Temporal transcriptional response during infection of type II alveolar epithelial cells with Francisella tularensis live vaccine strain (lvs) supports a general host suppression and bacterial uptake by macropinocytosis

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10780-10791

  Bradburne, Christopher E ^a,b   Verhoeven, Anne B ^c   Manyam, Ganiraju C ^c,d   Chaudhry, Saira A ^c   Chang, Eddie L ^a   Thach, Dzung C ^a,e   Bailey, Charles L ^c   Van Hoek, Monique L ^c  

^a NAVAL RESEARCH LABORATORY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c GEORGE MASON UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

AIRWAY EPITHELIAL CELLS; CYTOSKELETAL REARRANGEMENTS; DIFFERENTIAL GENE EXPRESSIONS; FRANCISELLA TULARENSIS; INTRACELLULAR TRANSPORT; POTENTIAL MECHANISM; TRANSCRIPTIONAL RESPONSE; TYPE II ALVEOLAR EPITHELIAL CELLS;

BACTERIA; CELL CULTURE; TISSUE; VACCINES;

CELLS;

AMILORIDE; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; INTERFERON;

ACTIN FILAMENT; ARTICLE; BACTERIAL STRAIN; CELL LINE; CELL STRAIN A549; CELL TRANSPORT; CONTROLLED STUDY; CYTOSKELETON; FRANCISELLA TULARENSIS; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; LIVE VACCINE STRAIN; LUNG ALVEOLUS EPITHELIUM; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TULAREMIA; UPREGULATION;

BACTERIAL VACCINES; CELL LINE; EPITHELIAL CELLS; FRANCISELLA TULARENSIS; GENE EXPRESSION REGULATION; HUMANS; PINOCYTOSIS; PULMONARY ALVEOLI; TIME FACTORS; TRANSCRIPTOME; TULAREMIA;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS; MURINAE;

EID: 84876262516     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.362178     Document Type: Article

References (80)

1. Dennis, D. T., Inglesby, T. V., Henderson, D. A., Bartlett, J. G., Ascher, M. S., Eitzen, E., Fine, A. D., Friedlander, A. M., Hauer, J., Layton, M., Lillibridge, S. R., McDade, J. E., Osterholm, M. T., O'Toole, T., Parker, G., Perl, T. M., Russell, P. K., Tonat, K., and Working Group on Civilian Biodefense (2001) Tularemia as a Biological Weapon. Medical and Public Health Management. JAMA 285, 2763-2773
2. Wu, T. H., Zsemlye, J. L., Statom, G. L., Hutt, J. A., Schrader, R. M., Scrymgeour, A. A., and Lyons, C. R. (2009) Vaccination of Fischer 344 rats against pulmonary infections by Francisella tularensis typeAstrains. Vaccine 27, 4684-4693
3. MacRedmond, R., Greene, C., Taggart, C. C., McElvaney, N., and O'Neill, S. (2005) Respiratory epithelial cells require Toll-like receptor 4 for induction of human β-defensin 2 by lipopolysaccharide. Respir. Res. 6, 116
4. Duits, L. A., Ravensbergen, B., Rademaker, M., Hiemstra, P. S., and Nibbering, P. H. (2002) Expression of β-defensin 1 and 2 mRNA by human monocytes, macrophages and dendritic cells. Immunology 106, 517-525
5. Sharma, J., Li, Q., Mishra, B. B., Pena, C., and Teale, J. M. (2009) Lethal pulmonary infection with Francisella novicida is associated with severe sepsis. J. Leukoc. Biol. 86, 491-504
6. Rohmer, L., Fong, C., Abmayr, S., Wasnick, M., Larson Freeman, T. J., Radey, M., Guina, T., Svensson, K., Hayden, H. S., Jacobs, M., Gallagher, L. A., Manoil, C., Ernst, R. K., Drees, B., Buckley, D., Haugen, E., Bovee, D., Zhou, Y., Chang, J., Levy, R., Lim, R., Gillett, W., Guenthener, D., Kang, A., Shaffer, S. A., Taylor, G., Chen, J., Gallis, B., D'Argenio, D. A., Forsman, M., Olson, M. V., Goodlett, D. R., Kaul, R., Miller, S. I., and Brittnacher, M. J. (2007) Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol. 8, R102
7. Drabick, J. J., Narayanan, R. B., Williams, J. C., Leduc, J. W., and Nacy, C. A. (1994) Passive protection of mice against lethal Francisella tularensis (live tularemia vaccine strain) infection by the sera of human recipients of the live tularemia vaccine. Am. J. Med. Sci. 308, 83-87
8. Waag, D. M., Sandstro?m, G., England, M. J., and Williams, J. C. (1996) Immunogenicity of a new lot of Francisella tularensis live vaccine strain in human volunteers. FEMS Immunol. Med. Microbiol. 13, 205-209
9. Saslaw, S., and Carhart, S. (1961) Studies with tularemia vaccines in volunteers. III. Serologic aspects following intracutaneous or respiratory challenge in both vaccinated and nonvaccinated volunteers. Am. J. Med. Sci. 241, 689-699
10. Saslaw, S., Eigelsbach, H. T., Prior, J. A., Wilson, H. E., and Carhart, S. (1961) Tularemia vaccine study. II. Respiratory challenge. Arch. Intern Med. 107, 702-714
11. Bolger, C. E., Forestal, C. A., Italo, J. K., Benach, J. L., and Furie, M. B. (2005) The live vaccine strain of Francisella tularensis replicates in human and murine macrophages but induces only the human cells to secrete proinflammatory cytokines. J. Leukocyte Biol. 77, 893-897
12. Elkins, K. L., Cowley, S. C., and Bosio, C. M. (2003) Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect. 5, 135-142
13. Shirey, K. A., Cole, L. E., Keegan, A. D., and Vogel, S. N. (2008) Francisella tularensis live vaccine strain induces macrophage alternative activation as a survival mechanism. J. Immunol. 181, 4159-4167
14. Cole, L. E., Santiago, A., Barry, E., Kang, T. J., Shirey, K. A., Roberts, Z. J., Elkins, K. L., Cross, A. S., and Vogel, S. N. (2008) Macrophage proinflammatory response to Francisella tularensis live vaccine strain requires coordination of multiple signaling pathways. J. Immunol. 180, 6885-6891
15. Hall, J. D., Craven, R. R., Fuller, J. R., Pickles, R. J., and Kawula, T. H. (2007) Francisella tularensis replicates within alveolar Type II epithelial cells in vitro and in vivo following Inhalation. Infect. Immun. 75, 1034-1039
16. Craven, R. R., Hall, J. D., Fuller, J. R., Taft-Benz, S., and Kawula, T. H. (2008) Francisella tularensis invasion of lung epithelial cells. Infect. Immun. 76, 2833-2842
17. Han, S., Bishop, B. M., and van Hoek, M. L. (2008) Antimicrobial activity of human β-defensins and induction by Francisella. Biochem. Biophys. Res. Commun. 371, 670-674
18. Lindemann, S. R., McLendon, M. K., Apicella, M. A., and Jones, B. D. (2007) An in vitro model system used to study adherence and invasion of Francisella tularensis live vaccine strain in nonphagocytic cells. Infect. Immun. 75, 3178-3182
19. Meier, O., Boucke, K., Hammer, S. V., Keller, S., Stidwill, R. P., Hemmi, S., and Greber, U. F. (2002) Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158, 1119-1131
20. Ahmad, S., Hunter, L., Qin, A., Mann, B. J., and van Hoek, M. L. (2010) Azithromycin effectiveness against intracellular infections of Francisella. BMC Microbiol. 10, 123
21. Reimers, M., and Carey, V. J. (2006) Bioconductor. An open source framework for bioinformatics and computational biology. Methods Enzymol. 411, 119-134
22. Gregory Alvord, W., Roayaei, J. A., Quin?ones, O. A., and Schneider, K. T. (2007) A microarray analysis for differential gene expression in the soybean genome using Bioconductor and R. Brief Bioinform. 8, 415-431
23. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B., and Speed, T. P. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15
24. Smyth, G. K. (2007) Limma: Linear Models for Microarray Data, 1st Ed., Springer, New York
25. Benjamini, Y., and Hochberg, Y. (2000)Onthe adaptive control of the false discovery rate in multiple testing with independent statistics. J. Educ. Behav. Stat. 25, 60-83
26. Roden, J. C., King, B. W., Trout, D., Mortazavi, A., Wold, B. J., and Hart, C. E. (2006) Mining gene expression data by interpreting principal components. BMC Bioinformatics 7, 194 Deleted in proof
27. Nikolsky, Y., Nikolskaya, T., and Bugrim, A. (2005) Biological networks and analysis of experimental data in drug discovery. Drug Discov. Today 10, 653-662
28. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002) Accurate normalization of real-time quantitative RTPCRdatabygeometricaveragingofmultipleinternalcontrolgenes. GenomeBiol. 3, RESEARCH0034.0031-RESEARCH0034.0011
29. Wehrly, T. D., Chong, A., Virtaneva, K., Sturdevant, D. E., Child, R., Edwards, J. A., Brouwer, D., Nair, V., Fischer, E. R., Wicke, L., Curda, A. J., Kupko, J. J., 3rd, Martens, C., Crane, D. D., Bosio, C. M., Porcella, S. F., and Celli, J. (2009) Intracellular biology and virulence determinants of Francisella tularensis revealed by transcriptional profiling inside macrophages. Cell Microbiol. 11, 1128-1150
30. Clemens, D. L., Lee, B.-Y., and Horwitz, M. A. (2005) Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect. Immun. 73, 5892-5902
31. Mares, C. A., Ojeda, S. S., Morris, E. G., Li, Q., and Teale, J. M. (2008) Initial delay in the immune response to Francisella tularensis is followed by hypercytokinemia characteristic of severe sepsis and correlating with upregulation and release of damage-associated molecular patterns. Infect. Immun. 76, 3001-3010
32. Reutershan, J., Morris, M. A., Burcin, T. L., Smith, D. F., Chang, D., Saprito, M. S., and Ley, K. (2006) Critical role of endothelial CXCR2 in LPSinduced neutrophil migration into the lung. J. Clin. Invest. 116, 695-702
33. Belperio, J. A., Keane, M. P., Burdick, M. D., Londhe, V., Xue, Y. Y., Li, K., Phillips, R. J., and Strieter, R. M. (2002) Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J. Clin. Invest. 110, 1703-1716
34. Li, H., Nookala, S., Bina, X. R., Bina, J. E., and Re, F. (2006) Innate immune response to Francisella tularensis is mediated by TLR2 and caspase-1 activation. J. Leukoc. Biol. 80, 766-773
35. Katz, J., Zhang, P., Martin, M., Vogel, S. N., and Michalek, S. M. (2006) Toll-like receptor 2 is required for inflammatory responses to Francisella tularensis LVS. Infect. Immun. 74, 2809-2816
36. Cole, L. E., Mann, B. J., Shirey, K. A., Richard, K., Yang, Y., Gearhart, P. J., Chesko, K. L., Viscardi, R. M., and Vogel, S. N. (2011) Role of TLR signaling in Francisella tularensis-LPS-induced, antibody-mediated protection against Francisella tularensis challenge. J. Leukoc. Biol. 90, 787-797
37. Cole, L. E., Laird, M. H., Seekatz, A., Santiago, A., Jiang, Z., Barry, E., Shirey, K. A., Fitzgerald, K. A., and Vogel, S. N. (2010) Phagosomal retention of Francisella tularensis results in TIRAP/Mal-independent TLR2 signaling. J. Leukoc. Biol. 87, 275-281
38. Cole, L. E., Shirey, K. A., Barry, E., Santiago, A., Rallabhandi, P., Elkins, K. L., Puche, A. C., Michalek, S. M., and Vogel, S. N. (2007) Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages. Infect. Immun. 75, 4127-4137
39. Cole, L. E., Elkins, K. L., Michalek, S. M., Qureshi, N., Eaton, L. J., Rallabhandi, P., Cuesta, N., and Vogel, S. N. (2006) Immunologic consequences of Francisella tularensis live vaccine strain infection. Role of the innate immune response in infection and immunity. J. Immunol. 176, 6888-6899
40. Razak, A. A., Ramadan, S. E., and el-Zawahry, K. (1990) Metabolism of selenium in a selenium-dependent bacterium. Biol. Trace Elem. Res. 25, 187-192
41. Stadtman, T. C., Davis, J. N., Zehelein, E., and Bo?ck, A. (1989) Biochemical and genetic analysis of Salmonella typhimurium and Escherichia coli mutants defective in specific incorporation of selenium into formate dehydrogenase and tRNAs. Biofactors 2, 35-44
42. Hrstka, R., Stuli'k, J., and Vojtesek, B. (2005) The role of MAPK signal pathways dring Francisella tularensis LVS infection-induced apoptosis in murine macrophages. Microbes Infect. 7, 619-625
43. Lai, X.-H., Golovliov, I., and Sjo?stedt, A. (2001) Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infect. Immun. 69, 4691-4694
44. Lai, X.-H., Golovliov, I., and Sjo?stedt, A (2004) Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis. Microb. Pathog. 37, 225-230
45. Lai, X.-H., and Sjo?stedt, A. (2003) Delineation of the molecular mechanisms of Francisella tularensis-induced apoptosis in murine macrophages. Infect. Immun. 71, 4642-4646
46. Rajaram, M. V., Ganesan, L. P., Parsa, K. V., Butchar, J. P., Gunn, J. S., and Tridandapani, S. (2006) Akt/protein kinase B modulates macrophage inflammatory response to Francisella infection and confers a survival advantage in mice. J. Immunol. 177, 6317-6324
47. Parsa, K. V., Butchar, J. P., Rajaram, M. V., Cremer, T. J., and Tridandapani, S. (2008) The tyrosine kinase Syk promotes phagocytosis of Francisella through the activation of Erk. Mol. Immunol. 45, 3012-3021
48. Parsa, K. V., Ganesan, L. P., Rajaram, M. V., Gavrilin, M. A., Balagopal, A., Mohapatra, N. P., Wewers, M. D., Schlesinger, L. S., Gunn, J. S., and Tridandapani, S. (2006) Macrophage pro-inflammatory response to Francisella novicida infection is regulated by SHIP. PLoS Pathog. 2, e71
49. Cremer, T. J., Butchar, J. P., and Tridandapani, S. (2011) Francisella subverts innate immune signaling. Focus on PI3K/Akt. Front. Microbiol. 5, 13
50. Asare, R., and Kwaik, Y. A. (2010) Exploitation of host cell biology and evasion of immunity by Francisella tularensis. Front. Microbiol. 1, 145
51. Rajaram, M. V., Butchar, J. P., Parsa, K. V., Cremer, T. J., Amer, A., Schlesinger, L. S., and Tridandapani, S. (2009) Akt and SHIP modulate Francisella escape from the phagosome and induction of the Fas-mediated death pathway. PLoS One 4, e7919
52. Butchar, J. P., Cremer, T. J., Clay, C. D., Gavrilin, M. A., Wewers, M. D., Marsh, C. B., Schlesinger, L. S., and Tridandapani, S. (2008) Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS One 3, e2924
53. Pei, L., Castrillo, A., Chen, M., Hoffmann, A., and Tontonoz, P. (2005) Induction of NR4A orphan nuclear receptor expression in macrophages in response to inflammatory stimuli. J. Biol. Chem. 280, 29256-29262
54. Lundequist, A., Calounova, G., Wensman, H., Ro?nnberg, E., and Pejler, G. (2011) Differential regulation of Nr4a subfamily nuclear receptors following mast cell activation. Mol. Immunol. 48, 1753-1761
55. Pei, L., Castrillo, A., and Tontonoz, P. (2006) Regulation of macrophage inflammatory gene expression by the orphan nuclear receptor Nur77. Mol. Endocrinol. 20, 786-794
56. Wilson, J. E., Katkere, B., and Drake, J. R. (2009) Francisella tularensis induces ubiquitin-dependent MHC class II degradation in activated macrophages. Infect. Immun. 77, 4953-4965
57. Akimana, C., Al-Khodor, S., and Abu Kwaik, Y. (2010) Host factors required for modulation of phagosome biogenesis and proliferation of Francisella tularensis within the cytosol. PLoS One 5, e11025
58. Veiga, E., and Cossart, P. (2005) Ubiquitination of intracellular bacteria. A new bacteria-sensing system? Trends Cell Biol. 15, 2-5
59. Perrin, A. J., Jiang, X., Birmingham, C. L., So, N. S., and Brumell, J. H. (2004) Recognition of bacteria in the cytosol of Mammalian cells by the ubiquitin system. Curr. Biol. 14, 806-811
60. Andersson, H., Hartmanová, B., Ryde'n, P., Noppa, L., Na?slund, L., and Sjo?stedt, A. (2006) A microarray analysis of the murine macrophage response to infection with Francisella tularensis LVS. J. Med. Microbiol. 55, 1023-1033
61. Garci'a-Pe'rez, B. E., Herna'ndez-Gonza'lez, J. C., Garci'a-Nieto, S., and Luna-Herrera, J. (2008) Internalization of a non-pathogenic mycobacteria by macropinocytosis in human alveolar epithelial A549 cells. Microb. Pathog. 45, 1-6
62. Koivusalo, M., Welch, C., Hayashi, H., Scott, C. C., Kim, M., Alexander, T., Touret, N., Hahn, K. M., and Grinstein, S. (2010) Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J. Cell Biol. 188, 547-563
63. Mariathasan, S., Weiss, D. S., Dixit, V. M., and Monack, D. M. (2005) Innate immunity against Francisella tularensis is dependent on the ASC/ caspase-1 axis. J. Exp. Med. 202, 1043-1049
64. Clemens, D. L., Lee, B. Y., and Horwitz, M. A. (2012) O-antigen-deficient Francisella tularensis live vaccine strain mutants are ingested via an aberrant form of loping phagocytosis and show altered kinetics of intracellular trafficking in human macrophages. Infect. Immun. 80, 952-967
65. Malik, M., Bakshi, C. S., McCabe, K., Catlett, S. V., Shah, A., Singh, R., Jackson, P. L., Gaggar, A., Metzger, D. W., Melendez, J. A., Blalock, J. E., and Sellati, T. J. (2007) Matrix metalloproteinase 9 activity enhances host susceptibility to pulmonary infection with type A and B strains of Francisella tularensis. J. Immunol. 178, 1013-1020
66. Ranjard, L., Nazaret, S., and Cournoyer, B. (2003) Freshwater bacteria can methylate selenium through the thiopurine methyltransferase pathway. Appl. Environ. Microbiol. 69, 3784-3790
67. Meibom, K. L., and Charbit, A. (2010) Francisella tularensis metabolism and its relation to virulence. Front. Microbiol. 1, 140
68. Nano, F. E., Zhang, N., Cowley, S. C., Klose, K. E., Cheung, K. K., Roberts, M. J., Ludu, J. S., Letendre, G. W., Meierovics, A. I., Stephens, G., and Elkins, K. L. (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J. Bacteriol. 186, 6430-6436
69. Stadtman, T. C. (2002) A gold mine of fascinating enzymes. Those remarkable, strictly anaerobic bacteria, Methanococcus vannielii and Clostridium sticklandii. J. Biol. Chem. 277, 49091-49100
70. Schmerk, C. L., Duplantis, B. N., Howard, P. L., and Nano, F. E. (2009) A Francisella novicida pdpA mutant exhibits limited intracellular replication and remains associated with the lysosomal marker LAMP-1. Microbiology 155, 1498-1504
71. Shin, S., and Roy, C. R. (2008) Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell. Microbiol. 10, 1209-1220
72. Telepnev, M., Golovliov, I., and Sjo?stedt, A. (2005) Francisella tularensis LVS initially activates but subsequently down-regulates intracellular signaling and cytokine secretion in mouse monocytic and human peripheral blood mononuclear cells. Microb. Pathog. 38, 239-247
73. Orth, K., Xu, Z., Mudgett, M. B., Bao, Z. Q., Palmer, L. E., Bliska, J. B., Mangel, W. F., Staskawicz, B., and Dixon, J. E. (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290, 1594-1597
74. Orth, K., Palmer, L. E., Bao, Z. Q., Stewart, S., Rudolph, A. E., Bliska, J. B., and Dixon, J. E. (1999) Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285, 1920-1923
75. Chong, A., and Celli, J. (2010) The Francisella intracellular life cycle. Toward molecular mechanisms of intracellular survival and proliferation. Front. Microbiol. 1, 138
76. Swanson, J. A. (2008) Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 9, 639-649
77. Law, H. T., Lin, A. E., Kim, Y., Quach, B., Nano, F. E., and Guttman, J. A. (2011) Francisella tularensis uses cholesterol and clathrin-based endocytic mechanisms to invade hepatocytes. Sci. Rep. 1, 192
78. García-Pe'rez, B. E., Mondrago'n-Flores, R., and Luna-Herrera, J. (2003) Internalization of Mycobacterium tuberculosis by macropinocytosis in non-phagocytic cells. Microb. Pathog. 35, 49-55
79. Haraga, A., Ohlson, M. B., and Miller, S. I. (2008) Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6, 53-66
80. Schroeder, G. N., and Hilbi, H. (2008) Molecular pathogenesis of Shigella spp. Controlling host cell signaling, invasion, and death by Type III secretion. Clin. Microbiol. Rev. 21, 134-156