Biomedical applications of nisin

Journal of Applied Microbiology

Volumn 120, Issue 6, 2016, Pages 1449-1465

  Shin, J M ^a,b   Gwak, J W ^a   Kamarajan, P ^a   Fenno, J C ^a   Rickard, A H ^b   Kapila, Y L ^a  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Antimicrobial peptide; Biofilm; Cancer; Infectious disease; Lantibiotic; Nisin; Oral disease

Indexed keywords

ANTIBIOTICS; BACTERIA; BIOFILMS; CANCER CELLS; DISEASES; MEDICAL APPLICATIONS;

ANTIMICROBIAL PEPTIDE; BACTERIOCINS; BIOMEDICAL APPLICATIONS; BIOPRESERVATIVE; CANCER; GRAM-POSITIVE BACTERIUM; INFECTIOUS DISEASE; LANTIBIOTICS; NISIN; ORAL DISEASE;

PEPTIDES;

ANTIINFECTIVE AGENT; BACTERIOCIN; NISIN; ANTINEOPLASTIC AGENT;

AMINO ACID; ANTIBIOTICS; BACTERIUM; BIOFILM; BIOTECHNOLOGY; CANCER; DISEASE INCIDENCE; IMMUNE RESPONSE; INFECTIOUS DISEASE; PEPTIDE; PRESERVATIVE; TOXIN;

ADAPTIVE IMMUNITY; ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BIOMEDICAL ENGINEERING; CANCER CELL; CYTOTOXICITY; ENTEROCOCCUS; FOOD AND DRUG ADMINISTRATION; HOST RESISTANCE; IMMUNOMODULATION; INFECTION; LACTOCOCCUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUTH DISEASE; NEOPLASM; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; REVIEW; STREPTOCOCCUS; STREPTOCOCCUS PNEUMONIAE; BACTERIAL INFECTIONS; BIOFILM; CHEMISTRY; DRUG EFFECTS; GENETICS; GRAM POSITIVE BACTERIUM; METABOLISM; MICROBIOLOGY; PRESERVATION; VIRUS DISEASES;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE; LACTOCOCCUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NEGIBACTERIA; POSIBACTERIA; STREPTOCOCCUS; STREPTOCOCCUS PNEUMONIAE;

ANTI-BACTERIAL AGENTS; ANTINEOPLASTIC AGENTS; BACTERIAL INFECTIONS; BACTERIOCINS; BIOFILMS; DRUG RESISTANCE, BACTERIAL; GRAM-POSITIVE BACTERIA; NISIN; PRESERVATION, BIOLOGICAL; VIRUS DISEASES;

EID: 84958818146     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13033     Document Type: Review

References (161)

1. Aas, J.A., Paster, B.J., Stokes, L.N., Olsen, I. and Dewhirst, F.E. (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43, 5721-5732.
2. Ahire, J. and Dicks, L. (2015) Nisin incorporated with 2, 3-dihydroxybenzoic acid in nanofibers inhibits biofilm formation by a methicillin-resistant strain of Staphylococcus aureus. Probiotics Antimicrob Proteins 7, 52-59.
3. Ahn, J., Chen, C.Y. and Hayes, R.B. (2012) Oral microbiome and oral and gastrointestinal cancer risk. Cancer Causes Control 23, 399-404.
4. Akerey, B., Le Lay, C., Fliss, I., Subirade, M. and Rouabhia, M. (2009) In vitro efficacy of nisin Z against Candida albicans adhesion and transition following contact with normal human gingival cells. J Appl Microbiol 107, 1298-1307.
5. Alifax, R. and Chevalier, R. (1962) Study of the nisinase produced by Streptococcus thermophilus. J Dairy Res 29, 233-240.
6. Arnold, R.R. and Cole, M.F. (1977) A bactericidal effect for human lactoferrin. Science 197, 263-265.
7. Asaduzzaman, S.M. and Sonomoto, K. (2009) Lantibiotics: diverse activities and unique modes of action. J Biosci Bioeng 107, 475-487.
8. Balciunas, E.M., Martinez, F.A.C., Todorov, S.D., de Melo Franco, B.D.G., Converti, A. and de Souza Oliveira, R.P. (2013) Novel biotechnological applications of bacteriocins: a review. Food Control 32, 134-142.
9. Bartoloni, A., Mantella, A., Goldstein, B.P., Dei, R., Benedetti, M., Sbaragli, S. and Paradisi, F. (2004) In vitro activity of nisin against clinical isolates of Clostridium difficile. J Chemother 16, 119-121.
10. Begde, D., Bundale, S., Mashitha, P., Rudra, J., Nashikkar, N. and Upadhyay, A. (2011) Immunomodulatory efficacy of nisin - a bacterial lantibiotic peptide. J Pept Sci 17, 438-444.
11. Begley, M., Cotter, P.D., Hill, C. and Ross, R.P. (2010) Glutamate decarboxylase-mediated nisin resistance in Listeria monocytogenes. Appl Environ Microbiol 76, 6541-6546.
12. Benmechernene, Z., Fernandez-No, I., Kihal, M., Bohme, K., Calo-Mata, P. and Barros-Velazquez, J. (2013) Recent patents on bacteriocins: food and biomedical applications. Recent Pat DNA Gene Seq 7, 66-73.
13. Blay, G.L., Lacroix, C., Zihler, A. and Fliss, I. (2007) In vitro inhibition activity of nisin A, nisin Z, pediocin PA-1 and antibiotics against common intestinal bacteria. Lett Appl Microbiol 45, 252-257.
14. Boohaker, R.J., Lee, M.W., Vishnubhotla, P., Perez, J.M. and Khaled, A.R. (2012) The use of therapeutic peptides to target and to kill cancer cells. Curr Med Chem 19, 3794-3804.
15. Bosch, A.A., Biesbroek, G., Trzcinski, K., Sanders, E.A. and Bogaert, D. (2013) Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 9, e1003057.
16. Breukink, E., Wiedemann, I., Van Kraaij, C., Kuipers, O.P., Sahl, H.G. and De Kruijff, B. (1999) Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286, 2361-2364.
17. Brumfitt, W., Salton, M.R. and Hamilton-Miller, J.M. (2002) Nisin, alone and combined with peptidoglycan-modulating antibiotics: activity against methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci. J Antimicrob Chemother 50, 731-734.
18. Bultman, S.J. (2014) Emerging roles of the microbiome in cancer. Carcinogenesis 35, 249-255.
19. Cao, L.T., Wu, J.Q., Xie, F., Hu, S.H. and Mo, Y. (2007) Efficacy of nisin in treatment of clinical mastitis in lactating dairy cows. J Dairy Sci 90, 3980-3985.
20. Carlson, S. and Bauer, H. (1957) A study of problems associated with resistance to nisin. Arch Hyg Bakteriol 141, 445-460.
21. Center for Disease Control and Prevention, Chronic Disease Prevention and Health Promotion (2015) Available at: http://www.cdc.gov/chronicdisease/ [Accessed: September 29, 2015].
22. Center for Disease Control and Prevention, Methicillin-resistant Staphylococcus Aureus (MRSA) Infections (2015) Available at: http://www.cdc.gov/mrsa/ [Accessed: September 29, 2015].
23. Centers for Disease Control and Prevention, Leading Causes of Death (2015) Available at: http://www.cdc.gov/nchs/fastats/leading-causes-of-death.htm [Accessed: September 29, 2015].
24. Chambers, H.F. (2001) The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 7, 178.
25. Cleveland, J., Montville, T.J., Nes, I.F. and Chikindas, M.L. (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71, 1-20.
26. Cornut, G., Fortin, C. and Soulières, D. (2008) Antineoplastic properties of bacteriocins: revisiting potential active agents. Am J Clin Oncol 31, 399-404.
27. Cotter, P.D., Hill, C. and Ross, R.P. (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3, 777-788.
28. Cotter, P.D., Ross, R.P. and Hill, C. (2013) Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol 11, 95-105.
29. Crandall, A.D. and Montville, T.J. (1998) Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. Appl Environ Microbiol 64, 231-237.
30. Dakota, N. (1999) Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus - Minnesota and North Dakota, 1997-1999. Arch Dermatol 135, 1566-1568.
31. Daum, R.S. (2007) Skin and soft-tissue infections caused by methicillin-resistant Staphylococcus aureus. N Engl J Med 357, 380-390.
32. De Arauz, L.J., Jozala, A.F., Mazzola, P.G. and Penna, T.C.V. (2009) Nisin biotechnological production and application: a review. Trends Food Sci Technol 20, 146-154.
33. De Freire Bastos, M., Coelho, M. and da Silva Santos, O. (2014) Resistance to bacteriocins produced by Gram-positive bacteria. Microbiology 161, 683-700.
34. De Kwaadsteniet, M., Doeschate, K.T. and Dicks, L.M.T. (2008) Characterization of the structural gene encoding nisin F, a new lantibiotic produced by a Lactococcus lactis subsp. lactis isolate from freshwater catfish (Clarias gariepinus). Appl Environ Microbiol 74, 547-549.
35. De Kwaadsteniet, M., Doeschate, K.T. and Dicks, L.M.T. (2009) Nisin F in the treatment of respiratory tract infections caused by Staphylococcus aureus. Lett Appl Microbiol 48, 65-70.
36. De Vos, W.M., Mulders, J.W., Siezen, R.J., Hugenholtz, J. and Kuipers, O.P. (1993) Properties of nisin Z and distribution of its gene, nisZ, in Lactococcus lactis. Appl Environ Microbiol 59, 213-218.
37. Delves-Broughton, J., Blackburn, P., Evans, R.J. and Hugenholtz, J. (1996) Applications of the bacteriocin, nisin. Antonie Van Leeuwenhoek 69, 193-202.
38. DeSantis, C.E., Lin, C.C., Mariotto, A.B., Siegel, R.L., Stein, K.D., Kramer, J.L., Alteri, R., Robbins, A.S. et al. (2014) Cancer treatment and survivorship statistics, 2014. CA Cancer J Clin 64, 252-271.
39. Diekema, D.J., Pfaller, M.A., Schmitz, F.J., Smayevsky, J., Bell, J., Jones, R.N. and Beach, M. (2001) Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis 32, S114-S132.
40. Dosler, S. and Gerceker, A.A. (2011) In vitro activities of nisin alone or in combination with vancomycin and ciprofloxacin against methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. Chemotherapy 57, 511-516.
41. Drago, L., Mombelli, B., De Vecchi, E., Bonaccorso, C., Fassina, M.C. and Gismondo, M.R. (2004) Candida albicans cellular internalization: a new pathogenic factor? Int J Antimicrob Agents 16, 545-547.
42. Draper, L.A., Cotter, P.D., Hill, C. and Ross, R.P. (2015) Lantibiotic resistance. Microbiol Mol Biol Rev 79, 171-191.
43. Eckert, R.L. (1989) Structure, function, and differentiation of the keratinocyte. Physiol Rev 69, 1316-1346.
44. Eversole, L.R., Reichart, P.A., Ficarra, G., Schmidt-Westhausen, A., Romagnoli, P. and Pimpinelli, N. (1997) Oral keratinocyte immune responses in HIV-associated candidiasis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 84, 372-380.
45. Farah, C.S., Ashman, R.B. and Challacombe, S.J. (2000) Oral candidosis. Clin Dermatol 18, 553-562.
46. Fauci, A.S. and Morens, D.M. (2012) The perpetual challenge of infectious diseases. N Engl J Med 366, 454-461.
47. Fernández, L., Delgado, S., Herrero, H., Maldonado, A. and Rodríguez, J.M. (2008) The bacteriocin nisin, an effective agent for the treatment of staphylococcal mastitis during lactation. J Hum Lact 24, 311-316.
48. Field, D., Connor, P.M., Cotter, P.D., Hill, C. and Ross, R.P. (2008) The generation of nisin variants with enhanced activity against specific Gram-positive pathogens. Mol Microbiol 69, 218-230.
49. Field, D., Begley, M., O'Connor, P.M., Daly, K.M., Hugenholtz, F., Cotter, P.D., Hill, C. and Ross, R.P. (2012) Bioengineered nisin A derivatives with enhanced activity against both Gram-positive and Gram-negative pathogens. PLoS ONE 7, e46884.
50. Field, D., Cotter, P.D., Ross, R.P. and Hill, C. (2015) Bioengineering of the model lantibiotic nisin. Bioengineered 6, 187-192.
51. Foxman, B., D'Arcy, H., Gillespie, B., Bobo, J.K. and Schwartz, K. (2002) Lactation mastitis: occurrence and medical management among 946 breastfeeding women in the United States. Am J Epidemiol 155, 103-114.
52. Frankel, A.E., Powell, B.L., Duesbery, N.S., Vande Woude, G.F. and Leppla, S.H. (2002) Anthrax fusion protein therapy of cancer. Curr Protein Pept Sci 3, 399-407.
53. Fridkin, S.K., Hageman, J.C., Morrison, M., Sanza, L.T., Como-Sabetti, K., Jernigan, J.A., Harriman, K., Harrison, L.H. et al. (2005) Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med 352, 1436-1444.
54. Ganz, T. (2004) Antimicrobial polypeptides. J Leukoc Biol 75, 34-38.
55. Gasparoni, A., Fonzi, L., Schneider, G.B., Wertz, P.W., Johnson, G.K. and Squier, C.A. (2004) Comparison of differentiation markers between normal and two squamous cell carcinoma cell lines in culture. Arch Oral Biol 49, 653-664.
56. Giffard, C.J., Ladha, S., Mackie, A.R., Clark, D.C. and Sanders, D. (1996) Interaction of nisin with planar lipid bilayers monitored by fluorescence recovery after photobleaching. J Membr Biol 151, 293-300.
57. Gilbert, P., Maira-Litran, T., McBain, A.J., Rickard, A.H. and Whyte, F.W. (2002) The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol 46, 203-256.
58. Gillor, O., Nigro, L.M. and Riley, M.A. (2005) Genetically engineered bacteriocins and their potential as the next generation of antimicrobials. Curr Pharm Des 11, 1067-1075.
59. Global Medical Discovery (2015) Available at: https://globalmedicaldiscovery.com/key-drug-discovery-articles/nisin-synergizes-with-cisplatin-induce-apoptosis-in-hnscc-cells-highly-resistant-to-ionizing-radiation-cisplatin/ [Accessed: November 12, 2015].
60. Goldstein, B.P., Wei, J., Greenberg, K. and Novick, R. (1998) Activity of nisin against Streptococcus pneumoniae, in vitro, and in a mouse infection model. J Antimicrob Chemother 42, 277-278.
61. Gravesen, A., Sørensen, K., Aarestrup, F.M. and Knøchel, S. (2001) Spontaneous nisin-resistant Listeria monocytogenes mutants with increased expression of a putative penicillin-binding protein and their sensitivity to various antibiotics. Microb Drug Resist 7, 127-135.
62. Gross, E. and Morell, J.L. (1971) Structure of nisin. J Am Chem Soc 93, 4634-4635.
63. Hament, J.M., Kimpen, J.L., Fleer, A. and Wolfs, T.F. (1999) Respiratory viral infection predisposing for bacterial disease: a concise review. FEMS Immunol Med Microbiol 26, 189-195.
64. Hancock, R.E. and Sahl, H.G. (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24, 1551-1557.
65. Hasper, H.E., de Kruijff, B. and Breukink, E. (2004) Assembly and stability of nisin-lipid II pores. Biochemistry 43, 11567-11575.
66. Healy, B., Field, D., O'Connor, P.M., Hill, C., Cotter, P.D. and Ross, R.P. (2013) Intensive mutagenesis of the nisin hinge leads to the rational design of enhanced derivatives. PLoS ONE 8, e79563.
67. Heunis, T.D., Smith, C. and Dicks, L.M.T. (2013) Evaluation of a nisin-eluting nanofiber scaffold to treat Staphylococcus aureus-induced skin infections in mice. Antimicrob Agents Chemother 57, 3928-3935.
68. Howell, T.H., Fiorellini, J.P., Blackburn, P., Projan, S.J., Harpe, J. and Williams, R.C. (1993) The effect of a mouthrinse based on nisin, a bacteriocin, on developing plaque and gingivitis in beagle dogs. J Clin Periodontol 20, 335-339.
69. Hsu, S.T.D., Breukink, E., Tischenko, E., Lutters, M.A., de Kruijff, B., Kaptein, R., Bonvin, A.M. and van Nuland, N.A. (2004) The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat Struct Biol 11, 963-967.
70. Huycke, M.M., Sahm, D.F. and Gilmore, M.S. (1998) Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis 4, 239.
71. Johnson, I.H., Hayday, H. and Colman, G. (1978) The effects of nisin on the microbial flora of the dental plaque of monkeys (Macaca fascicularis). J Appl Bacteriol 45, 99-109.
72. Joo, N.E., Ritchie, K., Kamarajan, P., Miao, D. and Kapila, Y.L. (2012) Nisin, an apoptogenic bacteriocin and food preservative, attenuates HNSCC tumorigenesis via CHAC1. Cancer Med 1, 295-305.
73. Kamarajan, P., Hayami, T., Matte, B., Liu, Y., Danciu, T., Ramamoorthy, A., Worden, F., Kapila, S. et al. (2015) Nisin ZP, a bacteriocin and food preservative, inhibits head and neck cancer tumorigenesis and prolongs survival. PLoS ONE 10, e0131008.
74. Karakas Sen, A., Narbad, A., Horn, N., Dodd, H.M., Parr, A.J., Colquhoun, I. and Gasson, M.J. (1999) Post-translational modification of nisin. Eur J Biochem 261, 524-532.
75. Kindrachuk, J., Jenssen, H., Elliott, M., Nijnik, A., Magrangeas-Janot, L., Pasupuleti, M., Thorson, L., Ma, S. et al. (2013) Manipulation of innate immunity by a bacterial secreted peptide: lantibiotic nisin Z is selectively immunomodulatory. Innate immun 19, 315-327.
76. Köck, R., Becker, K., Cookson, B., van Gemert-Pijnen, J.E., Harbarth, S., Kluytmans, J., Mielke, M., Peters, G., et al. (2010) Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill 15, 19688.
77. Kooy, J.S. (1952) Strains of Lactobacillus plantarum which inhibit the activity of the antibiotics produced by Streptococcus lactis. Ned Melk Zuiveltijdschr 6, 323-330.
78. Kramer, N.E., Smid, E.J., Kok, J., de Kruijff, B., Kuipers, O.P. and Breukink, E. (2004) Resistance of Gram-positive bacteria to nisin is not determined by lipid II levels. FEMS Microbiol Lett 239, 157-161.
79. Kramer, N.E., van Hijum, S.A., Knol, J., Kok, J. and Kuipers, O.P. (2006) Transcriptome analysis reveals mechanisms by which Lactococcus lactis acquires nisin resistance. Antimicrob Agents Chemother 50, 1753-1761.
80. Kramer, N.E., Hasper, H.E., van den Bogaard, P.T., Morath, S., de Kruijff, B., Hartung, T., Smid, E.J., Breukink, E., et al. (2008) Increased D-alanylation of lipoteichoic acid and a thickened septum are main determinants in the nisin resistance mechanism of Lactococcus lactis. Microbiology 154, 1755-1762.
81. Kuwano, K., Tanaka, N., Shimizu, T., Nagatoshi, K., Nou, S. and Sonomoto, K. (2005) Dual antibacterial mechanisms of nisin Z against Gram-positive and Gram-negative bacteria. Int J Antimicrob Agents 26, 396-402.
82. Lagos, R., Tello, M., Mercado, G., García, V. and Monasterio, O. (2009) Antibacterial and antitumorigenic properties of microcin E492, a pore-forming bacteriocin. Curr Pharm Biotechnol 10, 74-85.
83. Le Lay, C., Akerey, B., Fliss, I., Subirade, M. and Rouabhia, M. (2008) Nisin Z inhibits the growth of Candida albicans and its transition from blastospore to hyphal form. J Appl Microbiol 105, 1630-1639.
84. Ling, L.L., Schneider, T., Peoples, A.J., Spoering, A.L., Engels, I., Conlon, B.P., Mueller, A., Schäberle, T.F., et al. (2015) A new antibiotic kills pathogens without detectable resistance. Nature 517, 455-459.
85. Lubelski, J., Rink, R., Khusainov, R., Moll, G.N. and Kuipers, O.P. (2008) Biosynthesis, immunity, regulation, mode of action and engineering of the model lantibiotic nisin. Cell Mol Life Sci 65, 455-476.
86. Lubelski, J., Khusainov, R. and Kuipers, O.P. (2009) Directionality and coordination of dehydration and ring formation during biosynthesis of the lantibiotic nisin. J Biol Chem 284, 25962-25972.
87. Lundin, J.I. and Checkoway, H. (2009) Endotoxin and cancer. Environ Health Perspect 117, 1344-1350.
88. Mah, T.F.C. and O'Toole, G.A. (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9, 34-39.
89. Maher, S. and McClean, S. (2006) Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro. Biochem Pharmacol 71, 1289-1298.
90. Mantovani, H.C. and Russell, J.B. (2001) Nisin resistance of Streptococcus bovis. Appl Environ Microbiol 67, 808-813.
91. Marcenes, W., Kassebaum, N.J., Bernabé, E., Flaxman, A., Naghavi, M., Lopez, A. and Murray, C.J.L. (2013) Global burden of oral conditions in 1990-2010 a systematic analysis. J Dent Res 92, 592-597.
92. Marsh, P.D. (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149, 279-294.
93. Marsh, P.D. (2010) Controlling the oral biofilm with antimicrobials. J Dent 38, S11-S15.
94. Meyer, J.E. and Harder, J. (2007) Antimicrobial peptides in oral cancer. Curr Pharm Des 13, 3119-3130.
95. Micek, S.T., Kollef, K.E., Reichley, R.M., Roubinian, N. and Kollef, M.H. (2007) Health care-associated pneumonia and community-acquired pneumonia: a single-center experience. Antimicrob Agents Chemother 51, 3568-3573.
96. Michaud, D.S. and Izard, J. (2014) Microbiota, oral microbiome, and pancreatic cancer. Cancer J 20, 203.
97. Millette, M., Cornut, G., Dupont, C., Shareck, F., Archambault, D. and Lacroix, M. (2008) Capacity of human nisin-and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl Environ Microbiol 74, 1997-2003.
98. Moll, G.N., Clark, J., Chan, W.C., Bycroft, B.W., Roberts, G.C., Konings, W.N. and Driessen, A.J. (1997) Role of transmembrane pH gradient and membrane binding in nisin pore formation. J Bacteriol 179, 135-140.
99. Mulders, J.W., Boerrigter, I.J., Rollema, H.S., Siezen, R.J. and de Vos, W.M. (1991) Identification and characterization of the lantibiotic nisin Z, a natural nisin variant. Eur J Biochem 201, 581-584.
100. Mungrue, I.N., Pagnon, J., Kohannim, O., Gargalovic, P.S. and Lusis, A.J. (2009) CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J Immunol 182, 466-476.
101. Murdock, C.A., Cleveland, J., Matthews, K.R. and Chikindas, M.L. (2007) The synergistic effect of nisin and lactoferrin on the inhibition of Listeria monocytogenes and Escherichia coli O157: H7. Lett Appl Microbiol 44, 255-261.
102. Naghmouchi, K., Drider, D., Baah, J. and Teather, R. (2010) Nisin A and polymyxin B as synergistic inhibitors of Gram-positive and Gram-negative bacteria. Probiotics Antimicrob Proteins 2, 98-103.
103. Najjar, M.B., Kashtanov, D. and Chikindas, M.L. (2009) Natural antimicrobials ε-poly-l-lysine and nisin A for control of oral microflora. Probiotics Antimicrob Proteins 1, 143-147.
104. Nattress, F.M., Yost, C.K. and Baker, L.P. (2001) Evaluation of the ability of lysozyme and nisin to control meat spoilage bacteria. Int J Food Microbiol 70, 111-119.
105. Nobili, S., Lippi, D., Witort, E., Donnini, M., Bausi, L., Mini, E. and Capaccioli, S. (2009) Natural compounds for cancer treatment and prevention. Pharm Res 59, 365-378.
106. O'Connor, P.M., O'Shea, E.F., Guinane, C.M., O'Sullivan, O., Cotter, P.D., Ross, R.P. and Hill, C. (2015) Nisin H is a new nisin variant produced by the gut-derived strain Streptococcus hyointestinalis DPC6484. Appl Environ Microbiol 81, 3953-3960.
107. Okuda, K.I., Zendo, T., Sugimoto, S., Iwase, T., Tajima, A., Yamada, S., Sonomoto, K. and Mizunoe, Y. (2013) Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm. Antimicrob Agents Chemother 57, 5572-5579.
108. Pablo, M.A., Gaforio, J.J., Gallego, A.M., Ortega, E., Gálvez, A.M. and Alvarez de Cienfuegos López, G. (1999) Evaluation of immunomodulatory effects of nisin-containing diets on mice. FEMS Immunol Med Microbiol 24, 35-42.
109. Page, R.C. and Schroeder, H.E. (1976) Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 34, 235-249.
110. Patel, J.D., Krilov, L., Adams, S., Aghajanian, C., Basch, E., Brose, M.S., Carroll, W.L., de Lima, M. et al. (2014) Clinical cancer advances 2013: annual report on progress against cancer from the American Society of Clinical Oncology. J Clin Oncol 32, 129-160.
111. Peschel, A. and Sahl, H.G. (2006) The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4, 529-536.
112. Petersen, P.E. (2003) The World Oral Health Report 2003: continuous improvement of oral health in the 21st century-the approach of the WHO Global Oral Health Programme. Community Dent Oral Epidemiol 31(s1), 3-24.
113. Pfaller, M.A., Diekema, D.J., Jones, R.N., Messer, S.A. and Hollis, R.J. (2002) Trends in antifungal susceptibility of Candida spp. isolated from pediatric and adult patients with bloodstream infections: SENTRY Antimicrobial Surveillance Program, 1997 to 2000. J Clin Microbiol 40, 852-856.
114. Piper, C., Draper, L.A., Cotter, P.D., Ross, R.P. and Hill, C. (2009) A comparison of the activities of lacticin 3147 and nisin against drug-resistant Staphylococcus aureus and Enterococcus species. J Antimicrob Chemother 64, 546-551.
115. Piper, C., Draper, L.A., Cotter, P.D., Ross, R.P. and Hill, C. (2011) Bioengineering of a nisin A producing Lactococcus lactis to create isogenic strains producing the natural variants Nisin F, Q and Z. Microb Biotechnol 4, 375-382.
116. Ponec, M., Havekes, L., Kempenaar, J., Lavrijsen, S. and Vermeer, B.J. (1984) Defective low-density lipoprotein metabolism in cultured, normal, transformed, and malignant keratinocytes. J Invest Dermatol 83, 436-440.
117. Ponec, M., Kempenaar, J. and Boonstra, J. (1987) Regulation of lipid synthesis in relation to keratinocyte differentiation capacity. Biochim Biophys Acta 921, 512-521.
118. Pongtharangku, T. and Demirci, A. (2007) Online recovery of nisin during fermentation and its effect on nisin production in biofilm reactor. Appl Microbiol Biotechnol 74, 555-562.
119. Preet, S., Bharati, S., Panjeta, A., Tewari, R. and Rishi, P. (2015) Effect of nisin and doxorubicin on DMBA-induced skin carcinogenesis - a possible adjunct therapy. Tumour Biol 36, 1-8.
120. Rayman, K., Malik, N. and Hurst, A. (1983) Failure of nisin to inhibit outgrowth of Clostridium botulinum in a model cured meat system. Appl Environ Microbiol 46, 1450-1452.
121. Reunanen, J. and Saris, P.E.J. (2009) Survival of nisin activity in intestinal environment. Biotechnol Lett 31, 1229-1232.
122. Rogers, L.A. and Whittier, E.O. (1928) Limiting factors in the lactic fermentation. J Bacteriol 16, 211.
123. Ross, A.C. and Vederas, J.C. (2011) Fundamental functionality: recent developments in understanding the structure-activity relationships of lantibiotic peptides. J Antibiot 64, 27-34.
124. Rouse, S., Field, D., Daly, K.M., O'Connor, P.M., Cotter, P.D., Hill, C. and Ross, R.P. (2012) Bioengineered nisin derivatives with enhanced activity in complex matrices. Microb Biotechnol 5, 501-508.
125. Sahl, H.G. and Bierbaum, G. (2008) Multiple activities in natural antimicrobials-multiple activities of natural agents such as defensins and bacteriocins suggest a change in strategy when developing new antimicrobials. Microbe 3, 467.
126. Sahl, H.G., Jack, R.W. and Bierbaum, G. (1995) Biosynthesis and biological activities of lantibiotics with unique post-translational modifications. Eur J Biochem 230, 827-853.
127. Sahm, D.F., Marsilio, M.K. and Piazza, G. (1999) Antimicrobial resistance in key bloodstream bacterial isolates: electronic surveillance with the Surveillance Network Database - USA. Clin Infect Dis 29, 259-263.
128. Schweizer, F. (2009) Cationic amphiphilic peptides with cancer-selective toxicity. Eur J Pharm 625, 190-194.
129. Severina, E., Severin, A. and Tomasz, A. (1998) Antibacterial efficacy of nisin against multidrug-resistant Gram-positive pathogens. J Antimicrob Chemother 41, 341-347.
130. Shaikh, F., Abhinand, P.A. and Ragunath, P.K. (2012) Identification & characterization of Lactobacillus salavarius bacteriocins and its relevance in cancer therapeutics. Bioinformation 8, 589.
131. Shin, J.M., Ateia, I., Paulus, J.R., Liu, H., Fenno, J.C., Rickard, A.H. and Kapila, Y.L. (2015) Antimicrobial nisin acts against saliva derived multi-species biofilms without cytotoxicity to human oral cells. Front Microbiol 6, 617.
132. Singh, A.P., Prabha, V. and Rishi, P. (2013) Value addition in the efficacy of conventional antibiotics by nisin against Salmonella. PLoS ONE 8, e76844.
133. Smith, L. and Hillman, J.D. (2008) Therapeutic potential of type A (I) lantibiotics, a group of cationic peptide antibiotics. Curr Opin Microbiol 11, 401-408.
134. Smith, R.N., Andersen, R.N. and Kolenbrander, P.E. (1991) Inhibition of intergeneric coaggregation among oral bacteria by cetylpyridinium chloride, chlorhexidine digluconate and octenidine dihydrochloride. J Periodontal Res 26, 422-428.
135. Stewart, P.S. and Costerton, J.W. (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358, 135-138.
136. Stuart, C.H., Schwartz, S.A., Beeson, T.J. and Owatz, C.B. (2006) Enterococcus faecalis: its role in root canal treatment failure and current concepts in retreatment. J Endod 32, 93-98.
137. Sun, Z., Zhong, J., Liang, X., Liu, J., Chen, X. and Huan, L. (2009) Novel mechanism for nisin resistance via proteolytic degradation of nisin by the nisin resistance protein NSR. Antimicrob Agents Chemother 53, 1964-1973.
138. Tertoolen, L.G., Kempenaar, J., Boonstra, J., de Laat, S.W. and Ponec, M. (1988) Lateral mobility of plasma membrane lipids in normal and transformed keratinocytes. Biochem Biophys Res Commun 152, 491-496.
139. Thedieck, K., Hain, T., Mohamed, W., Tindall, B.J., Nimtz, M., Chakraborty, T., Wehland, J. and Jänsch, L. (2006) The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. Mol Microbiol 62, 1325-1339.
140. Tong, Z., Dong, L., Zhou, L., Tao, R. and Ni, L. (2010) Nisin inhibits dental caries-associated microorganism in vitro. Peptides 31, 2003-2008.
141. Tong, Z., Zhou, L., Li, J., Jiang, W., Ma, L. and Ni, L. (2011) In vitro evaluation of the antibacterial activities of MTAD in combination with nisin against Enterococcus faecalis. J Endod 37, 1116-1120.
142. Tong, Z., Zhang, Y., Ling, J., Ma, J., Huang, L. and Zhang, L. (2014) An in vitro study on the effects of nisin on the antibacterial activities of 18 antibiotics against Enterococcus faecalis. PLoS ONE 9, e99513.
143. Trick, W.E., Fridkin, S.K., Edwards, J.R., Hajjeh, R.A. and Gaynes, R.P. (2002) Secular trend of hospital-acquired candidemia among intensive care unit patients in the United States during 1989-1999. Clin Infect Dis 35, 627-630.
144. Tripathi, P., Kamarajan, P., Somashekar, B.S., MacKinnon, N., Chinnaiyan, A.M., Kapila, Y.L., Rajendiran, T.M. and Ramamoorthy, A.(2012) Delineating metabolic signatures of head and neck squamous cell carcinoma: phospholipase A 2, a potential therapeutic target. Int J Biochem Cell Biol 44, 1852-1861.
145. Turner, S.R., Love, R.M. and Lyons, K.M. (2004) An in vitro investigation of the antibacterial effect of nisin in root canals and canal wall radicular dentine. Int Endod J 37, 664-671.
146. Ugurlu, T., Turkoglu, M., Gurer, U.S. and Akarsu, B.G. (2007) Colonic delivery of compression coated nisin tablets using pectin/HPMC polymer mixture. Eur J Pharm Biopharm 67, 202-210.
147. Van Heel, A.J., Montalban-Lopez, M. and Kuipers, O.P. (2011) Evaluating the feasibility of lantibiotics as an alternative therapy against bacterial infections in humans. Expert Opin Drug Metab Toxicol 7, 675-680.
148. Van Staden, D.A., Brand, A.M., Endo, A. and Dicks, L.M.T. (2011) Nisin F, intraperitoneally injected, may have a stabilizing effect on the bacterial population in the gastro-intestinal tract, as determined in a preliminary study with mice as model. Lett Appl Microbiol 53, 198-201.
149. Weber, D.J., Rutala, W.A., Sickbert-Bennett, E.E., Samsa, G.P., Brown, V. and Niederman, M.S. (2007) Microbiology of ventilator-associated pneumonia compared with that of hospital-acquired pneumonia. Infect Control 28, 825-831.
150. Wiedemann, I., Breukink, E., van Kraaij, C., Kuipers, O.P., Bierbaum, G., de Kruijff, B. and Sahl, H.G. (2001) Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. J Biol Chem 276, 1772-1779.
151. Wirawan, R.E., Klesse, N.A., Jack, R.W. and Tagg, J.R. (2006) Molecular and genetic characterization of a novel nisin variant produced by Streptococcus uberis. Appl Environ Microbiol 72, 1148-1156.
152. Wroblewski, L.E., Peek, R.M. and Wilson, K.T. (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23, 713-739.
153. Wu, J., Hu, S. and Cao, L. (2007) Therapeutic effect of nisin Z on subclinical mastitis in lactating cows. Antimicrob Agents Chemother 51, 3131-3135.
154. Yang, S.C., Lin, C.H., Sung, C.T. and Fang, J.Y. (2014) Antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front Microbiol 5, 241.
155. Yates, K.R., Welsh, J., Udegbunam, N.O., Greenman, J., Maraveyas, A. and Madden, L.A. (2012) Duramycin exhibits antiproliferative properties and induces apoptosis in tumour cells. Blood Coagul Fibrinolysis 23, 396-401.
156. Yuan, J., Zhang, Z.Z., Chen, X.Z., Yang, W. and Huan, L.D. (2004) Site-directed mutagenesis of the hinge region of nisin Z and properties of nisin Z mutants. Appl Microbiol Biotechnol 64, 806-815.
157. Zendo, T., Fukao, M., Ueda, K., Higuchi, T., Nakayama, J. and Sonomoto, K. (2003) Identification of the lantibiotic nisin Q, a new natural nisin variant produced by Lactococcus lactis 61-14 isolated from a river in Japan. Biosci Biotechnol Biochem 67, 1616-1619.
158. Zetola, N., Francis, J.S., Nuermberger, E.L. and Bishai, W.R. (2005) Community-acquired methicillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis 5, 275-286.
159. Zhang, Q., Yu, Y., Vélasquez, J.E. and van der Donk, W.A. (2012) Evolution of lanthipeptide synthetases. Proc Natl Acad Sci USA 109, 18361-18366.
160. Zhou, L., van Heel, A.J. and Kuipers, O.P. (2015) The length of a lantibiotic hinge region has profound influence on antimicrobial activity and host specificity. Front Microbiol 6, 11.
161. Zijnge, V., Van Leeuwen, M.B., Degener, J.E., Abbas, F., Thurnheer, T., Gmür, R. and Harmsen, H.J. (2010) Oral biofilm architecture on natural teeth. PLoS ONE 5, e9321.