Manipulation of innate immunity by a bacterial secreted peptide: Lantibiotic nisin Z is selectively immunomodulatory

Innate Immunity

Volumn 19, Issue 3, 2013, Pages 315-327

  Kindrachuk, Jason ^a   Jenssen, Håvard ^a   Elliott, Melissa ^a   Nijnik, Anastasia ^a   Magrangeas Janot, Laure ^a   Pasupuleti, Mukesh ^a   Thorson, Lisa ^b   Ma, Shuhua ^a   Easton, Donna M ^a   Bains, Manjeet ^a   Finlay, Brett ^b   Breukink, Eefjan J ^c,d   Georg Sahl, Hans ^d   Hancock, Robert Ew ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

Antimicrobial peptide; immunomodulatory; innate immunity; lantibiotic; nisin

Indexed keywords

CHEMOKINE; GRO ALPHA PROTEIN; GROWTH FACTOR RECEPTOR; IMMUNOMODULATING AGENT; INTERLEUKIN 8; LANTIBIOTIC; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; NISIN Z; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; NISIN;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; CYTOTOXICITY; ESCHERICHIA COLI; FEMALE; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOMODULATION; INNATE IMMUNITY; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; ANALOGS AND DERIVATIVES; ANIMAL; BACTERIAL LOAD; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; RADIATION RESPONSE; SALMONELLA ENTERICA;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL LOAD; CELL LINE; CHEMOKINES; ESCHERICHIA COLI; FEMALE; HUMANS; IMMUNITY, INNATE; IMMUNOMODULATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NISIN; SALMONELLA ENTERICA; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84877744600     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425912461456     Document Type: Article

References (59)

1. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009 ; 9: 313-323
2. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005 ; 122: 107-118
3. Wu MH, Pan TM, Wu YJ, et al. Exopolysaccharide activities from probiotic bifidobacterium: Immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int J Food Microbiol. 2010 ; 144: 104-110
4. Maslowski KM, Vieira AT, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009 ; 461: 1282-1286
5. Cosseau C, Devine DA, Dullaghan E, et al. The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun. 2008 ; 76: 4163-4175
6. Villatoro-Hernandez J, Montes-de-Oca-Luna R, Kuipers OP. Targeting diseases with genetically engineered Lactococcus lactis and its course towards medical translation. Expert Opin Biol Ther. 2011 ; 11: 261-267
7. Audouy SA, van Selm S, van Roosmalen ML, et al. Development of lactococcal GEM-based pneumococcal vaccines. Vaccine. 2007 ; 25: 2497-2506
8. Smith L, Hillman J. Therapeutic potential of type A (I) lantibiotics, a group of cationic peptide antibiotics. Curr Opin Microbiol. 2008 ; 11: 401-408
9. Breukink E, de Kruijff B. The lantibiotic nisin, a special case or not?. Biochim Biophys Acta. 1999 ; 1462: 223-234
10. O'Sullivan L, Ross RP, Hill C. Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie. 2002 ; 84: 593-604
11. Cotter PD, Hill C, Ross RP. Bacteriocins: developing innate immunity for food. Nat Rev Microbiol. 2005 ; 3: 777-788
12. Ryan MP, Flynn J, Hill C, Ross RP, Meaney WJ. The natural food grade inhibitor, lacticin 3147, reduced the incidence of mastitis after experimental challenge with Streptococcus dysgalactiae in nonlactating dairy cows. J Dairy Sci. 1999 ; 82: 2625-2631
13. Hsu ST, Breukink E, Tischenko E, et al. The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat Struct Mol Biol. 2004 ; 11: 963-967
14. Breukink E, Wiedemann I, van Kraaij C, et al. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science. 1999 ; 286: 2361-2364
15. Wiedemann I, Breukink E, van Kraaij C, et al. 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. 2001 ; 276: 1772-1779
16. de Pablo MA, Gaforio JJ, Gallego AM, et al. Evaluation of immunomodulatory effects of nisin-containing diets on mice. FEMS Immunol Med Microbiol. 1999 ; 24: 35-42
17. Begde D, Bundale S, Mashitha P, et al. Immunomodulatory efficacy of nisin-a bacterial lantibiotic peptide. J Pept Sci. 2011 ; 17: 438-444
18. Hancock RE, Sahl HG. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol. 2006 ; 24: 1551-1557
19. Easton DM, Nijnik A, Mayer ML, Hancock RE. Potential of immunomodulatory host defense peptides as novel anti-infectives. Trends Biotechnol. 2009 ; 27: 582-590
20. Bowdish DM, Davidson DJ, Hancock RE. A re-evaluation of the role of host defence peptides in mammalian immunity. Curr Protein Pept Sci. 2005 ; 6: 35-51
21. Bowdish DM, Davidson DJ, Scott MG, Hancock RE. Immunomodulatory activities of small host defense peptides. Antimicrob Agents Chemother. 2005 ; 49: 1727-1732
22. Scott MG, Vreugdenhil AC, Buurman WA, et al. Cutting edge: cationic antimicrobial peptides block the binding of lipopolysaccharide (LPS) to LPS binding protein. J Immunol. 2000 ; 164: 549-553
23. Heilborn JD, Nilsson MF, Kratz G, et al. The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J Invest Dermatol. 2003 ; 120: 379-389
24. Niyonsaba F, Iwabuchi K, Someya A, et al. A cathelicidin family of human antibacterial peptide LL-37 induces mast cell chemotaxis. Immunology. 2002 ; 106: 20-26
25. Scott MG, Davidson DJ, Gold MR, et al. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J Immunol. 2002 ; 169: 3883-3891
26. Tjabringa GS, Aarbiou J, Ninaber DK, et al. The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J Immunol. 2003 ; 171: 6690-6696
27. Braff MH, Hawkins MA, Di Nardo A, et al. Structure-function relationships among human cathelicidin peptides: dissociation of antimicrobial properties from host immunostimulatory activities. J Immunol. 2005 ; 174: 4271-4278
28. Mookherjee N, Brown KL, Bowdish DM, et al. Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J Immunol. 2006 ; 176: 2455-2464
29. Semple F, Webb S, Li HN, et al. Human beta-defensin 3 has immunosuppressive activity in vitro and in vivo. Eur J Immunol. 40: 1073-1078
30. Presicce P, Giannelli S, Taddeo A, et al. Human defensins activate monocyte-derived dendritic cells, promote the production of proinflammatory cytokines, and up-regulate the surface expression of CD91. J Leukoc Biol. 2009 ; 86: 941-948
31. Grigat J, Soruri A, Forssmann U, et al. Chemoattraction of macrophages, T lymphocytes, and mast cells is evolutionarily conserved within the human alpha-defensin family. J Immunol. 2007 ; 179: 3958-3965
32. Scott MG, Dullaghan E, Mookherjee N, et al. An anti-infective peptide that selectively modulates the innate immune response. Nat Biotechnol. 2007 ; 25: 465-472
33. Nijnik A, Madera L, Ma S, et al. Synthetic cationic peptide IDR-1002 provides protection against bacterial infections through chemokine induction and enhanced leukocyte recruitment. J Immunol. 184: 2539-2550
34. Bierbaum G, Reis M, Szekat C, Sahl HG. Construction of an expression system for engineering of the lantibiotic Pep5. Appl Environ Microbiol. 1994 ; 60: 4332-4338
35. Bonelli RR, Schneider T, Sahl HG, Wiedemann I. Insights into in vivo activities of lantibiotics from gallidermin and epidermin mode-of-action studies. Antimicrob Agents Chemother. 2006 ; 50: 1449-1457
36. Abramoff MD, Magalhaes PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004 ; 11: 36-42
37. Bierbaum G, Gotz F, Peschel A, et al. The biosynthesis of the lantibiotics epidermin, gallidermin, Pep5 and epilancin K7. Antonie Van Leeuwenhoek. 1996 ; 69: 119-127
38. Wieczorek M, Jenssen H, Kindrachuk J, et al. Structural studies of a peptide with immune modulating and direct antimicrobial activity. Chem Biol. 2010 ; 17: 970-980
39. Kindrachuk J, Jenssen H, Elliott M, et al. A novel vaccine adjuvant comprised of a synthetic innate defence regulator peptide and CpG oligonucleotide links innate and adaptive immunity. Vaccine. 2009 ; 27: 4662-4671
40. Lau YE, Bowdish DM, Cosseau C, et al. Apoptosis of airway epithelial cells: human serum sensitive induction by the cathelicidin LL-37. Am J Respir Cell Mol Biol. 2006 ; 34: 399-409
41. Bowdish DM, Davidson DJ, Speert DP, Hancock RE. The human cationic peptide LL-37 induces activation of the extracellular signal-regulated kinase and p38 kinase pathways in primary human monocytes. J Immunol. 2004 ; 172: 3758-3765
42. Reddy KV, Aranha C, Gupta SM, Yedery RD. Evaluation of antimicrobial peptide nisin as a safe vaginal contraceptive agent in rabbits: in vitro and in vivo studies. Reproduction. 2004 ; 128: 117-126
43. Aranha CC, Gupta SM, Reddy KV. Assessment of cervicovaginal cytokine levels following exposure to microbicide Nisin gel in rabbits. Cytokine. 2008 ; 43: 63-70
44. Lynn DJ, Winsor GL, Chan C, et al. InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol Syst Biol. 2008 ; 4: 218-218
45. Girnita A, Zheng H, Gronberg A, et al. Identification of the cathelicidin peptide LL-37 as agonist for the type I insulin-like growth factor receptor. Oncogene. 2012 ; 31: 352-365
46. Koczulla R, von Degenfeld G, Kupatt C, et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Invest. 2003 ; 111: 1665-1672
47. Niyonsaba F, Ushio H, Hara M, et al. Antimicrobial peptides human beta-defensins and cathelicidin LL-37 induce the secretion of a pruritogenic cytokine IL-31 by human mast cells. J Immunol. 2010 ; 184: 3526-3534
48. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000 ; 351: 95-105
49. Tokumaru S, Sayama K, Shirakata Y, et al. Induction of keratinocyte migration via transactivation of the epidermal growth factor receptor by the antimicrobial peptide LL-37. J Immunol. 2005 ; 175: 4662-4668
50. Hosono A, Lee J, Ametani A, et al. Characterization of a water-soluble polysaccharide fraction with immunopotentiating activity from Bifidobacterium adolescentis M101-4. Biosci Biotechnol Biochem. 1997 ; 61: 312-316
51. Kitazawa H, Harata T, Uemura J, et al. Phosphate group requirement for mitogenic activation of lymphocytes by an extracellular phosphopolysaccharide from Lactobacillus delbrueckii ssp. bulgaricus. Int J Food Microbiol. 1998 ; 40: 169-175
52. Lee YJ, Choi HJ, Kang TW, et al. CBT-SL5, a bacteriocin from Enterococcus faecalis, suppresses the expression of interleukin-8 induced by Propionibacterium acnes in cultured human keratinocytes. J Microbiol Biotechnol. 2008 ; 18: 1308-1316
53. Nicholls EF, Madera L, Hancock RE. Immunomodulators as adjuvants for vaccines and antimicrobial therapy. Ann N Y Acad Sci. 2010 ; 1213: 46-61
54. Puertollano MA, Gaforio JJ, Galvez A, et al. Analysis of pro-inflammatory cytokine production in mouse spleen cells in response to the lantibiotic nisin. Int J Antimicrob Agents. 2003 ; 21: 601-603
55. Van Den Hooven HW, Doeland CC, Van De Kamp M, et al. Three-dimensional structure of the lantibiotic nisin in the presence of membrane-mimetic micelles of dodecylphosphocholine and of sodium dodecylsulphate. Eur J Biochem. 1996 ; 235: 382-393
56. Mookherjee N, Hamill P, Gardy J, et al. Systems biology evaluation of immune responses induced by human host defence peptide LL-37 in mononuclear cells. Mol Biosyst. 2009 ; 5: 483-496
57. Navarro-Nunez L, Lozano ML, Martinez C, et al. Effect of quercetin on platelet spreading on collagen and fibrinogen and on multiple platelet kinases. Fitoterapia. 2010 ; 81: 75-80
58. Hancock RE, Scott MG. The role of antimicrobial peptides in animal defenses. Proc Nat Acad Sci U S A. 2000 ; 97: 8856-8861
59. Madera L, Hancock REW. Synthetic immunomodulatory peptide IDR-1002 enhances monocyte migration and adhesion on fibronectin. J Innate Immun. 2012 ; 4: 553-568