Abstract
The genus Corynebacterium is part of the phylogenetic group nocardioform actinomycetes. Members of this group have a characteristic cell envelope structure composed primarily of branched long-chain lipids, termed mycolic acids, and a rich number of lipoglycans such as lipoarabinomanans (LAM) and lipomannans. In this study, we identified a novel LAM variant isolated from Corynebacterium diphtheriae named CdiLAM. The key structural features of CdiLAM are a linear α-1→6-mannan with side chains containing 2-linked α-D-Manp and 4-linked α-D-Araf residues. The polysaccharide backbone is linked to a phosphatidylinositol anchor. In contrast to the LAMs of other members of actinomycetales, CdiLAM presents an unusual substitution at position 4 of α-1→6-mannan backbone by α-D-Araf. Unlike the non-fimbrial adhesin 62–72p, CdiLAM did not function as a hemagglutinin to human red blood cells. Experimental evidences pointed to CdiLAM as an adhesin of C. diphtheriae to human respiratory epithelial cells, thereby, contributing to the pathogenesis of diphtheria.
Similar content being viewed by others
References
Bertuccini L, Baldassarri L, von Hunolstein C (2004) Internalization of non-toxigenic Corynebacterium diphtheriae by cultured human respiratory epithelial cells. Microb Pathog 37:111–118
Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64:29–63
Briken V, Porcelli SA, Besra GS, Kremer L (2004) Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 53:391–403
Chan J, Fan XD, Hunter SW, Brennan PJ, Bloom BR (1991) Lipoarabinomannan, a possible virulence factor involved in persistence of Mycobacterium tuberculosis within macrophages. Infect Immun 59:1755–1761
Chatterjee D, Hunter SW, McNeil M, Brennan PJ (1992) Lipoarabinomannan: multiglycosylated form of the mycobacterial mannosylphosphatidylinositols. J Biol Chem 267:6228–6233
Ciucanu I, Kerek F (1984) A simple and rapid method for the permetylation of carbohydrates. Carbohydr Res 131:209–271
Colombo AV, Hirata R Jr, de Souza CM, Monteiro-Leal LH, Previato JO, Formiga LC, Andrade AF, Mattos-Guaraldi AL (2001) Corynebacterium diphtheriae surface proteins as adhesins to human erythrocytes. FEMS Microbiol Lett 197:235–239
Dao DN, Kremer L, Guerardel Y, Molano A, Jacobs WR Jr, Porcelli SA, Briken V (2004) Mycobacterium tuberculosis lipomannan induces apoptosis and interleukin-12 production in macrophages. Infect Immun 72:2067–2074
Dittmann S, Wharton M, Vitek C, Ciotti M, Galazka A, Guichard S, Hardy I, Kartoglu U, Koyama S, Kreysler J, Martin B, Mercer D, Ronne T, Roure C, Steinglass R, Strebel P, Sutter R, Trostle M (2000) Successful control of epidemic diphtheria in the states of the former Union of Soviet Socialist Republics: lessons learned. J Infect Dis 181(Suppl 1):S10–S22
Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167
Flaherty C, Sutcliffe IC (1999) Identification of a lipoarabinomannan-like lipoglycan in Gordonia rubropertincta. Syst Appl Microbiol 22:530–533
Flaherty C, Minnikin DE, Sutcliffe IC (1996) A chemotaxonomic study of the lipoglycans of Rhodococcus rhodnii N445 (NCIMB 11279). Zentralbl Bakteriol 285:11–19
Galazka A (2000) The changing epidemiology of diphtheria in the vaccine era. J Infect Dis 181(Suppl 1):S2–S9
Garton NJ, Sutcliffe IC (2006) Identification of a lipoarabinomannan-like lipoglycan in the actinomycete Gordonia bronchialis. Arch Microbiol 184:425–427
Garton NJ, Gilleron M, Brando T, Dan HH, Giguere S, Puzo G, Prescott JF, Sutcliffe IC (2002) A novel lipoarabinomannan from the equine pathogen Rhodococcus equi. Structure and effect on macrophage cytokine production. J Biol Chem 277:31722–31733
Geijtenbeek TB, van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B, van Kooyk Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197:7–17
Gibson KJ, Gilleron M, Constant P, Puzo G, Nigou J, Besra GS (2003a) Structural and functional features of Rhodococcus ruber lipoarabinomannan. Microbiology 149:1437–1445
Gibson KJ, Gilleron M, Constant P, Puzo G, Nigou J, Besra GS (2003b) Identification of a novel mannose-capped lipoarabinomannan from Amycolatopsis sulphurea. Biochem J 372:821–829
Gibson KJ, Gilleron M, Constant P, Brando T, Puzo G, Besra GS, Nigou J (2004) Tsukamurella paurometabola lipoglycan, a new lipoarabinomannan variant with pro-inflammatory activity. J Biol Chem 279:22973–22982
Gibson KJ, Gilleron M, Constant P, Sichi B, Puzo G, Besra GS, Nigou J (2005) A lipomannan variant with strong TLR-2-dependent pro-inflammatory activity in Saccharothrix aerocolonigenes. J Biol Chem 280:28347–28356
Gilleron M, Garton NJ, Nigou J, Brando T, Puzo G, Sutcliffe IC (2005) characterization of a truncated lipoarabinomannan from the actinomycete Turicella otitidis. J Bacteriol 187:854–861
Goodfellow M, Weaver CR, Minnikin DE (1982) Numerical classification of some Rhodococci, Corynebacteria and related organisms. J Gen Microbiol 128:731–745
Guerardel Y, Maes E, Briken V, Chirat F, Leroy Y, Locht C, Strecker G, Kremer L (2003) Lipomannan and lipoarabinomannan from a clinical isolate of Mycobacterium kansasii: novel structural features and apoptosis-inducing properties. J Biol Chem 278:36637–36651
Harlow E, Lane D (1988) Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, pp 353
Hirata R, Napoleão F, Monteiro-Leal LH, Andrade AF, Nagao PE, Formiga LC, Fonseca LS, Mattos-Guaraldi AL (2002) Intracellular viability of toxigenic Corynebacterium diphtheriae strains in HEp-2 cells. FEMS Microbiol Lett 215:115–119
Hirata R Jr, Souza SM, Rocha-de-Souza CM, Andrade AF, Monteiro-Leal LH, Formiga LC, Mattos-Guaraldi AL (2004) Patterns of adherence to HEp-2 cells and actin polymerisation by toxigenic Corynebacterium diphtheriae strains. Microb Pathog 36:125–130
Kokeguchi S, Kato K, Ohta H, Fukui K, Tsujimoto M, Ogawa T, Takada H, Kotani S (1987) Isolation and characterization of an amphipathic antigen from Corynebacterium diphtheriae. Microbios 50:183–199
Mandlik A, Swierczynski A, Das A, Ton-That H (2007) Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 64(1):111–124
Mattos KA, Todeschini AR, Heise N, Jones C, Previato JO, Mendonça-Previato L (2005) Nitrogen-fixing bacterium Burkholderia brasiliensis produces a novel yersiniose A-containing O-polysaccharide. Glycobiology 15:313–321
Mattos-Guaraldi AL, Formiga LC (1986) Agglutination of sheep erythrocytes by Corynebacterium diphtheriae. Braz J Med Biol Res 19:75–77
Mattos-Guaraldi AL, Formiga LC, Andrade AF (1998) trans-Sialidase activity for sialic acid incorporation on Corynebacterium diphtheriae. FEMS Microbiol Lett 168:167–172
Mattos-Guaraldi AL, Cappelli EA, Previato JO, Formiga LC, Andrade AF (1999) Characterization of surface saccharides in two Corynebacterium diphtheriae strains. FEMS Microbiol Lett 170:159–166
Mattos-Guaraldi AL, Formiga LC, Pereira GA (2000) Cell surface components and adhesion in Corynebacterium diphtheriae. Microbes Infect 2:1507–1512
Mattos-Guaraldi AL, Moreira LO, Damasco PV, Hirata R Jr (2003) Diphtheria remains a threat to health in the developing world—an overview. Mem Inst Oswaldo Cruz 98:987–993
Moreira LdeO, Andrade AF, Vale MD, Souza SM, Hirata R Jr, Asad LM, Asad NR, Monteiro-Leal LH, Previato JO, Mattos-Guaraldi AL (2003) Effects of iron limitation on adherence and cell surface carbohydrates of Corynebacterium diphtheriae strains. Appl Environ Microbiol 69:5907–5913
Nigou J, Zelle-Rieser C, Gilleron M, Thurnher M, Puzo G (2001) Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: evidence for a negative signal delivered through the mannose receptor. J Immunol 166:7477–7485
Pizarro-Cerdá J, Cossart P (2006) Bacterial adhesion and entry into host cells. Cell 124:715–727
Puissegur MP, Lay G, Gilleron M, Botella L, Nigou J, Marrakchi H, Mari B, Duteyrat JL, Guerardel Y, Kremer L, Barbry P, Puzo G, Altare F (2007) Mycobacterial lipomannan induces granuloma macrophage fusion via a TLR2-dependent, ADAM9- and beta1 integrin-mediated pathway. Am J Immunol 178:3161–3169
Sharma NC, Banavaliker JN, Ranjan R, Kumar R (2007) Bacteriological and epidemiological characteristics of diphtheria cases in and around Delhi: a retrospective study. Indian J Med Res 126:545–552
Strohmeier GR, Fenton MJ (1999) Roles of lipoarabinomannan in the pathogenesis of tuberculosis. Microbes Infect 1:709–717
Sutcliffe IC (1995) Identification of a lipoarabinomannan-like lipoglycan in Corynebacterium matruchotii. Arch Oral Biol 40:1119–1124
Sutcliffe IC (2000) Characterization of a lipomannan lipoglycan from the mycolic acid containing actinomycete Dietzia maris. Antonie Van Leeuwenhoek 78:195–201
Sweely CC, Bentley R, Makita M, Well WW (1963) Gas-liquid chromatography of trymethylsilyl derivates of sugars and related substances. J Am Chem Soc 85:2497
Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A, Legres L, Dreher D, Nicod LP, Gluckman JC, Lagrange PH, Gicquel B, Neyrolles O (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197:121–127
Tatituri RV, Illarionov PA, Dover LG, Nigou J, Gilleron M, Hitchen P, Krumbach K, Morris HR, Spencer N, Dell A, Eggeling L, Besra GS (2007) Inactivation of Corynebacterium glutamicum NCgl0452 and the role of MgtA in the biosynthesis of a novel mannosylated glycolipid involved in lipomannan biosynthesis. J Biol Chem 282:4561–4572
Westphal O, Jann K (1965) Bacterial lipopolissacharides; extraction with phenol-water and further applications of procedure. Method Carbohydr Chem 5:83–91
Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley JL, Sykes BD (1995) 1H, 13C and 15 N chemical shift referencing in biomolecular NMR. J Biomol NMR 6:135–140
Acknowledgments
We are grateful to Dr. José Osvaldo Previato and Dr. Adriane Regina Todeschini for technical assistance with lipoglycan analysis and the Centro Nacional de Ressonância Mangnética Nuclear, UFRJ, Brasil, for the NMR facilities. This work was supported by a grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ), SR2-UERJ and Programa de Núcleo de Excelência (PRONEX) of the Brazilian Ministry of Science and Technology.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Axel Brakhage.
Rights and permissions
About this article
Cite this article
Moreira, L.O., Mattos-Guaraldi, A.L. & Andrade, A.F.B. Novel lipoarabinomannan-like lipoglycan (CdiLAM) contributes to the adherence of Corynebacterium diphtheriae to epithelial cells. Arch Microbiol 190, 521–530 (2008). https://doi.org/10.1007/s00203-008-0398-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-008-0398-y