Ciprofloxacin affects host cells by suppressing expression of the endogenous antimicrobial peptides cathelicidins and beta-defensin-3 in colon Epithelia

Antibiotics

Volumn 3, Issue 3, 2014, Pages 353-374

  Sarker, Protim ^a   Mily, Akhirunnesa ^a   Al Mamun, Abdullah ^a   Jalal, Shah ^b   Bergman, Peter ^b   Raqib, Rubhana ^a   Gudmundsson, Gudmundur H ^c   Agerberth, Birgitta ^b  

^a INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF ICELAND   (Iceland)

Author keywords

Antibiobic; Antibiotic associated diarrhea; Butyrate; Clostridium difficile; Histone modifications; Host defense peptides; Impaired immune responses; Innate immunity; LL 37; Microbiota

Indexed keywords

AMPICILLIN; AZITHROMYCIN; BETA DEFENSIN 3; CATHELICIDIN; CEFTRIAXONE; CIPROFLOXACIN; CLINDAMYCIN; HISTONE; ISONIAZID; LEVOFLOXACIN; OFLOXACIN; PIVMECILLINAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC ASSOCIATED DIARRHEA; ANTIMICROBIAL ACTIVITY; ARTICLE; CLOSTRIDIUM DIFFICILE; COLON MUCOSA; CONTROLLED STUDY; CYTOLYSIS; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INNATE IMMUNITY; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 84969368741     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics3030353     Document Type: Article

References (51)

1. Gottler, L.M.; Ramamoorthy, A. Structure, membrane orientation, mechanism, and function of pexiganan-A highly potent antimicrobial peptide designed from magainin. Biochim. Biophys. Acta 2009, 1788, 1680-1686.
2. Hilchie, A.L.; Wuerth, K.; Hancock, R.E. Immune modulation by multifaceted cationic host defense (antimicrobial) peptides. Nat. Chem. Biol. 2013, 9, 761-768.
3. Hoskin, D.W.; Ramamoorthy, A. Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta 2008, 1778, 357-375
4. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415, 389-395.
5. Durr, U.H.; Sudheendra, U.S.; Ramamoorthy, A. LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta 2006, 1758, 1408-1425.
6. Dhople, V.; Krukemeyer, A.; Ramamoorthy, A. The human beta-defensin-3, an antibacterial peptide with multiple biological functions. Biochim. Biophys. Acta 2006, 1758, 1499-1512.
7. Selsted, M.E.; Ouellette, A.J. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 2005, 6, 551-557.
8. Jarczak, J.; Kosciuczuk, E.M.; Lisowski, P.; Strzalkowska, N.; Jozwik, A.; Horbanczuk, J.; Krzyzewski, J.; Zwierzchowski, L.; Bagnicka, E. Defensins: Natural component of human innate immunity. Human Immunol. 2013, 74, 1069-1079.
9. Baroni, A.; Donnarumma, G.; Paoletti, I.; Longanesi-Cattani, I.; Bifulco, K.; Tufano, M.A.; Carriero, M.V. Antimicrobial human beta-defensin-2 stimulates migration, proliferation and tube formation of human umbilical vein endothelial cells. Peptides 2009, 30, 267-272.
10. Kai-Larsen, Y.; Agerberth, B. The role of the multifunctional peptide LL-37 in host defense. Front. Biosci. 2008, 13, 3760-3767.
11. Koczulla, R.; von Degenfeld, G.; Kupatt, C.; Krotz, F.; Zahler, S.; Gloe, T.; Issbrucker, K.; Unterberger, P.; Zaiou, M.; Lebherz, C.; et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J. Clin. Invest. 2003, 111, 1665-1672.
12. Salzman, N.H.; Hung, K.; Haribhai, D.; Chu, H.; Karlsson-Sjoberg, J.; Amir, E.; Teggatz, P.; Barman, M.; Hayward, M.; Eastwood, D.; et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 2010, 11, 76-83.
13. Shaykhiev, R.; Beisswenger, C.; Kandler, K.; Senske, J.; Puchner, A.; Damm, T.; Behr, J.; Bals, R. Human endogenous antibiotic LL-37 stimulates airway epithelial cell proliferation and wound closure. Am. J. Physiol. Lung. Cell. Mol. Physiol. 2005, 289, L842-L848.
14. Vandamme, D.; Landuyt, B.; Luyten, W.; Schoofs, L. A comprehensive summary of LL-37, the factotum human cathelicidin peptide. Cell. Immunol. 2012, 280, 22-35.
15. Schauber, J.; Dorschner, R.A.; Yamasaki, K.; Brouha, B.; Gallo, R.L. Control of the innate epithelial antimicrobial response is cell-type specific and dependent on relevant microenvironmental stimuli. Immunology 2006, 118, 509-519.
16. Raqib, R.; Sarker, P.; Bergman, P.; Ara, G.; Lindh, M.; Sack, D.A.; Nasirul Islam, K.M.; Gudmundsson, G.H.; Andersson, J.; Agerberth, B. Improved outcome in shigellosis associated with butyrate induction of an endogenous peptide antibiotic. Proc. Natl. Acad. Sci. USA 2006, 103, 9178-9183.
17. Schauber, J.; Svanholm, C.; Termen, S.; Iffland, K.; Menzel, T.; Scheppach, W.; Melcher, R.; Agerberth, B.; Luhrs, H.; Gudmundsson, G.H. Expression of the cathelicidin LL-37 is modulated by short chain fatty acids in colonocytes: Relevance of signalling pathways. Gut 2003, 52, 735-741.
18. Mandell, L.A.; Afnan, M. Mechanisms of interaction among subinhibitory concentrations of antibiotics, human polymorphonuclear neutrophils, and gram-negative bacilli. Antimicrob. Agents Chemother. 1991, 35, 1291-1297.
19. Nau, R.; Eiffert, H. Modulation of release of proinflammatory bacterial compounds by antibacterials: Potential impact on course of inflammation and outcome in sepsis and meningitis. Clin. Microbiol. Rev. 2002, 15, 95-110.
20. Tauber, S.C.; Nau, R. Immunomodulatory properties of antibiotics. Curr. Mol. Pharmacol. 2008, 1, 68-79.
21. Bartlett, J.G. Clinical practice. Antibiotic-associated diarrhea. N. Engl. J. Med. 2002, 346, 334-339.
22. Ubeda, C.; Pamer, E.G. Antibiotics, microbiota, and immune defense. Trends Immunol. 2012, 33, 459-466.
23. Blondeau, J.M. What have we learned about antimicrobial use and the risks for Clostridium difficile-associated diarrhoea? J. Antimicrob. Chemother. 2009, 63, 238-242.
24. Expression data from HT-29, a human colonic epithelial cell line. Available online: http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE45220 (accessed on 16 March 2013).
25. Kida, Y.; Shimizu, T.; Kuwano, K. Sodium butyrate up-regulates cathelicidin gene expression via activator protein-1 and histone acetylation at the promoter region in a human lung epithelial cell line, EBC-1. Mol. Immunol. 2006, 43, 1972-1981.
26. Schauber, J.; Iffland, K.; Frisch, S.; Kudlich, T.; Schmausser, B.; Eck, M.; Menzel, T.; Gostner, A.; Luhrs, H.; Scheppach, W. Histone-deacetylase inhibitors induce the cathelicidin LL-37 in gastrointestinal cells. Mol. Immunol. 2004, 41, 847-854.
27. Steinmann, J.; Halldorsson, S.; Agerberth, B.; Gudmundsson, G.H. Phenylbutyrate induces antimicrobial peptide expression. Antimicrob. Agents Chemother. 2009, 53, 5127-5133.
28. Bode, A.M.; Dong, Z. Inducible covalent posttranslational modification of histone H3. Sci. STKE 2005, 2005, re4.
29. Dalhoff, A. Immunomodulatory activities of fluoroquinolones. Infection 2005, 33, 55-70.
30. Cacchillo, D.A.; Walters, J.D. Effect of ciprofloxacin on killing of Actinobacillus actinomycetemcomitans by polymorphonuclear leukocytes. Antimicrob. Agents Chemother. 2002, 46, 1980-1984.
31. Wong, J.P.; Schnell, G.; Simpson, M.; Saravolac, E. Effects of liposome-encapsulated ciprofloxacin on phagocytosis, nitric oxide and intracellular killing of Staphylcoccus aureus by murine macrophages. Artif. Cells Blood Substit. Immobil. Biotechnol. 2000, 28, 415-428.
32. Kaji, M.; Tanaka, J.; Sugita, J.; Kato, N.; Ibata, M.; Shono, Y.; Ohta, S.; Kondo, T.; Asaka, M.; Imamura, M. Ciprofloxacin inhibits lipopolysaccharide-induced toll-like receptor-4 and 8 expression on human monocytes derived from adult and cord blood. Ann. Hematol. 2008, 87, 229-231.
33. Katsuno, G.; Takahashi, H.K.; Iwagaki, H.; Sugita, S.; Mori, S.; Saito, S.; Yoshino, T.; Nishibori, M.; Tanaka, N. The effect of ciprofloxacin on CD14 and toll-like receptor-4 expression on human monocytes. Shock 2006, 25, 247-253.
34. Kolios, G.; Manousou, P.; Bourikas, L.; Notas, G.; Tsagarakis, N.; Mouzas, I.; Kouroumalis, E. Ciprofloxacin inhibits cytokine-induced nitric oxide production in human colonic epithelium. Eur. J. Clin. Invest. 2006, 36, 720-729.
35. Dalhoff, A.; Shalit, I. Immunomodulatory effects of quinolones. Lancet Infect. Dis. 2003, 3, 359-371.
36. Islam, D.; Bandholtz, L.; Nilsson, J.; Wigzell, H.; Christensson, B.; Agerberth, B.; Gudmundsson, G. Downregulation of bactericidal peptides in enteric infections: A novel immune escape mechanism with bacterial DNA as a potential regulator. Nat. Med. 2001, 7, 180-185.
37. Shalit, I.; Kletter, Y.; Weiss, K.; Gruss, T.; Fabian, I. Enhanced hematopoiesis in sublethally irradiated mice treated with various quinolones. Eur. J. Haematol. 1997, 58, 92-98.
38. Yamashita, Y.; Ashizawa, T.; Morimoto, M.; Hosomi, J.; Nakano, H. Antitumor quinolones with mammalian topoisomerase II mediated DNA cleavage activity. Cancer Res. 1992, 52, 2818-2822.
39. Hsu, K.; Champaiboon, C.; Guenther, B.D.; Sorenson, B.S.; Khammanivong, A.; Ross, K.F.; Geczy, C.L.; Herzberg, M.C. Anti-Infective Protective Properties of S100 Calgranulins. Antiinflamm. Antiallergy Agents Med. Chem. 2009, 8, 290-305.
40. Dyer, K.D.; Rosenberg, H.F. The RNase a superfamily: Generation of diversity and innate host defense. Mol. Divers. 2006, 10, 585-597.
41. Yamasaki, K.; Schauber, J.; Coda, A.; Lin, H.; Dorschner, R.A.; Schechter, N.M.; Bonnart, C.; Descargues, P.; Hovnanian, A.; Gallo, R.L. Kallikrein-mediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J. 2006, 20, 2068-2080.
42. Kanada, K.N.; Nakatsuji, T.; Gallo, R.L. Doxycycline Indirectly Inhibits Proteolytic Activation of Tryptic Kallikrein-Related Peptidases and Activation of Cathelicidin. J. Invest. Dermatol. 2012, 132, 1435-1442.
43. Le Poul, E.; Loison, C.; Struyf, S.; Springael, J.Y.; Lannoy, V.; Decobecq, M.E.; Brezillon, S.; Dupriez, V.; Vassart, G.; van Damme, J.; et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J. Biol. Chem. 2003, 278, 25481-25489.
44. Maslowski, K.M.; Vieira, A.T.; Ng, A.; Kranich, J.; Sierro, F.; Yu, D.; Schilter, H.C.; Rolph, M.S.; Mackay, F.; Artis, D.; et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461, 1282-1286.
45. Vaishnavi, C. Established and potential risk factors for Clostridum difficile infection. Indian J. Med. Microbiol. 2009, 27, 289-300.
46. Hing, T.C.; Ho, S.; Shih, D.Q.; Ichikawa, R.; Cheng, M.; Chen, J.; Chen, X.; Law, I.; Najarian, R.; Kelly, C.P.; et al. The antimicrobial peptide cathelicidin modulates Clostridium difficile-associated colitis and toxin A-mediated enteritis in mice. Gut 2012, 62, 1295-1305.
47. Giesemann, T.; Guttenberg, G.; Aktories, K. Human alpha-defensins inhibit Clostridium difficile toxin B. Gastroenterology 2008, 134, 2049-2058.
48. Brandl, K.; Plitas, G.; Mihu, C.N.; Ubeda, C.; Jia, T.; Fleisher, M.; Schnabl, B.; DeMatteo, R.P.; Pamer, E.G. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 2008, 455, 804-807.
49. Yoshio, H.; Tollin, M.; Gudmundsson, G.H.; Lagercrantz, H.; Jornvall, H.; Marchini, G.; Agerberth, B. Antimicrobial polypeptides of human vernix caseosa and amniotic fluid: Implications for newborn innate defense. Pediatr. Res. 2003, 53, 211-216.
50. Lee, A.Y.; Paweletz, C.P.; Pollock, R.M.; Settlage, R.E.; Cruz, J.C.; Secrist, J.P.; Miller, T.A.; Stanton, M.G.; Kral, A.M.; Ozerova, N.D.; et al. Quantitative analysis of histone deacetylase-1 selective histone modifications by differential mass spectrometry. J. Proteome. Res. 2008, 7, 5177-5186.
51. Cunnane, G.; Bjork, L.; Ulfgren, A.K.; Lindblad, S.; FitzGerald, O.; Bresnihan, B.; Andersson, U. Quantitative analysis of synovial membrane inflammation: A comparison between automated and conventional microscopic measurements. Ann. Rheum. Dis. 1999, 58, 493-499.