The truncated Rv2820c of Mycobacterium tuberculosis Beijing family augments intracellular survival of M. smegmatis by altering cytokine profile and inhibiting NO generation

The truncated Rv2820c of Mycobacterium tuberculosis Beijing family augments intracellular... Genetic variations among genes of Mycobacterium tuberculosis may be associated with antigenic variation and immune evasion, which complicates the pathogenesis of M. tuberculosis. The hyper-virulent M. tuberculosis Beijing strains harbored several large sequence deletions, among which RD207 attributed to the deletion of CRISPR loci and several Cas genes. RD207 also gave rise to a truncated gene Rv2820c-Bj with 60% deletion in length at the 3′-end and a new 3′-end of five amino acid mutations. It has been reported that Rv2820c-Bj correlated with enhanced intracellular survival of M. smegmatis in macrophages when compared to its full-length counterpart Rv2820c in M. tuberculosis, however, the respective contribution of the truncation and the new 3′-end of Rv2820c-Bj to this enhancement was unclear. Here, by infecting THP-1 macrophages with Ms_Rv2820c-Bj, Ms_Rv2820c and MS_Rv2820c-Tr (expressing the truncated Rv2820c without five amino acid mutations at 3′-end), we found only Ms_Rv2820c-Bj was responsible for the enhancement of survival of M. smegmatis in macrophages. Furthermore, we detected that Ms_Rv2820c-Tr and Ms_Rv2820c-Bj induced similar cytokine profile and NO production after infection of macrophages, which was distinctly different from Ms_Rv2820c. However, Ms_Rv2820c-Bj evoked higher levels of interleukin-10 (IL-10) and lower levels of interleukin- 6 (IL-6), interleukin-1β (IL-1β) and interleukin-12 (IL-12) in infected THP-1 macrophages than Ms_Rv2820c-Tr. Accordingly, we concluded that the new 3′-end of Rv2820c-Bj was important to dampen host defense and enhance the intracellular survival of M. smegmatis. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Infection, Genetics and Evolution Elsevier

The truncated Rv2820c of Mycobacterium tuberculosis Beijing family augments intracellular survival of M. smegmatis by altering cytokine profile and inhibiting NO generation

9 pages
Read Article

Loading next page...
 
/lp/elsevier/the-truncated-rv2820c-of-mycobacterium-tuberculosis-beijing-family-Ws1GfofQkj
Publisher
Elsevier
Copyright
Copyright © 2018 Elsevier B.V.
ISSN
1567-1348
D.O.I.
10.1016/j.meegid.2018.01.027
Publisher site
See Article on Publisher Site

Abstract

Genetic variations among genes of Mycobacterium tuberculosis may be associated with antigenic variation and immune evasion, which complicates the pathogenesis of M. tuberculosis. The hyper-virulent M. tuberculosis Beijing strains harbored several large sequence deletions, among which RD207 attributed to the deletion of CRISPR loci and several Cas genes. RD207 also gave rise to a truncated gene Rv2820c-Bj with 60% deletion in length at the 3′-end and a new 3′-end of five amino acid mutations. It has been reported that Rv2820c-Bj correlated with enhanced intracellular survival of M. smegmatis in macrophages when compared to its full-length counterpart Rv2820c in M. tuberculosis, however, the respective contribution of the truncation and the new 3′-end of Rv2820c-Bj to this enhancement was unclear. Here, by infecting THP-1 macrophages with Ms_Rv2820c-Bj, Ms_Rv2820c and MS_Rv2820c-Tr (expressing the truncated Rv2820c without five amino acid mutations at 3′-end), we found only Ms_Rv2820c-Bj was responsible for the enhancement of survival of M. smegmatis in macrophages. Furthermore, we detected that Ms_Rv2820c-Tr and Ms_Rv2820c-Bj induced similar cytokine profile and NO production after infection of macrophages, which was distinctly different from Ms_Rv2820c. However, Ms_Rv2820c-Bj evoked higher levels of interleukin-10 (IL-10) and lower levels of interleukin- 6 (IL-6), interleukin-1β (IL-1β) and interleukin-12 (IL-12) in infected THP-1 macrophages than Ms_Rv2820c-Tr. Accordingly, we concluded that the new 3′-end of Rv2820c-Bj was important to dampen host defense and enhance the intracellular survival of M. smegmatis.

Journal

Infection, Genetics and Evolution – Elsevier

Published: Apr 1, 2018

References

  • Interleukin-10 family and tuberculosis: an old story renewed
    Abdalla, A.E.; Lambert, N.; Duan, X.; Xie, J.
  • Role of large sequence polymorphisms (LSPs) in generating genomic diversity among clinical isolates of Mycobacterium tuberculosis and the utility of LSPs in phylogenetic analysis
    Alland, D.; Lacher, D.W.; Hazbón, M.H.; Motiwala, A.S.; Qi, W.; Fleischmann, R.D.; Whittam, T.S.
  • Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes
    Armstrong, J.A.; Hart, P.D.A.
  • Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy?
    Behar, S.M.; Divangahi, M.; Remold, H.G.
  • Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis
    Behar, S.M.; Martin, C.J.; Booty, M.G.; Nishimura, T.; Zhao, X.; Gan, H.; Divangahi, M.; Remold, H.G.
  • Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains
    Bifani, P.J.; Mathema, B.; Kurepina, N.E.; Kreiswirth, B.N.
  • What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge
    Chan, E.D.; Chan, J.; Schluger, N.W.
  • The pattern of cytokine production in vitro induced by ancient and modern Beijing Mycobacterium tuberculosis strains
    Chen, Y.-Y.; Chang, J.-R.; Huang, W.-F.; Hsu, S.-C.; Kuo, S.-C.; Sun, J.-R.; Dou, H.-Y.
  • A point mutation in the two-component regulator PhoP-PhoR accounts for the absence of polyketide-derived Acyltrehaloses but not that of Phthiocerol dimycocerosates in Mycobacterium tuberculosis H37Ra
    Chesne-Seck, M.-L.; Barilone, N.; Boudou, F.; Asensio, J.G.; Kolattukudy, P.E.; Martín, C.; Cole, S.T.; Gicquel, B.; Gopaul, D.N.; Jackson, M.
  • Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved
    Comas, I.; Chakravartti, J.; Small, P.M.; Galagan, J.; Niemann, S.; Kremer, K.; Ernst, J.D.; Gagneux, S.
  • Role of the pks15/1 gene in the biosynthesis of Phenolglycolipids in the Mycobacterium tuberculosis complex: evidence that all strains synthesize glycosylatedp-hydroxybenzoic methyl esters and that strains devoid of phenolglycolipids harbor a frameshift mutation in thepks15/1 gene
    Constant, P.; Perez, E.; Malaga, W.; Lanéelle, M.-A.; Saurel, O.; Daffé, M.; Guilhot, C.
  • Consequences of genomic diversity in Mycobacterium tuberculosis
    Coscolla, M.; Gagneux, S.
  • Interleukin-10 (IL-10) inhibits the induction of nitric oxide synthase by interferon-gamma in murine macrophages
    Cunha, F.Q.; Moncada, S.; Liew, F.Y.
  • Expression of the Mycobacterium tuberculosis PPE37 protein in mycobacterium smegmatis induces low tumour necrosis factor alpha and interleukin 6 production in murine macrophages
    Daim, S.; Kawamura, I.; Tsuchiya, K.; Hara, H.; Kurenuma, T.; Shen, Y.; Dewamitta, S.R.; Sakai, S.; Nomura, T.; Qu, H.; Mitsuyama, M.
  • Mycobacterium tuberculosis PPE32 promotes cytokines production and host cell apoptosis through caspase cascade accompanying with enhanced ER stress response
    Deng, W.; Yang, W.; Zeng, J.; Abdalla, A.E.; Xie, J.
  • Interferon-γ-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis
    Desvignes, L.; Ernst, J.D.
  • Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis
    Dos, V.T.; Mestre, O.; Rauzier, J.; Golec, M.; Rastogi, N.; Rasolofo, V.; Tonjum, T.; Sola, C.; Matic, I.; Gicquel, B.
  • Strains of the East Asian (W/Beijing) lineage of Mycobacterium tuberculosis are DosS/DosT-DosR two-component regulatory system natural mutants
    Fallow, A.; Domenech, P.; Reed, M.B.
  • Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set
    Filliol, I.; Motiwala, A.S.; Cavatore, M.; Qi, W.; Hazbón, M.H.; Bobadilla, d.V.M.; Fyfe, J.; García-García, L.; Rastogi, N.; Sola, C.
  • Variable host–pathogen compatibility in Mycobacterium tuberculosis
    Gagneux, S.; DeRiemer, K.; Van, T.; Kato-Maeda, M.; de Jong, B.C.; Narayanan, S.; Nicol, M.; Niemann, S.; Kremer, K.; Gutierrez, M.C.; Hilty, M.; Hopewell, P.C.; Small, P.M.
  • The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA
    Garneau, J.E.; Dupuis, M.-E.; Villion, M.; Romero, D.A.; Barrangou, R.; Boyaval, P.; Fremaux, C.; Horvath, P.; Magadan, A.H.; Moineau, S.
  • Determination of nitrite/nitrate in human biological material by the simple Griess reaction
    Guevara, I.; Iwanejko, J.; Dembinska-Kiec, A.; Pankiewicz, J.; Wanat, A.; Anna, P.; Golabek, I.; Bartus, S.; Malczewska-Malec, M.; Szczudlik, A.
  • Impact of CRISPR immunity on the emergence and virulence of bacterial pathogens
    Hatoum-Aslan, A.; Marraffini, L.A.
  • Comparative genomic structures of mycobacterium CRISPR-Cas
    He, L.; Fan, X.; Xie, J.
  • High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography
    Hershberg, R.; Lipatov, M.; Small, P.M.; Sheffer, H.; Niemann, S.; Homolka, S.; Roach, J.C.; Kremer, K.; Petrov, D.A.; Feldman, M.W.; Gagneux, S.
  • The effect of Mycobacterium tuberculosis CRISPR-associated Cas2 (Rv2816c) on stress response genes expression, morphology and macrophage survival of mycobacterium smegmatis
    Huang, Q.; Luo, H.; Liu, M.; Zeng, J.; Abdalla, A.E.; Duan, X.; Li, Q.; Xie, J.
  • Polymorphisms in the PE35 and PPE68 antigens in Mycobacterium tuberculosis strains may affect strain virulence and reflect ongoing immune evasion
    Jiang, Y.; Wei, J.; Liu, H.; Li, G.; Guo, Q.; Qiu, Y.; Zhao, L.; Li, M.; Zhao, X.; Dou, X.; Wan, K.
  • Distribution of insertion- and deletion-associated genetic polymorphisms among four Mycobacterium tuberculosis phospholipase C genes and associations with Extrathoracic tuberculosis: a population-based study
    Kong, Y.; Cave, M.D.; Yang, D.; Zhang, L.; Marrs, C.F.; Foxman, B.; Bates, J.H.; Wilson, F.; Mukasa, L.N.; Yang, Z.H.
  • Truncated Rv2820c enhances mycobacterial virulence ex vivo and in vivo
    Lam, J.T.; Yuen, K.Y.; Ho, P.L.; Weng, X.H.; Zhang, W.H.; Chen, S.; Yam, W.C.
  • Genetic features of Mycobacterium tuberculosis modern Beijing sublineage
    Liu, Q.; Luo, T.; Dong, X.; Sun, G.; Liu, Z.; Gan, M.; Wu, J.; Shen, X.; Gao, Q.
  • Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method
    Livak, K.J.; Schmittgen, T.D.
  • Mycobacterium tuberculosis Rv1265 promotes mycobacterial intracellular survival and alters cytokine profile of the infected macrophage
    Luo, H.; Zeng, J.; Huang, Q.; Liu, M.; Abdalla, A.E.; Xie, L.; Wang, H.; Xie, J.
  • Annotation and classification of CRISPR-Cas systems
    Makarova, K.S.; Koonin, E.V.
  • An updated evolutionary classification of CRISPR–Cas systems
    Makarova, K.S.; Wolf, Y.I.; Alkhnbashi, O.S.; Costa, F.; Shah, S.A.; Saunders, S.J.; Barrangou, R.; Brouns, S.J.J.; Charpentier, E.; Haft, D.H.; Horvath, P.; Moineau, S.; Mojica, F.J.M.; Terns, R.M.; Terns, M.P.; White, M.F.; Yakunin, A.F.; Garrett, R.A.; van der Oost, J.; Backofen, R.; Koonin, E.V.
  • CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA
    Marraffini, L.A.; Sontheimer, E.J.
  • Type I IFN induces IL-10 production in an IL-27–independent manner and blocks responsiveness to IFN-γ for production of IL-12 and bacterial killing in Mycobacterium tuberculosis–infected macrophages
    McNab, F.W.; Ewbank, J.; Howes, A.; Moreira-Teixeira, L.; Martirosyan, A.; Ghilardi, N.; Saraiva, M.; O'Garra, A.
  • Mycobacterium tuberculosis PPE25 and PPE26 proteins expressed in mycobacterium smegmatis modulate cytokine secretion in mouse macrophages and enhance mycobacterial survival
    Mi, Y.; Bao, L.; Gu, D.; Luo, T.; Sun, C.; Yang, G.
  • Genomic deletions suggest a phylogeny for the Mycobacterium tuberculosis complex
    Mostowy, S.; Cousins, D.; Brinkman, J.; Aranaz, A.; Behr, M.A.
  • The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage
    Nair, S.; Ramaswamy, P.A.; Ghosh, S.; Joshi, D.C.; Pathak, N.; Siddiqui, I.; Sharma, P.; Hasnain, S.E.; Mande, S.C.; Mukhopadhyay, S.
  • Infergen stimulated macrophages restrict Mycobacterium tuberculosis growth by autophagy and release of nitric oxide
    Pahari, S.; Khan, N.; Aqdas, M.; Negi, S.; Kaur, J.; Agrewala, J.N.
  • Impaired M. tuberculosis-mediated apoptosis in alveolar macrophages from HIV+ persons: potential role of IL-10 and BCL-3
    Patel, N.R.; Swan, K.; Li, X.; Tachado, S.D.; Koziel, H.
  • Mycobacterium tuberculosis and the macrophage: maintaining a balance
    Pieters, J.
  • STAT3 represses nitric oxide synthesis in human macrophages upon Mycobacterium tuberculosis infection
    Queval, C.J.; Song, O.-R.; Deboosère, N.; Delorme, V.; Debrie, A.-S.; Iantomasi, R.; Veyron-Churlet, R.; Jouny, S.; Redhage, K.; Deloison, G.; Baulard, A.; Chamaillard, M.; Locht, C.; Brodin, P.
  • Mycobacterium tuberculosis resists stress by regulating PE19 expression
    Ramakrishnan, P.; Aagesen, A.M.; McKinney, J.D.; Tischler, A.D.
  • A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response
    Reed, M.B.; Domenech, P.; Manca, C.; Su, H.; Barczak, A.K.; Kreiswirth, B.N.; Kaplan, G.; Barry, C.E.
  • The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated
    Reed, M.B.; Gagneux, S.; DeRiemer, K.; Small, P.M.; Barry, C.E.
  • Toll-like receptor 2-dependent extracellular signal-regulated kinase signaling in Mycobacterium tuberculosis-infected macrophages drives anti-inflammatory responses and inhibits Th1 polarization of responding T cells
    Richardson, E.T.; Shukla, S.; Sweet, D.R.; Wearsch, P.A.; Tsichlis, P.N.; Boom, W.H.; Harding, C.V.
  • Mapping of genotype-phenotype diversity among clinical isolates of Mycobacterium tuberculosis by sequence-based transcriptional profiling
    Rose, G.; Cortes, T.; Comas, I.; Coscolla, M.; Gagneux, S.; Young, D.B.
  • SOCS3 and STAT3, major controllers of the outcome of infection with Mycobacterium tuberculosis
    Rottenberg, M.E.; Carow, B.
  • A CRISPR/Cas system mediates bacterial innate immune evasion and virulence
    Sampson, T.R.; Saroj, S.D.; Llewellyn, A.C.; Tzeng, Y.L.; Weiss, D.S.
  • Hypervirulent mutant of Mycobacterium tuberculosis resulting from disruption of the mce1 operon
    Shimono, N.; Morici, L.; Casali, N.; Cantrell, S.; Sidders, B.; Ehrt, S.; Riley, L.W.
  • Lack of acidification in mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase
    Sturgill-Koszycki, S.; Schlesinger, P.H.; Chakraborty, P.; Haddix, P.L.; Collins, H.L.; Fok, A.K.; Allen, R.D.; Gluck, S.L.; Heuser, J.; Russell, D.G.
  • The Mycobacterium tuberculosis PE proteins Rv0285 and Rv1386 modulate innate immunity and mediate bacillary survival in macrophages
    Tiwari, B.M.; Kannan, N.; Vemu, L.; Raghunand, T.R.
  • Genomic deletions classify the Beijing/W strains as a distinct genetic lineage of Mycobacterium tuberculosis
    Tsolaki, A.G.; Gagneux, S.; Pym, A.S.; Goguet de la Salmoniere, Y.O.; Kreiswirth, B.N.; Van Soolingen, D.; Small, P.M.
  • A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis
    Vandal, O.H.; Pierini, L.M.; Schnappinger, D.; Nathan, C.F.; Ehrt, S.
  • Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium
    Volkman, H.E.; Pozos, T.C.; Zheng, J.; Davis, J.M.; Rawls, J.F.; Ramakrishnan, L.
  • Global TB Rep.
    WHO
  • Comparative proteomic analysis of Mycobacterium tuberculosis lineage 7 and lineage 4 strains reveals differentially abundant proteins linked to slow growth and virulence
    Yimer, S.A.; Birhanu, A.G.; Kalayou, S.; Riaz, T.; Zegeye, E.D.; Beyene, G.T.; Holm-Hansen, C.; Norheim, G.; Abebe, M.; Aseffa, A.
  • Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin
    Yuk, J.M.; Shin, D.M.; Lee, H.M.; Yang, C.S.; Jin, H.S.; Kim, K.K.; Lee, Z.W.; Lee, S.H.; Kim, J.M.; Jo, E.K.

You’re reading a free preview. Subscribe to read the entire article.

Try 2 weeks free now

DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

or browse the journals available

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off

Sign up
for free
Start 14 day
Free Trial