Comparative proteogenomic analysis of the Leptospira interrogans virulence-attenuated strain IPAV against the pathogenic strain 56601

Cell Research

Volumn 21, Issue 8, 2011, Pages 1210-1229

  Zhong, Yi ^a,b   Chang, Xiao ^c,d   Cao, Xing Jun ^c   Zhang, Yan ^a   Zheng, Huajun ^e   Zhu, Yongzhang ^a   Cai, Chengsong ^a   Cui, Zelin ^a   Zhang, Yunyi ^b   Li, Yuan Yuan ^c   Jiang, Xiu Gao ^f   Zhao, Guo Ping ^b,e   Wang, Shengyue ^e   Li, Yixue ^c   Zeng, Rong ^c   Li, Xuan ^b   Guo, Xiao Kui ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^c INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^e CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

^f CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

genome; Leptospira; mutation; proteome; virulence

Indexed keywords

BACTERIAL PROTEIN; PROTEOME;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL MODEL; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; CHEMISTRY; COMPARATIVE STUDY; GENETIC VARIABILITY; GENETICS; GUINEA PIG; LEPTOSPIRA INTERROGANS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOGENICITY; SEQUENCE ALIGNMENT; UPREGULATION; VIRULENCE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CHROMOSOMES, BACTERIAL; GENES, BACTERIAL; GENETIC VARIATION; GUINEA PIGS; LEPTOSPIRA INTERROGANS; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; MUTATION; PROTEOME; SEQUENCE ALIGNMENT; UP-REGULATION; VIRULENCE;

LEPTOSPIRA; LEPTOSPIRA INTERROGANS; LEPTOSPIRA INTERROGANS SEROVAR LAI;

EID: 79961209179     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2011.46     Document Type: Article

References (83)

1. Paster BJ, Dewhirst FE, Weisburg WG, et al. Phylogenetic analysis of the spirochetes. J Bacteriol 1991; 173:6101-6109.
2. Haake DA. Spirochaetal lipoproteins and pathogenesis. Microbiology 2000; 146 (Pt 7):1491-1504. (Pubitemid 30458704)
3. Bharti AR, Nally JE, Ricaldi JN, et al. Leptospirosis: A zoonotic disease of global importance. Lancet Infect Dis 2003; 3:757-771. (Pubitemid 37489960)
4. Ko AI, Goarant C, Picardeau M. Leptospira: The dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat Rev Microbiol 2009; 7:736-747.
5. Faine S, Adler B, Bolin C, Perolat P. Leptospira and Leptospirosis. Melbourne: Medisci, 1999.
6. Bulach DM, Zuerner RL, Wilson P, et al. Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proc Natl Acad Sci USA 2006; 103:14560-14565. (Pubitemid 44484789)
7. Ren SX, Fu G, Jiang XG, et al. Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 2003; 422:888-893. (Pubitemid 36520040)
8. Murray GL, Srikram A, Henry R, et al. Leptospira interrogans requires heme oxygenase for disease pathogenesis. Microbes Infect 2009; 11:311-314.
9. Murray GL, Morel V, Cerqueira GM, et al. Genome-wide transposon mutagenesis in pathogenic Leptospira species. Infect Immun 2009; 77:810-816.
10. Zapata S, Trueba G, Bulach DM, et al. Characterization of a lipopolysaccharide mutant of Leptospira derived by growth in the presence of an anti-lipopolysaccharide monoclonal antibody. FEMS Microbiol Lett 2010; 309:144-150.
11. Margulies M, Egholm M, Altman WE, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005; 437:376-380. (Pubitemid 41613494)
12. Ristow P, Bourhy P, da Cruz McBride FW, et al. The OmpAlike protein Loa22 is essential for leptospiral virulence. PLoS Pathog 2007; 3:e97.
13. Yang HL, Jiang XC, Zhang XY, et al. Thrombocytopenia in the experimental leptospirosis of guinea pig is not related to disseminated intravascular coagulation. BMC Infect Dis 2006; 6:19.
14. Yang J, Zhang Y, Xu J, et al. Serum activity of plateletactivating factor acetylhydrolase is a potential clinical marker for leptospirosis pulmonary hemorrhage. PLoS ONE 2009; 4:e4181.
15. Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science 1997; 278:631-637. (Pubitemid 27464953)
16. Bourhy P, Salaun L, Lajus A, et al. A genomic island of the pathogen Leptospira interrogans serovar Lai can excise from its chromosome. Infect Immun 2007; 75:677-683. (Pubitemid 46203429)
17. Cao XJ, Dai J, Xu H, et al. High-coverage proteome analysis reveals the first insight of protein modification systems in the pathogenic spirochete Leptospira interrogans. Cell Res 2010; 20:197-210.
18. Jaffe JD, Berg HC, Church GM. Proteogenomic mapping as a complementary method to perform genome annotation. Proteomics 2004; 4:59-77. (Pubitemid 38140875)
19. Jaffe JD, Stange-Thomann N, Smith C, et al. The complete genome and proteome of Mycoplasma mobile. Genome Res 2004; 14:1447-1461. (Pubitemid 39193397)
20. Malmstrom J, Beck M, Schmidt A, et al. Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 2009; 460:762-765.
21. Nascimento AL, Ko AI, Martins EA, et al. Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J Bacteriol 2004; 186:2164-2172. (Pubitemid 38381206)
22. Piekarowicz A, Klyz A, Kwiatek A, Stein DC. Analysis of type I restriction modification systems in the Neisseriaceae: Genetic organization and properties of the gene products. Mol Microbiol 2001; 41:1199-1210. (Pubitemid 36124713)
23. Murray GL, Srikram A, Henry R, et al. Mutations affecting Leptospira interrogans lipopolysaccharide attenuate virulence. Mol Microbiol 2010; 78:701-709.
24. Owens RM, Pritchard G, Skipp P, et al. A dedicated translation factor controls the synthesis of the global regulator Fis. Embo J 2004; 23:3375-3385. (Pubitemid 39209161)
25. Samant S, Lee H, Ghassemi M, et al. Nucleotide biosynthesis is critical for growth of bacteria in human blood. PLoS Pathog 2008; 4:e37.
26. Kannan N, Taylor SS, Zhai Y, Venter JC, Manning G. Structural and functional diversity of the microbial kinome. PLoS Biol 2007; 5:e17.
27. Shi L. Manganese-dependent protein O-phosphatases in prokaryotes and their biological functions. Front Biosci 2004; 9:1382-1397.
28. Wehenkel A, Bellinzoni M, Grana M, et al. Mycobacterial Ser/Thr protein kinases and phosphatases: Physiological roles and therapeutic potential. Biochim Biophys Acta 2008; 1784:193-202.
29. Hussain H, Branny P, Allan E. A eukaryotic-type serine/threonine protein kinase is required for biofilm formation, genetic competence, and acid resistance in Streptococcus mutans. J Bacteriol 2006; 188:1628-1632. (Pubitemid 43228697)
30. Eshghi A, Cullen PA, Cowen L, Zuerner RL, Cameron CE. Global proteome analysis of Leptospira interrogans. J Proteome Res 2009; 8:4564-4578.
31. Wolanin PM, Thomason PA, Stock JB. Histidine protein kinases: Key signal transducers outside the animal kingdom. Genome Biol 2002; 3:REVIEWS3013.
32. Lamarche MG, Wanner BL, Crepin S, Harel J. The phosphate regulon and bacterial virulence: A regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 2008; 32:461-473. (Pubitemid 351538744)
33. Matin A. The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol 1991; 5:3-10. (Pubitemid 21895934)
34. Matin A. Role of alternate sigma factors in starvation protein synthesis-novel mechanisms of catabolite repression. Res Microbiol 1996; 147:494-505. (Pubitemid 26338129)
35. Schultz JE, Matin A. Molecular and functional characterization of a carbon starvation gene of Escherichia coli. J Mol Biol 1991; 218:129-140. (Pubitemid 121003334)
36. Tenor JL, McCormick BA, Ausubel FM, Aballay A. Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 2004; 14:1018-1024. (Pubitemid 38722618)
37. Hogg T, Mechold U, Malke H, Cashel M, Hilgenfeld R. Conformational antagonism between opposing active sites in a bifunctional RelA/SpoT homolog modulates (p)ppGpp metabolism during the stringent response. Cell 2004; 117:57-68. (Pubitemid 38469898)
38. Taylor CM, Beresford M, Epton HA, et al. Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J Bacteriol 2002; 184:621-628. (Pubitemid 34150207)
39. Haralalka S, Nandi S, Bhadra RK. Mutation in the relA gene of Vibrio cholerae affects in vitro and in vivo expression of virulence factors. J Bacteriol 2003; 185:4672-4682. (Pubitemid 36962273)
40. Erickson DL, Lines JL, Pesci EC, Venturi V, Storey DG. Pseudomonas aeruginosa relA contributes to virulence in Drosophila melanogaster. Infect Immun 2004; 72:5638-5645. (Pubitemid 39303672)
41. Pizarro-Cerda J, Tedin K. The bacterial signal molecule, ppGpp, regulates Salmonella virulence gene expression. Mol Microbiol 2004; 52:1827-1844. (Pubitemid 38822688)
42. Potrykus K, Cashel M. (p)ppGpp: Still magical? Annu Rev Microbiol 2008; 62:35-51.
43. Mimura H, Nakanishi Y, Hirono M, Maeshima M. Membrane topology of the H+-pyrophosphatase of Streptomyces coelicolor determined by cysteine-scanning mutagenesis. J Biol Chem 2004; 279:35106-35112. (Pubitemid 39318147)
44. Lin HH, Pan YJ, Hsu SH, et al. Deletion mutation analysis on C-terminal domain of plant vacuolar H(+)-pyrophosphatase. Arch Biochem Biophys 2005; 442:206-213.
45. Persson BL, Petersson J, Fristedt U, et al. Phosphate permeases of Saccharomyces cerevisiae: Structure, function and regulation. Biochim Biophys Acta 1999; 1422:255-272. (Pubitemid 29512380)
46. Versaw WK, Metzenberg RL. Repressible cation-phosphate symporters in Neurospora crassa. Proc Natl Acad Sci USA 1995; 92:3884-3887.
47. Gill HS, Pfluegl GM, Eisenberg D. Multicopy crystallographic refinement of a relaxed glutamine synthetase from Mycobacterium tuberculosis highlights flexible loops in the enzymatic mechanism and its regulation. Biochemistry 2002; 41:9863-9872. (Pubitemid 34839734)
48. Liaw SH, Kuo I, Eisenberg D. Discovery of the ammonium substrate site on glutamine synthetase, a third cation binding site. Protein Sci 1995; 4:2358-2365.
49. Thongboonkerd V, Chiangjong W, Saetun P, et al. Analysis of differential proteomes in pathogenic and non-pathogenic Leptospira: Potential pathogenic and virulence factors. Proteomics 2009; 9:3522-3534.
50. Buist G, Steen A, Kok J, Kuipers OP. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 2008; 68:838-847. (Pubitemid 351581067)
51. Kajimura J, Fujiwara T, Yamada S, et al. Identification and molecular characterization of an N-acetylmuramyl-L-alanine amidase Sle1 involved in cell separation of Staphylococcus aureus. Mol Microbiol 2005; 58:1087-1101. (Pubitemid 41667227)
52. Hogan RJ, Mathews SA, Kutlin A, Hammerschlag MR, Timms P. Differential expression of genes encoding membrane proteins between acute and continuous Chlamydia pneumoniae infections. Microb Pathog 2003; 34:11-16. (Pubitemid 36287210)
53. Lowder BJ, Duyvesteyn MD, Blair DF. FliG subunit arrangement in the flagellar rotor probed by targeted cross-linking. J Bacteriol 2005; 187:5640-5647. (Pubitemid 41134299)
54. Brown PN, Hill CP, Blair DF. Crystal structure of the middle and C-terminal domains of the flagellar rotor protein FliG. EMBO J 2002; 21:3225-3234. (Pubitemid 34760555)
55. Jacobson EL, Cervantes-Laurean D, Jacobson MK. Glycation of proteins by ADP-ribose. Mol Cell Biochem 1994; 138:207-212. (Pubitemid 24365415)
56. Okuda K, Hayashi H, Nishiyama Y. Systematic characterization of the ADP-ribose pyrophosphatase family in the Cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 2005; 187:4984-4991. (Pubitemid 40962216)
57. Kang LW, Gabelli SB, Cunningham JE, O'Handley SF, Amzel LM. Structure and mechanism of MT-ADPRase, a nudix hydrolase from Mycobacterium tuberculosis. Structure 2003; 11:1015-1023. (Pubitemid 36966790)
58. Hinnerwisch J, Fenton WA, Furtak KJ, Farr GW, Horwich AL. Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 2005; 121:1029-1041. (Pubitemid 40894633)
59. Guo F, Maurizi MR, Esser L, Xia D. Crystal structure of ClpA, an Hsp100 chaperone and regulator of ClpAP protease. J Biol Chem 2002; 277:46743-46752. (Pubitemid 35417677)
60. Ansong C, Purvine SO, Adkins JN, Lipton MS, Smith RD. Proteogenomics: Needs and roles to be filled by proteomics in genome annotation. Brief Funct Genomic Proteomic 2008; 7:50-62. (Pubitemid 351721150)
61. Tanner S, Shen Z, Ng J, et al. Improving gene annotation using peptide mass spectrometry. Genome Res 2007; 17:231-239. (Pubitemid 46220768)
62. Wang R, Prince JT, Marcotte EM. Mass spectrometry of the M. smegmatis proteome: Protein expression levels correlate with function, operons, and codon bias. Genome Res 2005; 15:1118-1126. (Pubitemid 41126867)
63. Vieira ML, Pimenta DC, de Morais ZM, Vasconcellos SA, Nascimento AL. Proteome analysis of Leptospira interrogans virulent strain. Open Microbiol J 2009; 3:69-74.
64. Nascimento AL, Verjovski-Almeida S, Van Sluys MA, et al. Genome features of Leptospira interrogans serovar Copenhageni. Braz J Med Biol Res 2004; 37:459-477.
65. Louvel H, Bommezzadri S, Zidane N, et al. Comparative and functional genomic analyses of iron transport and regulation in Leptospira spp. J Bacteriol 2006; 188:7893-7904. (Pubitemid 44764526)
66. Matsunaga J, Barocchi MA, Croda J, et al. Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol Microbiol 2003; 49:929-945. (Pubitemid 36981340)
67. Lin YP, Raman R, Sharma Y, Chang YF. Calcium binds to leptospiral immunoglobulin-like protein, LigB, and modulates fibronectin binding. J Biol Chem 2008; 283:25140-25149.
68. Croda J, Figueira CP, Wunder EA Jr., et al. Targeted mutagenesis in pathogenic Leptospira species: Disruption of the LigB gene does not affect virulence in animal models of leptospirosis. Infect Immun 2008; 76:5826-5833.
69. Haake DA, Matsunaga J. Leptospira: A spirochaete with a hybrid outer membrane. Mol Microbiol 2010; 77:805-814.
70. Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 1998; 8:175-185. (Pubitemid 28177229)
71. Gordon D, Abajian C, Green P. Consed: A graphical tool for sequence finishing. Genome Res 1998; 8:195-202. (Pubitemid 28177231)
72. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999; 27:4636-4641.
73. Lukashin AV, Borodovsky M. GeneMark.hmm: New solutions for gene finding. Nucleic Acids Res 1998; 26:1107-1115. (Pubitemid 28291669)
74. Marchler-Bauer A, Anderson JB, Cherukuri PF, et al. CDD: A Conserved Domain Database for protein classification. Nucleic Acids Res 2005; 33:D192-196. (Pubitemid 40207858)
75. Lowe TM, Eddy SR. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955-964. (Pubitemid 27298263)
76. Carver TJ, Rutherford KM, Berriman M, et al. ACT: The artemis comparison tool. Bioinformatics 2005; 21:3422-3423. (Pubitemid 41222448)
77. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007; 24:1596-1599. (Pubitemid 47236692)
78. Kumar A, Tyagi NK, Arevalo E, Miller KW, Kinne RK. A proteomic study of sodium/D-glucose cotransporter 1 (SGLT1): Topology of loop 13 and coverage of other functionally important domains. Biochim Biophys Acta 2007; 1774:968-974. (Pubitemid 47176954)
79. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: The yeast proteome. J Proteome Res 2003; 2:43-50. (Pubitemid 36207189)
80. Baerenfaller K, Grossmann J, Grobei MA, et al. Genomescale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics. Science 2008; 320:938-941. (Pubitemid 351929590)
81. Mallick P, Schirle M, Chen SS, et al. Computational prediction of proteotypic peptides for quantitative proteomics. Nat Biotechnol 2007; 25:125-131. (Pubitemid 46098780)
82. Kal AJ, van Zonneveld AJ, Benes V, et al. Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. Mol Biol Cell 1999; 10:1859-1872. (Pubitemid 29272637)
83. Lu P, Vogel C, Wang R, Yao X, Marcotte EM. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol 2007; 25:117-124. (Pubitemid 46087910)