Characterization and reactivity of broiler chicken sera to selected recombinant Campylobacter jejuni chemotactic proteins

Archives of Microbiology

Volumn 196, Issue 5, 2014, Pages 375-383

  Yeh, Hung Yueh ^a   Hiett, Kelli L ^a   Line, John E ^a   Seal, Bruce S ^a  

^a RUSSELL RESEARCH CENTER   (United States)

Author keywords

Campylobacter jejuni; Chemotaxis; Foodborne pathogen; Methyl accepting chemotaxis proteins; Poultry; Zoonoses; Proteobacteria

Indexed keywords

BACTERIAL PROTEIN; POLYHISTIDINE TAG; RECOMBINANT PROTEIN;

ANTIBODY SCREENING; ARTICLE; BROILER; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION SYSTEM; GENE PRODUCT; IMMUNOBLOTTING; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; EPSILONPROTEOBACTERIA; ESCHERICHIA COLI; GALLUS GALLUS; NEGIBACTERIA;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CHEMOTAXIS; CHICKENS; ESCHERICHIA COLI; MEMBRANE PROTEINS; RECOMBINANT PROTEINS;

EID: 84899960970     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-014-0969-z     Document Type: Article

References (64)

1. Alam MM, Tsai LL, Rollins SM, Sheikh A, Khanam F, Bufano MK, Yu Y, Wu-Freeman Y, Kalsy A, Sultana T, Sayeed MA, Jahan N, LaRocque RC, Harris JB, Leung DT, Brooks WA, Calderwood SB, Charles RC, Qadri F, Ryan ET (2013) Identification of in vivo-induced bacterial proteins during human infection with Salmonella enterica serotype Paratyphi A. Clin Vaccine Immunol 20:712-719
2. Alex LA, Simon MI (1994) Protein histidine kinases and signal transduction in prokaryotes and eukaryotes. Trends Genet 10:133-138 (Pubitemid 24107646)
3. Bannantine JP, Bayles DO, Waters WR, Palmer MV, Stabel JR, Paustian ML (2008a) Early antibody response against Mycobacterium avium subspecies paratuberculosis antigens in subclinical cattle. Proteome Sci 6:5
4. Bannantine JP, Waters WR, Stabel JR, Palmer MV, Li L, Kapur V, Paustian ML (2008b) Development and use of a partial Mycobacterium avium subspecies paratuberculosis protein array. Proteomics 8:463-474 (Pubitemid 351252005)
5. Bilwes AM, Alex LA, Crane BR, Simon MI (1999) Structure of CheA, a signal-transducing histidine kinase. Cell 96:131-141 (Pubitemid 29044160)
6. Boukhvalova MS, Dahlquist FW, Stewart RC (2002) CheW binding interactions with CheA and Tar. Importance for chemotaxis signaling in Escherichia coli. J Biol Chem 277:22251-22259 (Pubitemid 34967191)
7. Burgess-Brown NA, Sharma S, Sobott F, Loenarz C, Oppermann U, Gileadi O (2008) Codon optimization can improve expression of human genes in Escherichia coli: a multi-gene study. Protein Expr Purif 59:94-102
8. Chang C, Miller JF (2006) Campylobacter jejuni colonization of mice with limited enteric flora. Infect Immun 74:5261-5271 (Pubitemid 44300445)
9. Day CJ, Hartley-Tassell LE, Shewell LK, King RM, Tram G, Day SK, Semchenko EA, Korolik V (2012) Variation of chemosensory receptor content of Campylobacter jejuni strains and modulation of receptor gene expression under different in vivo and in vitro growth conditions. BMC Microbiol 12:128
10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797
11. Elliott KT, Dirita VJ (2008) Characterization of CetA and CetB, a bipartite energy taxis system in Campylobacter jejuni. Mol Microbiol 69:1091-1103
12. European Food Safety Authority (2010) The community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J 8:1496
13. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186-194 (Pubitemid 28177230)
14. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175-185 (Pubitemid 28177229)
15. Ewing CP, Andreishcheva E, Guerry P (2009) Functional characterization of flagellin glycosylation in Campylobacter jejuni 81-176. J Bacteriol 191:7086-7093
16. Fath S, Bauer AP, Liss M, Spriestersbach A, Maertens B, Hahn P, Ludwig C, Schäfer F, Graf M, Wagner R (2011) Multiparameter RNA and codon optimization: a standardized tool to assess and enhance autologous mammalian gene expression. PLoS One 6:e17596
17. Gershoni JM (1988) Protein blotting: a manual. Methods Biochem Anal 33:1-58
18. Griswold IJ, Dahlquist FW (2002) The dynamic behavior of CheW from Thermotoga maritima in solution, as determined by nuclear magnetic resonance: implications for potential protein-protein interaction sites. Biophys Chem 101-102:359-373 (Pubitemid 35462059)
19. Guerry P, Ewing CP, Schirm M, Lorenzo M, Kelly J, Pattarini D, Majam G, Thibault P, Logan S (2006) Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol Microbiol 60:299-311
20. Hames BD (1990) One-dimensional polyacrylamide gel electrophoresis. In: Hames BD, Rickwood D (eds) Gel electrophoresis of proteins: a practical approach, 2nd edn. Oxford University Press, New York, pp 1-147
21. Handfield M, Brady LJ, Progulske-Fox A, Hillman JD (2000) IVIAT: a novel method to identify microbial genes expressed specifically during human infections. Trends Microbiol 8:336-339 (Pubitemid 30421068)
22. Hang L, John M, Asaduzzaman M, Bridges EA, Vanderspurt C, Kirn TJ, Taylor RK, Hillman JD, Progulske-Fox A, Handfield M, Ryan ET, Calderwood SB (2003) Use of in vivo-induced antigen technology (IVIAT) to identify genes uniquely expressed during human infection with Vibrio cholerae. Proc Natl Acad Sci USA 100:8508-8513 (Pubitemid 36842575)
23. Hannu T, Mattila L, Rautelin H, Pelkonen P, Lahdenne P, Siitonen A, Leirisalo-Repo M (2002) Campylobacter-triggered reactive arthritis: a population-based study. Rheumatology 41:312-318 (Pubitemid 34537868)
24. Harris JB, Baresch-Bernal A, Rollins SM, Alam A, LaRocque RC, Bikowski M, Peppercorn AF, Handfield M, Hillman JD, Qadri F, Calderwood SB, Hohmann E, Breiman RF, Brooks WA, Ryan ET (2006) Identification of in vivo-induced bacterial protein antigens during human infection with Salmonella enterica serovar Typhi. Infect Immun 74:5161-5168 (Pubitemid 44300434)
25. Hartley-Tassell LE, Shewell LK, Day CJ, Wilson JC, Sandhu R, Ketley JM, Korolik V (2010) Identification and characterization of the aspartate chemosensory receptor of Campylobacter jejuni. Mol Microbiol 75:710-730
26. Hendrixson DR, DiRita VJ (2004) Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52:471-484 (Pubitemid 38520716)
27. Hendrixson DR, Akerley BJ, DiRita VJ (2001) Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40:214-224 (Pubitemid 32322874)
28. Hermans D, Van Deun K, Martel A, Van Immerseel F, Messens W, Heyndrickx M, Haesebrouck F, Pasmans F (2011) Colonization factors of Campylobacter jejuni in the chicken gut. Vet Res 42:82
29. Hermans D, Pasmans F, Messens W, Martel A, Van Immerseel F, Rasschaert G, Heyndrickx M, Van Deun K, Haesebrouck F (2012) Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector Borne Zoonotic Dis 12:89-98
30. Hess JF, Bourret RB, Simon MI (1988) Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature 336:139-143 (Pubitemid 18266139)
31. Hiett KL, Stintzi A, Andacht TM, Kuntz RL, Seal BS (2008) Genomic differences between Campylobacter jejuni isolates identify surface membrane and flagellar function gene products potentially important for colonizing the chicken intestine. Funct Integr Genomics 8:407-420
32. Howard SL, Jagannathan A, Soo EC, Hui JP, Aubry AJ, Ahmed I, Karlyshev A, Kelly JF, Jones MA, Stevens MP, Logan SM, Wren BW (2009) Campylobacter jejuni glycosylation island important in cell charge, legionaminic acid biosynthesis, and colonization of chickens. Infect Immun 77:2544-2556
33. Hughes RA, Cornblath DR (2005) Guillain-Barré syndrome. Lancet 366:1653-1666
34. Humphrey T, O'Brien S, Madsen M (2007) Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117:237-257 (Pubitemid 46978410)
35. Janssen R, Krogfelt KA, Cawthraw SA, van Pelt W, Wagenaar JA, Owen RJ (2008) Host-pathogen interactions in Campylobacter infections: the host perspective. Clin Microbiol Rev 21:505-518
36. Kane JF (1995) Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr Opin Biotechnol 6:494-500
37. Kubota K, Kasuga F, Iwasaki E, Inagaki S, Sakurai Y, Komatsu M, Toyofuku H, Angulo FJ, Scallan E, Morikawa K (2011) Estimating the burden of acute gastroenteritis and foodborne illness caused by Campylobacter, Salmonella, and Vibrio parahaemolyticus by using population-based telephone survey data, Miyagi Prefecture, Japan, 2005 to 2006. J Food Prot 74:1592-1598
38. Lawes JR, Vidal A, Clifton-Hadley FA, Sayers R, Rodgers J, Snow L, Evans SJ, Powell LF (2012) Investigation of prevalence and risk factors for Campylobacter in broiler flocks at slaughter: results from a UK survey. Epidemiol Infect 140:1725-1737
39. Lertsethtakarn P, Ottemann KM, Hendrixson DR (2011) Motility and chemotaxis in Campylobacter and Helicobacter. Annu Rev Microbiol 65:389-410
40. Li S, Chou H-H (2004) LUCY (2): an interactive DNA sequence quality trimming and vector removal tool. Bioinformatics 20:2865-2866 (Pubitemid 39530183)
41. Lin J (2009) Novel approaches for Campylobacter control in poultry. Foodborne Pathog Dis 6:755-765
42. Logan SM (2006) Flagellar glycosylation-a new component of the motility repertoire? Microbiology 152:1249-1262
43. Lowry JE, Goodridge L, Vernati G, Fluegel AM, Edwards WH, Andrews GP (2010) Identification of Brucella abortus genes in elk (Cervus elaphus) using in vivo-induced antigen technology (IVIAT) reveals novel markers of infection. Vet Microbiol 142:367-372
44. Marchant J, Wren B, Ketley J (2002) Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. Trends Microbiol 10:155-159 (Pubitemid 34242945)
45. McEvoy MM, Muhandiram DR, Kay LE, Dahlquist FW (1996) Structure and dynamics of a CheY-binding domain of the chemotaxis kinase CheA determined by nuclear magnetic resonance spectroscopy. Biochemistry 35:5633-5640 (Pubitemid 26143658)
46. Moore JE, Corcoran D, Dooley JS, Fanning S, Lucey B, Matsuda M, McDowell DA, Mégraud F, Millar BC, O'Mahony R, O'Riordan L, O'Rourke M, Rao JR, Rooney PJ, Sails A, Whyte P (2005) Campylobacter. Vet Res 36:351-382 (Pubitemid 40716370)
47. Mourey L, Da Re S, Pédelacq JD, Tolstykh T, Faurie C, Guillet V, Stock JB, Samama JP (2001) Crystal structure of the CheA histidine phosphotransfer domain that mediates response regulator phosphorylation in bacterial chemotaxis. J Biol Chem 276:31074-31082
48. Nielsen LN, Luijkx TA, Vegge CS, Johnsen CK, Nuijten P, Wren BW, Ingmer H, Krogfelt KA (2012) Identification of immunogenic and virulence-associated Campylobacter jejuni proteins. Clin Vaccine Immunol 19:113-119
49. Rollins SM, Peppercorn A, Young JS, Drysdale M, Baresch A, Bikowski MV, Ashford DA, Quinn CP, Handfield M, Hillman JD, Lyons CR, Koehler TM, Calderwood SB, Ryan ET (2008) Application of in vivo induced antigen technology (IVIAT) to Bacillus anthracis. PLoS One 3:e1824
50. Sahin O, Luo N, Huang S, Zhang Q (2003) Effect of Campylobacter-specific maternal antibodies on Campylobacter jejuni colonization in young chickens. Appl Environ Microbiol 69:5372-5379 (Pubitemid 37150761)
51. Schäffer AA, Aravind L, Madden TL, Shavirin S, Spouge JL, Wolf YI, Koonin EV, Altschul SF (2001) Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. Nucleic Acids Res 29:2994-3005 (Pubitemid 32685225)
52. Shoaf-Sweeney KD, Larson CL, Tang X, Konkel ME (2008) Identification of Campylobacter jejuni proteins recognized by maternal antibodies of chickens. Appl Environ Microbiol 74:6867-6875
53. Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Christensen MB, Schjoldager KT, Lavrsen K, Dabelsteen S, Pedersen NB, Marcos-Silva L, Gupta R, Bennett EP, Mandel U, Brunak S, Wandall H, Levery SB, Clausen H (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J 32:1478-1488
54. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
55. Thibault P, Logan SM, Kelly JF, Brisson JR, Ewing CP, Trust TJ, Guerry P (2001) Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J Biol Chem 276:34862-34870
56. Vu A, Wang X, Zhou H, Dahlquist FW (2012) The receptor-CheW binding interface in bacterial chemotaxis. J Mol Biol 415:759-767
57. Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024-1037 (Pubitemid 39611538)
58. Wuichet K, Zhulin IB (2010) Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 3:ra50
59. Wuichet K, Alexander RP, Zhulin IB (2007) Comparative genomic and protein sequence analyses of a complex system controlling bacterial chemotaxis. Methods Enzymol 422:1-31
60. Wyszyńska A, Raczko A, Lis M, Jagusztyn-Krynicka EK (2004) Oral immunization of chickens with avirulent Salmonella vaccine strain carrying C. jejuni 72Dz/92 cjaA gene elicits specific humoral immune response associated with protection against challenge with wild-type Campylobacter. Vaccine 22:1379-1389 (Pubitemid 38446914)
61. Yeh H, Klesius PH (2011) Over-expression, purification and immune responses to Aeromonas hydrophila AL09-73 flagellar proteins. Fish Shellfish Immunol 31:1278-1283
62. Yeh H, Hiett KL, Line JE, Oakley BB, Seal BS (2013) Construction, expression, purification and antigenicity of recombinant Campylobacter jejuni flagellar proteins. Microbiol Res 168:192-198
63. Yeh H, Hiett KL, Line JE, Seal BS (2014) Characterization and antigenicity of recombinant Campylobacter jejuni flagellar capping protein FliD. J Med Microbiol. doi:10.1099/jmm.0.060095-0
64. Zilbauer M, Dorrell N, Wren BW, Bajaj-Elliott M (2008) Campylobacter jejuni-mediated disease pathogenesis: an update. Trans R Soc Trop Med Hyg 102:123-129