46), 19256–19261 (2009).
  • Kyne L, Kelly CP. Recurrent Clostridium difficile diarrhoea. Gut 49(1), 152–153 (2001).
  • Warny M, Vaerman JP, Avesani V, Delmée M. Human antibody response to Clostridium difficile toxin A in relation to clinical course of infection. Infect. Immun. 62(2), 384–389 (1994).
  • Hassett J, Meyers S, McFarland L, Mulligan ME. Recurrent Clostridium difficile infection in a patient with selective IgG1 deficiency treated with intravenous immune globulin and Saccharomyces boulardii. Clin. Infect. Dis. 20(Suppl. 2), S266–S268 (1995).
  • Wright A, Drudy D, Kyne L, Brown K, Fairweather NF. Immunoreactive cell wall proteins of Clostridium difficile identified by human sera. J. Med. Microbiol. 57(Pt 6), 750–756 (2008).
  • Zelensky AN, Gready JE. The C-type lectin-like domain superfamily. FEBS J. 272(24), 6179–6217 (2005).
  • Teunis PF, Nagelkerke NJ, Haas CN. Dose response models for infectious gastroenteritis. Risk Anal. 19(6), 1251–1260 (1999).
  • Kerrigan AM, Brown GD. Phagocytes: fussy about carbs. Curr. Biol. 21(13), R500–R502 (2011).
  • Presicce P, Taddeo A, Conti A, Villa ML, Della Bella S. Keyhole Limpet Hemocyanin induces the activation and maturation of human dendritic cells through the involvement of mannose receptor. Mol. Immunol. 45(4), 1136–1145 (2008).
  • Burgdorf S, Lukacs-Kornek V, Kurts C. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 176(11), 6770–6776 (2006).
  • Chow H, Sundsmo J, Sagermann M. Keyhole Limpet Hemocyanin (KLH): A unique, unlikely pharmaceutical product. The Immunotherapeutics & Vaccine Summit, Cambridge, MA, USA. Cambridge Healthtech Institute, Cambridge, MA, USA (2012).
  • Kantele A, Häkkinen MP, Zivny J, Elson CO, Mestecky J, Kantele JM. Humoral immune response to keyhole limpet haemocyanin, the protein carrier in cancer vaccines. Clin. Dev. Immunol. 2011, 614383 (2011).
  • Waldo FB, van den Wall Bake AW, Mestecky J, Husby S. Suppression of the immune response by nasal immunization. Clin. Immunol. Immunopathol. 72(1), 30–34 (1994).
  • Krejci J, Nechvatalova K, Kudlackova H et al. Effects of adjuvants on the immune response of pigs after intradermal administration of antigen. Res. Vet. Sci. 94(1), 73–76 (2013).
  • Milgrom H, Kesler K, Byron M, Harbeck R, Holliday R, Leung DY. Response to cutaneous immunization with low-molecular-weight subunit Keyhole Limpet Hemocyanin. Int. Arch. Allergy Immunol. 157(3), 269–274 (2012).
  • Benveniste J, Lespinats G, Adam C, Salomon JC. Immunoglobulins in intact, immunized, and contaminated axenic mice: study of serum IgA. J. Immunol. 107(6), 1647–1655 (1971).
  • de Moreno de LeBlanc A, Dogi CA, Galdeano CM, Carmuega E, Weill R, Perdigón G. Effect of the administration of a fermented milk containing Lactobacillus casei DN-114001 on intestinal microbiota and gut associated immune cells of nursing mice and after weaning until immune maturity. BMC Immunol. 9, 27 (2008).
  • Obata T, Goto Y, Kunisawa J et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc. Natl Acad. Sci. USA 107(16), 7419–7424 (2010).

Patent

  • Monteiro MA, Ganeshapillai J: WO033268A1 (2009); US0330125A1 (2010); NZ583750 (2012).

Website

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.