Directed evolution and targeted mutagenesis to murinize listeria monocytogenes internalin A for enhanced infectivity in the murine oral infection model

BMC Microbiology

Volumn 10, Issue , 2010, Pages

  Monk, Ian R ^a,c   Casey, Pat G ^a   Hill, Colin ^a   Gahan, Cormac Gm ^b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; INTERNALIN A; OLIGONUCLEOTIDE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; CLONE; CODON; EVOLUTION; FEMALE; GENE LIBRARY; GENE MUTATION; INFECTION; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOUSE; MOUTH INFECTION; MUTAGENESIS; NONHUMAN; PLASMID; RANDOMIZED CONTROLLED TRIAL; VIRULENCE; AMINO ACID SUBSTITUTION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; DIRECTED MOLECULAR EVOLUTION; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MOUTH DISEASE; PATHOGENICITY; SITE DIRECTED MUTAGENESIS;

LACTOCOCCUS LACTIS; LISTERIA; LISTERIA MONOCYTOGENES; LISTERIA MONOCYTOGENES EGD-E; MURINAE; MUS;

AMINO ACID SUBSTITUTION; ANIMALS; BACTERIAL PROTEINS; CELL LINE; DIRECTED MOLECULAR EVOLUTION; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, INBRED BALB C; MOUTH DISEASES; MUTAGENESIS, SITE-DIRECTED; VIRULENCE FACTORS;

EID: 78649929088     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-10-318     Document Type: Article

References (41)

1. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. JL Gaillard P Berche C Frehel E Gouin P Cossart, Cell 1991 65 1127 1141 10.1016/0092-8674(91) 90009-N 1905979
2. Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. H Bierne C Sabet N Personnic P Cossart, Microbes Infect 2007 9 1156 1166 10.1016/j.micinf.2007.05.003 17764999
3. Antibodies to the leucine-rich repeat region of internalin block entry of Listeria monocytogenes into cells expressing E-cadherin. J Mengaud M Lecuit M Lebrun F Nato JC Mazie P Cossart, Infect Immun 1996 64 5430 5433 8945603
4. Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. M Lecuit H Ohayon L Braun J Mengaud P Cossart, Infect Immun 1997 65 5309 5319 9393831
5. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. J Mengaud H Ohayon P Gounon R-M Mege P Cossart, Cell 1996 84 923 932 10.1016/S0092-8674(00)81070-3 8601315 (Pubitemid 26106861)
6. E-cadherin germline mutations in familial gastric cancer. P Guilford J Hopkins J Harraway M McLeod N McLeod P Harawira H Taite R Scoular A Miller AE Reeve, Nature 1998 392 402 405 10.1038/32918 9537325
7. Comprehensive study of the intestinal stage of listeriosis in a rat ligated ileal loop system. B Pron C Boumaila F Jaubert S Sarnacki JP Monnet P Berche JL Gaillard, Infect Immun 1998 66 747 755 9453636
8. Penetration of Listeria monocytogenes in mice infected by the oral route. AJ Marco J Altimira N Prats S Lopez L Dominguez M Domingo V Briones, Microb Pathog 1997 23 255 263 10.1006/mpat.1997.0144 9405203
9. Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental listeria infection. P Racz K Tenner E Mero, Lab Invest 1972 26 694 700 4624183
10. Effect of cell polarization and differentiation on entry of Listeria monocytogenes into the enterocyte-like Caco-2 cell line. JL Gaillard BB Finlay, Infect Immun 1996 64 1299 1308 8606093
11. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. M Lecuit S Dramsi C Gottardi M Fedor-Chaiken B Gumbiner P Cossart, EMBO J 1999 18 3956 3963 10.1093/emboj/18.14.3956 10406800
12. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. M Lecuit S Vandormael-Pournin J Lefort M Huerre P Gounon C Dupuy C Babinet P Cossart, Science 2001 292 1722 1725 10.1126/science.1059852 11387478
13. Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. M Pentecost G Otto JA Theriot MR Amieva, PLoS Pathog 2006 2 3 10.1371/journal.ppat.0020003 16446782
14. Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. O Disson S Grayo E Huillet G Nikitas F Langa-Vives O Dussurget M Ragon A Le Monnier C Babinet P Cossart M Lecuit, Nature 2008 455 1114 1118 10.1038/nature07303 18806773
15. Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. WD Schubert C Urbanke T Ziehm V Beier MP Machner E Domann J Wehland T Chakraborty DW Heinz, Cell 2002 111 825 836 10.1016/S0092-8674(02)01136-4 12526809
16. Species specificity of the Listeria monocytogenes InlB protein. N Khelef M Lecuit H Bierne P Cossart, Cell Microbiol 2006 8 457 470 10.1111/j.1462-5822. 2005.00634.x 16469057
17. Extending the host range of Listeria monocytogenes by rational protein design. T Wollert B Pasche M Rochon S Deppenmeier J van den Heuvel AD Gruber DW Heinz A Lengeling WD Schubert, Cell 2007 129 891 902 10.1016/j.cell.2007.03.049 17540170
18. Development of multiple strain competitive index assays for Listeria monocytogenes using pIMC; a new site-specific integrative vector. IR Monk PG Casey M Cronin CG Gahan C Hill, BMC Microbiol 2008 8 96 10.1186/1471-2180-8-96 18554399
19. High-Frequency Transformation, by Electroporation, of Lactococcus lactis subsp. cremoris Grown with Glycine in Osmotically Stabilized Media. H Holo IF Nes, Appl Environ Microbiol 1989 55 3119 3123 16348073
20. Tools for functional postgenomic analysis of Listeria monocytogenes. IR Monk CG Gahan C Hill, Appl Environ Microbiol 2008 74 3921 3934 10.1128/AEM.00314-08 18441118
21. Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange Site-Directed Mutagenesis. W Wang BA Malcolm, Biotechniques 1999 26 680 682 10343905
22. Morphotypic conversion in Listeria monocytogenes biofilm formation: biological significance of rough colony isolates. IR Monk GM Cook BC Monk PJ Bremer, Appl Environ Microbiol 2004 70 6686 6694 10.1128/AEM.70.11.6686-6694. 2004 15528535
23. Production, characterisation and potential application of a novel monoclonal antibody for rapid identification of virulent Listeria monocytogenes. S Hearty P Leonard J Quinn R O'Kennedy, J Microbiol Methods 2006 66 294 312 10.1016/j.mimet.2005.12.009 16457899
24. Tumor induction relationships in development of transplantable cancers of the colon in mice for chemotherapy assays, with a note on carcinogen structure. TH Corbett DPJ Griswold BJ Roberts JC Peckham FMJ Schabel, Cancer Res 1975 35 2434 2439 1149045
25. Establishment of mouse colonic carcinoma cell lines with different metastatic properties. MG Brattain J Strobel-Stevens D Fine M Webb AM Sarrif, Cancer Res 1980 40 2142 2146 6992981
26. 10 years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis. I Mierau M Kleerebezem, Appl Microbiol Biotechnol 2005 68 705 717 10.1007/s00253-005-0107-6 16088349
27. Internalin-expressing Lactococcus lactis is able to invade small intestine of guinea pigs and deliver DNA into mammalian epithelial cells. VD Guimaraes JE Gabriel F Lefevre D Cabanes A Gruss P Cossart V Azevedo P Langella, Microbes Infect 2005 7 836 844 10.1016/j.micinf.2005.02.012 15878681
28. Novel luciferase reporter system for in vitro and organ-specific monitoring of differential gene expression in Listeria monocytogenes. PA Bron IR Monk SC Corr C Hill CG Gahan, Appl Environ Microbiol 2006 72 2876 2884 10.1128/AEM.72.4.2876-2884.2006 16597994
29. Extracellular replication of Listeria monocytogenes in the murine gall bladder. J Hardy KP Francis M DeBoer P Chu K Gibbs CH Contag, Science 2004 303 851 853 10.1126/science.1092712 14764883
30. Induced biliary excretion of Listeria monocytogenes. J Hardy JJ Margolis CH Contag, Infect Immun 2006 74 1819 1827 10.1128/IAI.74.3.1819-1827.2006 16495556
31. Recombination and positive selection contribute to evolution of Listeria monocytogenes inlA. RH Orsi DR Ripoll M Yeung KK Nightingale M Wiedmann, Microbiology 2007 153 2666 2678 10.1099/mic.0.2007/007310-0 17660431
32. Rational Pathogen Design: Extending the Host Range of Listeria monocytogenes by Thermodynamically Re-engineering the Internalin/E-Cadherin Interface. T Wollert, PhD thesis, Technical University Carolo-Wilhelmina, Braunschweig 2007
33. Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and -independent mechanisms. A Lingnau E Domann M Hudel M Bock T Nichterlein J Wehland T Chakraborty, Infect Immun 1995 63 3896 3903 7558297
34. New Listeria monocytogenes prfA* mutants, transcriptional properties of PrfA* proteins and structure-function of the virulence regulator PrfA. Y Vega M Rauch MJ Banfield S Ermolaeva M Scortti W Goebel JA Vazquez-Boland, Mol Microbiol 2004 52 1553 1565 10.1111/j.1365-2958.2004.04052.x 15186408
35. Thermodynamically reengineering the listerial invasion complex InlA/E-cadherin. T Wollert DW Heinz WD Schubert, Proc Natl Acad Sci USA 2007 104 13960 13965 10.1073/pnas.0702199104 17715295
36. Heterologous protein expression is enhanced by harmonizing the codon usage frequencies of the target gene with those of the expression host. E Angov CJ Hillier RL Kincaid JA Lyon, PLoS ONE 2008 3 2189 10.1371/journal.pone.0002189 18478103
37. Selecting and screening recombinant antibody libraries. HR Hoogenboom, Nat Biotechnol 2005 23 1105 1116 10.1038/nbt1126 16151404
38. The generation of nisin variants with enhanced activity against specific Gram-positive pathogens. D Field PM Connor PD Cotter C Hill RP Ross, Mol Microbiol 2008 69 218 230 10.1111/j.1365-2958.2008.06279.x 18485077
39. Comparative genomics of Listeria species. P Glaser L Frangeul C Buchrieser C Rusniok A Amend F Baquero P Berche H Bloecker P Brandt T Chakraborty A Charbit F Chetouani E Couve A de Daruvar P Dehoux E Domann G Dominguez-Bernal E Duchaud L Durant O Dussurget KD Entian H Fsihi F Garcia-del Portillo P Garrido L Gautier W Goebel N Gomez-Lopez T Hain J Hauf D Jackson LM Jones U Kaerst J Kreft M Kuhn F Kunst G Kurapkat E Madueno A Maitournam JM Vicente E Ng H Nedjari G Nordsiek S Novella B de Pablos JC Perez-Diaz R Purcell B Remmel M Rose T Schlueter N Simoes A Tierrez JA Vazquez-Boland H Voss J Wehland P Cossart, Science 2001 294 849 852 11679669
40. A lactococcal pWV01-based integration toolbox for bacteria. K Leenhouts G Venema J Kok, Methods in Cell Science 1998 20 35 50 10.1023/A:1009862119114 (Pubitemid 29241680)
41. New thermosensitive plasmid for Gram-positive bacteria. E Maguin P Duwat T Hege D Ehrlich A Gruss, J Bacteriol 1992 174 5633 5638 1324906