Extracellular vesicles in plant host-microbe interaction

Extracellular vesicles (EVs) are secreted lipid bilayer membrane particles that are increasingly drawing attention due to their potential role in intercellular communication. EVs have been mainly reported in mammalian systems, but are also found in non-mammalian classes, such as Archeae, bacteria, fungi, oomycetes, protozoa, invertebrates and plants. Over the last decade, EV research on mammalian systems has been massively advanced driven by the interests and applications of the biomedical field, while research on non-mammalian EVs that aims to understand the biological origins and functions of EVs remains rather descriptive and premature. Nevertheless, recent pioneering works resulted in novel concepts that place EVs carrying regulatory small RNAs as central players in inter-species and cross-kingdom communication with emphasis on host-pathogen, host-parasite and host-microbiome interactions. EVs transport small RNAs from microbe/pathogen/parasite to animal or plant hosts, and vice versa, which results in the manipulation of host immunity or microbial virulence, respectively. This article highlights some of the latest discoveries regarding EV-mediated communication across species and kingdoms with a special focus on plants and their interacting microbes.

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Message in a Bubble: Shuttling Small RNAs and Proteins Between Cells and Interacting Organisms Using Extracellular Vesicles

Annual Review of Plant Biology ◽

10.1146/annurev-arplant-081720-010616 ◽

2021 ◽

Vol 72 (1) ◽

pp. 497-524

Author(s):

Qiang Cai ◽

Baoye He ◽

Shumei Wang ◽

Stephen Fletcher ◽

Dongdong Niu ◽

...

Keyword(s):

Rna Interference ◽

Lipid Bilayer ◽

Extracellular Vesicles ◽

Small Rnas ◽

Plant Cells ◽

Host Immunity ◽

Defense System ◽

Cellular Processes ◽

Pathogen Virulence ◽

Extracellular Environment

Communication between plant cells and interacting microorganisms requires the secretion and uptake of functional molecules to and from the extracellular environment and is essential for the survival of both plants and their pathogens. Extracellular vesicles (EVs) are lipid bilayer–enclosed spheres that deliver RNA, protein, and metabolite cargos from donor to recipient cells and participate in many cellular processes. Emerging evidencehas shown that both plant and microbial EVs play important roles in cross-kingdom molecular exchange between hosts and interacting microbes to modulate host immunity and pathogen virulence. Recent studies revealed that plant EVs function as a defense system by encasing and delivering small RNAs (sRNAs) into pathogens, thereby mediating cross-species and cross-kingdom RNA interference to silence virulence-related genes. This review focuses on the latest advances in our understanding of plant and microbial EVs and their roles in transporting regulatory molecules, especially sRNAs, between hosts and pathogens. EV biogenesis and secretion are also discussed, as EV function relies on these important processes.

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Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes

Science ◽

10.1126/science.aar4142 ◽

2018 ◽

Vol 360 (6393) ◽

pp. 1126-1129 ◽

Cited By ~ 222

Author(s):

Qiang Cai ◽

Lulu Qiao ◽

Ming Wang ◽

Baoye He ◽

Feng-Mao Lin ◽

...

Keyword(s):

Rna Interference ◽

Immune Responses ◽

Extracellular Vesicles ◽

Fungal Pathogen ◽

Small Rnas ◽

Virulence Genes ◽

Host Immunity ◽

Arms Race ◽

Host Cells ◽

Fungal Genes

Some pathogens and pests deliver small RNAs (sRNAs) into host cells to suppress host immunity. Conversely, hosts also transfer sRNAs into pathogens and pests to inhibit their virulence. Although sRNA trafficking has been observed in a wide variety of interactions, how sRNAs are transferred, especially from hosts to pathogens and pests, is still unknown. Here, we show that hostArabidopsiscells secrete exosome-like extracellular vesicles to deliver sRNAs into fungal pathogenBotrytis cinerea. These sRNA-containing vesicles accumulate at the infection sites and are taken up by the fungal cells. Transferred host sRNAs induce silencing of fungal genes critical for pathogenicity. Thus,Arabidopsishas adapted exosome-mediated cross-kingdom RNA interference as part of its immune responses during the evolutionary arms race with the pathogen.

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Small RNA trafficking at the forefront of plant–pathogen interactions

F1000Research ◽

10.12688/f1000research.15761.1 ◽

2018 ◽

Vol 7 ◽

pp. 1633 ◽

Cited By ~ 3

Author(s):

Yan Zhao ◽

Xiangxiu Liang ◽

Jian-Min Zhou

Keyword(s):

Extracellular Vesicles ◽

Small Rna ◽

Plant Pathogen ◽

Small Rnas ◽

Plant Cells ◽

Host Immunity ◽

Lytic Enzymes ◽

Pathogen Virulence ◽

Pathogenic Microbes ◽

Plant Pathogen Interactions

Plants and pathogenic microbes are engaged in constant attacks and counterattacks at the interface of the interacting organisms. Much of the molecular warfare involves cross-kingdom trafficking of proteins, nucleic acids, lipids, and metabolites that act as toxins, inhibitors, lytic enzymes, and signaling molecules. How various molecules are transported across the boundaries of plants and pathogens has remained largely unknown until now. Extracellular vesicles have emerged as likely carriers of molecular ammunition for both plants and pathogens. Recent advances are beginning to show how extracellular vesicles serve as powerful vehicles that transfer small RNAs from plants to fungal cells to diminish pathogen virulence and from fungi to plant cells to dampen host immunity.

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Different miRNA Profiles in Plasma Derived Small and Large Extracellular Vesicles from Patients with Neurodegenerative Diseases

International Journal of Molecular Sciences ◽

10.3390/ijms22052737 ◽

2021 ◽

Vol 22 (5) ◽

pp. 2737

Author(s):

Daisy Sproviero ◽

Stella Gagliardi ◽

Susanna Zucca ◽

Maddalena Arigoni ◽

Marta Giannini ◽

...

Keyword(s):

Neurodegenerative Diseases ◽

Extracellular Vesicles ◽

Small Rnas ◽

Biomarker Discovery ◽

Toll Like Receptor ◽

Neurotrophin Signaling ◽

Next Generation Sequencing Ngs ◽

Generation Sequencing ◽

Lateral Sclerosis ◽

Glycosphingolipid Biosynthesis

Identifying biomarkers is essential for early diagnosis of neurodegenerative diseases (NDs). Large (LEVs) and small extracellular vesicles (SEVs) are extracellular vesicles (EVs) of different sizes and biological functions transported in blood and they may be valid biomarkers for NDs. The aim of our study was to investigate common and different miRNA signatures in plasma derived LEVs and SEVs of Alzheimer’s disease (AD), Parkinson’s disease (PD), Amyotrophic Lateral Sclerosis (ALS) and Fronto-Temporal Dementia (FTD) patients. LEVs and SEVs were isolated from plasma of patients and healthy volunteers (CTR) by filtration and differential centrifugation and RNA was extracted. Small RNAs libraries were carried out by Next Generation Sequencing (NGS). MiRNAs discriminate all NDs diseases from CTRs and they can provide a signature for each NDs. Common enriched pathways for SEVs were instead linked to ubiquitin mediated proteolysis and Toll-like receptor signaling pathways and for LEVs to neurotrophin signaling and Glycosphingolipid biosynthesis pathway. LEVs and SEVs are involved in different pathways and this might give a specificity to their role in the spreading of the disease. The study of common and different miRNAs transported by LEVs and SEVs can be of great interest for biomarker discovery and for pathogenesis studies in neurodegeneration.

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The Cellular and Biological Impact of Extracellular Vesicles in Pancreatic Cancer

Cancers ◽

10.3390/cancers13123040 ◽

2021 ◽

Vol 13 (12) ◽

pp. 3040

Author(s):

Zainab Hussain ◽

Jeremy Nigri ◽

Richard Tomasini

Keyword(s):

Pancreatic Cancer ◽

Tumor Cells ◽

Extracellular Vesicles ◽

Cell Communication ◽

Pancreatic Tumors ◽

Mediated Communication ◽

Biological Impact ◽

Physiological Relevance ◽

Cellular Components ◽

Tumoral Cells

Deciphering the interactions between tumor and stromal cells is a growing field of research to improve pancreatic cancer-associated therapies and patients’ care. Indeed, while accounting for 50 to 90% of the tumor mass, many pieces of evidence reported that beyond their structural role, the non-tumoral cells composing the intra-tumoral microenvironment influence tumor cells’ proliferation, metabolism, cell death and resistance to therapies, among others. Simultaneously, tumor cells can influence non-tumoral neighboring or distant cells in order to shape a tumor-supportive and immunosuppressive environment as well as influencing the formation of metastatic niches. Among intercellular modes of communication, extracellular vesicles can simultaneously transfer the largest variety of signals and were recently reported as key effectors of cell–cell communication in pancreatic cancer, from its development to its evolution as well as its ability to resist available treatments. This review focuses on extracellular vesicles-mediated communication between different cellular components of pancreatic tumors, from the modulation of cellular activities and abilities to their biological and physiological relevance. Taking into consideration the intra-tumoral microenvironment and its extracellular-mediated crosstalk as main drivers of pancreatic cancer development should open up new therapeutic windows.

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The Yin and Yang of tumour-derived extracellular vesicles in tumour immunity

The Journal of Biochemistry ◽

10.1093/jb/mvaa132 ◽

2020 ◽

Author(s):

Takayoshi Yamauchi ◽

Toshiro Moroishi

Keyword(s):

Extracellular Vesicles ◽

Tumour Progression ◽

Tumour Microenvironment ◽

Host Immunity ◽

Biological Processes ◽

Small Particles ◽

Tumour Immunity ◽

Heterogeneous Nature ◽

Yin And Yang ◽

Cellular Components

Abstract Extracellular vesicles (EVs) are small particles that are naturally released from various types of cells. EVs contain a wide variety of cellular components, such as proteins, nucleic acids, lipids and metabolites, which facilitate intercellular communication in diverse biological processes. In the tumour microenvironment, EVs have been shown to play important roles in tumour progression, including immune system–tumour interactions. Although previous studies have convincingly demonstrated the immunosuppressive functions of tumour-derived EVs, some studies have suggested that tumour-derived EVs can also stimulate host immunity, especially in therapeutic conditions. Recent studies have revealed the heterogeneous nature of EVs with different structural and biological characteristics that may account for the divergent functions of EVs in tumour immunity. In this review article, we provide a brief summary of our current understanding of tumour-derived EVs in immune activation and inhibition. We also highlight the emerging utility of EVs in the diagnosis and treatment of cancers and discuss the potential clinical applications of tumour-derived EVs.

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Host-parasite dynamics and the evolution of host immunity and parasite fecundity strategies

Bulletin of Mathematical Biology ◽

10.1007/bf02459459 ◽

1997 ◽

Vol 59 (3) ◽

pp. 427-450 ◽

Cited By ~ 19

Author(s):

Veijo Kaitala ◽

Mikko Heino ◽

Wayne M. Getz

Keyword(s):

Host Immunity ◽

Host Parasite ◽

Parasite Dynamics

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Potential Role of Small RNAs during Stress in Plants

Molecular Approaches in Plant Abiotic Stress ◽

10.1201/b15538-8 ◽

2013 ◽

pp. 85-107

Keyword(s):

Small Rnas ◽

Potential Role

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Immune Cell-Derived Extracellular Vesicles – New Strategies in Cancer Immunotherapy

Frontiers in Immunology ◽

10.3389/fimmu.2021.771551 ◽

2021 ◽

Vol 12 ◽

Author(s):

Pengxiang Yang ◽

Yong Peng ◽

Yuan Feng ◽

Zhuoying Xu ◽

Panfeng Feng ◽

...

Keyword(s):

Extracellular Vesicles ◽

Immune Cell ◽

Bilayer Membrane ◽

Innate Immune ◽

Antitumor Effects ◽

Comprehensive Overview ◽

Surface Receptors ◽

Effector Molecules ◽

Therapeutic Modalities ◽

Pass Through

Immune cell-derived extracellular vesicles (EVs) have increasingly become the focus of research due to their unique characteristics and bioinspired applications. They are lipid bilayer membrane nanosized vesicles harboring a range of immune cell-derived surface receptors and effector molecules from parental cells. Immune cell-derived EVs are important mediators of intercellular communication that regulate specific mechanisms of adaptive and innate immune responses. However, the mechanisms underlying the antitumor effects of EVs are still being explored. Importantly, immune cell-derived EVs have some unique features, including accessibility, storage, ability to pass through blood-brain and blood-tumor barriers, and loading of various effector molecules. Immune cell-derived EVs have been directly applied or engineered as potent antitumor vaccines or for the diagnosis of clinical diseases. More research applications involving genetic engineering, membrane engineering, and cargo delivery strategies have improved the treatment efficacy of EVs. Immune cell-derived EV-based therapies are expected to become a separate technique or to complement immunotherapy, radiotherapy, chemotherapy and other therapeutic modalities. This review aims to provide a comprehensive overview of the characteristics and functions of immune cell-derived EVs derived from adaptive (CD4+ T, CD8+ T and B cells) and innate immune cells (macrophages, NK cells, DCs, and neutrophils) and discuss emerging therapeutic opportunities and prospects in cancer treatment.

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