Mycobacterial membrane vesicles administered systemically in mice induce a protective immune response to surface compartments of mycobacterium tuberculosis

Rafael Prados-Rosales, Leandro J. Carreño, Ana Batista-Gonzalez, Andres Baena, Manjunatha M. Venkataswamy, Jiayong Xu, Xiaobo Yu, Garrick Wallstrom, Dewey Magee, Joshua LaBaer, Jacqueline M. Achkar, William R. Jacobs, John Chan, Steven A. Porcelli, Arturo Casadevall

Research output: Contribution to journalArticle

39 Citations (Scopus)

Abstract

Pathogenic and nonpathogenic species of bacteria and fungi release membrane vesicles (MV), containing proteins, polysaccharides, and lipids, into the extracellular milieu. Previously, we demonstrated that several mycobacterial species, including bacillus Calmette-Guerin (BCG) and Mycobacterium tuberculosis, release MV containing lipids and proteins that subvert host immune response in a Toll-like receptor 2 (TLR2)-dependent manner (R. Prados-Rosales et al., J. Clin. Invest. 121:1471–1483, 2011, doi:10.1172/JCI44261). In this work, we analyzed the vaccine potential of MV in a mouse model and compared the effects of immunization with MV to those of standard BCG vaccination. Immunization with MV from BCG or M. tuberculosis elicited a mixed humoral and cellular response directed to both membrane and cell wall components, such as lipoproteins. However, only vaccination with M. tuberculosis MV was able to protect as well as live BCG immunization. M. tuberculosis MV boosted BCG vaccine efficacy. In summary, MV are highly immunogenic without adjuvants and elicit immune responses comparable to those achieved with BCG in protection against M. tuberculosis.

IMPORTANCE: This work offers a new vaccine approach against tuberculosis using mycobacterial MV. Mycobacterium MV are a naturally released product combining immunogenic antigens in the context of a lipid structure. The fact that MV do not need adjuvants and elicit protection comparable to that elicited by the BCG vaccine encourages vaccine approaches that combine protein antigens and lipids. Consequently, mycobacterium MV establish a new type of vaccine formulation.

Original languageEnglish (US)
Article numbere01921-14
JournalmBio
Volume5
Issue number5
DOIs
StatePublished - Sep 30 2014

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Mycobacterium tuberculosis
Membranes
Mycobacterium bovis
Vaccines
BCG Vaccine
Lipids
Immunization
Mycobacterium
Vaccination
Antigens
Toll-Like Receptor 2
Proteins
Cellular Structures
Membrane Potentials
Cell Wall
Lipoproteins
Polysaccharides
Tuberculosis
Fungi
Bacteria

ASJC Scopus subject areas

  • Microbiology
  • Virology

Cite this

Prados-Rosales, R., Carreño, L. J., Batista-Gonzalez, A., Baena, A., Venkataswamy, M. M., Xu, J., ... Casadevall, A. (2014). Mycobacterial membrane vesicles administered systemically in mice induce a protective immune response to surface compartments of mycobacterium tuberculosis. mBio, 5(5), [e01921-14]. https://doi.org/10.1128/mBio.01921-14

Mycobacterial membrane vesicles administered systemically in mice induce a protective immune response to surface compartments of mycobacterium tuberculosis. / Prados-Rosales, Rafael; Carreño, Leandro J.; Batista-Gonzalez, Ana; Baena, Andres; Venkataswamy, Manjunatha M.; Xu, Jiayong; Yu, Xiaobo; Wallstrom, Garrick; Magee, Dewey; LaBaer, Joshua; Achkar, Jacqueline M.; Jacobs, William R.; Chan, John; Porcelli, Steven A.; Casadevall, Arturo.

In: mBio, Vol. 5, No. 5, e01921-14, 30.09.2014.

Research output: Contribution to journalArticle

Prados-Rosales, R, Carreño, LJ, Batista-Gonzalez, A, Baena, A, Venkataswamy, MM, Xu, J, Yu, X, Wallstrom, G, Magee, D, LaBaer, J, Achkar, JM, Jacobs, WR, Chan, J, Porcelli, SA & Casadevall, A 2014, 'Mycobacterial membrane vesicles administered systemically in mice induce a protective immune response to surface compartments of mycobacterium tuberculosis', mBio, vol. 5, no. 5, e01921-14. https://doi.org/10.1128/mBio.01921-14
Prados-Rosales, Rafael ; Carreño, Leandro J. ; Batista-Gonzalez, Ana ; Baena, Andres ; Venkataswamy, Manjunatha M. ; Xu, Jiayong ; Yu, Xiaobo ; Wallstrom, Garrick ; Magee, Dewey ; LaBaer, Joshua ; Achkar, Jacqueline M. ; Jacobs, William R. ; Chan, John ; Porcelli, Steven A. ; Casadevall, Arturo. / Mycobacterial membrane vesicles administered systemically in mice induce a protective immune response to surface compartments of mycobacterium tuberculosis. In: mBio. 2014 ; Vol. 5, No. 5.
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abstract = "Pathogenic and nonpathogenic species of bacteria and fungi release membrane vesicles (MV), containing proteins, polysaccharides, and lipids, into the extracellular milieu. Previously, we demonstrated that several mycobacterial species, including bacillus Calmette-Guerin (BCG) and Mycobacterium tuberculosis, release MV containing lipids and proteins that subvert host immune response in a Toll-like receptor 2 (TLR2)-dependent manner (R. Prados-Rosales et al., J. Clin. Invest. 121:1471–1483, 2011, doi:10.1172/JCI44261). In this work, we analyzed the vaccine potential of MV in a mouse model and compared the effects of immunization with MV to those of standard BCG vaccination. Immunization with MV from BCG or M. tuberculosis elicited a mixed humoral and cellular response directed to both membrane and cell wall components, such as lipoproteins. However, only vaccination with M. tuberculosis MV was able to protect as well as live BCG immunization. M. tuberculosis MV boosted BCG vaccine efficacy. In summary, MV are highly immunogenic without adjuvants and elicit immune responses comparable to those achieved with BCG in protection against M. tuberculosis.IMPORTANCE: This work offers a new vaccine approach against tuberculosis using mycobacterial MV. Mycobacterium MV are a naturally released product combining immunogenic antigens in the context of a lipid structure. The fact that MV do not need adjuvants and elicit protection comparable to that elicited by the BCG vaccine encourages vaccine approaches that combine protein antigens and lipids. Consequently, mycobacterium MV establish a new type of vaccine formulation.",
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AU - Baena, Andres

AU - Venkataswamy, Manjunatha M.

AU - Xu, Jiayong

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AU - Magee, Dewey

AU - LaBaer, Joshua

AU - Achkar, Jacqueline M.

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