Advertisement

Applied Microbiology and Biotechnology

, Volume 102, Issue 24, pp 10393–10408 | Cite as

Bacteriocins: perspective for the development of novel anticancer drugs

  • Piyush Baindara
  • Suresh Korpole
  • Vishakha GroverEmail author
Mini-Review

Abstract

Antimicrobial peptides (AMPs) from prokaryotic source also known as bacteriocins are ribosomally synthesized by bacteria belonging to different eubacterial taxonomic branches. Most of these AMPs are low molecular weight cationic membrane active peptides that disrupt membrane by forming pores in target cell membranes resulting in cell death. While these peptides known to exhibit broad-spectrum antimicrobial activity, including antibacterial and antifungal, they displayed minimal cytotoxicity to the host cells. Their antimicrobial efficacy has been demonstrated in vivo using diverse animal infection models. Therefore, we have discussed some of the promising peptides for their ability towards potential therapeutic applications. Further, some of these bacteriocins have also been reported to exhibit significant biological activity against various types of cancer cells in different experimental studies. In fact, differential cytotoxicity towards cancer cells as compared to normal cells by certain bacteriocins directs for a much focused research to utilize these compounds as novel therapeutic agents. In this review, bacteriocins that demonstrated antitumor activity against diverse cancer cell lines have been discussed emphasizing their biochemical features, selectivity against extra targets and molecular mechanisms of action.

Keywords

Antimicrobial peptides Bacteriocin Lantibiotic Cationic Cell lines Anticancer 

Notes

Compliance with ethical standards

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdi-Ali A, Worobec EA, Deezagi A, Malekzadeh F (2004) Cytotoxic effects of pyocin S2 produced by Pseudomonas aeruginosa on the growth of three human cell lines. Can J Microbiol 50:375–381PubMedGoogle Scholar
  2. Agarwal V, Metlitskaya A, Severinov K, Nair SK (2011) Structural basis for microcin C7 inactivation by the MccE acetyltransferase. J Biol Chem 286:21295–21303PubMedPubMedCentralGoogle Scholar
  3. Agrawal N, Bettegowda C, Cheong I, Geschwind J-F, Drake CG, Hipkiss EL, Tatsumi M, Dang LH, Diaz LA, Pomper M, Abusedera M, Wahl RL, Kinzler KW, Zhou S, Huso DL, Vogelstein B (2004) Bacteriolytic therapy can generate a potent immune response against experimental tumors. Proc Natl Acad Sci U S A 101:15172–15177PubMedPubMedCentralGoogle Scholar
  4. Ahmadi S, Ghollasi M, Hosseini HM (2017) The apoptotic impact of nisin as a potent bacteriocin on the colon cancer cells. Microb Pathog 111:193–197PubMedGoogle Scholar
  5. Ahn J, Chen CY, Hayes RB (2012) Oral microbiome and oral and gastrointestinal cancer risk. Cancer Causes Control 23:399–404PubMedPubMedCentralGoogle Scholar
  6. Alexandroff AB, Jackson AM, O’Donnell M, James K (1999) BCG immunotherapy of bladder cancer: 20 years on. Lancet 353:1689–1694PubMedGoogle Scholar
  7. Andersland K, Jølle GF, Sand O, Haug TM (2010) Peptide pheromone plantaricin a produced by Lactobacillus plantarum permeabilizes liver and kidney cells. J Membr Biol 235:121–129PubMedGoogle Scholar
  8. Aranha C, Gupta S, Reddy KVR (2004) Contraceptive efficacy of antimicrobial peptide Nisin: in vitro and in vivo studies. Contraception 69:333–338PubMedGoogle Scholar
  9. Arnold T, Zeth K, Linke D (2009) Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. J Biol Chem 284:6403–6413PubMedPubMedCentralGoogle Scholar
  10. Aymerich T, Garriga M, Ylla J (2000) Application of enterocins as biopreservatives against Listeria innocua in meat products. J Food Prot 63:721–726PubMedGoogle Scholar
  11. Baindara P, Chaudhry V, Mittal G, Liao LM, Matos CO, Khathri N, Franco OL, Patil PB, Korpole S (2015) Characterization of the antimicrobial peptide Penisin, a class Ia novel Lantibiotic from Paenibacillus sp. strain A3. Antimicob Agents Chemother 60:580–591PubMedPubMedCentralGoogle Scholar
  12. Baindara P, Singh N, Ranjan M, Nallabelli N, Chaudhry V, Pathania GL, Sharma N, Kumar A, Patil PB, Korpole S (2016) Laterosporulin10: a novel defensin like class IId bacteriocin from Brevibacillus sp. strain SKDU10 with inhibitory activity against microbial pathogens. Microbiol 162:1286–1299Google Scholar
  13. Baindara P, Gautam A, Raghava GPS, Korpole S (2017a) Anticancer properties of a defensin like class IId bacteriocin Laterosporulin10. Sci Rep 19;7:46541.  https://doi.org/10.1038/srep46541
  14. Baindara P, Kapoor A, Korpole S, Grover V (2017b) Cysteine-rich low molecular weight antimicrobial peptides from Brevibacillus and related genera for biotechnological applications. World J Microbiol Biotechnol 33:124PubMedGoogle Scholar
  15. Bastos MDCDF, Coutinho BG, Coelho MLV (2010) Lysostaphin: a staphylococcal bacteriolysin with potential clinical applications. Pharmaceuticals 3:1139–1161PubMedPubMedCentralGoogle Scholar
  16. Bevers EM, Comfurius P, van Rijn JL, Hemker HC, Zwaal RF (1982) Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem 122:429–436PubMedGoogle Scholar
  17. Bizzarri AR, Santini S, Coppari E, Bucciantini M, Di Agostino S, Yamada T, Beattie CW, Cannistraro S (2011) Interaction of an anticancer peptide fragment of azurin with p53 and its isolated domains studied by atomic force spectroscopy. Int J Nanomedicine 6:3011–3019PubMedPubMedCentralGoogle Scholar
  18. Brader P, Stritzker J, Riedl CC, Zanzonico P, Cai S, Burnazi EM, Ghani ER, Hricak H, Szalay AA, Fong Y, Blasberg R (2008) Escherichia coli Nissle 1917 facilitates tumor detection by positron emission tomography and optical imaging. Clin Cancer Res 14:2295–2302PubMedGoogle Scholar
  19. Brand M, de Kwaadsteniet M, Dicks LMT (2010) The ability of nisin F to control Staphylococcus aureus infection in the peritoneal cavity, as studied in mice. Lett Appl Microbiol 51:645–649PubMedGoogle Scholar
  20. Braun V, Pilsl H, Groß P (1994) Colicins: structures, modes of action, transfer through membranes, and evolution. Arch Microbiol 161:199–206PubMedGoogle Scholar
  21. Breukink E, Wiedemann I, van Kraaij C, Kuipers OP, Sahl H, de Kruijff B (1999) Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286:2361–2364PubMedGoogle Scholar
  22. Burdick MD, Harris A, Reid CJ, Iwamura T, M A H (1997) Oligosaccharides expressed on MUC1 produced by pancreatic and colon tumor cell lines. J Biol Chem 272:24198–24202PubMedGoogle Scholar
  23. Burton JP, Cowley S, Simon RR, McKinney J, Wescombe PA, Tagg JR (2011) Evaluation of safety and human tolerance of the oral probiotic Streptococcus salivarius K12: a randomized, placebo-controlled, double-blind study. Food Chem Toxicol 49:2356–2364PubMedGoogle Scholar
  24. Campion A, Casey PG, Field D, Cotter PD, Hill C, Ross RP (2013) In vivo activity of nisin A and nisin V against Listeria monocytogenes in mice. BMC Microbiol 13:23PubMedPubMedCentralGoogle Scholar
  25. Cao LT, Wu JQ, Xie F, Hu SH, Mo Y (2007) Efficacy of nisin in treatment of clinical mastitis in lactating dairy cows. J Dairy Sci 90:3980–3985PubMedGoogle Scholar
  26. Carswell EA, Old LJ, Kassel RL, Green S, Fiore N, Williamson B (1975) An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci U S A 72:3666–3670PubMedPubMedCentralGoogle Scholar
  27. Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubès R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71:158–229PubMedPubMedCentralGoogle Scholar
  28. Castiglione F, Lazzarini A, Carrano L, Corti E, Ciciliato I, Gastaldo L, Candiani P, Losi D, Marinelli F, Selva E, Parenti F (2008) Determining the structure and mode of action of microbisporicin, a potent lantibiotic active against multi-resistant pathogens. Chem Biol 15:22–31PubMedGoogle Scholar
  29. Chaudhari A, Mahfouz M, Fialho AM, Yamada T, Granja AT, Zhu Y, Hashimoto W, Schlarb-Ridley B, Cho W, Das Gupta TK, Chakrabarty AM (2007) Cupredoxin-cancer interrelationship: azurin binding with EphB2, interference in EphB2 tyrosine phosphorylation, and inhibition of cancer growth. Biochem 46:1799–1810Google Scholar
  30. Chaudhary J, Munshi M (1995) Scanning electron microscopic analysis of breast aspirates. Cytopathology 6:162–167PubMedGoogle Scholar
  31. Chen H, Hoover DG (2003) Bacteriocins and their food applications. Compr Rev Food Sci Food Saf 2:82–100Google Scholar
  32. Chen Y-LS, Li J-H, Yu C-Y, Lin C-J, Chiu P-H, Chen P-W, Lin C-C, Chen W-J (2012) Novel cationic antimicrobial peptide GW-H1 induced caspase-dependent apoptosis of hepatocellular carcinoma cell lines. Peptides 36:257–265PubMedGoogle Scholar
  33. Cho J, Hwang IS, Choi H, Hwang JH, Hwang JS, Lee DG (2012) The novel biological action of antimicrobial peptides via apoptosis induction. J Microbiol Biotechnol 22:1457–1466PubMedGoogle Scholar
  34. Chu H-L, Yip B-S, Chen K-H, Yu H-Y, Chih Y-H, Cheng H-T, Chou Y-T, Cheng J-W (2015) Novel antimicrobial peptides with high anticancer activity and selectivity. PLoS One 10:e0126390PubMedPubMedCentralGoogle Scholar
  35. Chumchalová J, Smarda J (2003) Human tumor cells are selectively inhibited by colicins. Folia Microbiol (Praha) 48:111–115Google Scholar
  36. Cintas LM, Rodriguez JM, Fernandez MF, Sletten K, Nes IF, Hernandez PE, Holo H (1995) Isolation and characterization of pediocin L50, a new bacteriocin from Pediococcus acidilactici with a broad inhibitory spectrum. Appl Environ Microbiol 61:2643–2648PubMedPubMedCentralGoogle Scholar
  37. Coburn PS, Gilmore MS (2003) The Enterococcus faecalis cytolysin: a novel toxin active against eukaryotic and prokaryotic cells. Cell Microbiol 5(10):661–669PubMedGoogle Scholar
  38. Coley WB (1910) The treatment of inoperable sarcoma by bacterial toxins (the mixed toxins of the Streptococcus erysipelas and the Bacillus prodigiosus). Proc R Soc Med 3:1–48PubMedPubMedCentralGoogle Scholar
  39. Connor J, Bucana C, Fidler IJ, Schroit J (1989) Differentiation-dependent expression of phosphatidylserine in mammalian plasma membranes: quantitative assessment of outer-leaflet lipid by prothrombinase complex formation. Proc Natl Acad Sci U S A 86:3184–3188PubMedPubMedCentralGoogle Scholar
  40. Cornut G, Fortin C, Soulières D (2008) Antineoplastic properties of bacteriocins: revisiting potential active agents. Am J Clin Oncol 31:399–404PubMedGoogle Scholar
  41. Cotter PD (2012) A bacteriocin perspective. Bioengineered 3:313–319PubMedPubMedCentralGoogle Scholar
  42. Crowther GS, Baines SD, Todhunter SL, Freeman J, Chilton CH, Wilcox MH (2013) Evaluation of NVB302 versus vancomycin activity in an in vitro human gut model of Clostridium difficile infection. J Antimicrob Chemother 68:168–176PubMedGoogle Scholar
  43. Cursino L, Šmarda J, Chartone-Souza E, Nascimento AMA (2002) Recent updated aspects of colicins of enterobacteriaceae. Braz J Microbiol 33:185–195Google Scholar
  44. Cursino L, Smajs D, Smarda J, Nardi RMD, Nicoli JR, Chartone-Souza E, Nascimento AMA (2006) Exoproducts of the Escherichia coli strain H22 inhibiting some enteric pathogens both in vitro and in vivo. J Appl Microbiol 100:821–829PubMedGoogle Scholar
  45. Cutter CN, Siragusa GR (1998) Incorporation of nisin into a meat binding system to inhibit bacteria on beef surfaces. Lett Appl Microbiol 27:19–23PubMedGoogle Scholar
  46. Dabour N, Zihler A, Kheadr E, Lacroix C, Fliss I (2009) In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes. Int J Food Microbiol 133:225–233PubMedGoogle Scholar
  47. Dang LH, Bettegowda C, Huso DL, Kinzler KW, Vogelstein B (2001) Combination bacteriolytic therapy for the treatment of experimental tumors. Proc NatlAcad Sci USA 98:15155–15160Google Scholar
  48. Dethlefsen L, Eckburg PB, Bik EM, Relman D (2006) Assembly of the human intestinal microbiota. Trends Ecol Evol 21:517–523PubMedGoogle Scholar
  49. Dobrzyńska I, Szachowicz-Petelska B, Sulkowski S, Figaszewski Z (2005) Changes in electric charge and phospholipids composition in human colorectal cancer cells. Mol Cell Biochem 276:113–119PubMedGoogle Scholar
  50. Domagala WKL (1980) Surface configuration of human tumor cells obtained by fine needle aspiration biopsy. Scan Electron Microsc 3:101–108Google Scholar
  51. Drider D, Fimland G, Héchard Y, McMullen LM, Prévost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564–582PubMedPubMedCentralGoogle Scholar
  52. Duquesne S, Destoumieux-Garzón D (2007) Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat Prod Rep 24:75005Google Scholar
  53. Elegado FB, Kim WJ, Kwon DY (1997) Rapid purification, partial characterization, and antimicrobial spectrum of the bacteriocin, Pediocin AcM, from Pediococcus acidilactici M. Int J Food Microbiol 37:1–11PubMedGoogle Scholar
  54. Ennahar S, Aoude-Werner D, Sorokine O, Van Dorsselaer A, Bringel F, Hubert JC, Hasselmann C (1996) Production of pediocin AcH by Lactobacillus plantarum WHE 92 isolated from cheese. Appl Environ Microbiol 62:4381–4387PubMedPubMedCentralGoogle Scholar
  55. Ennahar S, Sashihara T, Sonomoto K, Ishizaki A (2000) Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol Rev 24:85–106PubMedGoogle Scholar
  56. Fadeel B, Xue D (2009) The ins and outs of phospholid asymmetry in the plasma membrane: roles in health and disease. Crit Rev Biochem Mol Biol 44:264–277PubMedPubMedCentralGoogle Scholar
  57. Farkas-Himsley H, Cheung R (1976) Bacterial proteinaceous products (bacteriocins) as cytotoxic agents of neoplasia. Cancer Res 36:3561–3567PubMedGoogle Scholar
  58. Farkas-Himsley H, Hill R, Rosen B, Arab S, Lingwood C a (1995) The bacterial colicin active against tumor cells in vitro and in vivo is verotoxin 1. Proc Natl Acad Sci U S A 92:6996–7000PubMedPubMedCentralGoogle Scholar
  59. Feldgarden M, Riley MA (1999) The phenotypic and fitness effects of colicin resistance in Escherichia coli K-12. Evolution (N Y) 53:1019–1027PubMedGoogle Scholar
  60. Fernández L, Delgado S, Herrero H, Maldonado A, Rodríguez JM (2008) The bacteriocin nisin, an effective agent for the treatment of staphylococcal mastitis during lactation. J Hum Lact 24:311–316PubMedGoogle Scholar
  61. Fialho AM, Salunkhe P, Manna S, Mahali S, Chakrabarty AM (2012) Glioblastoma multiforme: novel therapeutic approaches. ISRN Neurol 2012:1–10Google Scholar
  62. Fimland G, Johnsen L, Dalhus B, Nissen-Meyer J (2005) Pediocin-like antimicrobial peptides (class IIa bacteriocins) and their immunity proteins: biosynthesis, structure, and mode of action. J Pept Sci 11:688–696PubMedGoogle Scholar
  63. Fons AG, Tuomo Karjalainen M (2000) Mechanisms of colonisation and colonisation resistance of the digestive tract part 2: bacteria/bacteria interactions. Microb Ecol Health Dis 12:240–246Google Scholar
  64. Fontana MBC, de Bastos MDCF, Brandelli A, Freire De Bastos MDC, Brandelli A (2006) Bacteriocins Pep5 and epidermin inhibit Staphylococcus epidermidis adhesion to catheters. Curr Microbiol 52:350–353PubMedGoogle Scholar
  65. Frana TS, Carlson SA, Rauser DC, Jones BD, Fergen BJ, Griffith RW (2004) Effects of microcin 24-producing Escherichia coli on shedding and multiple-antimicrobial resistance of Salmonella enterica serotype Typhimurium in pigs. Am J Vet Res 65:1616–1620PubMedGoogle Scholar
  66. Fuska J, Fuskova A, Smarda JMJ (1979) Effect of colicin E3 on leukemia cells P388 in vitro. Experientia 35:406–407PubMedGoogle Scholar
  67. Gandhi NM, Morales A, Lamm DL (2013) Bacillus Calmette-Guérin immunotherapy for genitourinary cancer. BJU Int 112:288–297PubMedGoogle Scholar
  68. Goldstein BP, Wei J, Greenberg K, Novick R (1998) Activity of nisin against Streptococcus pneumoniae, in vitro, and in a mouse infection model. J Antimicrob Chemother 42:277–278PubMedGoogle Scholar
  69. Goto M, Yamada T, Kimbara K, Horner J, Newcomb M, Das Gupta TK, Chakrabarty a M (2003) Induction of apoptosis in macrophages by Pseudomonas aeruginosa azurin: tumour-suppressor protein p53 and reactive oxygen species, but not redox activity, as critical elements in cytotoxicity. Mol Microbiol 47:549–559PubMedGoogle Scholar
  70. Grasemann H, Stehling F, Brunar H, Widmann R, Laliberte TW, Molina L, Döring G, Ratjen F (2007) Inhalation of Moli1901 in patients with cystic fibrosis. Chest 131:1461–1466PubMedGoogle Scholar
  71. Gratia A (1925) Sur un remarquable example d’antagonisme entre deux souches de colibacille. Compt Rend Soc Biol 93(Cross reference):1040–1042Google Scholar
  72. Gray MW (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4:a011403PubMedPubMedCentralGoogle Scholar
  73. Gray M, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2: reviews 1018:1–1018Google Scholar
  74. Grover V, Kapoor A, Sehgal K, Kaur G (2016) Chronic inflammation and carcinogenesis—emerging role of chronic inflammatory periodontal disease. Cancer Res Front 2:200–225Google Scholar
  75. Gunther J (1991) Lantibiotics—ribosomally synthesized biologically active polypeptides containing sulfide bridges and α,β-didehydroamino acids. Angew Chem Int Ed 30:1051–1068Google Scholar
  76. Gupta DT (2002) Bacterial redox protein azurin, tumor suppressor protein p53, and regression of cancer. Proc Natl Acad Sci U S A:14098–14103Google Scholar
  77. Hammami R, Zouhir A, Ben Hamida J, Fliss I (2007) BACTIBASE: a new web-accessible database for bacteriocin characterization. BMC Microbiol 7:89PubMedPubMedCentralGoogle Scholar
  78. Hammami R, Zouhir A, Le Lay C, Ben Hamida J, Fliss I (2010) BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiol 10:22PubMedPubMedCentralGoogle Scholar
  79. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70PubMedGoogle Scholar
  80. Haugen HS, Kristiansen PE, Fimland G, Nissen-Meyer J (2008) Mutational analysis of the class IIa bacteriocin curvacin A and its orientation in target cell membranes. Appl Environ Microbiol 74:6766–6773PubMedPubMedCentralGoogle Scholar
  81. Helbig S, Braun V (2011) Mapping functional domains of colicin M. J Bacteriol 193:815–821PubMedGoogle Scholar
  82. Herr HW, Morales A (2008) History of bacillus Calmette-Guerin and bladder cancer: an immunotherapy success story. J Urol 179:53–56PubMedGoogle Scholar
  83. Hetz C, Bono MR, Barros LF, Lagos R (2002) Microcin E492, a channel-forming bacteriocin from Klebsiella pneumoniae, induces apoptosis in some human cell lines. Proc Natl Acad Sci U S A 99:2696–2701PubMedPubMedCentralGoogle Scholar
  84. Hillman JD, Mo J, McDonell E, Cvitkovitch D, Hillman CH (2007) Modification of an effector strain for replacement therapy of dental caries to enable clinical safety trials. J Appl Microbiol 102:1209–1219PubMedGoogle Scholar
  85. Howlader N, Noone AM, Krapcho M, Garshell J, Miller D, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z,Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds). SEER Cancer Statistics Review, 1975-2012, National Cancer Institute. Bethesda, MD, https://seer.cancer.gov/archive/csr/1975_2012/ Accessed 20 Aug 2018
  86. Huang Y-B, Wang X-F, Wang H-Y, Liu Y, Chen Y (2011) Studies on mechanism of action of anticancer peptides by modulation of hydrophobicity within a defined structural framework. Mol Cancer Ther 10:416–426PubMedGoogle Scholar
  87. Ingham A, Ford M, Moore RJ, Tizard M (2003) The bacteriocin piscicolin 126 retains antilisterial activity in vivo. J Antimicrob Chemother 51:1365–1371PubMedGoogle Scholar
  88. Jabés D, Brunati C, Candiani G, Riva S, Romanó G, Donadio S (2011) Efficacy of the new lantibiotic NAI-107 in experimental infections induced by multidrug-resistant gram-positive pathogens. Antimicrob Agents Chemother 55:1671–1676PubMedPubMedCentralGoogle Scholar
  89. Jasniewski J, Cailliez-Grimal C, Chevalot I, Millière J-B, Revol-Junelles A-M (2009) Interactions between two carnobacteriocins Cbn BM1 and Cbn B2 from Carnobacterium maltaromaticum CP5 on target bacteria and Caco-2 cells. Food Chem Toxicol 47:893–897PubMedGoogle Scholar
  90. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59:225–249PubMedGoogle Scholar
  91. Jeuken LJ, Ubbink M, Bitter JH, van Vliet P, Meyer-Klaucke W, Canters GW (2000) The structural role of the copper-coordinating and surface-exposed histidine residue in the blue copper protein azurin. J Mol Biol 299:737–755PubMedGoogle Scholar
  92. Jeziorowski A, Gordon DM (2007) Evolution of microcin V and colicin Ia plasmids in Escherichia coli. J Bacteriol 189:7045–7052PubMedPubMedCentralGoogle Scholar
  93. Jia L, Gorman GS, Coward LU, Noker PE, McCormick D, Horn TL, Harder JB, Muzzio M, Prabhakar B, Ganesh B, Das Gupta TK, Beattie CW (2011) Preclinical pharmacokinetics, metabolism, and toxicity of azurin-p28 (NSC745104) a peptide inhibitor of p53 ubiquitination. Cancer Chemother Pharmacol 68:513–524PubMedGoogle Scholar
  94. Johnson CL, Ridley H, Pengelly RJ, Salleh MZ, Lakey JH (2013) The unstructured domain of colicin N kills Escherichia coli. Mol Microbiol 89:84–95PubMedPubMedCentralGoogle Scholar
  95. Johnstone SA, Gelmon K, Mayer LD, Hancock RE, Bally MB (2000) In vitro characterization of the anticancer activity of membrane-active cationic peptides. I. Peptide-mediated cytotoxicity and peptide-enhanced cytotoxic activity of doxorubicin against wild-type and p-glycoprotein over-expressing tumor cell lines. Anticancer Drug Des 15:151–160PubMedGoogle Scholar
  96. Joo NE, Ritchie K, Kamarajan P, Miao D, Kapila YL (2012) Nisin, an apoptogenic bacteriocin and food preservative, attenuates HNSCC tumorigenesis via CHAC1. Cancer Med 1:295–305PubMedPubMedCentralGoogle Scholar
  97. Kageyama M (1964) Studies of a pyocin. J Biochem 55:49–53PubMedGoogle Scholar
  98. Kamarajan P, Hayami T, Matte B, Liu Y, Danciu T, Ramamoorthy A, Worden F, Kapila S, Kapila Y (2015) Nisin ZP, a bacteriocin and food preservative, inhibits head and neck cancer tumorigenesis and prolongs survival. PLoS One 10:e0131008PubMedPubMedCentralGoogle Scholar
  99. Kang BS, Seo JG, Lee GS, Kim JH, Kim SY, Han YW, Kang H, Kim HO, Rhee JH, Chung MJ, Park YM (2009) Antimicrobial activity of enterocins from Enterococcus faecalis SL-5 against Propionibacterium acne, the causative agent in acne vulgaris, and its therapeutic effect. J Microbiol 47:101–109PubMedGoogle Scholar
  100. Kaur S, Kaur S (2015) Bacteriocins as potential anticancer agents. Front Pharmacol 6:272PubMedPubMedCentralGoogle Scholar
  101. Kawai K, Miyazaki J, Joraku A, Nishiyama H, Akaza H (2013) Bacillus Calmette-Guerin (BCG) immunotherapy for bladder cancer: current understanding and perspectives on engineered BCG vaccine. Cancer Sci 104:22–27PubMedGoogle Scholar
  102. Kim R, Emi M, Tanabe K (2006) Role of mitochondria as the gardens of cell death. Cancer Chemother Pharmacol 57:545–553PubMedGoogle Scholar
  103. Klener P (1999) Chemotherapy side effects and their management. Basic Clin Oncol 19:279–295 STGoogle Scholar
  104. Kozłowska K, Nowak J, Kwiatkowski B, Cichorek M (1999) ESR study of plasmatic membrane of the transplantable melanoma cells in relation to their biological properties. Exp Toxicol Pathol 51:89–92PubMedGoogle Scholar
  105. Kristiansen PE, Fimland G, Mantzilas D, Nissen-Meyer J (2005) Structure and mode of action of the membrane-permeabilizing antimicrobial peptide pheromone plantaricin A. J Biol Chem 280:22945–22950PubMedGoogle Scholar
  106. de Kroon AI, Dolis D, Mayer A, Lill R, de Kruijff B (1997) Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim Biophys Acta 1325:108–116PubMedGoogle Scholar
  107. Kruis W (2004) Antibiotics and probiotics in inflammatory bowel disease. Aliment Pharmacol Ther 20(Suppl 4):75–78PubMedGoogle Scholar
  108. Kruszewska D, Sahl H-G, Bierbaum G, Pag U, Hynes SO, Ljungh A (2004) Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J Antimicrob Chemother 54:648–653PubMedGoogle Scholar
  109. Kumar B, Balgir PP, Kaur B, Garg N (2011) Cloning and expression of bacteriocins of Pediococcus spp.: a review. Arch Clin Microbiol 2:1–18Google Scholar
  110. de Kwaadsteniet M, Doeschate KT, Dicks LMT (2009) Nisin F in the treatment of respiratory tract infections caused by Staphylococcus aureus. Lett Appl Microbiol 48(1):65–70Google Scholar
  111. Kwan JM, Fialho AM, Kundu M, Thomas J, Hong CS, Das Gupta TK, Chakrabarty AM (2009) Bacterial proteins as potential drugs in the treatment of leukemia. Leuk Res 33:1392–1399PubMedGoogle Scholar
  112. Lagos R, Wilkens M, Vergara C, Cecchi X, Monasterio O (1993) Microcin E492 forms ion channels in phospholipid bilayer membranes. FEBS Lett 321:145–148PubMedGoogle Scholar
  113. Lagos R, Tello M, Mercado G, García V, Monasterio O (2009) Antibacterial and antitumorigenic properties of microcin E492, a pore-forming bacteriocin. Curr Pharm Biotechnol 10:74–85PubMedGoogle Scholar
  114. Lao Y, Wang X, Xu N, Zhang H, Xu H (2014) Application of proteomics to determine the mechanism of action of traditional Chinese medicine remedies. J Ethnopharmacol 155(1):1–8PubMedGoogle Scholar
  115. Laverty G, Gilmore B (2014) Cationic antimicrobial peptide cytotoxicity. SOJ Microbiol Infect Dis 2:1Google Scholar
  116. Lee DG, Hahm K-S, Park Y, Kim H-Y, Lee W, Lim S-C, Seo Y-K, Choi C-H (2005) Functional and structural characteristics of anticancer peptide Pep27 analogues. Cancer Cell Int 5:21PubMedPubMedCentralGoogle Scholar
  117. Leisner JJ, Greer GG, Stiles ME (1996) Control of beef spoilage by a sulfide-producing Lactobacillus sake strain with bacteriocinogenic Leuconostoc gelidum UAL187 during anaerobic storage at 2 degrees C. Appl Environ Microbiol 62:2610–2614PubMedPubMedCentralGoogle Scholar
  118. Letzel A, Pidot SJ, Hertweck C (2014) Genome mining for ribosomally synthesized and post-translationally modified peptides (RiPPs) in anaerobic bacteria. BMC Genomics 15:983PubMedPubMedCentralGoogle Scholar
  119. Lopez FE, Vincent PA, Zenoff AM, Salomón RA, Farías RN (2007) Efficacy of microcin J25 in biomatrices and in a mouse model of Salmonella infection. J Antimicrob Chemother 59:676–680PubMedGoogle Scholar
  120. de Lorenzo V (1984) Isolation and characterization of microcin E492 from Klebsiella pneumoniae. Arch Microbiol 139:72–75PubMedGoogle Scholar
  121. de Lorenzo V, Pugsley AP (1985) Microcin E492, a low-molecular-weight peptide antibiotic which causes depolarization of the Escherichia coli cytoplasmic membrane. Antimicrob Agents Chemother 27:666–669PubMedPubMedCentralGoogle Scholar
  122. Mader JS, Hoskin DW (2006) Cationic antimicrobial peptides as novel cytotoxic agents for cancer treatment. Expert Opin Investig Drugs 15:933–946PubMedGoogle Scholar
  123. Maher S, McClean S (2006) Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro. Biochem Pharmacol 71:1289–1298PubMedGoogle Scholar
  124. Maletzki C, Gock M, Klier U, Klar E, Linnebacher M (2010) Bacteriolytic therapy of experimental pancreatic carcinoma. World J Gastroenterol 16:3546–3552PubMedPubMedCentralGoogle Scholar
  125. Manno S, Takakuwa Y, Mohandas N (2002) Identification of a functional role for lipid asymmetry in biological membranes: phosphatidylserine-skeletal protein interactions modulate membrane stability. Proc Natl Acad Sci U S A 99:1943–1948PubMedPubMedCentralGoogle Scholar
  126. Manosroi A, Khanrin P, Lohcharoenkal W, Werner RG, Gtz F, Manosroi W, Manosroi J (2010) Transdermal absorption enhancement through rat skin of gallidermin loaded in niosomes. Int J Pharm 392:304–310PubMedGoogle Scholar
  127. Mantovani HC, Hu H, Worobo RW, Russell JB (2002) Bovicin HC5, a bacteriocin from Streptococcus bovis HC5. Microbiology 148:3347–3352PubMedGoogle Scholar
  128. Martín R, Escobedo S, Martín C, Crespo A, Quiros LMSJ (2015) Surface glycosaminoglycans protect eukaryotic cells against membrane-driven peptide bacteriocins. Antimicrob Agents Chemother 59:677–681PubMedGoogle Scholar
  129. Mehta RR, Hawthorne M, Peng X, Shilkaitis A, Mehta RG, Beattie CW, Das Gupta TK (2010) A 28-amino-acid peptide fragment of the cupredoxin azurin prevents carcinogen-induced mouse mammary lesions. Cancer Prev Res 3:1351–1360Google Scholar
  130. Mehta RR, Yamada T, Taylor BN, Christov K, King ML, Majumdar D, Lekmine F, Tiruppathi C, Shilkaitis A, Bratescu L, Green A, Beattie CW, Das Gupta TK (2011) A cell penetrating peptide derived from azurin inhibits angiogenesis and tumor growth by inhibiting phosphorylation of VEGFR-2, FAK and Akt. Angiogenesis 14:355–369PubMedGoogle Scholar
  131. Metlitskaya AZ, Katrukha GS, Shashkov AS, Zaitsev DA, Egorov TA, Khmel IA (1995) Structure of microcin C51, a new antibiotic with a broad spectrum of activity. FEBS Lett 357:235–238PubMedGoogle Scholar
  132. Michaud DS, Izard J (2014) Microbiota, oral microbiome, and pancreatic cancer. Cancer J 20:203–206PubMedPubMedCentralGoogle Scholar
  133. Michel-Briand Y, Baysse C (2002) The pyocins of Pseudomonas aeruginosa. Biochimie 84:499–510PubMedGoogle Scholar
  134. Mohimani H, Kersten RD, Liu WT, Wang M, Purvine SO, Wu S, Brewer HM, Pasa-Tolic L, Bandeira N, Moore BS, Pevzner PA, Dorrestein PC (2014) Automated genome mining of ribosomal peptide natural products. ACS Chem Biol 9:1545–1551PubMedPubMedCentralGoogle Scholar
  135. Moll GN, Konings WN, Driessena JM (1999) Bacteriocins: mechanism of membrane insertion and pore formation. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 76:185–198Google Scholar
  136. Mota-Meira M, Morency H, Lavoie MC (2005) In vivo activity of mutacin B-Ny266. J Antimicrob Chemother 56:869–871PubMedGoogle Scholar
  137. Murinda SE, Rashid KARR (2003) In vitro assessment of the cytotoxicity of nisin, pediocin, and selected colicins on simian virus 40-transfected human colon and Vero monkey kidney cells with trypan blue staining viability assays. J Food Prot 66:847–853PubMedGoogle Scholar
  138. Nakazawa I, Iwaizumi M (1989) A role of the cancer cell membrane fluidity in the cancer metastases: an ESR study. Tohoku J Exp Med 157:193PubMedGoogle Scholar
  139. Nes IF, Holo H (2000) Class II antimicrobial peptides from lactic acid bacteria. Biopolymers 55:50–61PubMedGoogle Scholar
  140. Nguyen CNVD (2016) Discovery of azurin-like anticancer bacteriocins from human gut microbiome through homology modeling and molecular docking against the tumor suppressor p53. Biomed Res Int 2016:12Google Scholar
  141. Nuñez M, Rodríguez JL, García E, Gaya P, Medina M (1997) Inhibition of Listeria monocytogenes by enterocin 4 during the manufacture and ripening of Manchego cheese. J Appl Microbiol 83:671–677PubMedGoogle Scholar
  142. O’Shea EF, O’Connor PM, Cotter PD, Ross RP, Hill C (2010) Synthesis of trypsin-resistant variants of the listeria-active bacteriocin salivaricin P. Appl Environ Microbiol 76:5356–5362PubMedPubMedCentralGoogle Scholar
  143. Op den Kamp J (1979) Lipid asymmetry in membranes. Annu Rev Biochem 48:47–71Google Scholar
  144. Oppegård C, Fimland G, Thorbaek L, Nissen-Meyer J (2007) Analysis of the two-peptide bacteriocins lactococcin G and enterocin 1071 by site-directed mutagenesis. Appl Environ Microbiol 73:2931–2938PubMedPubMedCentralGoogle Scholar
  145. Oppegård C, Rogne P, Kristiansen PE, Nissen-Meyer J (2010) Structure analysis of the two-peptide bacteriocin lactococcin G by introducing D-amino acid residues. Microbiology 156:1883–1889PubMedGoogle Scholar
  146. Paiva AD, de Oliveira MD, de Paula SO, Baracat-Pereira MC, Breukink E, Mantovani HC (2012) Toxicity of bovicin HC5 against mammalian cell lines and the role of cholesterol in bacteriocin activity. Microbiol (United Kingdom) 158:2851–2858Google Scholar
  147. Papagianni M (2003) Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnol Adv 21:465–499PubMedGoogle Scholar
  148. Patyar S, Joshi R, Byrav DSP, Prakash MB, Das BK (2010) Bacteria in cancer therapy: a novel experimental strategy. J Biomed Sci 17:21PubMedPubMedCentralGoogle Scholar
  149. Perez RH, Zendo T, Sonomoto K (2014) Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microb Cell Factories 13(Suppl 1):S3Google Scholar
  150. Pieterse R, Todorov SD (2010) Bacteriocins: exploring alternatives to antibiotics in mastitis treatment. Braz J Microbiol 41:542–562PubMedPubMedCentralGoogle Scholar
  151. Piper C, Hill C, Cotter PD, Ross RP (2011) Bioengineering of a Nisin A-producing Lactococcus lactis to create isogenic strains producing the natural variants Nisin F, Q and Z. Microb Biotechnol 4:375–382PubMedPubMedCentralGoogle Scholar
  152. Piper C, Casey PG, Hill C, Cotter PD, Ross RP (2012) The lantibiotic Lacticin 3147 prevents systemic spread of Staphylococcus aureus in a murine infection model. Int J Microbiol 2012:806230.  https://doi.org/10.1155/2012/806230 Google Scholar
  153. Pons AM, Delalande F, Duarte M, Benoit S, Lanneluc I, Sablé S, Van Dorsselaer A, Cottenceau G (2004) Genetic analysis and complete primary structure of microcin L. Antimicrob Agents Chemother 48:505–513PubMedPubMedCentralGoogle Scholar
  154. Porta C, Cosmai L, Gallieni M, Pedrazzoli P, Malberti F (2015) Renal effects of targeted anticancer therapies. Nat Rev Nephrol 11:354–370PubMedGoogle Scholar
  155. Punj V, Bhattacharyya S, Saint-Dic D, Vasu C, E a C, Graves J, Yamada T, Constantinou AI, Christov K, White B, Li G, Majumdar D, Chakrabarty AM, Das Gupta TK (2004) Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer. Oncogene 23:2367–2378PubMedGoogle Scholar
  156. Ramachandran S, Mandal M (2011) Induction of apoptosis of azurin synthesized from P. aeruginosa MTCC 2453 against Dalton’s lymphoma ascites model. Biomed Pharmacother 65:461–466PubMedGoogle Scholar
  157. Reddy KVR, Aranha C, Gupta SM, Yedery RD (2004) Evaluation of antimicrobial peptide nisin as a safe vaginal contraceptive agent in rabbits: in vitro and in vivo studies. Reprod 128:117–126Google Scholar
  158. Rembacken BJ, Snelling AM, Hawkey PM, Chalmers DM, Axon ATR (1999) Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 354:635–639PubMedGoogle Scholar
  159. Ren J, Hamada J, Okada F, Takeichi N, Morikawa K, Hosokawa MKH (1990) Correlation between the presence of microvilli and the growth or metastatic potential of tumor cells. Jpn J Cancer Res 81:920–926PubMedPubMedCentralGoogle Scholar
  160. Riedl SJ, Pasquale EB (2015) Targeting the Eph system with peptides and peptide conjugates. Curr Drug Targets 16:1031–1047PubMedPubMedCentralGoogle Scholar
  161. Riedl S, Zweytick D, Lohner K (2011) Membrane-active host defense peptides—challenges and perspectives for the development of novel anticancer drugs. Chem Phys Lipids 164:766–781PubMedPubMedCentralGoogle Scholar
  162. Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56:117–137PubMedGoogle Scholar
  163. Rothman JE, Lenard J (1977) Membrane asymmetry. Science 195:743–753PubMedGoogle Scholar
  164. Ryan MP, Meaney WJ, Ross RP, Hill C (1998) Evaluation of lacticin 3147 and a teat seal containing this bacteriocin for inhibition of mastitis pathogens. Appl Environ Microbiol 64:2287–2290PubMedPubMedCentralGoogle Scholar
  165. Sahl H (2000) New insights into the mechanism of action of lantibiotics—diverse. J Antimicrob Chemother 46:1–6PubMedGoogle Scholar
  166. Saito H, Watanabe T (1979) Effect of a bacteriocin produced by Mycobacterium smegmatis on growth of cultured tumor and normal cells. Cancer Res 39:5114–5117PubMedGoogle Scholar
  167. Salvucci E, Saavedra L, Hebert EM, Haro C, Sesma F (2012) Enterocin CRL35 inhibits Listeria monocytogenes in a murine model. Foodborne Pathog Dis 9:68–74PubMedGoogle Scholar
  168. Sand SL, Oppegård C, Ohara S, Iijima T, Naderi S, Blomhoff HK, Nissen-Meyer J, Sand O (2010) Plantaricin A, a peptide pheromone produced by Lactobacillus plantarum, permeabilizes the cell membrane of both normal and cancerous lymphocytes and neuronal cells. Peptides 31:1237–1244PubMedGoogle Scholar
  169. Sand SL, Nissen-Meyer J, Sand O, Haug TM (2013) Plantaricin A, a cationic peptide produced by Lactobacillus plantarum, permeabilizes eukaryotic cell membranes by a mechanism dependent on negative surface charge linked to glycosylated membrane proteins. Biochim Biophys Acta Biomembr 1828:249–259Google Scholar
  170. Schenkel LC, Bakovic M (2014) Formation and regulation of mitochondrial membranes. Int J Cell Biol 2014:709828PubMedPubMedCentralGoogle Scholar
  171. Schved F, Lalazar A, Henis Y, Juven BJ (1993) Purification, partial characterization and plasmid linkage of pediocin SJ1, a bacteriocin produced by Pediococcus acidilactici. J Appl Bacteriol 74:67–77PubMedGoogle Scholar
  172. Schwartz B, Bresalier RS, Kim YS (1992) The role of mucin in colon-cancer metastasis. Int J Cancer 52:60–65PubMedGoogle Scholar
  173. Settanni L, Corsetti A (2008) Application of bacteriocins in vegetable food biopreservation. Int J Food Microbiol 121:123–138PubMedGoogle Scholar
  174. Shaikh F, Abhinand P, Ragunath P (2012) Identification & characterization of Lactobacillus salavarius bacteriocins and its relevance in cancer therapeutics. Bioinformation 8:589–594PubMedPubMedCentralGoogle Scholar
  175. Shin JM, Gwak JW, Kamarajan P, Fenno JC, Rickard AH, Kapila YL (2016) Biomedical applications of nisin. J Appl Microbiol 120:1449–14465PubMedPubMedCentralGoogle Scholar
  176. Siegel RL, Miller KD, Jemal A (2015) Cancer statistics, 2015. CA Cancer J Clin 65:5–29PubMedGoogle Scholar
  177. Silkin L, Hamza S, Kaufman S, Cobb SL, Vederas JC (2008) Spermicidal bacteriocins: lacticin 3147 and subtilosin A. Bioorg Med Chem Lett 18:3103–3106PubMedGoogle Scholar
  178. Singh PK, Solanki V, Sharma S, Thakur KG, Krishnan B, Korpole S (2014) The intramolecular disulfide-stapled structure of laterosporulin, a class IId bacteriocin, conceals a human defensin-like structural module. FEBS J 282:203–214PubMedGoogle Scholar
  179. Smarda JKJ (1987) Cytotoxic effects of colicins E1-E5 and K on hamster fibroblasts. Folia Microbiol (Praha) 32:133–136Google Scholar
  180. Smarda J, Smajs D (1998) Colicins—exocellular lethal proteins of Escherichia coli. Folia Microbiol (Praha) 43:563–582Google Scholar
  181. Smarda J, Obdrzalek V, Taborsky I, Mach J (1978) The cytotoxic and cytocidal effect of colicin E3 on mammalian tissue cells. Folia Microbiol (Praha) 23:272–277Google Scholar
  182. Smarda J, Oravec C (1989) Cytocidal effect of bacteriocin on lymphoma cells. Akt Klin Onkol 21:209–212Google Scholar
  183. Smarda J, Fialova M, Šmarda J (2001) Cytotoxic effects of colicins E1 and E3 on v-myb-transformed chicken monoblasts. Folia Biol (Praha) 47:11–13Google Scholar
  184. Smith L, Hillman JD (2008) Therapeutic potential of type A (I) lantibiotics, a group of cationic peptide antibiotics. Curr Opin Microbiol 11:401–408PubMedPubMedCentralGoogle Scholar
  185. Smolarczyk R, Cichoń T, Kamysz W, Głowala-Kosińska M, Szydło A, Szultka L, Sieroń AL, Szala S (2010) Anticancer effects of CAMEL peptide. Lab Investig 90:940–952PubMedGoogle Scholar
  186. Sok M, Sentjurc M, Schara M (1999) Membrane fluidity characteristics of human lung cancer. Cancer Lett 139:215–220PubMedGoogle Scholar
  187. van Staden D, Brand M, Dicks LMT (2012) Nisin F-loaded brushite bone cement prevented the growth of Staphylococcus aureus in vivo. J Appl Microbiol 112:831–840PubMedGoogle Scholar
  188. Steiner I, Errhalt P, Kubesch K, Hubner M, Holy M, Bauer M, Muller M, Hinterberger S, Widmann R, Mascher D, Freissmuth M, Kneussl M (2008) Pulmonary pharmacokinetics and safety of nebulized duramycin in healthy male volunteers. Naunyn Schmiedeberg's Arch Pharmacol 378:323–333Google Scholar
  189. Stern NJ, E a S, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Pokhilenko VD, Levchuk VP, Svetoch OE, Seal BS (2006) Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother 50:3111–3116PubMedPubMedCentralGoogle Scholar
  190. Sun L, Song H, Zheng W (2015) Improvement of antimicrobial activity of pediocin PA-1 by site-directed mutagenesis in C-terminal domain. Protein Pept Lett (11):1007–1012Google Scholar
  191. Sung WS, Park Y, Choi C-H, Hahm K-S, Lee DG (2007) Mode of antibacterial action of a signal peptide, Pep27 from Streptococcus pneumoniae. Biochem Biophys Res Commun 363:806–810PubMedGoogle Scholar
  192. Sutyak KE, Anderson RA, Dover SE, Feathergill KA, Aroutcheva AA, Faro S, Chikindas ML (2008) Spermicidal activity of the safe natural antimicrobial peptide subtilosin. Infect Dis Obstet Gynecol 2008Google Scholar
  193. Turovskiy Y, Ludescher RD, Aroutcheva AA, Faro S, Chikindas ML (2009) Lactocin 160, a bacteriocin produced by vaginal Lactobacillus rhamnosus, targets cytoplasmic membranes of the vaginal pathogen, Gardnerella vaginalis. Probiotics Antimicrob Proteins 1:67–74PubMedPubMedCentralGoogle Scholar
  194. Utsugi T, Schroita J, Connor J, Bucana CD, Fidler IJ (1991) Elevated expression of phosphatidylserine in the outer-membrane leaflet of human tumor-cells and recognition by activated human blood monocytes. Cancer Res 51:3062–3066PubMedGoogle Scholar
  195. Vassiliadis G, Destoumieux-Garzón D, Lombard C, Rebuffat S, Peduzzi J (2010) Isolation and characterization of two members of the siderophore-microcin family, microcins M and H47. Antimicrob Agents Chemother 54:288–297PubMedGoogle Scholar
  196. Vaucher R, Teixeira ML, Brandelli A (2010) Investigation of the cytotoxicity of antimicrobial peptide P40 on eukaryotic cells. Curr Microbiol 60:1–5PubMedGoogle Scholar
  197. Verkleija J, Zwaal RF, Roelofsen B, Comfurius P, Kastelijn D, van Deenen LL (1973) The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim Biophys Acta 323:178–193Google Scholar
  198. Vignolo G, Fadda S, de Kairuz MN, Holgado d R, Oliver G (1996) Control of Listeria monocytogenes in ground beef by “Lactocin 705”, a bacteriocin produced by Lactobacillus casei CRL 705. Int J Food Microbiol 29:397–402PubMedGoogle Scholar
  199. Villarante KI, Elegado FB, Iwatani S, Zendo T, Sonomoto K, de Guzman EE (2011) Purification, characterization and in vitro cytotoxicity of the bacteriocin from Pediococcus acidilactici K2a2-3 against human colon adenocarcinoma (HT29) and human cervical carcinoma (HeLa) cells. World J Microbiol Biotechnol 27:975–980Google Scholar
  200. Walsh CJ, Guinane CM, Hill C, Ross RP, O’Toole PW, Cotter PD (2015) In silico identification of bacteriocin gene clusters in the gastrointestinal tract, based on the Human Microbiome Project’s reference genome database. BMC Microbiol 15:183PubMedPubMedCentralGoogle Scholar
  201. Wang C, Tian L-L, Li S, Li H-B, Zhou Y, Wang H, Yang Q-Z, Ma L-J, Shang D-J (2013) Rapid cytotoxicity of antimicrobial peptide tempoprin-1CEa in breast cancer cells through membrane destruction and intracellular calcium mechanism. PLoS One 8:e60462PubMedPubMedCentralGoogle Scholar
  202. Wang G, Manns DC, Churey JJ, Worobo RW (2014) Development of a homologous expression system for and systematic site-directed mutagenesis analysis of thurincin H, a bacteriocin produced by Bacillus thuringiensis SF361. Appl Environ Microbiol 80:3576–3584PubMedPubMedCentralGoogle Scholar
  203. Wiemann B, Starnes CO (1994) Coley’s toxins, tumor necrosis factor and cancer research: a historical perspective. Pharmacol Ther 64:529–564PubMedGoogle Scholar
  204. Wilson KA, Kalkum M, Ottesen J, Yuzenkova J, Chait BT, Landick R, Muir T, Severinov K, Darst SA (2003) Structure of microcin J25, a peptide inhibitor of bacterial RNA polymerase, is a lassoed tail. J Am Chem Soc 125:12475–12483PubMedGoogle Scholar
  205. Wriessnegger T, Leitner E, Belegratis MR, Ingolic E, Daum G (2009) Lipid analysis of mitochondrial membranes from the yeast Pichia pastoris. Biochim Biophys Acta 1791:166–172PubMedGoogle Scholar
  206. Wu J, Hu S, Cao L (2007) Therapeutic effect of nisin Z on subclinical mastitis in lactating cows. Antimicrob Agents Chemother 51:3131–3135PubMedPubMedCentralGoogle Scholar
  207. Yamada T, Goto M, Punj V, Zaborina O, Kimbara K, Das Gupta TK, Chakrabarty AM (2002) The bacterial redox protein azurin induces apoptosis in J774 macrophages through complex formation and stabilization of the tumor suppressor protein p53. Infect Immun 70:7054–7062PubMedPubMedCentralGoogle Scholar
  208. Yamada T, Fialho AM, Punj V, Bratescu L, Das Gupta TK, Chakrabarty AM (2005) Internalization of bacterial redox protein azurin in mammalian cells: entry domain and specificity. Cell Microbiol 7:1418–1431PubMedGoogle Scholar
  209. Yamada T, Mehta RR, Lekmine F, Christov K, King ML, Majumdar D, Shilkaitis A, Green A, Bratescu L, Beattie CW, Das Gupta TK (2009) A peptide fragment of azurin induces a p53-mediated cell cycle arrest in human breast cancer cells. Mol Cancer Ther 8:2947–2958PubMedGoogle Scholar
  210. Yamada T, Christov K, Shilkaitis a, Bratescu L, Green a, Santini S, Bizzarri a R, Cannistraro S, Gupta TKD, Beattie CW (2013) P28, a first in class peptide inhibitor of Cop1 binding to P53. Br J Cancer 108:2495–2504PubMedPubMedCentralGoogle Scholar
  211. Yang DS, Miao XD, Ye ZM, Feng J, Xu RZ, Huang X, Ge FF (2005) Bacterial redox protein azurin induce apoptosis in human osteosarcoma U2OS cells. Pharmacol Res 52:413–421PubMedGoogle Scholar
  212. Ye JS, Zheng XJ, Leung KW, Chen HM, Sheu FS (2004) Induction of transient ion channel-like pores in a cancer cell by antibiotic peptide. J Biochem 136:255–259PubMedGoogle Scholar
  213. Yoon WH, Park HD, Lim K, Hwang BD (1996) Effect of O-glycosylated mucin on invasion and metastasis of HM7 human colon cancer cells. Biochem Biophys Res Commun 222:694–699PubMedGoogle Scholar
  214. Zaborina O, Dhiman N, Chen ML, Kostal J, Holder IA, Chakrabarty AM (2000) Secreted products of a nonmucoid Pseudomonas aeruginosa strain induce two modes of macrophage killing: external-ATP-dependent, P2Z-receptor-mediated necrosis and ATP-independent, caspase-mediated apoptosis. Microbiol 146:2521–2530Google Scholar
  215. Zeisig R, Koklic T, Wiesner B, Fichtner I, Sentjurc M (2007) Increase in fluidity in the membrane of MT3 breast cancer cells correlates with enhanced cell adhesion in vitro and increased lung metastasis in NOD/SCID mice. Arch Biochem Biophys 459:98–106PubMedGoogle Scholar
  216. Zhao H, Sood R, Jutila A, Bose S, Fimland G, Nissen-Meyer J, Kinnunen PKJ (2006) Interaction of the antimicrobial peptide pheromone plantaricin A with model membranes: implications for a novel mechanism of action. Biochim Biophys Acta Biomembr 1758:1461–1474Google Scholar
  217. Zhao J, Hao X, Liu D, Huang Y, Chen Y (2015) In vitro characterization of the rapid cytotoxicity of anticancer peptide HPRP-A2 through membrane destruction and intracellular mechanism against gastric cancer cell lines. PLoS One 10:e0139578PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Piyush Baindara
    • 1
  • Suresh Korpole
    • 1
  • Vishakha Grover
    • 2
    Email author
  1. 1.MTCC and Gene BankCSIR-Institute of Microbial TechnologyChandigarhIndia
  2. 2.Dr. HS Judge Dental Institute and HospitalPunjab UniversityChandigarhIndia

Personalised recommendations