Hijacking Host Cell Highways: Manipulation of the Host Actin Cytoskeleton by Obligate Intracellular Bacterial Pathogens

Colonne, Punsiri M.; Winchell, Caylin G.; Voth, Daniel E.

doi:10.3389/fcimb.2016.00107

Cited by 81 publications

(64 citation statements)

References 67 publications

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“…From invasion to dissemination, all stages of the intracellular bacterial life cycle share the same three-dimensional cytosolic space containing the host cytoskeleton. For successful infection and replication, many pathogens hijack the cytoskeleton using effector proteins introduced into the host cytosol by specialized secretion systems ( Colonne et al, 2016 ). Cytoskeletal rearrangement promotes numerous events that are beneficial to the pathogen, including internalization of bacteria, structural support for bacteria-containing vacuoles, altered vesicular trafficking, actin-dependent bacterial movement, and pathogen dissemination.…”

Section: Discussionmentioning

confidence: 99%

Modulation of Microtubule Dynamics Affects Brucella abortus Intracellular Survival, Pathogen-Containing Vacuole Maturation, and Pro-inflammatory Cytokine Production in Infected Macrophages

et al. 2017

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The microtubule (MT) cytoskeleton regulates several cellular processes related to the immune system. For instance, an intricate intracellular transport mediated by MTs is responsible for the proper localization of vesicular receptors of innate immunity and its adaptor proteins. In the present study, we used nocodazole to induce MTs depolymerization and paclitaxel or recombinant (r) TIR (Toll/interleukin-1 receptor) domain containing protein (TcpB) to induce MT stabilization in bone marrow-derived macrophages infected with Brucella abortus. Following treatment of the cells, we evaluated their effects on pathogen intracellular replication and survival, and in pro-inflammatory cytokine production. First, we observed that intracellular trafficking and maturation of Brucella-containing vesicles (BCVs) is affected by partial destabilization or stabilization of the MTs network. A typical marker of early BCVs, LAMP-1, is retained in late BCVs even 24 h after infection in the presence of low doses of nocodazole or paclitaxel and in the presence of different amounts of rTcpB. Second, microscopy and colony forming unit analysis revealed that bacterial load was increased in infected macrophages treated with lower doses of nocodazole or paclitaxel and with rTcpB compared to untreated cells. Third, innate immune responses were also affected by disturbing MT dynamics. MT depolymerization by nocodazole reduced IL-12 production in infected macrophages. Conversely, rTcpB-treated cells augmented IL-12 and IL-1β secretion in infected cells. In summary, these findings demonstrate that modulation of MTs affects several crucial steps of B. abortus pathogenesis, including BCV maturation, intracellular survival and IL-12 secretion in infected macrophages.

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Section: Discussionmentioning

confidence: 99%

Modulation of Microtubule Dynamics Affects Brucella abortus Intracellular Survival, Pathogen-Containing Vacuole Maturation, and Pro-inflammatory Cytokine Production in Infected Macrophages

et al. 2017

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“…The cytoskeleton is critical for the maintenance of cell shape, cell motility and intracellular transport, and bacterial and viral infections require the cytoskeleton [59]. Bacteria in the process of invasion and proliferation, at all stages of the intracellular bacterial life cycle, have the same three-dimensional cytosolic space containing the cytoskeleton [60]. In this instance, a total of 15 DEGs associated with the cytoskeleton were identified, and most were upregulated in the CLas-infected groups compared to the CLas-free groups.…”

Section: Endocytosis the Cytoskeleton And Insecticide Resistance Maymentioning

confidence: 99%

Transcriptome Analyses of Diaphorina citri Midgut Responses to Candidatus Liberibacter Asiaticus Infection

Zeng

et al. 2020

Insects

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The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Liviidae), is an important transmission vector of the citrus greening disease Candidatus Liberibacter asiaticus (CLas). The D. citri midgut exhibits an important tissue barrier against CLas infection. However, the molecular mechanism of the midgut response to CLas infection has not been comprehensively elucidated. In this study, we identified 778 differentially expressed genes (DEGs) in the midgut upon CLas infection, by comparative transcriptome analyses, including 499 upregulated DEGs and 279 downregulated DEGs. Functional annotation analysis showed that these DEGs were associated with ubiquitination, the immune response, the ribosome, endocytosis, the cytoskeleton and insecticide resistance. KEGG enrichment analysis revealed that most of the DEGs were primarily involved in endocytosis and the ribosome. A total of fourteen DEG functions were further validated by reverse transcription quantitative PCR (RT-qPCR). This study will contribute to our understanding of the molecular interaction between CLas and D. citri.Insects 2020, 11, 171 2 of 16 poisoning of farmers, environmental pollution and insect resistance [8,9]. Some researchers have focused on the olfactory system of D. citri, revealing a suite of odorants that can be used to develop affordable and safe odor-based surveillance for D. citri control [10]. Yu et al. revealed that the silencing of D. citri muscle protein 20 (DcMP20) resulted in significant mortality and reduced the body weight of D. citri [11]. By RNA interference (RNAi) technology, the knockdown of D. citri tropomyosin1-X1 (DcTm1-X1) significantly increased the mortality rate of nymphs [12]. Although some success regarding the control of D. citri has been achieved, the threats caused by HLB are going to continue. It is essential to investigate the molecular mechanisms of HLB transmission in D. citri.Both D. citri adults and nymphs can transmit CLas. Recent studies suggested that the pathogen multiplies in D. citri after acquisition and becomes distributed among various internal tissues, including the alimentary canal, salivary glands, hemolymph, filter chamber, midgut, fat body, muscle tissues and ovaries [13][14][15]. Among these tissues, the midgut is the first barrier that the bacterium must breach before entry into the hemolymph, indicating that the midgut plays an important role in CLas infection [16]. Pathogens can manipulate the host's essential biological processes during the host-pathogen interaction, e.g., by changing protein translation, vesicular transport and protein metabolism [17,18]. In the midgut, many genes and proteins are involved in the defense against pathogens. Wang et al. identified 869 differentially expressed genes (DEGs) in the Bombyx mori larval midgut via comparative transcriptome analysis. The results showed that many of the DEGs were associated with protein metabolism, the cytoskeleton and apoptosis [19]. Bao et al. performed a transcriptome-wide analysis on the Nilaparvata lugens intestine, an...

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“…Loss of cytoskeletal integrity and increased epithelial permeability are usually hallmarks of inflammation. Cytoskeletal rearrangement promotes numerous events that are beneficial to the pathogen, including internalization of bacteria, structural support for bacteria-containing vacuoles, altered vesicular trafficking, actin-dependent bacterial movement, and pathogen dissemination (45). Also, MVs could trigger vacuolization for L. monocytogenes to survive or persist inside the vacuoles during infection.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome responses of intestinal epithelial cells induced by membrane vesicles ofListeria monocytogenesunveil novel insights into the host-pathogen cross talk

Karthikeyan

Gayathri

Gunasekaran

et al. 2019

Preprint

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32Membrane vesicles (MVs) serve as a vital source of virulence factors in many pathogenic organisms. The 33 release of MVs by Listeria monocytogenes is only recently recognized, but its role in the pathogenesis is 34 poorly understood. Here, we investigated the role of MVs of L. monocytogenes in virulence and host 35interactions. Proteomic analyses of whole cells and MVs of L. monocytogenes were performed using 36 LC/MS/MS. A total of 1376 and 456 proteins were identified in the L. monocytogenes cells and MVs, 37 respectively. Also, we have found that MVs contains active pore-forming listeriolysin (LLO), internalin 38 B (inlB), phosphatidylinositol-specific phospholipase C (PI-PLC-A). We have previously reported that 39MVs of L. monocytogenes can infect and induce cytotoxicity in Caco-2 cells. In this study, we report the 40 transcriptome response of Caco-2 cells upon infection with MVs as well as L. monocytogenes. In 41 particular, we observed the up-regulation of autophagy-related genes in the early phase of infection with 42 MVs. Transcription of inflammatory cytokines (CCL2, CXCL6, CXCL8, CXCL15, CXCL5, CXCL10) 43 peaked at four h of infection. A large number of differentially expressed genes was associated with actin 44 cytoskeleton rearrangement, autophagy, cell cycle arrest, and induction of oxidative stress. At a later time 45 point, transcriptional programs generated upon infection with MVs point toward to evade innate immune 46 signals, by modulating the expression of anti-inflammatory genes. KEGG pathway enrichment analysis 47 revealed that MVs induce several signaling pathways such as PI3k-Akt signaling pathway, mitogen-48 activated protein kinase (MAPK) pathway, NOD-like receptor signaling pathway, cAMP signaling 49 pathway, TNF, and NF-kB signaling pathway. Moreover, MVs induced the expression of cell cycle 50 regulatory genes, which may result in the ability to prolong host cell survival, thus protecting the 51 replicative niche for L. monocytogenes. Notably, we identified several non-coding RNAs (ncRNAs) are 52 regulated during infection, suggesting that an early manipulation of the host gene expression may be 53 essential for L. monocytogenes persistence and replication in host cells. 54 55 56 57 58 59 60 61 62 63 64 Introduction 65Several Gram-negative and Gram-positive bacteria release membrane vesicles (MVs). MVs are a 66 spherical structure of 50-300 nm in diameter composed of the single membrane that is derived from the 67 outer membrane (OM) and contains OM proteins, lipopolysaccharide (LPS), and other lipids, while the 68 vesicle lumen mainly contains periplasmic proteins (1). Many pathogenic Gram-negative bacteria species 69 extend their virulence potential by releasing spherical buds, derived from the outer membrane, so-called 70 outer membrane vesicles (2). The release of MVs can benefit the microbe, mediating microbial 71 interactions with the human host and within bacterial communities (3,2). Also, MV production protects 72 bacteria under stressful conditions by eliminating the accumu...

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Hijacking Host Cell Highways: Manipulation of the Host Actin Cytoskeleton by Obligate Intracellular Bacterial Pathogens

Cited by 81 publications

References 67 publications

Modulation of Microtubule Dynamics Affects Brucella abortus Intracellular Survival, Pathogen-Containing Vacuole Maturation, and Pro-inflammatory Cytokine Production in Infected Macrophages

Modulation of Microtubule Dynamics Affects Brucella abortus Intracellular Survival, Pathogen-Containing Vacuole Maturation, and Pro-inflammatory Cytokine Production in Infected Macrophages

Transcriptome Analyses of Diaphorina citri Midgut Responses to Candidatus Liberibacter Asiaticus Infection

Transcriptome responses of intestinal epithelial cells induced by membrane vesicles ofListeria monocytogenesunveil novel insights into the host-pathogen cross talk

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