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 Table of Contents  
REVIEW
Year : 2016  |  Volume : 5  |  Issue : 4  |  Page : 379-383

Assuming the role of mitochondria inmycobacterial infection


Division of Microbiology, Council of Scientific and Industrial Research-Central Drug Research Institute, Lucknow 226031, India

Date of Web Publication14-Feb-2017

Correspondence Address:
Rikesh K Dubey
Division of Microbiology, Council of Scientific and Industrial Research-Central Drug Research Institute, Lucknow
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.1016/j.ijmyco.2016.06.001

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  Abstract 


Tuberculosis is one of the leading causes of death by Mycobacterium tuberculosis (Mtb) affecting millions of people worldwide. Mycobacterium species enter host macrophages during infection and target various cellular organelles and their function for their own benefit. Mitochondria appear to be among the important targets for bacterial pathogens. Mtb and other pathogenic bacteria secrete various proteins that initiate structural changes in mitochondria to modulate its function. Additionally, virulent mycobacteria interfere with the balance between pro- and anti-apoptotic factors to inhibit apoptosis and, in later stages, promote necrosis. Furthermore, mitochondria perform multiple biological functions in the cell, and the inhibition of these functions by bacterial proteins promotes Mtb survival, growth, and successful infection.

Keywords: Tuberculosis, Mtb, Mitochondria, Apoptosis, Autophagy, Necrosis


How to cite this article:
Dubey RK. Assuming the role of mitochondria inmycobacterial infection. Int J Mycobacteriol 2016;5:379-83

How to cite this URL:
Dubey RK. Assuming the role of mitochondria inmycobacterial infection. Int J Mycobacteriol [serial online] 2016 [cited 2022 May 20];5:379-83. Available from: https://www.ijmyco.org/text.asp?2016/5/4/379/200119




  Introduction Top


Tuberculosis (TB) caused by Mycobacterium tuberculosis (Mtb) continues to be a major cause of morbidity and mortality throughout the world. Despite the availability of various effective drugs and Bacillus Calmette–Guérin (BCG) vaccines, TB-control programs have failed to reduce this problem in most parts of the world. In 2013, it was estimated that approximately one-third of the world population was asymptomatically infected with Mtb, of which nine million people developed TB and 1.5million died from this deadly disease, including one-fourth who were human immunodeficiency virus (HIV)-positive [1]. Emergence of new resistant strains, such as multidrug-resistant and extensively drug-resistant strains, as well as other complicating factors, such as HIV coinfection, has posed an extra burden on TB-control programs [2]. Therefore, there is an urgent need to find new mycobacterial targets to allow for the development of drugs against this deadly disease.

Mtb is the causal organism of TB that engulfs host macrophages through various available phagocytic receptors, of which the complement of mannose receptors are the most prevalent [3],[4]. Virulent Mtb has adapted itself to enable its survival in the host macrophage by utilizing various strategies, such as preventing the fusion of phagosomes with lysosomes, restriction to phagosomal acidification, and targeting cellular organelles, such as mitochondria, to disturb the balance of pro- and anti-apoptotic factors in order to escape the immune response [5]. Mitochondria are double-membrane-bound organelles that have evolved from an endosymbiotic proteobacterium and perform various biological functions, such as adenosine triphosphate (ATP) synthesis, ion homeostasis, biosynthesis of fatty acids, calcium storage, iron-sulfur-cluster biogenesis, and regulation of cell-death pathways. Due to the multiple and diverse roles of mitochondria, it is an attractive target organelle for bacterial pathogens. Therefore, one could hypothesize that interference with mitochondrial functions would be useful to pathogens for establishment of successful infection.


  Mtb and apoptosis Top


Apoptosis is an evolutionarily preserved mechanism for cell self-destruction, and it plays an important role in many physiological processes, such as morphogenetic changes in embryonic development, aging, and homeostatic maintenance [6]. Most pathological conditions are linked to the misregulation of programmed cell death, with examples involving neurodegenerative diseases, cardiovascular diseases, cancers, and acquired immune deficiency syndrome [7],[8]. Apoptosis induction in response to viral infection is also well established. Many viral pathogens are known to encode genes whose products inhibit host cell death to provide a suitable niche for viral replication and survival [9],[10]. Apoptosis is an innate cellular defense mechanism that is usually initiated under stress conditions. Pathogenic bacteria have evolved various strategies to target host cells to either to inhibit apoptosis for their survival and growth or promote apoptosis. Virulent strains of Mtb inhibit apoptosis in macrophages through upregulation of antiapoptotic proteins, such as B-cell lymphoma (Bcl)-2 and Mcl-1, through destruction of mitochondrial transmembrane potential and by depletion of cytochrome c [11],[12],[13].

In addition to Mtb, other pathogenic bacteria of the Mycobacterium species include Mycobacterium leprae, which causes leprosy and induces apoptosis through upregulation of Mcl-1 expression and downregulation of the Bcl-2-associated death promoter and Bcl-2 homologous antagonist/killer (Bak) proteins [12], wild-type Mycobacterium bovis, which induces low levels of apoptosis by increasing production of interleukin-10 and Bcl-2 and reduces production of tumor necrosis factor (TNF)-α [14]. TNF-α production is critical for the induction of apoptosis in mycobacteria-infected macrophages [15]. Other bacteria known to induce apoptosis include Pseudomonas aeruginosa, Escherichia coli, Listeria monocytogenes, Neisseriae spp., Yersinia pseudotuberculosis, Yersinia pestis, Yersinia enterocolitica, Salmonella typhimurium, and Shigella Flexneri [16].

Mtb infection predominantly leads to necrosis, a form of cell death characterized by plasma-membrane disruption that differs from apoptosis, where the integrity of the plasma membrane is preserved. Mtb induces necrosis to evade host defenses and to exit macrophages in order to disseminate to and infect surrounding cells. H37Rv, a pathogenic strain of Mycobacterium, promotes necrosis by inducing substantial alterations to mitochondrial transmembrane potential [17]. A recent study reported that Mtb PPE68 and Rv2626c genes encoded proteins involved in aiding bacterial escape from host macrophages by promoting necrosis. Deletion of the Rv2626c gene resulted in decreased necrosis induction, while overexpression promoted significant necrosis [18]. However, there is limited information available regarding the mechanism used by bacteria to promote necrosis.


  Mitochondrial roles in induction of apoptosis and necrosis Top


Mitochondrion plays a key role in the regulation of apoptotic cell death [8]. These organelles are not only involved in intrinsic cell-death pathways, but they are also involved in extrinsic cell-death pathways in some cell types. Intrinsic mitochondria-mediated cell death differs from extrinsic cell-death pathways in how it is elicited in the presence of various stressors associated with the intracellular environment, such as DNA damage, microbial infection, and oxidative stress. In contrast, the extrinsic pathway is initiated by extracellular cell-death signals. In response to specific apoptotic stimuli, mitochondria release the proapoptotic factor cytochrome c and apoptosis inducing factor (AIF). Cytochrome c associates with a scaffold protein, apoptotic protease activating factor-1, to drive the assembly of a supramolecular complex known as the apoptosome, which leads to the activation of caspase cascades that lead to cell death [19]. X-linked inhibitor of apoptosis protein possesses caspase-inhibitory activity, which is counteracted by second mitochondria-derived activator of caspase/direct inhibitor of apoptosis-binding protein, a mitochondrion-derived activator of caspases [20]. However, some factors, such as AIF, can trigger cell death in a caspase-independent manner through translocation to the nucleus and induction of DNA degradation [21],[22]. Bcl-2-family members include pro- and anti-apoptotic proteins that regulate mitochondrial outer membrane permeabilization [23]. Antiapoptotic proteins, such as Bcl-2 or Bcl-extra-large and other members, prevent apoptosis, whereas proapoptotic proteins, such as Bcl-2-like protein 11, Bcl-2-associated X Protein, or Bak, promote apoptosis [24]. Besides apoptosis, necrosis is also a form of cell death that is uncontrolled or pathological. Early alteration of the mitochondrial permeability transition pore in the inner membrane of mitochondria is a key event in primary necrosis that occurs in the absence of cytochrome c release. Opening of this pore leads to the loss of the proton gradient and a cessation of ATP generation through oxidative phosphorylation and massive inflow of water into the solute-rich matrix, resulting in severe swelling of the mitochondrion. While pore opening releases apoptogenic factors that initiate apoptosis, persistent opening of pores leads to necrotic cell death [25],[26].


  Mitochondrial autophagy Top


Mitochondrial autophagy or mitophagy is the selective elimination of damaged mitochondria in order to maintain homeostasis and regulate mitochondrial load to balance the biological and metabolic demands of the cell [27],[28]. It prevents the fusion of damaged mitochondria with healthy mitochondria to contribute to the maintenance of healthy mitochondrial networks [29]. Damaged mitochondrion can induce apoptosis through the release of cytochrome c and calcium [30]. Phosphatase and tensin homolog-induced putative kinase 1 (PINK1) and the ubiquitin ligase Parkin regulate mitophagy. In normal cases, PINK1 is imported into mitochondria, where its N-terminal mitochondria-targeting sequence is processed in the matrix, and the kinase is degraded by cytosolic and mitochondrial proteases [31]. In cases of severe depletion of mitochondrial inner-membrane potential, PINK1 import leads to its accumulation in the outer-mitochondrial membrane (OMM) and recruitment of Parkin from the cytosol. Phosphorylation of Parkin by PINK1 activates its ubiquitin ligase activity to enable OMM protein polyubiquitination. Parkin is able to ubiquitinate various proteins available on the OMM and in the cytosol to facilitate the recruitment of autophagy machinery for degradation of defective mitochondria [32].

Recent studies demonstrated the role of Parkin in ubiquitin-mediated Mtb autophagy. Parkin protein, a ubiquitin ligase, mediates resistance to intracellular pathogens, and deletion of this gene is associated with increased susceptibility to such intracellular pathogens in humans. In cases of defective Parkin, Mtb proliferation increases in macrophages [33]. A recent finding observed that virulent Mtb after macrophage infection affects mitochondria in a number of ways, including mitochondria distribution, size, number, and fragmentation, while nonpathogenic strains of mycobacteria, such as M. bovis BCG, were unable to elicit the same effect [34]. Similar patterns of mitochondrial disruption and network fragmentation were observed in L. monocytogenes-infected epithelial cells [35].


  Mitochondria targeted by bacterial proteins Top


To exert effects on mitochondrial function, bacterial proteins must bind to and be taken up by mitochondria during infection [36]. Various pathogenic bacterial proteins interact with host mitochondria and determine the fate of the cell by affecting processes, such as inhibition of apoptosis and necrosis. Some bacterial porins that form β-barrel structures in the outer membrane of Gram negative bacteria can induce cell death by targeting mitochondria [37]. Acinetobacter baumannii Omp38 targets mitochondria to induce the formation of channels for the release of cytochrome c, which promotes apoptosis [38]. Neisseria gonorrhoeae PorB induces apoptosis, while the homolog from Neisseria meningitidis inhibits host-cell apoptosis during infection [39]. Pneumolysin, a bacterial toxin secreted by Staphylococcus aureus and vacuolating cytotoxin, a virulent factor of Helicobacter pylori, were reported to modulate host-cell mitochondria and, in turn, induce apoptosis [40]. Bioinformatics studies of Mycobacterium avium (subsp. Paratuberculosis) and Mtb, causative agents of Johne's disease and tuberculosis, respectively, confirmed that some mycobacterial proteins target the mitochondria [41],[42]; however, no experimental evidence currently exists.


  Conclusion Top


Virulence factors are mainly involved in the interaction of mycobacteria with host macrophages ([Figure 1]). Few of these factors are implicated in the adaptation of the bacilli inside the macrophage to limited nutritional conditions. The factors include proteins required for the uptake of nutrients and ions, as well as metabolic switching that occurs when mycobacteria is inside host cells. Proteins that participate in the mechanisms triggered by mycobacteria offset microbicidal host-cell responses, such as: (1) arresting the encounter of the phagosome and enhancing resistance to host toxic components (cell-wall barriers and specific effectors); (2) escaping from the intracellular compartment; and (3) avoiding the development of localized and productive immune responses. In these physiological events, the mitochondrion is an important host target for pathogenic bacteria due to its multiple roles in programmed cell death, cellular metabolism, and the innate-immune system. Mitochondria are dynamic organelles that play defensive roles against many bacterial pathogens; however, many bacteria have evolved to utilize multiple self-defense mechanisms. Various bacterial pathogens produce pathogenicity factors that participate in the modulation of mitochondrial functions that ultimately decide the fate of the host cell. Knowledge of mycobacterial proteins and the precise mechanisms by which they interact with important host organelles, including mitochondria, to affect their function will provide better understanding of mycobacterial pathogenesis.
Figure 1: Mitochondrial behavior in response to pathogenic and nonpathogenic mycobacteria. (1) Pathogenic mycobacteria modulate cell-death pathways by inhibiting or promoting apoptosis through multiple mechanisms, including regulating expression of antiapoptotic and proapoptotic proteins. Most virulent mycobacteria downregulate proapoptotic genes and upregulate antiapoptotic genes to promote apoptosis, while avirulent species promote upregulation of proapoptotic genes and downregulation of antiapoptotic genes. (2) Pathogenic mycobacteria may affect the outer membrane of mitochondria, causing mitochondrial outer-membrane permeabilization (MOMP) and release of cytochrome c from the intermembrane space to the cytosol, thereby activating caspases and leading to apoptosis. This pathway is also utilized by several nonpathogenicmycobacteria to initiate apoptosis. Pathogenicmycobacteria are also capable of affecting the inner membrane of mitochondria, which alters the mitochondrial permeability transition pore complex (mPTPC) and leads to necrosis. (3) Generation of mitochondrial reactive oxygen species in conjunction with excessive tumor necrosis factor activation upon pathogenic mycobacteria infection alters the mPTPC and promotes necrosis. Reactive oxygen species (ROS) is also capable of inducing autophagy to promote acidification of phagosomes containing bacteria and phagolysosomal fusion. (4) In order for pathogenic mycobacteria to evade host defenses, they also inhibit autophagy, phagosome acidification and phagolysosomal fusion, while nonpathogenic mycobacteria inhibit phagosome acidification and phagolysosomal fusion, and induce autophagy. Inhibitors of apoptosis protein(s) (IAP) = ; TNF = tumor necrosis factor.

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  Conflicts of interest Top


There are no conflicts of interest.


  Acknowledgments Top


I am thankful to Dr. Kishore K. Srivastava, Professor, AcSIR Senior Principal Scientist, CSIR-Central Drug Research Institute, Lucknow, India, for his help and support in carrying out this research.



 
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