Bacillus anthracis overcomes an amino acid auxotrophy by cleaving host serum proteins

Journal of Bacteriology

Volumn 197, Issue 14, 2015, Pages 2400-2411

  Terwilliger, Austen ^a   Swick, Michelle C ^b   Pflughoeft, Kathryn J ^b,e   Pomerantsev, Andrei ^c   Lyons, C Rick ^d   Koehler, Theresa M ^b   Maresso, Anthony ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d Department of Environmental and Radiological Health Sciences   (United States)

^e UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; ARGININE; ASPARAGINE; ASPARTIC ACID; ESSENTIAL AMINO ACID; GLUTAMIC ACID; GLUTAMINE; GLYCINE; HEMOGLOBIN; HISTIDINE; IRON; ISOLEUCINE; LEUCINE; LYSINE; METHIONINE; PHENYLALANINE; PLASMA PROTEIN; PROLINE; SERINE; SERUM ALBUMIN; SYNTHETIC PEPTIDE; THREONINE; TRYPTOPHAN; TYROSINE; VALINE; BACTERIAL PROTEIN; CULTURE MEDIUM; HEME;

ADULT; AMINO ACID SYNTHESIS; ARTICLE; AUXOTROPHY; BACILLUS ANTHRACIS; BACTERIAL GROWTH; BACTERIUM CULTURE; CHEMICAL COMPOSITION; CONTROLLED STUDY; ENZYME DEGRADATION; GROWTH INHIBITION; HOST PATHOGEN INTERACTION; HUMAN; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN DEGRADATION; SERUM; AMINO ACID SEQUENCE; CHEMISTRY; CULTURE MEDIUM; GENETICS; METABOLISM; MOLECULAR GENETICS;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS);

AMINO ACID SEQUENCE; AMINO ACIDS; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; BLOOD PROTEINS; CULTURE MEDIA; HEME; HEMOGLOBINS; HUMANS; IRON; MOLECULAR SEQUENCE DATA; SERUM;

EID: 84932177800     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00073-15     Document Type: Article

References (65)

1. McKevitt MT, Bryant KM, Shakir SM, Larabee JL, Blanke SR, Lovchik J, Lyons CR, Ballard JD. 2007. Effects of endogenous D-alanine synthesis and autoinhibition of Bacillus anthracis germination on in vitro and in vivo infections. Infect Immun 75:5726-5734. http://dx.doi.org/10.1128/IAI.00727-07.
2. Stenz L, Francois P, Whiteson K, Wolz C, Linder P, Schrenzel J. 2011. The CodY pleiotropic repressor controls virulence in gram-positive pathogens. FEMS Immunol Med Microbiol 62:123-139. http://dx.doi.org/10.1111/j.1574-695X.2011.00812.x.
3. Bono H, Ogata H, Goto S, Kanehisa M. 1998. Reconstruction of amino acid biosynthesis pathways from the complete genome sequence. Genome Res 8:203-210. http://dx.doi.org/10.1101/gr.8.3.203.
4. Yu X-J, Walker DH, Liu Y, Zhang L. 2009. Amino acid biosynthesis deficiency in bacteria associated with human and animal hosts. Infect Genet Evol 9:514-517. http://dx.doi.org/10.1016/j.meegid.2009.02.002.
5. Nuxoll AS, Halouska SM, Sadykov MR, Hanke ML, Bayles KW, Kielian T, Powers R, Fey PD. 2012. CcpA regulates arginine biosynthesis in Staphylococcus aureus through repression of proline catabolism. PLoS Pathog 8:e1003033. http://dx.doi.org/10.1371/journal.ppat.1003033.
6. Van Ravenzwaay B, Cunha GC-P, Leibold E, Looser R, Mellert W, Prokoudine A, Walk T, Wiemer J. 2007. The use of metabolomics for the discovery of new biomarkers of effect. Toxicol Lett 172:21-28. http://dx.doi.org/10.1016/j.toxlet.2007.05.021.
7. Abu Kwaik Y, Bumann D. 2013. Microbial quest for food in vivo: "nutritional virulence" as an emerging paradigm. Cell Microbiol 15:882-890. http://dx.doi.org/10.1111/cmi.12138.
8. Ascoli F, Fanelli MR, Antonini E. 1981. Preparation and properties of apohemoglobin and reconstituted hemoglobins. Methods Enzymol 76: 72-87. http://dx.doi.org/10.1016/0076-6879(81)76115-9.
9. Pflughoeft KJ, Sumby P, Koehler TM. 2011. Bacillus anthracis sin locus and regulation of secreted proteases. J Bacteriol 193:631-639. http://dx.doi.org/10.1128/JB.01083-10.
10. Sterne M. 1946. Avirulent anthrax vaccine. Onderstepoort J Vet Sci Anim Ind 21:41-43.
11. Cataldi A, Labruyere E, Mock M. 1990. Construction and characterization of a protective antigen-deficient Bacillus anthracis strain. Mol Microbiol 4:1111-1117. http://dx.doi.org/10.1111/j.1365-2958.1990.tb00685.x.
12. Green BD, Battisti L, Koehler TM, Thorne CB, Ivins BE. 1985. Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun 49: 291-297.
13. Pomerantsev AP, Pomerantseva OM, Moayeri M, Fattah R, Tallant C, Leppla SH. 2011. A Bacillus anthracis strain deleted for six proteases serves as an effective host for production of recombinant proteins. Protein Expr Purif 80:80-90. http://dx.doi.org/10.1016/j.pep.2011.05.016.
14. Pflughoeft KJ, Swick MC, Engler DA, Yeo H-J, Koehler TM. 2014. Modulation of the Bacillus anthracis secretome by the immune inhibitor A1 protease. J Bacteriol 196:424-435. http://dx.doi.org/10.1128/JB.00690-13.
15. 2 and a trans-acting element activate transcription from one of two promoters. J Bacteriol 176:586-595.
16. Marrero R, Welkos SL. 1995. The transformation frequency of plasmids into Bacillus anthracis is affected by adenine methylation. Gene 152:75-78. http://dx.doi.org/10.1016/0378-1119(94)00647-B.
17. Chen Y, Tenover FC, Koehler TM. 2004. β-Lactamase gene expression in a penicillin-resistant Bacillus anthracis strain. Antimicrob Agents Chemother 48:4873-4877. http://dx.doi.org/10.1128/AAC.48.12.4873-4877.2004.
18. Cendrowski S, MacArthur W, Hanna P. 2004. Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Mol Microbiol 51:407-417. http://dx.doi.org/10.1046/j.1365-2958.2003.03861.x.
19. Di Iorio E. 1981. Preparation of derivatives of ferrous and ferric hemoglobin. Methods Enzymol 76:57-72. http://dx.doi.org/10.1016/0076-6879(81)76114-7.
20. Marraffini LA, Schneewind O. 2006. Targeting proteins to the cell wall of sporulating Bacillus anthracis. Mol Microbiol 62:1402-1417. http://dx.doi.org/10.1111/j.1365-2958.2006.05469.x.
21. Gladstone GP. 1939. Inter-relationships between amino acids in the nutrition of B. anthracis. Br J Exp Pathol 20:189-200.
22. Read TD, Peterson SN, Tourasse N. 2003. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423:81-86. http://dx.doi.org/10.1038/nature01586.
23. Antelmann H, Williams RC, Miethke M, Wipat A, Albrecht D, Harwood CR, Hecker M. 2005. The extracellular and cytoplasmic proteomes of the non-virulent Bacillus anthracis strain UM23C1-2. Proteomics 5:3684-3695. http://dx.doi.org/10.1002/pmic.200401218.
24. 2-dependent cross talk mechanisms modulate extracellular proteolytic activities. J Bacteriol 188:3551-3571. http://dx.doi.org/10.1128/JB.188.10.3551-3571.2006.
25. Ristroph JD, Ivins BE. 1983. Elaboration of Bacillus anthracis antigens in a new, defined culture medium. Infect Immun 39:483-486.
26. Neidhardt FC, Bloch PL, Smith DF. 1974. Culture medium for enterobacteria. J Bacteriol 119:736-747.
27. Burtis CA, Ashwood ER, Burns DE. 2005. Tietz textbook of clinical chemistry and molecular diagnostics. Saunders, St. Louis, MO.
28. Van Schaik W, Prigent J, Fouet A. 2007. The stringent response of Bacillus anthracis contributes to sporulation but not to virulence. Microbiology 153:4234-4239. http://dx.doi.org/10.1099/mic.0.2007/010355-0.
29. Schechter AN. 2008. Hemoglobin research and the origins of molecular medicine. Blood 112:3927-3938. http://dx.doi.org/10.1182/blood-2008-04-078188.
30. Cescau S, Cwerman H, Létoffé S, Delepelaire P, Wandersman C, Biville F. 2007. Heme acquisition by hemophores. Biometals 20:603-613. http://dx.doi.org/10.1007/s10534-006-9050-y.
31. Pishchany G, Skaar EP. 2012. Taste for blood: hemoglobin as a nutrient source for pathogens. PLoS Pathog 8:e1002535. http://dx.doi.org/10.1371/journal.ppat.1002535.
32. Crosa JH, Mey AR, Payne SM (ed). 2004. Iron transport in bacteria. ASM Press, Washington, DC.
33. Nobles CL, Maresso AW. 2011. The theft of host heme by Gram-positive pathogenic bacteria. Metallomics 3:788-796. http://dx.doi.org/10.1039/c1mt00047k.
34. Stauff DL, Skaar EP. 2009. Bacillus anthracis HssRS signalling to HrtAB regulates haem resistance during infection. Mol Microbiol 72:763-778. http://dx.doi.org/10.1111/j.1365-2958.2009.06684.x.
35. Raven PH, Johnson GB, Mason KA, Losos J, Singer S. 2010. Biology, 9th ed. McGraw-Hill, New York, NY.
36. Smalley JW, Birss AJ, Szmigielski B, Potempa J. 2007. Sequential action of R-and K-specific gingipains of Porphyromonas gingivalis in the generation of the haem-containing pigment from oxyhaemoglobin. Arch Biochem Biophys 465:44-49. http://dx.doi.org/10.1016/j.abb.2007.05.011.
37. Smalley JW, Birss AJ, Szmigielski B, Potempa J. 2008. Mechanism of methaemoglobin breakdown by the lysine-specific gingipain of the periodontal pathogen Porphyromonas gingivalis. Biol Chem 389:1235-1238. http://dx.doi.org/10.1515/BC.2008.140.
38. Chung M-C, Popova TG, Millis BA, Mukherjee DV, Zhou W, Liotta La, Petricoin EF, Chandhoke V, Bailey C, Popov SG. 2006. Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J Biol Chem 281:31408-31418. http://dx.doi.org/10.1074/jbc.M605526200.
39. Kastrup CJ, Boedicker JQ, Pomerantsev AP, Moayeri M, Pompano RR, Kline TR, Sylvestre P, Shen F, Leppla H, Tang W, Ismagilov RF. 2008. Spatial localization of bacteria controls coagulation of human blood by "quorum acting." Nat Chem Biol 4:742-750. http://dx.doi.org/10.1038/nchembio.124.
40. Tonry JH, McNichol BA, Ramarao N, Chertow DS, Kim KS, Stibitz S, Schneewind O, Kashanchi F, Bailey CL, Popov S, Chung M-C. 2012. Bacillus anthracis protease InhA regulates BslA-mediated adhesion in human endothelial cells. Cell Microbiol 14:1219-1230. http://dx.doi.org/10.1111/j.1462-5822.2012.01791.x.
41. Pomerantsev AP, Sitaraman R, Galloway CR, Kivovich V, Leppla SH. 2006. Genome engineering in Bacillus anthracis using Cre recombinase. Infect Immun 74:682-693. http://dx.doi.org/10.1128/IAI.74.1.682-693.2006.
42. Dalhammar G, Steiner H. 1984. Characterization of inhibitor A, a protease from Bacillus thuringiensis which degrades attacins and cecropins, two classes of antibacterial proteins in insects. Eur J Biochem 139:247-252. http://dx.doi.org/10.1111/j.1432-1033.1984.tb08000.x.
43. Newport GR, Page CR, Ashman PU, Stibbs HH, Seed JR. 1977. Alteration of free serum amino acids in voles infected with Trypanosoma brucei gambiense. J Parasitol 63:15-24. http://dx.doi.org/10.2307/3280098.
44. Cynober LA. 2002. Plasma amino acid levels with a note on membrane transport: characteristics, regulation, and metabolic significance. Nutrition 18:761-766. http://dx.doi.org/10.1016/S0899-9007(02)00780-3.
45. Halter R, Pohlner J, Meyer TF. 1984. IgA protease of Neisseria gonorrhoeae: isolation and characterization of the gene and its extracellular product. EMBO J 3:1595-1601.
46. Tsuji T, Alborno RM, Ehara M, Honda T, Miwatani T. 1989. Detection of IgA protease from Haemophilus influenzae by immunoblotting. Eur J Epidemiol 5:199-201. http://dx.doi.org/10.1007/BF00156830.
47. Hendrixson DR, St Geme JW. 1998. The Haemophilus influenzae Hap serine protease promotes adherence and microcolony formation, potentiated by a soluble host protein. Mol Cell 2:841-850. http://dx.doi.org/10.1016/S1097-2765(00)80298-1.
48. Brezski RJ, Jordan RE. 2010. Cleavage of IgGs by proteases associated with invasive diseases: an evasion tactic against host immunity?. MAbs 2:212-220. http://dx.doi.org/10.4161/mabs.2.3.11780.
49. Harrington DJ. 1996. Bacterial collagenases and collagen-degrading enzymes and their potential role in human disease. Infect Immun 64:1885-1891.
50. Matsuka YV, Pillai S, Gubba S, Musser JM, Olmsted SB. 1999. Fibrinogen cleavage by the Streptococcus pyogenes extracellular cysteine protease and generation of antibodies that inhibit enzyme proteolytic activity. Infect Immun 67:4326-4333.
51. Smalley JW, Birss AJ, Withnall R, Silver J. 2002. Interactions of Porphyromonas gingivalis with oxyhaemoglobin and deoxyhaemoglobin. J Biochem 362:239-245. http://dx.doi.org/10.1042/0264-6021:3620239.
52. Lewis JP, Dawson JA, Hannis JC, Muddiman D, Macrina FL. 1999. Hemoglobinase activity of the lysine gingipain protease (Kgp) of Porphyromonas gingivalis W83. J Bacteriol 181:4905-4913.
53. Bramanti TE, Holt SC. 1991. Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50. J Bacteriol 173:7330-7339.
54. Smalley JW, Byrne DP, Birss AJ, Wojtowicz H, Sroka A, Potempa J, Olczak T. 2011. HmuY haemophore and gingipain proteases constitute a unique syntrophic system of haem acquisition by Porphyromonas gingivalis. PLoS One 6:e17182. http://dx.doi.org/10.1371/journal.pone.0017182.
55. Smalley JW, Silver J, Birss AJ, Withnall R, Titler PJ. 2003. The haem pigment of the oral anaerobes Prevotella nigrescens and Prevotella intermedia is composed of iron(III) protoporphyrin IX in the monomeric form. Microbiology 149:1711-1718. http://dx.doi.org/10.1099/mic.0.26258-0.
56. Byrne DP, Wawrzonek K, Jaworska A, Birss AJ, Potempa J, Smalley JW. 2010. Role of the cysteine protease interpain A of Prevotella intermedia in breakdown and release of haem from haemoglobin. Biochem J 425:257-264. http://dx.doi.org/10.1042/BJ20090343.
57. Popov SG, Popova TG, Hopkins S, Weinstein RS, MacAfee R, Fryxell KJ, Chandhoke V, Bailey C, Alibek K. 2005. Effective antiproteaseantibiotic treatment of experimental anthrax. BMC Infect Dis 5:25. http://dx.doi.org/10.1186/1471-2334-5-25.
58. Mukherjee DV, Tonry JH, Kim KS, Ramarao N, Popova TG, Bailey C, Popov S, Chung M-C. 2011. Bacillus anthracis protease InhA increases blood-brain barrier permeability and contributes to cerebral hemorrhages. PLoS One 6:e17921. http://dx.doi.org/10.1371/journal.pone.0017921.
59. Guillemet E, Cadot C, Tran S-L, Guinebretière M-H, Lereclus D, Ramarao N. 2010. The InhA metalloproteases of Bacillus cereus contribute concomitantly to virulence. J Bacteriol 192:286-294. http://dx.doi.org/10.1128/JB.00264-09.
60. Gominet M, Slamti L, Gilois N, Rose M, Lereclus D. 2001. Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence. Mol Microbiol 40:963-975. http://dx.doi.org/10.1046/j.1365-2958.2001.02440.x.
61. Rudner DZ, Ledeaux JR, Ireton K, Grossman AD. 1991. The spoOK locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J Bacteriol 173:1388-1398.
62. Shannon JG, Ross CL, Koehler TM, Rest RF. 2003. Characterization of anthrolysin O, the Bacillus anthracis cholesterol-dependent cytolysin. Infect Immun 71:3183-3189. http://dx.doi.org/10.1128/IAI.71.6.3183-3189.2003.
63. Maresso AW, Garufi G, Schneewind O. 2008. Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin. PLoS Pathog 4:e1000132. http://dx.doi.org/10.1371/journal.ppat.1000132.
64. Ekworomadu MT, Poor CB, Owens CP, Balderas MA, Fabian M, Olson JS, Murphy F, Balkabasi E, Honsa ES, He C, Goulding CW, Maresso AW. 2012. Differential function of lip residues in the mechanism and biology of an anthrax hemophore. PLoS Pathog 8:e1002559. http://dx.doi.org/10.1371/journal.ppat.1002559.
65. Balderas MA, Nobles CL, Honsa ES, Maresso AW. 2012. Hal is a Bacillus anthracis heme acquisition protein. J Bacteriol 194:5513-5521. http://dx.doi.org/10.1128/JB.00685-12.