Screening for new surface anchoring domains for lactococcus lactis

Frontiers in Microbiology

Volumn 10, Issue AUG, 2019, Pages

  Plavec, Tina Vida ^a,b   Štrukelj, Borut ^a,b   Berlec, Aleš ^a,b  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Anchor; ChW; Endolysin; Lactococcus lactis; LPXTG; Phage AM12; Surface display

Indexed keywords

EID: 85071956357     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2019.01879     Document Type: Article

References (58)

1. Almeida, J. F., Breyner, N. M., Mahi, M., Ahmed, B., Benbouziane, B., Boas, P. C., et al. (2016). Expression of fibronectin binding protein A (FnBPA) from Staphylococcus aureus at the cell surface of Lactococcus lactis improves its immunomodulatory properties when used as protein delivery vector. Vaccine 34, 1312–1318. doi: 10.1016/j.vaccine.2016.01.022
2. Andre, G., Leenhouts, K., Hols, P., and Dufrene, Y. F. (2008). Detection and localization of single LysM-peptidoglycan interactions. J. Bacteriol. 190, 7079– 7086. doi: 10.1128/JB.00519-08
3. Berlec, A., Malovrh, T., Zadravec, P., Steyer, A., Ravnikar, M., Sabotic, J., et al. (2013). Expression of a hepatitis a virus antigen in Lactococcus lactis and Escherichia coli and evaluation of its immunogenicity. Appl. Microbiol. Biotechnol. 97, 4333–4342. doi: 10.1007/s00253-013-4722-3
4. Berlec, A., Perse, M., Ravnikar, M., Lunder, M., Erman, A., Cerar, A., et al. (2017). Dextran sulphate sodium colitis in C57BL/6J mice is alleviated by Lactococcus lactis and worsened by the neutralization of tumor necrosis factor α. Int. Immunopharmacol. 43, 219–226. doi: 10.1016/j.intimp.2016.12.027
5. Brinster, S., Furlan, S., and Serror, P. (2007). C-terminal WxL domain mediates cell wall binding in Enterococcus faecalis and other gram-positive bacteria. J. Bacteriol. 189, 1244–1253. doi: 10.1128/JB.00773-06
6. Buist, G., Steen, A., Kok, J., and Kuipers, O. P. (2008). LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68, 838–847. doi: 10.1111/j.1365-2958.2008.06211.x
7. Davis, N. G., and Model, P. (1985). An artificial anchor domain: hydrophobicity suffices to stop transfer. Cell 41, 607–614. doi: 10.1016/S0092-8674(85)80033-7
8. de Azevedo, M., Meijerink, M., Taverne, N., Pereira, V. B., LeBlanc, J. G., Azevedo, V., et al. (2015). Recombinant invasive Lactococcus lactis can transfer DNA vaccines either directly to dendritic cells or across an epithelial cell monolayer. Vaccine 33, 4807–4812. doi: 10.1016/j.vaccine.2015.07.077
9. de Vrese, M., and Schrezenmeir, J. (2008). Probiotics, prebiotics, and synbiotics. Adv. Biochem. Eng. Biotechnol. 111, 1–66. doi: 10.1007/10_2008_097
10. Desvaux, M., Candela, T., and Serror, P. (2018). Surfaceome and proteosurfaceome in parietal monoderm bacteria: focus on protein cell-surface display. Front. Microbiol. 9:100. doi: 10.3389/fmicb.2018.00100
11. Dieye, Y., Oxaran, V., Ledue-Clier, F., Alkhalaf, W., Buist, G., Juillard, V., et al. (2010). Functionality of sortase a in Lactococcus lactis. Appl. Environ. Microbiol. 76, 7332–7337. doi: 10.1128/AEM.00928-10
12. Dieye, Y., Usai, S., Clier, F., Gruss, A., and Piard, J. C. (2001). Design of a protein-targeting system for lactic acid bacteria. J. Bacteriol. 183, 4157–4166. doi: 10. 1128/JB.183.14.4157-4166.2001
13. El-Gebali, S., Mistry, J., Bateman, A., Eddy, S. R., Luciani, A., Potter, S. C., et al. (2019). The Pfam protein families database in 2019. Nucleic Acids Res. 47, D427–D432. doi: 10.1093/nar/gky995
14. Fernandez-Tornero, C., Lopez, R., Garcia, E., Gimenez-Gallego, G., and Romero, A. (2001). A novel solenoid fold in the cell wall anchoring domain of the pneumococcal virulence factor LytA. Nat. Struct. Biol. 8, 1020–1024. doi: 10. 1038/nsb724
15. Georgiou, G., Stathopoulos, C., Daugherty, P. S., Nayak, A. R., and Iverson, B. L. (1997). Display of heterologous proteins on the surface of microorganisms: from the screening of combinatorial libraries to live recombinant vaccines. Nat. Biotechnol. 15, 29–34. doi: 10.1038/nbt0197-29
16. Godon, J. J., Jury, K., Shearman, C. A., and Gasson, M. J. (1994). The Lactococcus lactis sex-factor aggregation gene cluA. Mol. Microbiol. 12, 655–663. doi: 10. 1111/j.1365-2958.1994.tb01053.x
17. Hu, S., Kong, J., Kong, W., Guo, T., and Ji, M. (2010). Characterization of a novel LysM domain from Lactobacillus fermentum bacteriophage endolysin and its use as an anchor to display heterologous proteins on the surfaces of lactic acid bacteria. Appl. Environ. Microbiol. 76, 2410–2418. doi: 10.1128/AEM.01752-09
18. Hu, S., Kong, J., Sun, Z., Han, L., Kong, W., and Yang, P. (2011). Heterologous protein display on the cell surface of lactic acid bacteria mediated by the s-layer protein. Microb. Cell Fact. 10:86. doi: 10.1186/1475-2859-10-86
19. Jee, P. F., Tiong, V., Shu, M. H., Khoo, J. J., Wong, W. F., Abdul Rahim, R., et al. (2017). Oral immunization of a non-recombinant Lactococcus lactis surface displaying influenza hemagglutinin 1 (HA1) induces mucosal immunity in mice. PLoS One 12:e0187718. doi: 10.1371/journal.pone.0187718
20. Kosler, S., Strukelj, B., and Berlec, A. (2017). Lactic acid bacteria with concomitant IL-17, IL-23 and TNFα-binding ability for the treatment of inflammatory bowel disease. Curr. Pharm. Biotechnol. 18, 318–326. doi: 10. 2174/1389201018666170210152218
21. Kyla-Nikkila, K., Alakuijala, U., and Saris, P. E. (2010). Immobilization of Lactococcus lactis to cellulosic material by cellulose-binding domain of Cellvibrio japonicus. J. Appl. Microbiol. 109, 1274–1283. doi: 10.1111/j.1365-2672.2010.04757.x
22. Le Loir, Y., Azevedo, V., Oliveira, S. C., Freitas, D. A., Miyoshi, A., Bermudez-Humaran, L. G., et al. (2005). Protein secretion in Lactococcus lactis: an efficient way to increase the overall heterologous protein production. Microb. Cell Fact. 4:2.
23. Le Loir, Y., Nouaille, S., Commissaire, J., Bretigny, L., Gruss, A., and Langella, P. (2001). Signal peptide and propeptide optimization for heterologous protein secretion in Lactococcus lactis. Appl. Environ. Microbiol. 67, 4119–4127. doi: 10.1128/aem.67.9.4119-4127.2001
24. Lee, S. Y., Choi, J. H., and Xu, Z. (2003). Microbial cell-surface display. Trends Biotechnol. 21, 45–52. doi: 10.1016/S0167-7799(02)00006-9
25. Lindholm, A., Smeds, A., and Palva, A. (2004). Receptor binding domain of Escherichia coli F18 fimbrial adhesin FedF can be both efficiently secreted and surface displayed in a functional form in Lactococcus lactis. Appl. Environ. Microbiol. 70, 2061–2071. doi: 10.1128/AEM.70.4.2061-2071.2004
26. Liu, S., Kyla-Nikkila, K., and Saris, P. E. (2011). Cell immobilization studies using a cellulose-binding domain fused to PrtP in Lactococcus lactis. Bioeng. Bugs 2, 160–162. doi: 10.4161/bbug.2.3.15348
27. Mahony, J., Kot, W., Murphy, J., Ainsworth, S., Neve, H., Hansen, L. H., et al. (2013). Investigation of the relationship between lactococcal host cell wall polysaccharide genotype and 936 phage receptor binding protein phylogeny. Appl. Environ. Microbiol. 79, 4385–4392. doi: 10.1128/AEM.00653-13
28. Mahony, J., Moscarelli, A., Kelleher, P., Lugli, G. A., Ventura, M., Settanni, L., et al. (2017). Phage biodiversity in artisanal cheese wheys reflects the complexity of the fermentation process. Viruses 9:45. doi: 10.3390/v9030045
29. Mao, R., Wu, D., Hu, S., Zhou, K., Wang, M., and Wang, Y. (2017). Secretory expression and surface display of a new and biologically active single-chain insulin (SCI-59) analog by lactic acid bacteria. Appl. Microbiol. Biotechnol. 101, 3259–3271. doi: 10.1007/s00253-017-8125-8
30. Michon, C., Langella, P., Eijsink, V. G., Mathiesen, G., and Chatel, J. M. (2016). Display of recombinant proteins at the surface of lactic acid bacteria: strategies and applications. Microb. Cell Fact. 15:70. doi: 10.1186/s12934-016-0468-9
31. Moks, T., Abrahmsen, L., Nilsson, B., Hellman, U., Sjoquist, J., and Uhlen, M. (1986). Staphylococcal protein a consists of five IgG-binding domains. Eur. J. Biochem. 156, 637–643. doi: 10.1111/j.1432-1033.1986.tb09 625.x
32. Nguyen, H.-M., Mathiesen, G., Stelzer, E. M., Pham, M. L., Kuczkowska, K., Mackenzie, A., et al. (2016). Display of a β-mannanase and a chitosanase on the cell surface of Lactobacillus plantarum towards the development of whole-cell biocatalysts. Microb. Cell Fact. 15:169. doi: 10.1186/s12934-016-0570-z
33. Nolling, J., Breton, G., Omelchenko, M. V., Makarova, K. S., Zeng, Q., Gibson, R., et al. (2001). Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183, 4823–4838. doi: 10.1128/JB.183.16.4823-4838.2001
34. Okano, K., Zhang, Q., Kimura, S., Narita, J., Tanaka, T., Fukuda, H., et al. (2008). System using tandem repeats of the cA peptidoglycan-binding domain from Lactococcus lactis for display of both N-and C-terminal fusions on cell surfaces of lactic acid bacteria. Appl. Environ. Microbiol. 74, 1117–1123. doi: 10.1128/AEM.02012-07
35. Oliveira, H., Melo, L. D., Santos, S. B., Nobrega, F. L., Ferreira, E. C., Cerca, N., et al. (2013). Molecular aspects and comparative genomics of bacteriophage endolysins. J. Virol. 87, 4558–4570. doi: 10.1128/JVI.03277-12
36. Piard, J. C., Hautefort, I., Fischetti, V. A., Ehrlich, S. D., Fons, M., and Gruss, A. (1997). Cell wall anchoring of the Streptococcus pyogenes M6 protein in various lactic acid bacteria. J. Bacteriol. 179, 3068–3072. doi: 10.1128/jb.179.9.3068-3072.1997
37. Plavec, T. V., and Berlec, A. (2019). Engineering of lactic acid bacteria for delivery of therapeutic proteins and peptides. Appl. Microbiol. Biotechnol. 103, 2053– 2066. doi: 10.1007/s00253-019-09628-y
38. Poquet, I., Saint, V., Seznec, E., Simoes, N., Bolotin, A., and Gruss, A. (2000). HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing. Mol. Microbiol. 35, 1042–1051. doi: 10.1046/j.1365-2958.2000.01757.x
39. Ramasamy, R., Yasawardena, S., Zomer, A., Venema, G., Kok, J., and Leenhouts, K. (2006). Immunogenicity of a malaria parasite antigen displayed by Lactococcus lactis in oral immunisations. Vaccine 24, 3900–3908. doi: 10.1016/j.vaccine. 2006.02.040
40. Ravnikar, M., Strukelj, B., Obermajer, N., Lunder, M., and Berlec, A. (2010). Engineered lactic acid bacterium Lactococcus lactis capable of binding antibodies and tumor necrosis factor alpha. Appl. Environ. Microbiol. 76, 6928–6932. doi: 10.1128/AEM.00190-10
41. Skrlec, K., Pucer Janez, A., Rogelj, B., Strukelj, B., and Berlec, A. (2017). Evasin-displaying lactic acid bacteria bind different chemokines and neutralize CXCL8 production in Caco-2 cells. Microb. Biotechnol. 10, 1732–1743. doi: 10.1111/1751-7915.12781
42. Skrlec, K., Strukelj, B., and Berlec, A. (2015). Non-immunoglobulin scaffolds: a focus on their targets. Trends Biotechnol. 33, 408–418. doi: 10.1016/j.tibtech. 2015.03.012
43. Stahl, S., and Uhlen, M. (1997). Bacterial surface display: trends and progress. Trends Biotechnol. 15, 185–192. doi: 10.1016/S0167-7799(97)01034-2
44. Steen, A., Buist, G., Horsburgh, G. J., Venema, G., Kuipers, O. P., Foster, S. J., et al. (2005). AcmA of Lactococcus lactis is an N-acetylglucosaminidase with an optimal number of LysM domains for proper functioning. FEBS J. 272, 2854–2868. doi: 10.1111/j.1742-4658.2005.04706.x
45. Steiner, D., Forrer, P., and Pluckthun, A. (2008). Efficient selection of DARPins with sub-nanomolar affinities using SRP phage display. J. Mol. Biol. 382, 1211–1227. doi: 10.1016/j.jmb.2008.07.085
46. Stentz, R., Jury, K., Eaton, T., Parker, M., Narbad, A., Gasson, M., et al. (2004). Controlled expression of CluA in Lactococcus lactis and its role in conjugation. Microbiology 150(Pt 8), 2503–2512. doi: 10.1099/mic.0.27 149-0
47. Stern, J., Morais, S., Ben-David, Y., Salama, R., Shamshoum, M., Lamed, R., et al. (2018). Assembly of synthetic functional cellulosomal structures onto the cell surface of Lactobacillus plantarum, a potent member of the gut microbiome. Appl. Environ. Microbiol. 84:e00282-18. doi: 10.1128/AEM.00 282-18
48. Van Braeckel-Budimir, N., Haijema, B. J., and Leenhouts, K. (2013). Bacterium-like particles for efficient immune stimulation of existing vaccines and new subunit vaccines in mucosal applications. Front. Immunol. 4:282. doi: 10.3389/fimmu. 2013.00282
49. van Roosmalen, M. L., Kanninga, R., El Khattabi, M., Neef, J., Audouy, S., Bosma, T., et al. (2006). Mucosal vaccine delivery of antigens tightly bound to an adjuvant particle made from food-grade bacteria. Methods 38, 144–149. doi: 10.1016/j.ymeth.2005.09.015
50. Visweswaran, G. R., Kurek, D., Szeliga, M., Pastrana, F. R., Kuipers, O. P., Kok, J., et al. (2017). Expression of prophage-encoded endolysins contributes to autolysis of Lactococcus lactis. Appl. Microbiol. Biotechnol. 101, 1099–1110. doi: 10.1007/s00253-016-7822-z
51. Visweswaran, G. R., Leenhouts, K., van Roosmalen, M., Kok, J., and Buist, G. (2014). Exploiting the peptidoglycan-binding motif, LysM, for medical and industrial applications. Appl. Microbiol. Biotechnol. 98, 4331–4345. doi: 10. 1007/s00253-014-5633-7
52. Visweswaran, G. R., Steen, A., Leenhouts, K., Szeliga, M., Ruban, B., Hesseling-Meinders, A., et al. (2013). AcmD, a homolog of the major autolysin AcmA of Lactococcus lactis, binds to the cell wall and contributes to cell separation and autolysis. PLoS One 8:e72167. doi: 10.1371/journal.pone.0072167
53. Wieczorek, A. S., and Martin, V. J. (2012). Effects of synthetic cohesin-containing scaffold protein architecture on binding dockerin-enzyme fusions on the surface of Lactococcus lactis. Microb. Cell Fact. 11:160. doi: 10.1186/1475-2859-11-160
54. Yin, S., Zhu, H., Shen, M., Li, G., Lu, S., Zhao, Y., et al. (2018). Surface display of heterologous beta-galactosidase in food-grade recombinant Lactococcus lactis. Curr. Microbiol. 75, 1362–1371. doi: 10.1007/s00284-018-1531-z
55. Zadravec, P., Mavrič, A., Bogovič Matijašić, B., Štrukelj, B., and Berlec, A. (2014). Engineering BmpA as a carrier for surface display of IgG-binding domain on Lactococcus lactis. Protein Eng. Des. Sel. 27, 21–27. doi: 10.1093/protein/gzt059
56. Zadravec, P., Strukelj, B., and Berlec, A. (2015a). Heterologous surface display on lactic acid bacteria: non-GMO alternative? Bioengineered 6, 179–183. doi: 10.1080/21655979.2015.1040956
57. Zadravec, P., Strukelj, B., and Berlec, A. (2015b). Improvement of LysM-mediated surface display of designed ankyrin repeat proteins (DARPins) in recombinant and nonrecombinant strains of Lactococcus lactis and Lactobacillus Species. Appl. Environ. Microbiol. 81, 2098–2106. doi: 10.1128/AEM.03694-14
58. Zhou, M., Boekhorst, J., Francke, C., and Siezen, R. J. (2008). LocateP: genome-scale subcellular-location predictor for bacterial proteins. BMC Bioinform. 9:173. doi: 10.1186/1471-2105-9-173