RNAseq reveals hypervirulence-specific host responses to M. Tuberculosis infection

Virulence

Volumn 8, Issue 6, 2017, Pages 848-858

  Leisching, Gina ^a   Pietersen, Ray Dean ^a   van Heerden, Carel ^b   van Helden, Paul ^a   Wiid, Ian ^a   Baker, Bienyameen ^a  

^a UNIVERSITY OF STELLENBOSCH   (South Africa)

^b STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Host response; Infection; Mycobacterium tuberculosis; RNAseq; Virulence

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; INTERLEUKIN 1 ANTIBODY; INTERLEUKIN 12P40; INTERLEUKIN 1B; INTERLEUKIN 6; PATTERN RECOGNITION RECEPTOR; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; GADD45A PROTEIN, MOUSE; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; IRF3 PROTEIN, MOUSE; IRF7 PROTEIN, MOUSE; NUCLEAR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL SECRETION SYSTEM; BACTERIAL VIRULENCE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; EARLY RESPONSE GENE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOUSE; MRNA EXPRESSION LEVEL; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS GENE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; SERIAL ANALYSIS OF GENE EXPRESSION; TUBERCULOSIS; WESTERN BLOTTING; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MACROPHAGE; MICROBIOLOGY; PATHOGENICITY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIRULENCE;

ANIMALS; BLOTTING, WESTERN; CELL CYCLE PROTEINS; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTOR-7; MACROPHAGES; MICE; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUBERCULOSIS; VIRULENCE;

EID: 84994570945     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.1080/21505594.2016.1250994     Document Type: Article

References (41)

1. Ehlers MRW, Daffe M. Interactions between Mycobacterium tuberculosis and host cells:are mycobacterial sugars the key? Trends Microbiol 1998; 6:328-335; https://doi.org/10.1016/S0966-842X(98)01301-8
2. Reiling N, Homolka S, Walter K, Brandenburg J, Niwin-ski L, Ernst M, Herzmann C, Lange C, Diel R, Ehlers S, et al. Clade-specific virulence patterns of Mycobacterium tuberculosis complex strains in human primary macro-phages and aerogenically infected mice. MBio 2013; 4:e00250-00213; https://doi.org/10.1128/mBio.00250-13
3. Wu K, Dong D, Fang H, Levillain F, Jin W, Mei J, Gic-quel B, Du Y, Wang K, Gao Q, et al. An interferon-related signature in the transcriptional core response of human macrophages to Mycobacterium tuberculosis infection. PLoS One 2012; 7:e38367; https://doi.org/10.1371/journal.pone.0038367
4. Manca C, Tsenova L, Barry CE 3rd, Bergtold A, Freeman S, Haslett PA, Musser JM, Freedman VH, Kaplan G. Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. J Immunol 1999; 162:6740-6;
5. Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, Musser JM, Barry CE 3rd, Freedman VH, Kaplan G. Vir-ulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immu-nity and is associated with induction of IFN-a /b. Proc Natl Acad Sci U S A 2001; 98:5752-7; https://doi.org/10.1073/pnas.091096998
6. Reed MB, Domenech P, Manca C, Su H, Barczak AK, Kreiswirth BN, Kaplan G, Barry CE 3rd. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 2004; 430:84-7
7. Sinsimer D, Huet G, Manca C, Tsenova L, Koo MS, Kurepina N, Kana B, Mathema B, Marras SA, Kreiswirth BN, et al. The phenolic glycolipid of Mycobacterium tubercu-losis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 2008; 76:3027-36; https://doi.org/10.1128/IAI.01663-07
8. Hernandez-Pando R, Marquina-Castillo B, Barrios-Payan J, Mata-Espinosa D. Use of mouse models to study the vari-ability in virulence associated with specific genotypic lineages of Mycobacterium tuberculosis. Infect Genet Evol 2012; 12:725-31; https://doi.org/10.1016/j.meegid.2012.02.013
9. Meissner-Roloff RJ, Koekemoer G, Warren RM. A metabolomics investigation of a hyper-and hypo-virulent phenotype of Beijing lineage M. tuberculosis. Metabolomics 2012; 8:1194-203; https://doi.org/10.1007/s11306-012-0424-6
10. de Souza GA, Fortuin S, Aguilar D, Pando RH, McEvoy CR, van Helden PD, Koehler CJ, Thiede B, Warren RM, et al. Using a label-free proteomics method to identify differen-tially abundant proteins in closely related hypo-and hyper-virulent clinical Mycobacterium tuberculosis Beijing isolates. Mol Cell Proteomics 2010; 9:2414-23; https://doi.org/10.1074/mcp.M900422-MCP200
11. Aguilar D, Hanekom M, Mata D, Gey van Pittius NC, van Helden PD, Warren RM, Hernandez-Pando R. Mycobacte-rium tuberculosis strains with the Beijing genotype demon-strate variability in virulence associated with transmission. Tuberculosis 2010; 90:319-25; https://doi.org/10.1016/j.tube.2010.08.004
12. Liebermann DA, Hoffman B. Gadd45 in stress signaling. J Mol Signal 2008; 3:15; https://doi.org/10.1186/1750-2187-3-15
13. Salvador JM, Brown-Clay JD, Fornace AJ Jr. in Gadd45 Stress Sensor Genes 1-19 (Springer, 2013)
14. Lee MS, Kim B, Oh GT, Kim YJ. OASL1 inhibits transla-tion of the type I interferon-regulating transcription fac-tor IRF7. Nat Immunol 2013; 14:346-55; https://doi.org/10.1038/ni.2535
15. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, Wilkinson KA, Banchereau R, Skinner J, Wilkinson RJ, et al. An interferon-inducible neutrophil-driven blood transcrip-tional signature in human tuberculosis. Nature 2010; 466:973-7; https://doi.org/10.1038/nature09247
16. Ordway D, Henao-Tamayo M, Harton M, Palanisamy G, Troudt J, Shanley C, Basaraba RJ, Orme IM. The hyperviru-lent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 2007; 179:522-31; https://doi.org/10.4049/jimmunol.179.1.522
17. Stanley SA, Johndrow JE, Manzanillo P, Cox JS. The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 2007; 178:3143-52; https://doi.org/10.4049/jimmunol.178.5.3143
18. Bost KL, Clements JD. Intracellular Salmonella dublin induces substantial secretion of the 40-kgdalton subunit of interleukin-12 (IL-12) but minimal secretion of IL-12 as a 70-kgdalton protein in murine macrophages. Infect Immun 1997; 65:3186-92;
19. Cooper A, Roberts AD, Rhoades ER, Callahan JE, Getzy DM, Orme IM. The role of interleukin-12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology 1995; 84:423;
20. Flynn J, Goldstein MM, Triebold KJ, Sypek J, Wolf S, Bloom BR. IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis infection. J Immunol 1995; 155:2515-24;
21. Khader SA, Pearl JE, Sakamoto K, Gilmartin L, Bell GK, Jelley-Gibbs DM, Ghilardi N, deSauvage F, Cooper AM. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-g responses if IL-12p70 is available. J Immunol 2005; 175:788-95; https://doi.org/10.4049/jimmunol.175.2.788
22. Mattner F, Fischer S, Guckes S, Jin S, Kaulen H, Schmitt E, Rude E, Germann T. The interleukin 12 subunit p40 specifically inhibits effects of the interleukin 12 hetero-dimer. Euro J Immunol 1993; 23:2202-8; https://doi.org/10.1002/eji.1830230923
23. Shimozato O, Ugai S, Chiyo M, Takenobu H, Naga-kawa H, Wada A, Kawamura K, Yamamoto H, Tagawa M. The secreted form of the p40 subunit of interleukin (IL) 12 inhibits IL 23 functions and abrogates IL 23 mediated antitumour effects. Immunology 2006; 117:22-8; https://doi.org/10.1111/j.1365-2567.2005.02257.x
24. Arlt A, Schafer H. Role of the immediate early response 3 (IER3) gene in cellular stress response, inflammation and tumorigenesis. Eur J Cell Biol 2011; 90:545-52; https://doi.org/10.1016/j.ejcb.2010.10.002
25. Schott J, Reitter S, Philipp J, Haneke K, Schafer H, Stoecklin G. Translational Regulation of Specific mRNAs Controls Feedback Inhibition and Survival during Mac-rophage Activation. PLoS Genet 2014; 10:e1004368; https://doi.org/10.1371/journal.pgen.1004368
26. Vinuesa CG, Preiss T. Inflammation:Gone with Translation. PLoS Genet 2014; 10:e1004442
27. Koo MS, Manca C, Yang G, O’Brien P, Sung N, Tsenova L, Subbian S, Fallows D, Muller G, Ehrt S, et al. Phospho-diesterase 4 inhibition reduces innate immunity and improves isoniazid clearance of Mycobacterium tuberculosis in the lungs of infected mice. PLoS One 2011; 6:e17091
28. Essone PN, Chegou NN, Loxton AG, Stanley K, Kriel M, van der Spuy G, Franken KL, Ottenhoff TH, Walzl G. Host cytokine responses induced after overnight stimula-tion with novel M. tuberculosis infection phase-depen-dent antigens show promise as diagnostic candidates for TB disease. PLoS One 2014; 9:e102584
29. Song C, Hsu K, Yamen E, Yan W, Fock J, Witting PK, Geczy CL, Freedman SB. Serum amyloid A induction of cytokines in monocytes/macrophages and lymphocytes. Atherosclerosis 2009; 207:374-83; https://doi.org/10.1016/j.atherosclerosis.2009.05.007
30. Nishimura J, Saiga H, Sato S, Okuyama M, Kayama H, Kuwata H, Matsumoto S, Nishida T, Sawa Y, Akira S, et al. Potent antimycobacterial activity of mouse secretory leukocyte protease inhibitor. J Immunol 2008; 180:4032-9; https://doi.org/10.4049/jimmunol.180.6.4032.
31. Gomez SA, Arguelles CL, Guerrieri D, Tateosian NL, Amiano NO, Slimovich R, Maffia PC, Abbate E, Musella RM, Garcia VE, et al. Secretory leukocyte protease inhibitor:a secreted pat-tern recognition receptor for mycobacteria. Am J Respir Crit Care Med 2009; 179:247-53; https://doi.org/10.1164/rccm.200804-615OC
32. Beisiegel M, Mollenkopf HJ, Hahnke K, Koch M, Dietrich I, Reece ST, Kaufmann SH. Combination of host susceptibility and Mycobacterium tuberculosis virulence define gene expression profile in the host. Euro J Immunol 2009; 39:3369-84; https://doi.org/10.1002/eji.200939615
33. Fakioglu E, Wilson SS, Mesquita PM, Hazrati E, Cheshenko N, Blaho JA, Herold BC. Herpes simplex virus downregu-lates secretory leukocyte protease inhibitor:a novel immune evasion mechanism. J Virol 2008; 82:9337-44; https://doi.org/10.1128/JVI.00603-08
34. Jin FY, Nathan C, Radzioch D, Ding A. Secretory leukocyte protease inhibitor:A macrophage product induced by and antagonistic to bacterial lipopolysaccharide. Cell 1997; 88:417-26; https://doi.org/10.1016/S0092-8674(00)81880-2
35. Lee MS, Park CH, Jeong YH, Kim YJ, Ha SJ. Negative regulation of type I IFN expression by OASL1 permits chronic viral infection and CD8 (C) T-cell exhaustion. PLoS Pathog 2013; 9:e1003478; https://doi.org/10.1371/journal.ppat.1003478
36. Zhu J, Ghosh A, Sarkar SN. OASL—a new player in con-trolling antiviral innate immunity. Curr Opin Virol 2015; 12:15-9; https://doi.org/10.1016/j.coviro.2015.01.010
37. Papatriantafyllou M. Cytokines:IRF7 lost in translation. Nat Rev Immunol 2013; 13:221; https://doi.org/10.1038/nri3425
38. Etna MP, Giacomini E, Pardini M, Severa M, Bottai D, Cruciani M, Rizzo F, Calogero R, Brosch R, Coccia EM. Impact of Mycobacterium tuberculosis RD1-locus on human primary dendritic cell immune functions. Sci Rep 2015; 5:17078; https://doi.org/10.1038/srep17078
39. de Chastellier C, Lang T, Thilo L. Phagocytic processing of the macrophage endoparasite, Mycobacterium avium, in comparison to phagosomes which contain Bacillus subtilis or latex beads. Eur J Cell Biol 1995; 68:167-82;
40. Leisching G, Pietersen RD, Mpongoshe V, van Heerden C, van Helden P, Wiid I, Baker B. The Host Response to a Clinical MDR Mycobacterial Strain Cultured in a Detergent-Free Environment:A Global Transcriptomics Approach. PLoS One 2016; 11:e0153079; https://doi.org/10.1371/journal.pone.0153079
41. Leisching G, Pietersen RD, Wiid I, Baker B. Virulence, biochemistry, morphology and host-interacting properties of detergent-free cultured mycobacteria:An update. Tuberculosis 2016; 100:53-60; https://doi.org/10.1016/j.tube.2016.07.002