Heparin stimulates biofilm formation of Escherichia coli strain Nissle 1917.
Biofilm
Escherichia coli
Heparin
Probiotic
Salmonella enterica
Journal
Biotechnology letters
ISSN: 1573-6776
Titre abrégé: Biotechnol Lett
Pays: Netherlands
ID NLM: 8008051
Informations de publication
Date de publication:
Jan 2021
Jan 2021
Historique:
received:
14
04
2020
accepted:
29
09
2020
pubmed:
5
10
2020
medline:
12
10
2021
entrez:
4
10
2020
Statut:
ppublish
Résumé
Escherichia coli strain Nissle 1917 (EcN), a gut probiotic competing with pathogenic bacteria, has been used to attenuate various intestinal dysfunctions. Heparin is a sulfated glycosaminoglycan enriched in the human and animal intestinal mucosa, which has a close connection with bacterial biofilm formation. However, the characteristics of heparin affecting bacterial biofilm formation remain obscure. In this study, we investigated the influence of heparin and its derivatives on EcN biofilm formation. Here, we found that heparin stimulated EcN biofilm formation in a dose-dependent manner. With the addition of native heparin, the EcN biofilm formation increased 6.9- to 10.8-fold than that without heparin, and was 1.4-, 3.1-, 3.0-, and 3.8-fold higher than that of N-desulfated heparin (N-DS), 2-O-desulfated heparin (2-O-DS), 6-O-desulfated heparin (6-O-DS), and N-/2-O-/6-O-desulfated heparin (N-/2-O-/6-O-DS), respectively. Depolymerization of heparin produced chain-shortened heparin fragments with decreased molecular weight. The depolymerized heparins did not stimulate EcN biofilm formation. The OD570 value of EcN biofilm with the addition of chain-shortened heparin fragments was 8.7-fold lower than that of the native heparin. Furthermore, the biofilm formation of Salmonella enterica serovar Typhimurium was also investigated with the addition of heparin derivatives, and the results were consistent with that of EcN biofilm formation. We conclude that heparin stimulated EcN biofilm formation. Both the sulfation and chain-length of heparin contributed to the enhancement of EcN biofilm formation. This study increases the understanding of how heparin affects biofilm formation, indicating the potential role of heparin in promoting intestinal colonization of probiotics that antagonize pathogen infections.
Identifiants
pubmed: 33011901
doi: 10.1007/s10529-020-03019-4
pii: 10.1007/s10529-020-03019-4
doi:
Substances chimiques
Heparin
9005-49-6
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
235-246Subventions
Organisme : National Natural Science Foundation of China
ID : 31670120
Références
An C, Zhao L, Wei Z, Zhou X (2017) Chemoenzymatic synthesis of 3′-phosphoadenosine-5′-phosphosulfate coupling with an ATP regeneration system. Appl Microbiol Biot 101(20):7535–7544
Aquino RS, Pereira MS, Vairo BC, Cinelli LP, Santos GR, Fonseca RJ, Mourao PA (2010) Heparins from porcine and bovine intestinal mucosa: are they similar drugs? Thromb Haemostasis 103(05):1005–1015
Ayotte L, Perlin AS (1986) NMR spectroscopic observations related to the function of sulfate groups in heparin. Calcium binding vs. biological activity. Carbohydr Res 145(2):267–277
pubmed: 3955564
Biran R, Pond D (2017) Heparin coatings for improving blood compatibility of medical devices. Adv Drug Deliver Rev 112:12–23
Capila I, Linhardt RJ (2002) Heparin–protein interactions. Angew Chem Int Ed 41(3):390–412
Casu B, Naggi A, Torri G (2010) Heparin-derived heparan sulfate mimics to modulate heparan sulfate–protein interaction in inflammation and cancer. Matrix Biol 29(6):442–452
pubmed: 20416374
pmcid: 3057403
Cauda F, Cauda V, Fiori C, Onida B, Garrone E (2008) Heparin coating on ureteral double J stents prevents encrustations: an in vivo case study. J Endourol 22(3):465–472
pubmed: 18307380
Chen X, Ling P, Duan R, Zhang T (2012) Effects of heparosan and heparin on the adhesion and biofilm formation of several bacteria in vitro. Carbohydr Polym 88(4):1288–1292
Chen Q, Zhu Z, Wang J, Lopez A, Li S, Kumar A, Yu F, Chen H, Cai C, Zhang L (2017) Probiotic E. coli Nissle 1917 biofilms on silicone substrates for bacterial interference against pathogen colonization. Acta Biomater. https://doi.org/10.1016/j.actbio.2017.01.011
pubmed: 29294376
pmcid: 5803415
Cress BF, Bhaskar U, Vaidyanathan D, Williams A, Cai C, Liu X, Fu L, M-Chari V, Zhang F, Mousa SA, Dordick JS, Koffas MA, Linhardt RJ (2019) Heavy heparin: a stable isotope-enriched, chemoenzymatically-synthesized, poly-component drug. Angew Chem Int Ed 58:5962–5966
Deriu E, Liu JZ, Pezeshki M, Edwards RA, Ochoa RJ, Contreras H, Libby SJ, Fang FC, Raffatellu M (2013) Probiotic bacteria reduce Salmonella Typhimurium intestinal colonization by competing for iron. Cell Host Microbe 14(1):26–37
pubmed: 23870311
pmcid: 3752295
Fang K, Jin X, Hong SH (2018) Probiotic Escherichia coli inhibits biofilm formation of pathogenic E. coli via extracellular activity of DegP. Sci Rep 8(1):4939. https://doi.org/10.1038/s41598-018-23180-1
pubmed: 29563542
pmcid: 5862908
Freudenberg U, Zieris A, Chwalek K, Tsurkan MV, Maitz MF, Atallah P, Levental KR, Eming SA, Werner C (2015) Heparin desulfation modulates VEGF release and angiogenesis in diabetic wounds. J Control Release 220:79–88
pubmed: 26478015
Grozdanov L, Raasch C, Schulze J, Sonnenborn U, Gottschalk G, Hacker J, Dobrindt U (2004) Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol 186(16):5432–5441
pubmed: 15292145
pmcid: 490877
Guo Y, Conrad HE (1989) The disaccharide composition of heparins and heparan sulfates. Anal Biochem 176(1):96–104
pubmed: 2523675
Hancock V, Dahl M, Klemm P (2010) Probiotic Escherichia coli strain Nissle 1917 outcompetes intestinal pathogens during biofilm formation. J Med Microbiol 59(Pt 4):392–399. https://doi.org/10.1099/jmm.0.008672-0
pubmed: 20110388
Irvine SA, Steele TW, Bhuthalingam R, Li M, Boujday S, Prawirasatya M, Neoh KG, Boey FYC, Venkatraman SS (2015) Quantification of aldehyde terminated heparin by SEC-MALLS–UV for the surface functionalization of polycaprolactone biomaterials. Colloid Surf B 132:253–263
Jiang Y, Kong Q, Roland KL, Wolf A, Curtiss R III (2014) Multiple effects of Escherichia coli Nissle 1917 on growth, biofilm formation, and inflammation cytokines profile of Clostridium perfringens type A strain CP4. Pathog Dis 70(3):390–400. https://doi.org/10.1111/2049-632x.12153
pubmed: 24532573
pmcid: 4038294
Jin Z, Jiang Q, Fang B, Sun B (2019) The ArlR-MgrA regulatory cascade regulates PIA-dependent and protein-mediated biofilm formation in Rbf-dependent and Rbf-independent pathways. Int J Med Microbiol 309(2):85–96
pubmed: 30606691
Kaplan O, Hierlemann T, Krajewski S, Kurz J, Nevoralova M, Houska M, Riedel T, Riedelova Z, Zarubova J, Wendel HP (2017) Low-thrombogenic fibrin‐heparin coating promotes in vitro endothelialization. J Biomed Mater Res A 105(11):2995–3005
pubmed: 28646555
Kruis W, Fric P, Pokrotnieks J, Lukas M, Fixa B, Kascak M, Kamm M, Weismueller J, Beglinger C, Stolte M, Wolff C, Schulze J (2004) Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53(11):1617–1623
pubmed: 15479682
pmcid: 1774300
Li W, Johnson DJD, Esmon CT, Huntington JA (2004) Structure of the antithrombin–thrombin–heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol 11(9):857–862. https://doi.org/10.1038/nsmb811
pubmed: 15311269
Linhardt RJ (2003) 2003 Claude S. Hudson Award address in carbohydrate chemistry. Heparin: structure and activity. J Med Chem 46(13):2551–2564
pubmed: 12801218
Liu Q, Valimaki S, Shaukat A, Shen B, Linko V, Kostiainen MA (2019) Serum albumin–peptide conjugates for simultaneous heparin binding and detection. ACS Omega 4:21891–21899
pubmed: 31891067
pmcid: 6933801
Massip C, Branchu P, Bossuet-Greif N, Chagneau CV, Gaillard D, Martin P, Boury M, Secher T, Dubois D, Nougayrede J-P, Oswald E (2019) Deciphering the interplay between the genotoxic and probiotic activities of Escherichia coli Nissle 1917. PLoS Pathog 15(9):e1008029
pubmed: 31545853
pmcid: 6776366
Mendes A, Meneghetti MC, Palladino MV, Justo GZ, Sassaki GL, Fareed J, Lima MA, Nader HB (2019) Crude heparin preparations unveil the presence of structurally diverse oversulfated contaminants. Molecules 24(16):2988
pmcid: 6721129
Mishra S, Horswill AR (2017) Heparin mimics extracellular DNA in binding to cell surface-localized proteins and promoting Staphylococcus aureus biofilm formation. mSphere 2(3):e00135–e00117
pubmed: 28656173
pmcid: 5480030
Mohsin M, Guenther S, Schierack P, Tedin K, Wieler LH (2015) Probiotic Escherichia coli Nissle 1917 reduces growth, Shiga toxin expression, release and thus cytotoxicity of enterohemorrhagic Escherichia coli. Int J Med Microbiol 305(1):20–26. https://doi.org/10.1016/j.ijmm.2014.10.003
pubmed: 25465158
Ohland CL, Macnaughton WK (2010) Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastr L 298(6):G807–G819. https://doi.org/10.1152/ajpgi.00243.2009
Onishi A, St AK, Dordick JS, Linhardt RJ (2016) Heparin and anticoagulation. Front Biosci 21(7):1372–1392
Patzer SI, Baquero MR, Bravo D, Moreno F, Hantke K (2003) The colicin G, H and X determinants encode microcins M and H47, which might utilize the catecholate siderophore receptors FepA, Cir, Fiu and IroN. Microbiology 149(9):2557–2570. https://doi.org/10.1099/mic.0.26396-0
pubmed: 12949180
Perlin A, Mackie D, Dietrich C (1971) Evidence for a (1→ 4)-linked 4-O-(α-L-idopyranosyluronic acid 2-sulfate)-(2-deoxy-2-sulfoamino-D-glucopyranosyl 6-sulfate) sequence in heparin: long-range H-H coupling in 4-deoxy-hex-4-enopyranosides. Carbohydr Res 18(2):185–194
pubmed: 5151386
Riedl CR, Witkowski M, Plas E, Pflueger H (2002) Heparin coating reduces encrustation of ureteral stents: a preliminary report. Int J Antimicrob AG 19(6):507–510
Ruggieri MR, Hanno PM, Levin RM (1987) Reduction of bacterial adherence to catheter surface with heparin. J Urol 138(2):423–426
pubmed: 3298698
Scaldaferri F, Gerardi V, Mangiola F, Lopetuso LR, Pizzoferrato M, Petito V, Papa A, Stojanovic J, Poscia A, Cammarota G, Gasbarrini A (2016) Role and mechanisms of action of Escherichia coli Nissle 1917 in the maintenance of remission in ulcerative colitis patients: an update. World J Gastroenterol 22(24):5505–5511
pubmed: 27350728
pmcid: 4917610
Schlee M, Wehkamp J, Altenhoefer A, Oelschlaeger TA, Stange EF, Fellermann K (2007) Induction of human beta-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect Immun 75(5):2399–2407. https://doi.org/10.1128/IAI.01563-06
pubmed: 17283097
pmcid: 1865783
Shanks RM, Donegan NP, Graber ML, Buckingham SE, Zegans ME, Cheung AL, O’Toole GA (2005) Heparin stimulates Staphylococcus aureus biofilm formation. Infect Immun 73(8):4596–4606
pubmed: 16040971
pmcid: 1201187
Shanks RM, Sargent JL, Martinez RM, Graber ML, O’Toole GA (2006) Catheter lock solutions influence staphylococcal biofilm formation on abiotic surfaces. Nephrol Dial Transpl 21(8):2247–2255. https://doi.org/10.1093/ndt/gfl170
Shteindel N, Yankelev D, Gerchman Y (2019) High-throughput quantitative measurement of bacterial attachment kinetics on seconds time scale. Microb Ecol 77(3):726–735. https://doi.org/10.1007/s00248-018-1254-5
pubmed: 30244277
Soundararajan M, von Bunau R, Oelschlaeger TA (2019) K5 capsule and lipopolysaccharide are important in resistance to T4 phage attack in probiotic E. coli strain Nissle 1917. Front Microbiol 10:2783
pubmed: 31849915
pmcid: 6895014
Spillmann D, Witt D, Lindahl U (1998) Defining the interleukin-8-binding domain of heparan sulfate. J Biol Chem 273(25):15487–15493
pubmed: 9624135
Toloza L, Gimenez R, Fabrega MJ, Alvarez CS, Aguilera L, Canas MA, Martin-Venegas R, Badia J, Baldoma L (2015) The secreted autotransporter toxin (Sat) does not act as a virulence factor in the probiotic Escherichia coli strain Nissle 1917. BMC Microbiol 15(1):250
pubmed: 26518156
pmcid: 4628265
Turnbull J, Powell A, Guimond S (2001) Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol 11(2):75–82
pubmed: 11166215
Waldrop R, McLaren A, Calara F, McLemore R (2014) Biofilm growth has a threshold response to glucose in vitro. Clin Orthop Relat R 472(11):3305–3310. https://doi.org/10.1007/s11999-014-3538-5
Wang Z, Yang B, Zhang Z, Ly M, Takieddin M, Mousa S, Liu J, Dordick JS, Linhardt RJ (2011) Control of the heparosan N-deacetylation leads to an improved bioengineered heparin. Appl Microbiol Biot 91(1):91–99
Xu X, Dai Y (2010) Heparin: an intervenor in cell communication. J Cell Mol Med 14(1-2):175–180
pubmed: 19659457
Xu D, Arnold K, Liu J (2018) Using structurally defined oligosaccharides to understand the interactions between proteins and heparan sulfate. Curr Opin Struct Biol 50:155–161
pubmed: 29684759
pmcid: 6078804
Yan H, Bao F, Zhao L, Yu Y, Tang J, Zhou X (2015) Cyclic AMP (cAMP) receptor protein-cAMP complex regulates heparosan production in Escherichia coli strain nissle 1917. Appl Environ Microbiol 81(22):7687–7696
pubmed: 26319872
pmcid: 4616935
Yu X, Lin C, Yu J, Qi Q, Wang Q (2019a) Bioengineered Escherichia coli Nissle 1917 for tumour-targeting therapy. Microb Biotechnol 0(0):1–8
Yu Y, Ye H, Wu D, Shi H, Zhou X (2019b) Chemoenzymatic quantification for monitoring unpurified polysaccharide in rich medium. Appl Microbiol Biot 103(18):7635–7645
Zhang C, Liu L, Teng L, Chen J, Liu J, Li J, Du G, Chen J (2012) Metabolic engineering of Escherichia coli BL21 for biosynthesis of heparosan, a bioengineered heparin precursor. Metab Eng 14(5):521–527
pubmed: 22781283
Zhou X, Chandarajoti K, Pham TQ, Liu R, Liu JJG (2011) Expression of heparan sulfate sulfotransferases in Kluyveromyces lactis and preparation of 3′-phosphoadenosine-5′-phosphosulfate. Glycobiology 21(6):771–780
pubmed: 21224284
pmcid: 3091527
Zhou X, Li L, Linhardt RJ, Liu J (2013) Neutralizing the anticoagulant activity of ultra-low-molecular-weight heparins using N-acetylglucosamine 6-sulfatase. FEBS J 280(10):2523–2532. https://doi.org/10.1111/febs.12169
pubmed: 23374371