期刊论文详细信息
BMC Microbiology
Surface glycosaminoglycans mediate adherence between HeLa cells and Lactobacillus salivarius Lv72
Luis M Quirós1  Juan E Suárez3  Susana Escobedo2  Carla Martín2  Rebeca Martín2 
[1] Instituto Univesitario de Oncología del Principado de Asturias (IUOPA), Universidad de Oviedo, Oviedo, Spain;Instituto Universitario de Biotecnología, Universidad de Oviedo, Oviedo, Spain;Instituto de Productos Lacteos de Asturias (IPLA-CSIC), Villaviciosa, Spain
关键词: Epithelial cell cultures;    Vaginal Lactobacillus;    Glycosaminoglycans;    Proteoglycans;   
Others  :  1143050
DOI  :  10.1186/1471-2180-13-210
 received in 2013-03-23, accepted in 2013-09-11,  发布年份 2013
PDF
【 摘 要 】

Background

The adhesion of lactobacilli to the vaginal surface is of paramount importance to develop their probiotic functions. For this reason, the role of HeLa cell surface proteoglycans in the attachment of Lactobacillus salivarius Lv72, a mutualistic strain of vaginal origin, was investigated.

Results

Incubation of cultures with a variety of glycosaminoglycans (chondroitin sulfate A and C, heparin and heparan sulfate) resulted in marked binding interference. However, no single glycosaminoglycan was able to completely abolish cell binding, the sum of all having an additive effect that suggests cooperation between them and recognition of specific adhesins on the bacterial surface. In contrast, chondroitin sulfate B enhanced cell to cell attachment, showing the relevance of the stereochemistry of the uronic acid and the sulfation pattern on binding. Elimination of the HeLa surface glycosaminoglycans with lyases also resulted in severe adherence impairment. Advantage was taken of the Lactobacillus-glycosaminoglycans interaction to identify an adhesin from the bacterial surface. This protein, identify as a soluble binding protein of an ABC transporter system (OppA) by MALDI-TOF/(MS), was overproduced in Escherichia coli, purified and shown to interfere with L. salivarius Lv72 adhesion to HeLa cells.

Conclusions

These data suggest that glycosaminoglycans play a fundamental role in attachment of mutualistic bacteria to the epithelium that lines the cavities where the normal microbiota thrives, OppA being a bacterial adhesin involved in the process.

【 授权许可】

   
2013 Martín et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150328225240882.pdf 938KB PDF download
Figure 6. 78KB Image download
Figure 5. 41KB Image download
Figure 4. 87KB Image download
Figure 3. 51KB Image download
Figure 2. 59KB Image download
Figure 1. 47KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】
  • [1]Martin R, Sanchez B, Suarez JE, Urdaci MC: Characterization of the adherence properties of human Lactobacilli strains to be used as vaginal probiotics. FEMS Microbiol Lett 2012, 328:166-173.
  • [2]Martín R, Soberón N, Vaneechoutte M, Flórez AB, Vázquez F, Suárez JE: Evaluation of newly isolated human vaginal lactobacilli and selection of probiotic candidates. Int Microbiol 2008, 11:261-266.
  • [3]Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ: Vaginal microbiome of reproductive-age. Proc Natl Acad Sci USA 2011, 15;108(1):4680-4687.
  • [4]Reid G: Probiotic and prebiotic applications for vaginal health. J AOAC Int 2012, 95(1):31-34.
  • [5]Andreu A, Stapleton AE, Fennell CL, Hillier SL, Stamm WE: Hemagglutination, adherence, and surface properties of vaginal Lactobacillus species. J Infect Dis 1995, 171:1237-1243.
  • [6]Boris S, Suarez JE, Barbes C: Characterization of the aggregation promoting factor from Lactobacillus gasseri, a vaginal isolate. J Appl Microbiol 1997, 83:413-420.
  • [7]Boris S, Suárez J, Vazquez F, Barbés C: Adherence of human vaginal lactobacilli to vaginal epithelial cells and interaction with uropathogens. Infect Immun 1998, 66:1985-1989.
  • [8]Vélez MP, De Keersmaecker SC, Vanderleyden J: Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol Lett 2007, 276:140-148.
  • [9]Martín R, Soberón N, Vázquez F, Suárez JE: Vaginal microbiota: composition, protective role, associated pathologies, and therapeutic perspectives. Enferm Infecc Microbiol Clin 2008, 26:160-167.
  • [10]Sánchez B, Bressolier P, Urdaci MC: Exported proteins in probiotic bacteria: adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. FEMS Immunol Med Microbiol 2008, 54:1-17.
  • [11]Tjalsma H, Lambooy L, Hermans PW, Swinkels DW: Shedding & shaving: disclosure of proteomic expression on a bacterial face. Proteomics 2008, 8:1415-1428.
  • [12]Munoz-Provencio D, Perez-Martinez G, Monedero V: Identification of surface proteins from Lactobacillus casei BL23 able to bind fibronectin and collagen. Probiotics & Antimicro Prot 2011, 3:15-20.
  • [13]Esko J, Lindahl U: Molecular diversity of heparan sulfate. J Clin Invest 2001, 108:169-173.
  • [14]Prydz K, Dalen KT: Synthesis and sorting of proteoglycans. J Cell Sci 2000, 113:193-205.
  • [15]Turnbull J, Powell A, Guimond S: Heparan sulpatem decoding a dynamicl multifunctional cell regulator. TRENDS Cell Biol 2001, 11:75-82.
  • [16]Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald M, Lincecum J, Zako M: Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999, 68:729-777.
  • [17]Rapraeger A, Jalkanen M, Bernfield M: Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J Cell Biol 1986, 103:2683-2696.
  • [18]Schmidt G, Robenek H, Harrach B, Glössl J, Nolte V, Hörmann H, Richter H, Kresse H: Interaction of small dermatan sulfate proteoglycan from fibroblasts with fibronectin. J Cell Biol 1987, 104:1683-1691.
  • [19]Kirn-Safran C, Farach-Carson MC, Carson DD: Multifunctionality of extracellular and cell surface heparan sulfate proteoglycans. Cell Mol Life Sci 2009, 66:3421-3434.
  • [20]Schaefer L, Schaefer RM: Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res 2010, 339:237-246.
  • [21]de Vries FP, Cole R, Dankert J, Frosch M, van Putten JP: Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 1998, 27:1203-1212.
  • [22]Chen T, Belland RJ, Wilson J, Swanson J: Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J Exp Med 1995, 182:511-517.
  • [23]Grant CC, Bos MP, Belland RJ: Proteoglycan receptor binding by Neisseria gonorrhoeae MS11 is determined by the HV-1 region of OpaA. Mol Microbiol 1999, 32:233-242.
  • [24]Dupres V, Verbelen C, Raze D, Lafont F, Dufrêne YF: Force spectroscopy of the interaction between mycobacterial adhesins and heparan sulphate proteoglycan receptors. Chemphyschem 2009, 10:1672-1675.
  • [25]Sava IG, Zhang F, Toma I, Theilacker C, Li B, Baumert TF, Holst O, Linhardt RJ, Huebner J: Novel interactions of glycosaminoglycans and bacterial glycolipids mediate binding of enterococci to human cells. J Biol Chem 2009, 284:18194-18201.
  • [26]Asano K, Kakizaki I, Nakane A: Interaction of Listeria monocytogenes autolysin amidase with glycosaminoglycans promotes listerial adhesion to mouse hepatocytes. Biochimie 2012, 94:1291-1299.
  • [27]Henry-Stanley M, Hess DJ, Erlandsen SL, Wells CL: Ability of the heparin sulfate proteoglycan syndecan‒1 to participate in bacterial translocation across the intestinal epithelial barrier. SHOCK 2005, 6:571-576.
  • [28]Castañeda-Roldan EI, Avelino-Flores F, Dall’Agnol M, Freer E, Cedillo L, Dornand J, Girón JA: Adherence of Brucella to human epithelial cells and macrophages is mediated by sialic acid residues. Cel Microbiol 2004, 6:435-445.
  • [29]Fleckenstein JM, Holland JT, Hasty DL: Interaction of an uuter membrane protein of enterotoxigenic Escherichia coli with cell surface heparan sulfate proteoglycans. Infect Immun 2002, 70:1530-1537.
  • [30]Wuppermann FN, Hegemann JH, Jantos CA: Heparan sulfate-like glycosaminoglycan is a cellular receptor for Chlamydia pneumoniae. J Infect Dis 2001, 184:181-187.
  • [31]Cywes C, Stamenkovic I, Wessels MR: CD44 as a receptor for colonization of the pharynx by group A Streptococcus. J Clin Invest 2000, 106:995-1002.
  • [32]Cywes C, Wessels MR: Group A Streptococcus tissue invasion by CD44-mediated cell signalling. Nature 2001, 414:648-652.
  • [33]Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M: Human papillomavirus infection requires cell surface heparan sulfate. J Virol 2001, 75:1565-1570.
  • [34]Akula SM, Wang FZ, Vieira J, Chandran B: Human herpesvirus 8 interaction with target cells involves heparan sulfate. Virology 2001, 282:245-255.
  • [35]Bobardt MD, Saphire AC, Hung HC, Yu X, Van der Schueren B, Zhang Z, David G, Gallay PA: Syndecan captures, protects, and transmits HIV to T lymphocytes. Immunity 2003, 18:27-39.
  • [36]Carruthers VB, Hakansson S, Giddings OK, Sibley LD: Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect Immun 2000, 68:4005-4011.
  • [37]Love DC, Esko JD, Mosser DM: A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans. J Cell Biol 1993, 123:759-766.
  • [38]Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, Bilker O, Sinnis P: Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe 2007, 2:316-327.
  • [39]Almeida RA, Fang W, Oliver SP: Adherence and internalization of Streptococcus uberis to bovine mammary epithelial cells are mediated by host cell proteoglycans. FEMS Microbiol Lett 1999, 177:313-317.
  • [40]Hess DJ, Henry Stanley MJ, Erlandsen SL, Wells CL: Heparan sulfate proteoglycans mediate Staphylococcus aureus interactions with intestinal epithelium. Med Microbiol Immunol 2006, 195:133-141.
  • [41]Landry JJ, Pyl PT, Rausch T, Zichner T, Tekkedil MM, Stütz AM, Jauch A, Aiyar RS, Pau G, Delhomme N, Gagneur J, Korbel JO, Huber W, Steinmetz LM: G3 (Bethesda). The genomic and transcriptomic landscape of a HeLa Cell Line 2013, 3(8):1213-1224. doi: 10.1534/g3.113.005777
  • [42]Falkow S: Bacterial entry into eukaryotic cells. Cell 1991, 65(7):1099-1102.
  • [43]Finlay BB: Cell adhesion and invasion mechanisms in microbial pathogenesis. Curr Opin Cell Biol 1990, 2:815-820.
  • [44]Westerlund B, Korhonen TK: Bacterial proteins binding to the mammalian extracellular matrix. Mol Microbiol 1993, 9:687-694.
  • [45]Muñoz-Provencio D, Pérez-Martínez G, Monedero V: Characterization of a fibronectin-binding protein from Lactobacillus casei BL23. J Appl Microbiol 2010, 108:1050-1059.
  • [46]Nagy E, Froman G, Mardh PA: Fibronectin binding of Lactobacillus species isolated from women with and without bacterial vaginosis. J Med Microbiol 1992, 37:38-42.
  • [47]Hawes SE, Hillier SL, Benedetti J, Stevens CE, Koutsky LA, Wolner-Hanssen P, Holmes KK: Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis 1996, 174:1058-1063.
  • [48]Courtney HS, Ofek I, Penfound T, Nizet V, Pence MA, Kreikemeyer B, Podbielski A, Hasty DL, Dale JB: Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Sreptococcus pyogenes. PLoS One 2009, 4:e4166.
  • [49]Mulley B, Forster MJ: Conformation and dynamics of heparin and heparan sulfate. Glycobiology 2000, 10:1147-1156.
  • [50]Lamanna WC, Kalus I, Padva M, Baldwin RJ, Merry CLR, Dierks T: The heparanome-the enigma of encoding and decoding heparan sulfate sulfation. J. of Biotechnology 2007, 129:290-307.
  • [51]Alvarez-Domínguez C, Vázquez-Boland JA, Carrasco-Marín E, López-Mato P, Leyva-Cobian F: Host cell heparan sulfate proteeoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface proteín ActA is envolved in heparan sulfate receptor cognition. Infect Immun 1997, 65:78-88.
  • [52]Srinoulprasert Y, Kongtawelert P, Chaiyaroj SC: Chondroitin sulfate B and heparin mediate adhesion of Penicillium marneffei conidia to host extracelular matrices. Microb Pathog 2006, 40:126-132.
  • [53]Tonnaer ELGM, Hafmans TG, Van Kuppevelt TH, Sanders EAM, Verweij PE, Curfs JHAJ: Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells. Microbes Infect 2006, 8:316-322.
  • [54]Zaretzky FR, Pearce-Pratt R, Phillips DM: Sulfated polyanions block Chlamydia trachomatis infection of cervix-derived human epithelia. Infect Immun 1995, 63:3520-3526.
  • [55]Plotkowski MC, Costa AO, Morandi V, Barbosa HS, Nader HB, De Bentzmann S, Puchelle E: Role of hepran sulfate proteoglycans as potential receptors for non-piliated Pseudomonas aeruginosa adherence to non-polarised airway epithelial cells. J Med Microbiol 2001, 50:183-190.
  • [56]Fischer JR, LeBlanc KT, Leong JM: Fibronectin binding protein BBK32 of the Lyme disease spirochete promotes bacterial attachment to glycosaminoglycans. Infect Immun 2006, 74:435-441.
  • [57]Breiner DD, Fahey M, Salvador R, Novakova J, Coburn J: Leptospira interrogans binds to human cell surface receptors including proteoglycans. Infect Immun 2009, 77:5528-5536.
  • [58]Caterson B, Mahmoodian F, Sorrell JM, Hardingham TE, Bayliss MT, Carney SL, Ratcliffe A, Muir H: Modulation of native chondroitin sulphate structure in tissue development and in disease. J Cell Sci 1990, 97:411-417.
  • [59]Lindahl U, Kusche-Gullberg M, Kjellén L: Regulated diversity of heparan sulfate. J Biol Chem 1998, 273:24979-24982.
  • [60]Peltoniemi K, Vesanto E, Palva A: Genetic characterization of an oligopeptide transport system from Lactobacillus delbrueckii subsp. bulgaricus. Arch Microbiol 2002, 177:457-467.
  • [61]Fenno JC, Tamura M, Hannam PM, Wong GW, Chan RA, McBride BC: Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect Immun 2000, 68:1884-1892.
  • [62]Henrich B, Hopfe M, Kitzerow A, Hadding U: The adherence-associated lipoprotein P100, encoded by an opp operon structure, functions as the oligopeptide-binding domain OppA of a putative oligopeptide transport system in Mycoplasma hominis. J Bacteriol 1999, 181:4873-4878.
  • [63]Hopfe M, Dahlmanns T, Henrich B: In Mycoplasma hominis the OppA-mediated cytoadhesion depends on its ATPase activity. BMC Microbiol 2011, 11:185. BioMed Central Full Text
  • [64]Miyoushi Y, Okada S, Uchimura T, Saoh E: A mucus adhesion promotin protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Biosci Biotechnol Biochem 2006, 70:1622-1628.
  • [65]Dasgupta A, Sureka K, Mitra D, Saha B, Sanyal S, Das AK, Chakrabarti P, Jackson M, Gicquel B, Kundu M, Basu J: An oligopeptide transporter of Mycobacterium tuberculosis regulates cytokine release and apoptosis of infected macrophages. PLoS One 2010, 5:e12225.
  • [66]Berntsson RP, Doeven MK, Fusetti F, Duurkens RH, Sengupta D, Marrink SJ, Thunnissen AM, Poolman B, Slotboom DJ: The structural basis for peptide selection by the transport receptor OppA. EMBO J 2009, 28(9):1332-1340.
  • [67]Tallon R, Arias S, Bressollier P, Urdaci MC: Strain and matrix-dependent adhesion of Lactobacillus plantarum is mediated by proteinaceous bacterial compounds. J Appl Microbiol 2007, 102:442-451.
  • [68]Hulme EC, Birdsall NJM: Strategy and tactics in receptor-binding studies. In Receptor-Ligand Interactions. A Practical Approach. Edited by Hulme EC. New York: IRL Press at Oxford University Press; 1992:63-176.
  • [69]Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
  • [70]Sambrook J, Fritsch EF, Maniatis T Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989:1,626. soft cover
  文献评价指标  
  下载次数:44次 浏览次数:17次