Bacillus anthracis spore interactions with mammalian cells: Relationship between germination state and the outcome of in vitro

BMC Microbiology

Volumn 11, Issue , 2011, Pages

  Gut, Ian M ^a   Tamilselvam, Batcha ^a   Prouty, Angela M ^a,b   Stojkovic, Bojana ^a,c   Czeschin, Stephanie ^a   Van Der Donk, Wilfred A ^a   Blanke, Steven R ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NAVAL MEDICAL RESEARCH CENTER   (United States)

^c Parkland College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE SERUM ALBUMIN;

ANIMAL CELL; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL SPORE; BACTERIAL VIABILITY; BACTERIUM CULTURE; CELL CULTURE; CONTROLLED STUDY; HOST CELL; IN VITRO STUDY; MACROPHAGE; MAMMAL CELL; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; SPORE GERMINATION; ANIMAL; CATTLE; CELL LINE; CELL SURVIVAL; CHEMISTRY; COMPARATIVE STUDY; CULTURE MEDIUM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY; SERUM;

BACILLUS ANTHRACIS; BOVINAE; MAMMALIA;

ANIMALS; BACILLUS ANTHRACIS; CATTLE; CELL LINE; CELL SURVIVAL; CULTURE MEDIA; CULTURE MEDIA, CONDITIONED; MACROPHAGES; MICE; MICROBIAL VIABILITY; SERUM; SPORES, BACTERIAL;

EID: 79952044522     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-11-46     Document Type: Article

References (54)

1. Anthrax. TC Dixon M Meselson J Guillemin PC Hanna, N Engl J Med 1999 341 11 815 826 10.1056/NEJM199909093411107 10477781 (Pubitemid 29420478)
2. Contribution of toxins to the pathogenesis of inhalational anthrax. JN Tournier A Quesnel-Hellmann A Cleret DR Vidal, Cell Microbiol 2007 9 3 555 565 10.1111/j.1462-5822.2006.00866.x 17223930 (Pubitemid 46231963)
3. Pathophysiology of anthrax. AE Frankel SR Kuo D Dostal L Watson NS Duesbery CP Cheng HJ Cheng SH Leppla, Front Biosci 2009 14 4516 4524 10.2741/3544 19273366
4. The use of a model of in vivo macrophage depletion to study the role of macrophages during infection with Bacillus anthracis spores. CK Cote KM Rea SL Norris N van Rooijen SL Welkos, Microb Pathog 2004 37 4 169 175 10.1016/j.micpath.2004.06.013 15458777 (Pubitemid 39349040)
5. Roles of macrophages and neutrophils in the early host response to Bacillus anthracis spores in a mouse model of infection. CK Cote N Van Rooijen SL Welkos, Infect Immun 2006 74 1 469 480 10.1128/IAI.74.1.469-480.2006 16369003 (Pubitemid 43023102)
6. Detection of Bacillus anthracis spore germination in vivo by bioluminescence imaging. P Sanz LD Teel F Alem HM Carvalho SC Darnell AD O'Brien, Infect Immun 2008 76 3 1036 1047 10.1128/IAI.00985-07 18195028 (Pubitemid 351428063)
7. Observations on the prophylaxis of experimental pulmonary anthrax in the monkey. DW Henderson S Peacock FC Belton, J Hyg (Lond) 1956 54 1 28 36 10.1017/S0022172400044272 13319688
8. Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. A Cleret A Quesnel-Hellmann A Vallon-Eberhard B Verrier S Jung D Vidal J Mathieu JN Tournier, J Immunol 2007 178 12 7994 8001 17548636 (Pubitemid 46898070)
9. Transport of Bacillus anthracis from the lungs to the draining lymph nodes is a rapid process facilitated by CD11c+ cells. LM Shetron-Rama AC Herring-Palmer GB Huffnagle P Hanna, Microb Pathog 2010 49 1-2 38 46 10.1016/j.micpath.2010.02.004 20188814
10. Potential dissemination of Bacillus anthracis utilizing human lung epithelial cells. BH Russell R Vasan DR Keene TM Koehler Y Xu, Cell Microbiol 2008 10 4 945 957 10.1111/j.1462-5822.2007.01098.x 18067609 (Pubitemid 351386949)
11. Bacillus anthracis internalization by human fibroblasts and epithelial cells. BH Russell R Vasan DR Keene Y Xu, Cell Microbiol 2007 9 5 1262 1274 10.1111/j.1462-5822.2006.00869.x 17474904 (Pubitemid 46547143)
12. In vivo demonstration and quantification of intracellular Bacillus anthracis in lung epithelial cells. BH Russell Q Liu SA Jenkins MJ Tuvim BF Dickey Y Xu, Infect Immun 2008 76 9 3975 3983 10.1128/IAI.00282-08 18625737
13. Early Bacillus anthracis-macrophage interactions: intracellular survival survival and escape. TC Dixon AA Fadl TM Koehler JA Swanson PC Hanna, Cell Microbiol 2000 2 6 453 463 10.1046/j.1462-5822.2000.00067.x 11207600 (Pubitemid 32049317)
14. Macrophage interactions. C Guidi-Rontani M Mock, Curr Top Microbiol Immunol 2002 271 115 141 12224520 (Pubitemid 34847397)
15. The alveolar macrophage: the Trojan horse of Bacillus anthracis. C Guidi-Rontani, Trends Microbiol 2002 10 9 405 409 10.1016/S0966-842X(02)02422-8 12217505 (Pubitemid 35246267)
16. Fate of germinated Bacillus anthracis spores in primary murine macrophages. C Guidi-Rontani M Levy H Ohayon M Mock, Mol Microbiol 2001 42 4 931 938 10.1046/j.1365-2958.2001.02695.x 11737637 (Pubitemid 33078377)
17. Cytokine response to infection with Bacillus anthracis spores. AK Pickering M Osorio GM Lee VK Grippe M Bray TJ Merkel, Infect Immun 2004 72 11 6382 6389 10.1128/IAI.72.11.6382-6389.2004 15501768 (Pubitemid 39425419)
18. Macrophages release tumor necrosis factor alpha and interleukin-12 in response to intracellular Bacillus anthracis spores. AK Pickering TJ Merkel, Infect Immun 2004 72 5 3069 3072 10.1128/IAI.72.5.3069-3072.2004 15102824 (Pubitemid 38542442)
19. Time-lapse confocal imaging of development of Bacillus anthracis in macrophages. G Ruthel WJ Ribot S Bavari TA Hoover, J Infect Dis 2004 189 7 1313 1316 10.1086/382656 15031802 (Pubitemid 38457258)
20. In-vitro characterisation of the phagocytosis and fate of anthrax spores in macrophages and the effects of anti-PA antibody. S Welkos A Friedlander S Weeks S Little I Mendelson, J Med Microbiol 2002 51 10 821 831 12435060 (Pubitemid 35222782)
21. Murine macrophages kill the vegetative form of Bacillus anthracis. TJ Kang MJ Fenton MA Weiner S Hibbs S Basu L Baillie AS Cross, Infect Immun 2005 73 11 7495 7501 10.1128/IAI.73.11.7495-7501.2005 16239551 (Pubitemid 41587654)
22. Inactivation of Bacillus anthracis spores in murine primary macrophages. H Hu Q Sa TM Koehler AI Aronson D Zhou, Cell Microbiol 2006 8 10 1634 1642 10.1111/j.1462-5822.2006.00738.x 16984418 (Pubitemid 44350022)
23. Germination of Bacillus anthracis spores within alveolar macrophages. C Guidi-Rontani M Weber-Levy E Labruyere M Mock, Mol Microbiol 1999 31 1 9 17 10.1046/j.1365-2958.1999.01137.x 9987105 (Pubitemid 29012143)
24. Postexposure prophylaxis against experimental inhalation anthrax. AM Friedlander SL Welkos ML Pitt JW Ezzell PL Worsham KJ Rose BE Ivins JR Lowe GB Howe P Mikesell WB Lawrence, J Infect Dis 1993 167 5 1239 1243 8486963 (Pubitemid 23115626)
25. Primary involvement of pharynx and peyer's patch in inhalational and intestinal anthrax. IJ Glomski A Piris-Gimenez M Huerre M Mock PL Goossens, PLoS Pathog 2007 3 6 76 10.1371/journal.ppat.0030076 17542645
26. Capsule synthesis by Bacillus anthracis is required for dissemination in murine inhalation anthrax. M Drysdale S Heninger J Hutt Y Chen CR Lyons TM Koehler, Embo J 2005 24 1 221 227 10.1038/sj.emboj.7600495 15616593 (Pubitemid 40188479)
27. The pathology of experimental anthrax in rabbits exposed by inhalation and subcutaneous inoculation. GM Zaucha LM Pitt J Estep BE Ivins AM Friedlander, Arch Pathol Lab Med 1998 122 11 982 992 9822127 (Pubitemid 28521045)
28. CD14-Mac-1 interactions in Bacillus anthracis spore internalization by macrophages. C Oliva CL Turnbough Jr JF Kearney, Proc Natl Acad Sci USA 2009 106 33 13957 13962 10.1073/pnas.0902392106 19666536
29. The integrin Mac-1 (CR3) mediates internalization and directs Bacillus anthracis spores into professional phagocytes. CR Oliva MK Swiecki CE Griguer MW Lisanby DC Bullard CL Turnbough Jr JF Kearney, Proc Natl Acad Sci USA 2008 105 4 1261 1266 10.1073/pnas.0709321105 18216258 (Pubitemid 351397041)
30. Gene expression profiling of human alveolar macrophages infected by B. anthracis spores demonstrates TNF- and NF-b are key components of the innate immune response to the pathogen. M Dozmorov W Wu K Chakrabarty JL Booth RE Hurst KM Coggeshall JP Metcalf, BMC Infect Dis 2009 9 152 10.1186/1471-2334-9-152 19744333
31. Bacillus anthracis spore entry into epithelial cells is an actin-dependent process requiring c-Src and PI3K. Q Xue SA Jenkins C Gu E Smeds Q Liu R Vasan BH Russell Y Xu, PLoS One 2010 5 7 11665 10.1371/journal.pone. 0011665 20652027
32. Factors involved in the germination and inactivation of Bacillus anthracis spores in murine primary macrophages. H Hu J Emerson AI Aronson, FEMS Microbiol Lett 2007 272 2 245 250 10.1111/j.1574-6968.2007.00766.x 17521404 (Pubitemid 47074612)
33. Murine macrophage transcriptional responses to Bacillus anthracis infection and intoxication. NH Bergman KD Passalacqua R Gaspard LM Shetron-Rama J Quackenbush PC Hanna, Infect Immun 2005 73 2 1069 1080 10.1128/IAI.73.2.1069- 1080.2005 15664951 (Pubitemid 40165768)
34. Modulation of cytokine production and enhancement of cell viability by TLR7 and TLR9 ligands during anthrax infection of macrophages. M Sabet HB Cottam DG Guiney, FEMS Immunol Med Microbiol 2006 47 3 369 379 10.1111/j.1574-695X. 2006.00096.x 16872373 (Pubitemid 44035887)
35. Spore germination. P Setlow, Curr Opin Microbiol 2003 6 6 550 556 10.1016/j.mib.2003.10.001 14662349 (Pubitemid 38020050)
36. Spore germination. A Moir BM Corfe J Behravan, Cell Mol Life Sci 2002 59 3 403 409 10.1007/s00018-002-8432-8 11964118 (Pubitemid 34267380)
37. How do spores germinate? A Moir, J Appl Microbiol 2006 101 3 526 530 10.1111/j.1365-2672.2006.02885.x 16907803 (Pubitemid 44222283)
38. Sequence of events during Bacillus megaterim spore germination. HS Levinson MT Hyatt, J Bacteriol 1966 91 5 1811 1818 4957022
39. Inhibition of Bacillus anthracis spore outgrowth by nisin. IM Gut AM Prouty JD Ballard WA van der Donk SR Blanke, Antimicrob Agents Chemother 2008 52 12 4281 4288 10.1128/AAC.00625-08 18809941
40. Macrophage-enhanced germination of Bacillus anthracis endospores requires gerS. JA Ireland PC Hanna, Infect Immun 2002 70 10 5870 5872 10.1128/IAI.70.10.5870-5872.2002 12228320
41. Characterization of Bacillus anthracis germinant receptors in vitro. N Fisher P Hanna, J Bacteriol 2005 187 23 8055 8062 10.1128/JB.187.23.8055-8062. 2005 16291679 (Pubitemid 41691699)
42. Germination of Bacillus cereus spores in response to L-alanine and to inosine: the roles of gerL and gerQ operons. PJ Barlass CW Houston MO Clements A Moir, Microbiology 2002 148 Pt 7 2089 2095 12101297 (Pubitemid 34785293)
43. Amino acid- and purine ribonucleoside-induced germination of Bacillus anthracis Sterne endospores: gerS mediates responses to aromatic ring structures. JA Ireland PC Hanna, J Bacteriol 2002 184 5 1296 1303 10.1128/JB.184.5.1296-1303.2002 11844758 (Pubitemid 34157551)
44. Role of ger proteins in nutrient and nonnutrient triggering of spore germination in Bacillus subtilis. M Paidhungat P Setlow, J Bacteriol 2000 182 9 2513 2519 10.1128/JB.182.9.2513-2519.2000 10762253 (Pubitemid 30212910)
45. Identification and characterization of the gerH operon of Bacillus anthracis endospores: a differential role for purine nucleosides in germination. MA Weiner TD Read PC Hanna, J Bacteriol 2003 185 4 1462 1464 10.1128/JB.185.4.1462-1464.2003 12562819 (Pubitemid 36176881)
46. High-throughput, single-cell analysis of macrophage interactions with fluorescently labeled Bacillus anthracis spores. B Stojkovic EM Torres AM Prouty HK Patel L Zhuang TM Koehler JD Ballard SR Blanke, Appl Environ Microbiol 2008 74 16 5201 5210 10.1128/AEM.02890-07 18552183
47. Anthrax toxin receptor 2 mediates Bacillus anthracis killing of macrophages following spore challenge. DJ Banks M Barnajian FJ Maldonado-Arocho AM Sanchez KA Bradley, Cell Microbiol 2005 7 8 1173 1185 10.1111/j.1462-5822. 2005.00545.x 16008584 (Pubitemid 41030942)
48. Bacillus anthracis endospores regulate ornithine decarboxylase and inducible nitric oxide synthase through ERK1/2 and p38 mitogen-activated protein kinases. S Porasuphatana GL Cao P Tsai F Tavakkoli T Huwar L Baillie AS Cross P Shapiro GM Rosen, Curr Microbiol 2010 61 6 567 573 10.1007/s00284-010-9654-x 20440620
49. Regulatory interactions of a virulence-associated serine/threonine phosphatase-kinase pair in Bacillus anthracis. SM Shakir KM Bryant JL Larabee EE Hamm J Lovchik CR Lyons JD Ballard, J Bacteriol 2010 192 2 400 409 10.1128/JB.01221-09 19915022
50. Effects of endogenous D-alanine synthesis and autoinhibition of Bacillus anthracis germination on in vitro and in vivo infections. MT McKevitt KM Bryant SM Shakir JL Larabee SR Blanke J Lovchik CR Lyons JD Ballard, Infect Immun 2007 75 12 5726 5734 10.1128/IAI.00727-07 17923523 (Pubitemid 350207810)
51. Transcriptional profiling of Bacillus anthracis during infection of host macrophages. NH Bergman EC Anderson EE Swenson BK Janes N Fisher MM Niemeyer AD Miyoshi PC Hanna, Infect Immun 2007 75 7 3434 3444 10.1128/IAI.01345-06 17470545 (Pubitemid 47040944)
52. Current Protocols in Immunology. JE Coligan, Hoboken: John Wiley & Sons 1991
53. The use of fluorescence quenching in flow cytofluorometry to measure the attachment and ingestion phases in phagocytosis in peripheral blood without prior cell separation. J Hed G Hallden SG Johansson P Larsson, J Immunol Methods 1987 101 1 119 125 10.1016/0022-1759(87)90224-9 3112235 (Pubitemid 17097906)
54. Analysis of extreme values. W Dixon, Ann Math Stat 1950 21 488 506 10.1214/aoms/1177729747