Augmentation of epithelial resistance to invading bacteria by using mRNA transfections

Infection and Immunity

Volumn 81, Issue 11, 2013, Pages 3975-3983

  Zou, Xianqiong ^a   Sorenson, Brent S ^a   Ross, Karen F ^a,b   Herzberg, Mark C ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; MESSENGER RNA;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOSOME; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INFECTION RESISTANCE; LISTERIA; MOUTH MUCOSA; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA; WESTERN BLOTTING;

ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; LEUKOCYTE L1 ANTIGEN COMPLEX; LISTERIA; RNA, MESSENGER; SALMONELLA; TRANSFECTION;

EID: 84886796723     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00539-13     Document Type: Article

References (48)

1. Bando M, Hiroshima Y, Kataoka M, Shinohara Y, Herzberg MC, Ross KF, Nagata T, Kido J. 2007. Interleukin-1alpha regulates antimicrobial peptide expression in human keratinocytes. Immunol. Cell Biol. 85:532-537.
2. Pasupuleti M, Schmidtchen A, Malmsten M. 2012. Antimicrobial peptides: key components of the innate immune system. Crit. Rev. Biotechnol. 32:143-171.
3. Lee HM, Shin DM, Choi DK, Lee ZW, Kim KH, Yuk JM, Kim CD, Lee JH, Jo EK. 2009. Innate immune responses to Mycobacterium ulcerans via Toll-like receptors and dectin-1 in human keratinocytes. Cell. Microbiol. 11:678-692.
4. Nisapakultorn K, Ross KF, Herzberg MC. 2001. Calprotectin expression in vitro by oral epithelial cells confers resistance to infection by Porphyromonas gingivalis. Infect. Immun. 69:4242-4247.
5. Zaia AA, Sappington KJ, Nisapakultorn K, Chazin WJ, Dietrich EA, Ross KF, Herzberg MC. 2009. Subversion of antimicrobial calprotectin (S100A8/S100A9 complex) in the cytoplasm of TR146 epithelial cells after invasion by Listeria monocytogenes. Mucosal Immunol. 2:43-53.
6. Champaiboon C, Sappington KJ, Guenther BD, Ross KF, Herzberg MC. 2009. Calprotectin S100A9 calcium-binding loops I and II are essential for keratinocyte resistance to bacterial invasion. J. Biol. Chem. 284: 7078-7090.
7. Burton MF, Steel PG. 2009. The chemistry and biology of LL-37. Nat. Prod. Rep. 26:1572-1584.
8. Yamasaki K, Schauber J, Coda A, Lin H, Dorschner RA, Schechter NM, Bonnart C, Descargues P, Hovnanian A, Gallo RL. 2006. Kallikreinmediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J. 20:2068-2080.
9. Nijnik A, Hancock RE. 2009. The roles of cathelicidin LL-37 in immune defences and novel clinical applications. Curr. Opin. Hematol. 16:41-47.
10. Turner J, Cho Y, Dinh NN, Waring AJ, Lehrer RI. 1998. Activities of LL-37, a cathelicidin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother. 42:2206-2214.
11. Larrick JW, Hirata M, Zhong J, Wright SC. 1995. Antimicrobial activity of human CAP18 peptides. Immunotechnology 1:65-72.
12. Dorschner RA, Pestonjamasp VK, Tamakuwala S, Ohtake T, Rudisill J, Nizet V, Agerberth B, Gudmundsson GH, Gallo RL. 2001. Cutaneous injury induces the release of cathelicidin antimicrobial peptides active against group A Streptococcus. J. Invest. Dermatol. 117:91-97.
13. Wang TT, Nestel FP, Bourdeau V, Nagai Y, Wang Q, Liao J, Tavera-Mendoza L, Lin R, Hanrahan JW, Mader S, White JH. 2004. Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J. Immunol. 173:2909-2912.
14. Nell MJ, Tjabringa GS, Vonk MJ, Hiemstra PS, Grote JJ. 2004. Bacterial products increase expression of the human cathelicidin hCAP-18/LL-37in cultured human sinus epithelial cells. FEMS Immunol. Med. Microbiol. 42:225-231.
15. Carlsson G, Wahlin YB, Johansson A, Olsson A, Eriksson T, Claesson R, Hänström L, Henter JI. 2006. Periodontal disease in patients from the original Kostmann family with severe congenital neutropenia. J. Periodontol. 77:744-751.
16. Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T, Gallo RL, Leung DY. 2002. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347:1151-1160.
17. Marenholz I, Heizmann CW, Fritz G. 2004. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 322:1111-1122.
18. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. 2006. Calciumdependent and -independent interactions of the S100 protein family. Biochem. J. 396:201-214.
19. Miyasaki KT, Bodeau AL, Murthy AR, Lehrer RI. 1993. In vitro antimicrobial activity of the human neutrophil cytosolic S-100 protein complex, calprotectin, against Capnocytophaga sputigena. J. Dent. Res. 72:517-523.
20. Sohnle PG, Collins-Lech C, Wiessner JH. 1991. Antimicrobial activity of an abundant calcium-binding protein in the cytoplasm of human neutrophils. J. Infect. Dis. 163:187-192.
21. Steinbakk M, Naess-Andresen CF, Lingaas E, Dale I, Brandtzaeg P, Fagerhol MK. 1990. Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet 336:763-765.
22. Chamilos G, Gregorio J, Meller S, Lande R, Kontoyiannis DP, Modlin RL, Gilliet M. 2012. Cytosolic sensing of extracellular self-DNA transported into monocytes by the antimicrobial peptide LL37. Blood 120: 3699-3707.
23. Tavernier G, Andries O, Demeester J, Sanders NN, De Smedt SC, Rejman J. 2011. mRNA as gene therapeutic: how to control protein expression. J. Control. Release 150:238-247.
24. Zhao Y, Moon E, Carpenito C, Paulos CM, Liu X, Brennan AL, Chew A, Carroll RG, Scholler J, Levine BL, Albelda SM, June CH. 2010. Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res. 70:9053-9061.
25. Rees S, Coote J, Stables J, Goodson S, Harris S, Lee MG. 1996. Bicistronic vector for the creation of stable mammalian cell lines that predisposes all antibiotic-resistant cells to express recombinant protein. Biotechniques 20:102-110.
26. Bochkov YA, Palmenberg AC. 2006. Translational efficiency of EMCV IRES in bicistronic vectors is dependent upon IRES sequence and gene location. Biotechniques 41:283, 284, 286, 288.
27. Pelicano H, Feng L, Zhou Y, Carew JS, Hileman EO, Plunkett W, Keating MJ, Huang P. 2003. Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J. Biol. Chem. 278:37832-37839.
28. Taylor RC, Cullen SP, Martin SJ. 2008. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell. Biol. 9:231-241.
29. Rudney JD, Chen R, Zhang G. 2005. Streptococci dominate the diverse flora within buccal cells. J. Dent. Res. 84:1165-1171.
30. Sorenson BS, Khammanivong A, Guenther BD, Ross KF, Herzberg MC. 2012. IL-1 receptor regulates S100A8/A9-dependent keratinocyte resistance to bacterial invasion. Mucosal Immunol. 5:66-75.
31. Mockey M, Bourseau E, Chandrashekhar V, Chaudhuri A, Lafosse S, Le Cam E, Quesniaux VF, Ryffel B, Pichon C, Midoux P. 2007. mRNAbased cancer vaccine: prevention of B16 melanoma progression and metastasis by systemic injection of MART1 mRNA histidylated lipopolyplexes. Cancer Gene Ther. 14:802-814.
32. Ryser MF, Ugarte F, Thieme S, Bornhäuser M, Roesen-Wolff A, Brenner S. 2008. mRNA transfection of CXCR4-GFP fusion-simply generated by PCR-results in efficient migration of primary human mesenchymal stem cells. Tissue Eng. Part C Methods 14:179-184.
33. Yamamoto A, Kormann M, Rosenecker J, Rudolph C. 2009. Current prospects formRNAgene delivery. Eur. J. Pharm. Biopharm. 71:484-489.
34. Hsu K, Champaiboon C, Guenther BD, Sorenson BS, Khammanivong A, Ross KF, Geczy CL, Herzberg MC. 2009. Anti-infective protective properties of S100 calgranulins. Antiinflamm. Antiallergy Agents Med. Chem. 8:290-305.
35. Karikó K, Muramatsu H, Ludwig J, Weissman D. 2011. Generating the optimal mRNA for therapy: HPLC purification eliminates immune activation and improves translation of nucleoside-modified, proteinencoding mRNA. Nucleic Acids Res. 39:e142.
36. Gonzalez G, Pfannes L, Brazas R, Striker R. 2007. Selection of an optimal RNA transfection reagent and comparison to electroporation for the delivery of viral RNA. J. Virol. Methods 145:14-21.
37. Kisich KO, Heifets L, Higgins M, Diamond G. 2001. Antimycobacterial agent based on mRNA encoding human beta-defensin 2 enables primary macrophages to restrict growth of Mycobacterium tuberculosis. Infect. Immun. 69:2692-2699.
38. Bettinger T, Carlisle RC, Read ML, Ogris M, Seymour LW. 2001. Peptide-mediated RNA delivery: a novel approach for enhanced transfection of primary and post-mitotic cells. Nucleic Acids Res. 29:3882-3891.
39. Benedyk M, Sopalla C, Nacken W, Bode G, Melkonyan H, Banfi B, Kerkhoff C. 2007. HaCaT keratinocytes overexpressing the S100 proteins S100A8 and S100A9 show increased NADPH oxidase and NF-kappaB activities. J. Invest. Dermatol. 127:2001-2011.
40. Lim SY, Raftery MJ, Goyette J, Hsu K, Geczy CL. 2009. Oxidative modifications of S100 proteins: functional regulation by redox. J. Leukoc. Biol. 86:577-587.
41. Simard JC, Simon MM, Tessier PA, Girard D. 2011. Damage-associated molecular pattern S100A9 increases bactericidal activity of human neutrophils by enhancing phagocytosis. J. Immunol. 186:3622-3631.
42. Braff MH, Zaiou M, Fierer J, Nizet V, Gallo RL. 2005. Keratinocyte production of cathelicidin provides direct activity against bacterial skin pathogens. Infect. Immun. 73:6771-6781.
43. Nielsen JS, Wick DA, Tran E, Nelson BH, Webb JR. 2010. An in vitro-transcribed-mRNA polyepitope construct encoding 32 distinctHLA class I-restricted epitopes from CMV, EBV, and influenza for use as a functional control in human immune monitoring studies. J. Immunol. Methods 360:149-156.
44. Lesterhuis WJ, De Vries IJ, Schreibelt G, Schuurhuis DH, Aarntzen EH, De Boer A, Scharenborg NM, Van De Rakt M, Hesselink EJ, Figdor CG, Adema GJ, Punt CJ. 2010. Immunogenicity of dendritic cells pulsed with CEA peptide or transfected with CEA mRNA for vaccination of colorectal cancer patients. Anticancer Res. 30:5091-5097.
45. Suso EM, Dueland S, Rasmussen AM, Vetrhus T, Aamdal S, Kvalheim G, Gaudernack G. 2011. hTERT mRNA dendritic cell vaccination: complete response in a pancreatic cancer patient associated with response against several hTERT epitopes. Cancer Immunol. Immunother. 60:809-818.
46. Lehner M, Götz G, Proff J, Schaft N, Dörrie J, Full F, Ensser A, Muller YA, Cerwenka A, Abken H, Parolini O, Ambros PF, Kovar H, Holter W. 2012. Redirecting T cells to Ewing's sarcoma family of tumors by a chimeric NKG2D receptor expressed by lentiviral transduction or mRNA transfection. PLoS One 7:e31210. doi:10.1371/journal.pone.0031210.
47. Karikó K, Muramatsu H, Keller JM, Weissman D. 2012. Increased erythropoiesis in mice injected with submicrogram quantities of pseudouridine-containing mRNA encoding erythropoietin. Mol. Ther. 20:948-953.
48. Hansen A, Schäfer I, Knappe D, Seibel P, Hoffmann R. 2012. Intracellular toxicity of proline-rich antimicrobial peptides shuttled into mammalian cells by the cell-penetrating peptide penetratin. Antimicrob. Agents Chemother. 56:5194-5201.