Publication Cover
Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 29, 2013 - Issue 6
476
Views
40
CrossRef citations to date
0
Altmetric
Articles

The specific degree-of-polymerization of A-type proanthocyanidin oligomers impacts Streptococcus mutans glucan-mediated adhesion and transcriptome responses within biofilms

, , , , &
Pages 629-640 | Received 15 Jan 2013, Accepted 28 Mar 2013, Published online: 22 May 2013

References

  • Ajdic , D , McShan , WM , McLaughlin , RE , Savic , G , Chang , J , Carson , MB , Primeaux , C , Tian , R , Kenton , S Jia , H . 2002 . Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen . Proc Natl Acad Sci USA , 99 : 14434 – 14439 .
  • Banas , JA and Vickerman , MM . 2003 . Glucan-binding proteins of the oral streptococci . Crit Rev Oral Biol Med , 14 : 89 – 99 .
  • Baxter , NJ , Lilley , TH , Haslam , E and Williamson , MP . 1997 . Multiple interactions between polyphenols and a salivary proline-rich protein repeat result in complexation and precipitation . Biochemistry , 36 : 5566 – 5577 .
  • Bennick , A . 2002 . Interaction of plant polyphenols with salivary proteins . Crit Rev Oral Biol Med , 13 : 184 – 196 .
  • Burger , O , Ofek , I , Tabak , M , Weiss , EI , Sharon , N and Neeman , I . 2000 . A high molecular mass constituent of cranberry juice inhibits Helicobacter pylori adhesion to human gastric mucus . FEMS Immunol Med Microbiol , 29 : 295 – 301 .
  • Bustin , SA , Benes , V , Garson , JA , Hellemans , J , Huggett , J , Kubista , M , Mueller , R , Nolan , T , Pfaffl , MW Shipley , GL . 2009 . The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments . Clin Chem , 55 : 611 – 622 .
  • Chia , JS , Lee , YY , Huang , PT and Chen , JY . 2001 . Identification of stress-responsive genes in Streptococcus mutans by differential display reverse transcription-PCR . Infect Immun , 69 : 2493 – 2501 .
  • Cote , J , Caillet , S , Doyon , G , Sylvain , JF and Lacroix , M . 2010 . Bioactive compounds in cranberries and their biological properties . Crit Rev Food Sci Nutr , 50 : 666 – 679 .
  • Cury , JA and Koo , H . 2007 . Extraction and purification of total RNA from Streptococcus mutans biofilms . Anal Biochem , 365 : 208 – 214 .
  • Cvitkovitch , DG , Gutierrez , JA and Bleiweis , AS . 1997 . Role of the citrate pathway in glutamate biosynthesis by Streptococcus mutans . J Bacteriol , 179 : 650 – 655 .
  • de Freitas , V and Mateus , N . 2001 . Structural features of procyanidin interactions with salivary proteins . J Agric Food Chem , 49 : 940 – 945 .
  • Duarte , S , Gregoire , S , Singh , AP , Vorsa , N , Schaich , K , Bowen , WH and Koo , H . 2006 . Inhibitory effects of cranberry polyphenols on formation and acidogenicity of Streptococcus mutans biofilms . FEMS Microbiol Lett , 257 : 50 – 56 .
  • Fajardo , D , Morales , J , Zhu , H , Steffan , S , Harbut , R , Bassil , N , Hummer , K , Polashock , J , Vorsa , N and Zalapa , J . 2012 . Discrimination of American cranberry cultivars and assessment of clonal heterogeneity using microsatellite markers . Plant Mol Biol Rep , 31 : 264 – 271 .
  • Falsetta , ML , Klein , MI , Lemos , JA , Silva , BB , Agidi , S , Scott-Anne , KK and Koo , H . 2012 . Novel antibiofilm chemotherapy targets exopolysaccharide synthesis and stress tolerance in Streptococcus mutans to modulate virulence expression in vivo . Antimicrob Agents Chemother , 56 : 6201 – 6211 .
  • Feldman , M , Tanabe , S , Howell , A and Grenier , D . 2012 . Cranberry proanthocyanidins inhibit the adherence properties of Candida albicans and cytokine secretion by oral epithelial cells . BMC Complement Altern Med , 12 : 6
  • Flemming , HC and Wingender , J . 2010 . The biofilm matrix . Nat Rev Microbiol , 8 : 623 – 633 .
  • Foo , LY , Lu , Y , Howell , AB and Vorsa , N . 2000a . A-type proanthocyanidin trimers from cranberry that inhibit adherence of uropathogenic P-fimbriated Escherichia coli . J Nat Prod , 63 : 1225 – 1228 .
  • Foo , LY , Lu , Y , Howell , AB and Vorsa , N . 2000b . The structure of cranberry proanthocyanidins which inhibit adherence of uropathogenic P-fimbriated Escherichia coli in vitro . Phytochemistry , 54 : 173 – 181 .
  • Gregoire , S , Singh , AP , Vorsa , N and Koo , H . 2007 . Influence of cranberry phenolics on glucan synthesis by glucosyltransferases and Streptococcus mutans acidogenicity . J Appl Microbiol , 103 : 1960 – 1968 .
  • Gregoire , S , Xiao , J , Silva , BB , Gonzalez , I , Agidi , PS , Klein , MI , Ambatipudi , KS , Rosalen , PL , Bauserman , R Waugh , RE . 2011 . Role of glucosyltransferase B in interactions of Candida albicans with Streptococcus mutans and with an experimental pellicle on hydroxyapatite surfaces . Appl Environ Microbiol , 77 : 6357 – 6367 .
  • Hall-Stoodley , L , Costerton , JW and Stoodley , P . 2004 . Bacterial biofilms: from the natural environment to infectious diseases . Nat Rev Microbiol , 2 : 95 – 108 .
  • Heydorn , A , Nielsen , AT , Hentzer , M , Sternberg , C , Givskov , M , Ersboll , BK and Molin , S . 2000 . Quantification of biofilm structures by the novel computer program COMSTAT . Microbiology , 146 : 2395 – 2407 .
  • Howell , AB , Reed , JD , Krueger , CG , Winterbottom , R , Cunningham , DG and Leahy , M . 2005 . A-type cranberry proanthocyanidins and uropathogenic bacterial anti-adhesion activity . Phytochemistry , 66 : 2281 – 2291 .
  • Howell , AB , Vorsa , N , Der Marderosian , A and Foo , LY . 1998 . Inhibition of the adherence of P-fimbriated Escherichia coli to uroepithelial-cell surfaces by proanthocyanidin extracts from cranberries . N Engl J Med , 339 : 1085 – 1086 .
  • Jayaraman , GC , Penders , JE and Burne , RA . 1997 . Transcriptional analysis of the Streptococcus mutans hrcA, grpE and dnaK genes and regulation of expression in response to heat shock and environmental acidification . Mol Microbiol , 25 : 329 – 341 .
  • Jobstl , E , O’Connell , J , Fairclough , JP and Williamson , MP . 2004 . Molecular model for astringency produced by polyphenol/protein interactions . Biomacromolecules , 5 : 942 – 949 .
  • Kajfasz , JK , Martinez , AR , Rivera-Ramos , I , Abranches , J , Koo , H , Quivey , RG Jr and Lemos , JA . 2009 . Role of clp proteins in expression of virulence properties of Streptococcus mutans . J Bacteriol , 191 : 2060 – 2068 .
  • Kessler , D , Herth , W and Knappe , J . 1992 . Ultrastructure and pyruvate formate-lyase radical quenching property of the multienzymic AdhE protein of Escherichia coli . J Biol Chem , 267 : 18073 – 18079 .
  • Klein , MI , DeBaz , L , Agidi , S , Lee , H , Xie , G , Lin , AH , Hamaker , BR , Lemos , JA and Koo , H . 2010 . Dynamics of Streptococcus mutans transcriptome in response to starch and sucrose during biofilm development . PLoS ONE , 5 : e13478
  • Klein , MI , Xiao , J , Lu , B , Delahunty , CM , Yates , JR 3rd and Koo , H . 2012 . Streptococcus mutans protein synthesis during mixed-species biofilm development by high-throughput quantitative proteomics . PLoS ONE , 7 : e45795
  • Koo , H , Duarte , S , Murata , RM , Scott-Anne , K , Gregoire , S , Watson , GE , Singh , AP and Vorsa , N . 2010 . Influence of cranberry proanthocyanidins on formation of biofilms by Streptococcus mutans on saliva-coated apatitic surface and on dental caries development in vivo . Caries Res , 44 : 116 – 126 .
  • Koo , H , Nino de Guzman , P , Schobel , BD , Vacca Smith , AV and Bowen , WH . 2006 . Influence of cranberry juice on glucan-mediated processes involved in Streptococcus mutans biofilm development . Caries Res , 40 : 20 – 27 .
  • Koo , H , Xiao , J , Klein , MI and Jeon , JG . 2010 . Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms . J Bacteriol , 192 : 3024 – 3032 .
  • Lemos , JA , Chen , YY and Burne , RA . 2001 . Genetic and physiologic analysis of the groE operon and role of the HrcA repressor in stress gene regulation and acid tolerance in Streptococcus mutans . J Bacteriol , 183 : 6074 – 6084 .
  • Lemos , JA , Luzardo , Y and Burne , RA . 2007 . Physiologic effects of forced down-regulation of dnaK and groEL expression in Streptococcus mutans . J Bacteriol , 189 : 1582 – 1588 .
  • Lewis , K . 2001 . Riddle of biofilm resistance . Antimicrob Agents Chemother , 45 : 999 – 1007 .
  • Liu , Y , Black , MA , Caron , L and Camesano , TA . 2006 . Role of cranberry juice on molecular-scale surface characteristics and adhesion behavior of Escherichia coli . Biotechnol Bioeng , 93 : 297 – 305 .
  • Lynch , DJ , Fountain , TL , Mazurkiewicz , JE and Banas , JA . 2007 . Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture . FEMS Microbiol Lett , 268 : 158 – 165 .
  • Marsh , PD . 2003 . Are dental diseases examples of ecological catastrophes? . Microbiology , 149 : 279 – 294 .
  • Nakayama , K . 1992 . Nucleotide sequence of Streptococcus mutans superoxide dismutase gene and isolation of insertion mutants . J Bacteriol , 174 : 4928 – 4934 .
  • O’May , C and Tufenkji , N . 2011 . The swarming motility of Pseudomonas aeruginosa is blocked by cranberry proanthocyanidins and other tannin-containing materials . Appl Environ Microbiol , 77 : 3061 – 3067 .
  • O’Toole , G , Kaplan , HB and Kolter , R . 2000 . Biofilm formation as microbial development . Annu Rev Microbiol , 54 : 49 – 79 .
  • Paes Leme , AF , Koo , H , Bellato , CM , Bedi , G and Cury , JA . 2006 . The role of sucrose in cariogenic dental biofilm formation – new insight . J Dent Res , 85 : 878 – 887 .
  • Polashock , J and Vorsa , N . 2002 . Development of SCAR markers for DNA fingerprinting and germplasm analysis of American cranberry . J Am Soc Hort Sci , 127 : 677 – 684 .
  • Sato , Y , Yamamoto , Y and Kizaki , H . 1997 . Cloning and sequence analysis of the gbpC gene encoding a novel glucan-binding protein of Streptococcus mutans . Infect Immun , 65 : 668 – 675 .
  • Schilling , KM and Bowen , WH . 1992 . Glucans synthesized in situ in experimental salivary pellicle function as specific binding sites for Streptococcus mutans . Infect Immun , 60 : 284 – 295 .
  • Schmidt , BM , Ribnicky , DM , Lipsky , PE and Raskin , I . 2007 . Revisiting the ancient concept of botanical therapeutics . Nat Chem Biol , 3 : 360 – 366 .
  • Schroeder , A , Mueller , O , Stocker , S , Salowsky , R , Leiber , M , Gassmann , M , Lightfoot , S , Menzel , W , Granzow , M and Ragg , T . 2006 . The RIN: an RNA integrity number for assigning integrity values to RNA measurements . BMC Mol Biol , 7 : 3
  • Singh , AP , Singh , RK , Kim , KK , Satyan , KS , Nussbaum , R , Torres , M , Brard , L and Vorsa , N . 2009 . Cranberry proanthocyanidins are cytotoxic to human cancer cells and sensitize platinum-resistant ovarian cancer cells to paraplatin . Phytother Res , 23 : 1066 – 1074 .
  • Stewart , PS and Franklin , MJ . 2008 . Physiological heterogeneity in biofilms . Nat Rev Microbiol , 6 : 199 – 210 .
  • Tao , L and Tanzer , JM . 2002 . Novel sucrose-dependent adhesion co-factors in Streptococcus mutans . J Dent Res , 81 : 505 – 510 .
  • Vacca-Smith , AM and Bowen , WH . 1998 . Binding properties of streptococcal glucosyltransferases for hydroxyapatite, saliva-coated hydroxyapatite, and bacterial surfaces . Arch Oral Biol , 43 : 103 – 110 .
  • Vvedenskaya , I and Vorsa , N . 2004 . Flavonoid composition over fruit development and maturation in American cranberry, Vaccinium macrocarpon ait . Plant Sci , 167 : 1043 – 1054 .
  • Xiao , J , Klein , MI , Falsetta , ML , Lu , B , Delahunty , CM , Yates , JR 3rd , Heydorn , A and Koo , H . 2012 . The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm . PLoS Pathog , 8 : e1002623
  • Yanagida , A , Kanda , T , Tanabe , M , Matsudaira , F and Oliveira Cordeiro , JG . 2000 . Inhibitory effects of apple polyphenols and related compounds on cariogenic factors of mutans streptococci . J Agric Food Chem , 48 : 5666 – 5671 .
  • Yin , JL , Shackel , NA , Zekry , A , McGuinness , PH , Richards , C , Putten , KV , McCaughan , GW , Eris , JM and Bishop , GA . 2001 . Real-time reverse transcriptase-polymerase chain reaction (RT-PCR) for measurement of cytokine and growth factor mRNA expression with fluorogenic probes or SYBR green . Immunol Cell Biol , 79 : 213 – 221 .
  • Koo , H , Hayacibara , F , Schobel , BD , Cury , JA , Rosalen , PL , Park , YK , Vacca-Smith , AM and Bowen , WH . 2003 . Inhibition of Streptococcus mutans biofilm accumulation and polysaccharide production by apigenin and tt-farnesol . J Antimicrob Chemother. , 52 : 782 – 789 .

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.