Contribution of Amino Acid Catabolism to the Tissue Specific Persistence of Campylobacter jejuni in a Murine Colonization Model

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Hofreuter, Dirk ^a   Mohr, Juliane ^a   Wensel, Olga ^a   Rademacher, Sebastian ^a   Schreiber, Kerstin ^b   Schomburg, Dietmar ^b   Gao, Beile ^c   Galán, Jorge E ^c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; HYDROGEN PEROXIDE; PERMEASE; PROLINE; PROLINE PERMEASE PUTP; PYRROLINE 5 CARBOXYLATE DEHYDROGENASE; PYRROLINE 5 CARBOXYLATE DEHYDROGENASE PUTA; SERINE; SERINE DEHYDRATASE; SERINE DEHYDRATASE SDAA; SERINE TRANSPORTER SDAC; UNCLASSIFIED DRUG;

ADAPTATION; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; CAMPYLOBACTER ENTERITIS; CAMPYLOBACTER JEJUNI; COLONY FORMING UNIT; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL MOUSE; GENE FUNCTION; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; OXIDATIVE STRESS; PHYSICAL TOLERANCE; PUTA GENE; PUTP GENE; SDAA GENE; SDAC GENE; SEQUENCE HOMOLOGY; TISSUE DISTRIBUTION;

ANIMALS; ANTIGENS, BACTERIAL; CAMPYLOBACTER JEJUNI; GLUCONEOGENESIS; GLUCOSE; MICE; ORGAN SPECIFICITY; OSMOTIC PRESSURE; OXIDATIVE STRESS; PROLINE; SERINE;

CAMPYLOBACTER JEJUNI; MURINAE;

EID: 84870619710     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050699     Document Type: Article

References (90)

1. Brown SA, Palmer KL, Whiteley M, (2008) Revisiting the host as a growth medium. Nat Rev Microbiol 6: 657-666.
2. Rohmer L, Hocquet D, Miller SI, (2011) Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19: 341-348.
3. Buysse JM, (2001) The role of genomics in antibacterial target discovery. Curr Med Chem 8: 1713-1726.
4. Plaimas K, Eils R, Konig R, (2010) Identifying essential genes in bacterial metabolic networks with machine learning methods. BMC Syst Biol 4: 56.
5. Allos BM, (2001) Campylobacter jejuni Infections: update on emerging issues and trends. Clin Infect Dis 32: 1201-1206.
6. de Zoete MR, van Putten JP, Wagenaar JA, (2007) Vaccination of chickens against Campylobacter. Vaccine 25: 5548-5557.
7. Lee MD, Newell DG, (2006) Campylobacter in poultry: filling an ecological niche. Avian Dis 50: 1-9.
8. Newell DG, Fearnley C, (2003) Sources of Campylobacter colonization in broiler chickens. Appl Environ Microbiol 69: 4343-4351.
9. Butzler JP, (2004) Campylobacter, from obscurity to celebrity. Clin Microbiol Infect 10: 868-876.
10. Blaser MJ, (1997) Epidemiologic and clinical features of Campylobacter jejuni infections. J Infect Dis 176 (Suppl 2): S103-105.
11. Yuki N, (2001) Infectious origins of, and molecular mimicry in, Guillain-Barre and Fisher syndromes. Lancet Infect Dis 1: 29-37.
12. Young KT, Davis LM, Dirita VJ, (2007) Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5: 665-679.
13. van Putten JP, van Alphen LB, Wosten MM, de Zoete MR, (2009) Molecular mechanisms of campylobacter infection. Curr Top Microbiol Immunol 337: 197-229.
14. Fox JG, Rogers AB, Whary MT, Ge Z, Taylor NS, et al. (2004) Gastroenteritis in NF-kappaB-deficient mice is produced with wild-type Camplyobacter jejuni but not with C. jejuni lacking cytolethal distending toxin despite persistent colonization with both strains. Infect Immun 72: 1116-1125.
15. Hickey TE, McVeigh AL, Scott DA, Michielutti RE, Bixby A, et al. (2000) Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect Immun 68: 6535-6541.
16. Krause-Gruszczynska M, Rohde M, Hartig R, Genth H, Schmidt G, et al. (2007) Role of the small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni. Cell Microbiol 9: 2431-2444.
17. van Alphen LB, Bleumink-Pluym NM, Rochat KD, van Balkom BW, Wosten MM, et al. (2008) Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells. Cell Microbiol 10: 53-66.
18. Watson RO, Galan JE, (2008) Campylobacter jejuni survives within epithelial cells by avoiding delivery to lysosomes. PLoS Pathog 4: e14.
19. Bereswill S, Fischer A, Plickert R, Haag LM, Otto B, et al. (2011) Novel murine infection models provide deep insights into the "menage a trois" of Campylobacter jejuni, microbiota and host innate immunity. PLoS One 6: e20953.
20. Hendrixson DR, DiRita VJ, (2004) Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52: 471-484.
21. Takata T, Fujimoto S, Amako K, (1992) Isolation of nonchemotactic mutants of Campylobacter jejuni and their colonization of the mouse intestinal tract. Infect Immun 60: 3596-3600.
22. Yao R, Burr DH, Guerry P, (1997) CheY-mediated modulation of Campylobacter jejuni virulence. Mol Microbiol 23: 1021-1031.
23. Bachtiar BM, Coloe PJ, Fry BN, (2007) Knockout mutagenesis of the kpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium-host interactions. FEMS Immunol Med Microbiol 49: 149-154.
24. Bacon DJ, Szymanski CM, Burr DH, Silver RP, Alm RA, et al. (2001) A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol Microbiol 40: 769-777.
25. Chang C, Miller JF, (2006) Campylobacter jejuni colonization of mice with limited enteric flora. Infect Immun 74: 5261-5271.
26. Jones MA, Marston KL, Woodall CA, Maskell DJ, Linton D, et al. (2004) Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect Immun 72: 3769-3776.
27. Karlyshev AV, Everest P, Linton D, Cawthraw S, Newell DG, et al. (2004) The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150: 1957-1964.
28. Morooka T, Umeda A, Amako K, (1985) Motility as an intestinal colonization factor for Campylobacter jejuni. J Gen Microbiol 131: 1973-1980.
29. Naito M, Frirdich E, Fields JA, Pryjma M, Li J, et al. (2010) Effects of sequential Campylobacter jejuni 81-176 lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J Bacteriol 192: 2182-2192.
30. Watson RO, Novik V, Hofreuter D, Lara-Tejero M, Galan JE, (2007) A MyD88-deficient mouse model reveals a role for Nramp1 in Campylobacter jejuni infection. Infect Immun 75: 1994-2003.
31. Metris A, Reuter M, Gaskin DJ, Baranyi J, van Vliet AH, (2011) In vivo and in silico determination of essential genes of Campylobacter jejuni. BMC Genomics 12: 535.
32. Stahl M, Stintzi A, (2011) Identification of essential genes in C. jejuni genome highlights hyper-variable plasticity regions. Funct Integr Genomics 11: 241-257.
33. Fouts DE, Mongodin EF, Mandrell RE, Miller WG, Rasko DA, et al. (2005) Major structural differences and novel potential virulence mechanisms from the genomes of multiple campylobacter species. PLoS Biol 3: e15.
34. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668.
35. Velayudhan J, Kelly DJ, (2002) Analysis of gluconeogenic and anaplerotic enzymes in Campylobacter jejuni: an essential role for phosphoenolpyruvate carboxykinase. Microbiology 148: 685-694.
36. Muraoka WT, Zhang Q, (2011) Phenotypic and genotypic evidence for L-fucose utilization by Campylobacter jejuni. J Bacteriol 193: 1065-1075.
37. Stahl M, Friis LM, Nothaft H, Liu X, Li J, et al. (2011) L-fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci U S A 108: 7194-7199.
38. Guccione E, Leon-Kempis Mdel R, Pearson BM, Hitchin E, Mulholland F, et al. (2008) Amino acid-dependent growth of Campylobacter jejuni: key roles for aspartase (AspA) under microaerobic and oxygen-limited conditions and identification of AspB (Cj0762), essential for growth on glutamate. Mol Microbiol 69: 77-93.
39. Leach S, Harvey P, Wali R, (1997) Changes with growth rate in the membrane lipid composition of and amino acid utilization by continuous cultures of Campylobacter jejuni. J Appl Microbiol 82: 631-640.
40. Leon-Kempis Mdel R, Guccione E, Mulholland F, Williamson MP, Kelly DJ, (2006) The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol Microbiol 60: 1262-1275.
41. Westfall HN, Rollins DM, Weiss E, (1986) Substrate utilization by Campylobacter jejuni and Campylobacter coli. Appl Environ Microbiol 52: 700-705.
42. Wright JA, Grant AJ, Hurd D, Harrison M, Guccione EJ, et al. (2009) Metabolite and transcriptome analysis of Campylobacter jejuni in vitro growth reveals a stationary-phase physiological switch. Microbiology 155: 80-94.
43. Hofreuter D, Novik V, Galan JE, (2008) Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell Host Microbe 4: 425-433.
44. Mohammed KA, Miles RJ, Halablab MA, (2004) The pattern and kinetics of substrate metabolism of Campylobacter jejuni and Campylobacter coli. Lett Appl Microbiol 39: 261-266.
45. Velayudhan J, Jones MA, Barrow PA, Kelly DJ, (2004) L-serine catabolism via an oxygen-labile L-serine dehydratase is essential for colonization of the avian gut by Campylobacter jejuni. Infect Immun 72: 260-268.
46. Mendz GL, Ball GE, Meek DJ, (1997) Pyruvate metabolism in Campylobacter spp. Biochim Biophys Acta 1334: 291-302.
47. Thomas MT, Shepherd M, Poole RK, van Vliet AH, Kelly DJ, et al. (2011) Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on L-lactate. Environ Microbiol 13: 48-61.
48. Davis LM, Kakuda T, DiRita VJ, (2009) A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J Bacteriol 191: 1631-1640.
49. Naikare H, Palyada K, Panciera R, Marlow D, Stintzi A, (2006) Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun 74: 5433-5444.
50. Xu F, Zeng X, Haigh RD, Ketley JM, Lin J, (2010) Identification and characterization of a new ferric enterobactin receptor, CfrB, in Campylobacter. J Bacteriol 192: 4425-4435.
51. Hofreuter D, Tsai J, Watson RO, Novik V, Altman B, et al. (2006) Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun 74: 4694-4707.
52. Pajaniappan M, Hall JE, Cawthraw SA, Newell DG, Gaynor EC, et al. (2008) A temperature-regulated Campylobacter jejuni gluconate dehydrogenase is involved in respiration-dependent energy conservation and chicken colonization. Mol Microbiol 68: 474-491.
53. Weingarten RA, Grimes JL, Olson JW, (2008) Role of Campylobacter jejuni respiratory oxidases and reductases in host colonization. Appl Environ Microbiol 74: 1367-1375.
54. Weingarten RA, Taveirne ME, Olson JW (2009) The dual-functioning fumarate reductase is the sole succinate:quinone reductase in Campylobacter jejuni and is required for full host colonization. J Bacteriol.
55. Ribardo DA, Hendrixson DR, (2011) Analysis of the LIV system of Campylobacter jejuni reveals alternative roles for LivJ and LivK in commensalism beyond branched-chain amino acid transport. J Bacteriol 193: 6233-6243.
56. Cooper KK, Cooper MA, Zuccolo A, Law B, Joens LA, (2011) Complete genome sequence of Campylobacter jejuni strain S3. J Bacteriol 193: 1491-1492.
57. Friis C, Wassenaar TM, Javed MA, Snipen L, Lagesen K, et al. (2010) Genomic characterization of Campylobacter jejuni strain M1. PLoS One 5: e12253.
58. Hepworth PJ, Ashelford KE, Hinds J, Gould KA, Witney AA, et al. (2011) Genomic variations define divergence of water/wildlife-associated Campylobacter jejuni niche specialists from common clonal complexes. Environ Microbiol 13: 1549-1560.
59. Pearson BM, Gaskin DJ, Segers RP, Wells JM, Nuijten PJ, et al. (2007) The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). J Bacteriol 189: 8402-8403.
60. Poly F, Read T, Tribble DR, Baqar S, Lorenzo M, et al. (2007) Genome sequence of a clinical isolate of Campylobacter jejuni from Thailand. Infect Immun 75: 3425-3433.
61. Poly F, Read TD, Chen YH, Monteiro MA, Serichantalergs O, et al. (2008) Characterization of two Campylobacter jejuni strains for use in volunteer experimental-infection studies. Infect Immun 76: 5655-5667.
62. Takamiya M, Ozen A, Rasmussen M, Alter T, Gilbert T, et al. (2011) Genome Sequence of Campylobacter jejuni strain 327, a strain isolated from a turkey slaughterhouse. Stand Genomic Sci 4: 113-122.
63. Takamiya M, Ozen A, Rasmussen M, Alter T, Gilbert T, et al. (2011) Genome sequences of two stress-tolerant Campylobacter jejuni poultry strains, 305 and DFVF1099. J Bacteriol 193: 5546-5547.
64. Zhang M, He L, Li Q, Sun H, Gu Y, et al. (2010) Genomic characterization of the Guillain-Barre syndrome-associated Campylobacter jejuni ICDCCJ07001 Isolate. PLoS One 5: e15060.
65. Pei Z, Blaser MJ, (1993) PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in gram-negative nutrient transport systems. J Biol Chem 268: 18717-18725.
66. Pei Z, Burucoa C, Grignon B, Baqar S, Huang XZ, et al. (1998) Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect Immun 66: 938-943.
67. Servet C, Ghelis T, Richard L, Zilberstein A, Savoure A, (2012) Proline dehydrogenase: a key enzyme in controlling cellular homeostasis. Front Biosci 17: 607-620.
68. Lin AE, Krastel K, Hobb RI, Thompson SA, Cvitkovitch DG, et al. (2009) Atypical roles for Campylobacter jejuni amino acid ATP binding cassette transporter components PaqP and PaqQ in bacterial stress tolerance and pathogen-host cell dynamics. Infect Immun 77: 4912-4924.
69. Day WA Jr, Sajecki JL, Pitts TM, Joens LA, (2000) Role of catalase in Campylobacter jejuni intracellular survival. Infect Immun 68: 6337-6345.
70. Kelly DJ (2001) The physiology and metabolism of Campylobacter jejuni and Helicobacter pylori. Symp Ser Soc Appl Microbiol: 16S-24S.
71. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ, (1988) Experimental Campylobacter jejuni infection in humans. J Infect Dis 157: 472-479.
72. Robinson DA, (1981) Infective dose of Campylobacter jejuni in milk. Br Med J (Clin Res Ed) 282: 1584.
73. Barnes IH, Bagnall MC, Browning DD, Thompson SA, Manning G, et al. (2007) Gamma-glutamyl transpeptidase has a role in the persistent colonization of the avian gut by Campylobacter jejuni. Microb Pathog 43: 198-207.
74. Novik V, Hofreuter D, Galan JE, (2010) Identification of Campylobacter jejuni genes involved in its interaction with epithelial cells. Infect Immun 78: 3540-3553.
75. Kavermann H, Burns BP, Angermuller K, Odenbreit S, Fischer W, et al. (2003) Identification and characterization of Helicobacter pylori genes essential for gastric colonization. J Exp Med 197: 813-822.
76. Krishnan N, Doster AR, Duhamel GE, Becker DF, (2008) Characterization of a Helicobacter hepaticus putA mutant strain in host colonization and oxidative stress. Infect Immun 76: 3037-3044.
77. Nakajima K, Inatsu S, Mizote T, Nagata Y, Aoyama K, et al. (2008) Possible involvement of put A gene in Helicobacter pylori colonization in the stomach and motility. Biomed Res 29: 9-18.
78. Jimenez-Zurdo JI, Garcia-Rodriguez FM, Toro N, (1997) The Rhizobium meliloti putA gene: its role in the establishment of the symbiotic interaction with alfalfa. Mol Microbiol 23: 85-93.
79. Schwan WR, Coulter SN, Ng EY, Langhorne MH, Ritchie HD, et al. (1998) Identification and characterization of the PutP proline permease that contributes to in vivo survival of Staphylococcus aureus in animal models. Infect Immun 66: 567-572.
80. Empadinhas N, da Costa MS, (2008) Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. Int Microbiol 11: 151-161.
81. Wood JM, (1988) Proline porters effect the utilization of proline as nutrient or osmoprotectant for bacteria. J Membr Biol 106: 183-202.
82. Booth IR, Higgins CF, (1990) Enteric bacteria and osmotic stress: intracellular potassium glutamate as a secondary signal of osmotic stress? FEMS Microbiol Rev 6: 239-246.
83. Coulter SN, Schwan WR, Ng EY, Langhorne MH, Ritchie HD, et al. (1998) Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments. Mol Microbiol 30: 393-404.
84. Peng K, Monack DM, (2010) Indoleamine 2,3-dioxygenase 1 is a lung-specific innate immune defense mechanism that inhibits growth of Francisella tularensis tryptophan auxotrophs. Infect Immun 78: 2723-2733.
85. Gripp E, Hlahla D, Didelot X, Kops F, Maurischat S, et al. (2011) Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics 12: 584.
86. Miller WG, Bates AH, Horn ST, Brandl MT, Wachtel MR, et al. (2000) Detection on surfaces and in Caco-2 cells of Campylobacter jejuni cells transformed with new gfp, yfp, and cfp marker plasmids. Appl Environ Microbiol 66: 5426-5436.
87. Colegio OR, Griffin TJ, Grindley ND, Galan JE, (2001) In vitro transposition system for efficient generation of random mutants of Campylobacter jejuni. J Bacteriol 183: 2384-2388.
88. Grabowski R, Buckel W, (1991) Purification and properties of an iron-sulfur-containing and pyridoxal-phosphate-independent L-serine dehydratase from Peptostreptococcus asaccharolyticus. Eur J Biochem 199: 89-94.
89. Abu Dawud R, Schreiber K, Schomburg D, Adjaye J, (2012) Human embryonic stem cells and embryonal carcinoma cells have overlapping and distinct metabolic signatures. PLoS One 7: e39896.
90. Hiller K, Hangebrauk J, Jager C, Spura J, Schreiber K, et al. (2009) MetaboliteDetector: comprehensive analysis tool for targeted and nontargeted GC/MS based metabolome analysis. Anal Chem 81: 3429-3439.