Potential Roles of Fungal Extracellular Vesicles during Infection

Joffe, Luna S.; Nimrichter, Leonardo; Rodrigues, Márcio L.; Poeta, Maurizio Del

doi:10.1128/msphere.00099-16

Cited by 103 publications

(80 citation statements)

References 90 publications

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“…TEM analysis of MalaEx isolated using sucrose gradient fractions with density 1.11–1.20 g/ml used for exosomes38 revealed the presence of exosome-like vesicles as previously described29. The cellular origin of fungal EV and the mechanisms to transverse the thick cell wall remains unknown1039. Future studies are needed to reveal the control of production and release of these vesicles.…”

Section: Discussionmentioning

confidence: 70%

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Identification of small RNAs in extracellular vesicles from the commensal yeast Malassezia sympodialis

Rayner

Bruhn

Vallhov

et al. 2017

Sci Rep

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Malassezia is the dominant fungus in the human skin mycobiome and is associated with common skin disorders including atopic eczema (AE)/dermatitis. Recently, it was found that Malassezia sympodialis secretes nanosized exosome-like vesicles, designated MalaEx, that carry allergens and can induce inflammatory cytokine responses. Extracellular vesicles from different cell-types including fungi have been found to deliver functional RNAs to recipient cells. In this study we assessed the presence of small RNAs in MalaEx and addressed if the levels of these RNAs differ when M. sympodialis is cultured at normal human skin pH versus the elevated pH present on the skin of patients with AE. The total number and the protein concentration of the released MalaEx harvested after 48 h culture did not differ significantly between the two pH conditions nor did the size of the vesicles. From small RNA sequence data, we identified a set of reads with well-defined start and stop positions, in a length range of 16 to 22 nucleotides consistently present in the MalaEx. The levels of small RNAs were not significantly differentially expressed between the two different pH conditions indicating that they are not influenced by the elevated pH level observed on the AE skin.Extracellular vesicles (EV) are released not only from different mammalian cell-types but also from microorganisms and parasites and have the capacity to transfer complex biological information [1][2][3][4][5] . Various types of EV ranging in size from 20 nm to 1,000 nm in diameter have been described and are classified mainly on their mechanisms of biogenesis and their physiological functions 1,6 . Those designated exosomes are nanosized vesicles of 50-100 nm which are released extracellularly after fusion of multicellular endosomes with the cell membrane, whereas microvesicles (MV) are larger vesicles (100-1,000 nm) generated through outward budding of the plasma membrane 1,5 . Gram-negative bacteria produce MV by outward budding of the outer membrane and these vesicles are therefore referred to as outer membrane vesicles (OMV) with a diameter in the range of 20-500 nm 6 . Exosomes can be detected in body fluids such as urine, bronchoalveolar lavage fluid (BAL), breast milk and serum 7 . The functions of exosomes include immunoregulatory mechanisms such as modulation of antigen presentation, immune activation, immune suppression, immune surveillance and intercellular communication 6 . EV from microorganisms with thick cell walls, such as Gram-positive bacteria and fungi, have been associated with cytotoxicity, the invasion of host cells, and the transfer of virulence factors 2 . As seen with exosomes 1,8 , fungal EV have been observed to deliver functional messenger (m)RNAs and micro (mi)RNA-like RNAs to recipient cells 9,10 . miRNAs are small non-coding RNAs with a length between 20 and 22 nucleotides (nt) 11 . They are spliced from precursor sequences that form the stable hairpin necessary for transportation from the nucleus to the cytoplasm. After the miRNA has been c...

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Section: Discussionmentioning

confidence: 70%

“…EV from microorganisms with thick cell walls, such as Gram-positive bacteria and fungi, have been associated with cytotoxicity, the invasion of host cells, and the transfer of virulence factors2. As seen with exosomes18, fungal EV have been observed to deliver functional messenger (m)RNAs and micro (mi)RNA-like RNAs to recipient cells910.…”

mentioning

confidence: 99%

Identification of small RNAs in extracellular vesicles from the commensal yeast Malassezia sympodialis

Rayner

Bruhn

Vallhov

et al. 2017

Sci Rep

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“…Fungal EVs are implicated in host pathogen interactions largely due to their activation of isolated immune cells. Several other functions have been postulated in fungal pathogenesis and disease . However, a better understanding of the basic EV biology is needed before studies on their role in disease can be progressed.…”

Section: What Does the Future Hold For Research On Fungal Evs?mentioning

confidence: 99%

Fungal Extracellular Vesicles with a Focus on Proteomic Analysis

2019

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Extracellular vesicles (EVs) perform crucial functions in cell–cell communication. The packaging of biomolecules into membrane‐enveloped vesicles prior to release into the extracellular environment provides a mechanism for coordinated delivery of multiple signals at high concentrations that is not achievable by classical secretion alone. Most of the understanding of the biosynthesis, composition, and function of EVs comes from mammalian systems. Investigation of fungal EVs, particularly those released by pathogenic yeast species, has revealed diverse cargo including proteins, lipids, nucleic acids, carbohydrates, and small molecules. Fungal EVs are proposed to function in a variety of biological processes including virulence and cell wall homeostasis with a focus on host–pathogen interactions. EVs also carry signals between fungal cells allowing for a coordinated attack on a host during infection. Research on fungal EVs in still in its infancy. Here a review of the literature thus far with a focus on proteomic analysis is provided with respect to techniques, results, and prospects.

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“…Two plant sRNAs were shown to be transferred to B. cinerea in EVs to target fungal genes involved in vesicle trafficking (Cai et al ., ). It is likely, but yet to be proven, that fungal EVs likewise ferry sRNA effectors into plant cells: although diverse sRNAs were detected in EVs from yeast species (Peres da Silva et al ., ; Joffe et al ., ), no data are currently available on the sRNA content of EVs from any filamentous fungus. EVs produced by ascomycete and basdiomycete yeasts have been intensively studied over the last decade, primarily for their protein, glycan and lipid contents, but they have so far only been characterized for their protein content from cultures of a single filamentous fungus, namely the wheat and human opportunistic pathogen Alternaria infectoria (Silva et al ., ).…”

Section: Translocation Of Fungal Npes Into Plant Cells: Are Extracellmentioning

confidence: 99%

Nonproteinaceous effectors: the terra incognita of plant–fungal interactions

2019

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Summary Molecular plant–fungal interaction studies have mainly focused on small secreted protein effectors. However, accumulating evidence shows that numerous fungal secondary metabolites are produced at all stages of plant colonization, especially during early asymptomatic/biotrophic phases. The discovery of fungal small RNAs targeting plant transcripts has expanded the fungal repertoire of nonproteinaceous effectors even further. The challenge now is to develop specific functional methods to fully understand the biological roles of these effectors. Studies on fungal extracellular vesicles are also needed because they could be the universal carriers of all kinds of fungal effectors. With this review, we aim to stimulate the nonproteinaceous effector research field to move from descriptive to functional studies, which should bring a paradigm shift in plant–fungal interactions.

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Potential Roles of Fungal Extracellular Vesicles during Infection

Cited by 103 publications

References 90 publications

Identification of small RNAs in extracellular vesicles from the commensal yeast Malassezia sympodialis

Identification of small RNAs in extracellular vesicles from the commensal yeast Malassezia sympodialis

Fungal Extracellular Vesicles with a Focus on Proteomic Analysis

Nonproteinaceous effectors: the terra incognita of plant–fungal interactions

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