4.6 Article

dRYBP Contributes to the Negative Regulation of the Drosophila Imd Pathway

Journal

PLOS ONE
Volume 8, Issue 4, Pages -

Publisher

PUBLIC LIBRARY SCIENCE
DOI: 10.1371/journal.pone.0062052

Keywords

-

Funding

  1. Direccion General de Investigacion [BFU2008-01154]
  2. Program of the Ministerio de Ciencia e Innovacion [CSD 2007-00008]
  3. Fundacion Ramon Areces to the Centro de Biologia Molecular Severo Ochoa
  4. National Research Fund Luxembourg (AFR) [08/037]
  5. Bettencourt-Schueller Foundation
  6. ERC Advanced Grant
  7. Swiss National Fund [3100A0-12079/1]

Ask authors/readers for more resources

The Drosophila humoral innate immune response fights infection by producing antimicrobial peptides (AMPs) through the microbe-specific activation of the Toll or the Imd signaling pathway. Upon systemic infection, the production of AMPs is both positively and negatively regulated to reach a balanced immune response required for survival. Here, we report the function of the dRYBP (drosophila Ring and YY1 Binding Protein) protein, which contains a ubiquitin-binding domain, in the Imd pathway. We have found that dRYBP contributes to the negative regulation of AMP production: upon systemic infection with Gram-negative bacteria, Diptericin expression is up-regulated in the absence of dRYBP and down-regulated in the presence of high levels of dRYBP. Epistatic analyses using gain and loss of function alleles of imd, Relish, or skpA and dRYBP suggest that dRYBP functions upstream or together with SKPA, a member of the SCF-E3-ubiquitin ligase complex, to repress the Imd signaling cascade. We propose that the role of dRYBP in the regulation of the Imd signaling pathway is to function as a ubiquitin adaptor protein together with SKPA to promote SCF-dependent proteasomal degradation of Relish. Beyond the identification of dRYBP as a novel component of Imd pathway regulation, our results also suggest that the evolutionarily conserved RYBP protein may be involved in the human innate immune response.

Authors

I am an author on this paper
Click your name to claim this paper and add it to your profile.

Reviews

Primary Rating

4.6
Not enough ratings

Secondary Ratings

Novelty
-
Significance
-
Scientific rigor
-
Rate this paper

Recommended

Article Biochemistry & Molecular Biology

Steroid-dependent switch of OvoL/Shavenbaby controls self-renewal versus differentiation of intestinal stem cells

Sandy Al Hayek, Ahmad Alsawadi, Zakaria Kambris, Jean-Philippe Boquete, Jerome Bohere, Clement Immarigeon, Brice Ronsin, Serge Plaza, Bruno Lemaitre, Francois Payre, Dani Osman

Summary: The research uncovers a cell-intrinsic role of the OvoL family transcription factor Shavenbaby (Svb) in balancing self-renewal and differentiation of Drosophila intestinal stem cells, mediated by the downstream target of Wnt and EGFR pathways. The switch between Svb repressor and activator is triggered by systemic steroid hormone, adjusting stem cell proliferation versus differentiation and suggesting a broad role of OvoL/Svb in adult and cancer stem cells.

EMBO JOURNAL (2021)

Editorial Material Cell Biology

Foundational Article: Mechnikov I, 1909: Intestinal Bacteriotherapy*

Claudine Neyen

JOURNAL OF LEUKOCYTE BIOLOGY (2021)

Article Genetics & Heredity

Rapid molecular evolution of Spiroplasma symbionts of Drosophila

Michael Gerth, Humberto Martinez-Montoya, Paulino Ramirez, Florent Masson, Joanne S. Griffin, Rodolfo Aramayo, Stefanos Siozios, Bruno Lemaitre, Mariana Mateos, Gregory D. D. Hurst

Summary: Studies have shown that Spiroplasma has a rapid evolutionary rate, high substitution rate, significant genomic structural differences, and the absence of mismatch repair loci may contribute to the elevated substitution rates. Different Spiroplasma lineages exhibit dynamic evolution in their morphology, and loci similar to the malekilling toxin Spaid have been identified in various Spiroplasma strains and other endosymbionts.

MICROBIAL GENOMICS (2021)

Article Multidisciplinary Sciences

Dual proteomics of Drosophila melanogaster hemolymph infected with the heritable endosymbiont Spiroplasma poulsonii

Florent Masson, Samuel Rommelaere, Alice Marra, Fanny Schuepfer, Bruno Lemaitre

Summary: Insects are frequently infected with heritable bacterial endosymbionts, which have a significant impact on host physiology and evolution. This study reveals the chronic activation of the Toll immune pathway by the endosymbiont Spiroplasma poulsonii in Drosophila hemolymph through dual proteomics analysis, which was not detected by transcriptomics-based approaches. Candidate proteins potentially involved in controlling S. poulsonii growth were also identified through Drosophila genetics.

PLOS ONE (2021)

Article Biochemistry & Molecular Biology

A secreted factor NimrodB4 promotes the elimination of apoptotic corpses by phagocytes in Drosophila

Bianca Petrignani, Samuel Rommelaere, Ketty Hakim-Mishnaevski, Florent Masson, Elodie Ramond, Reut Hilu-Dadia, Mickael Poidevin, Shu Kondo, Estee Kurant, Bruno Lemaitre

Summary: This study reveals the crucial role of the Nimrod family member NimB4 in the clearance of apoptotic cells in Drosophila, particularly in phagosome maturation, possibly through binding to apoptotic corpses to engage a phagosome maturation program dedicated to efferocytosis.

EMBO REPORTS (2021)

Article Microbiology

Drosophila Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance

A. Marra, M. A. Hanson, S. Kondo, B. Erkosar, B. Lemaitre

Summary: This study demonstrates that the immune effectors, antimicrobial peptides, and lysozymes actively regulate the composition and abundance of gut microbiota in fruit flies. Loss of these immune effectors exacerbates during aging, leading to increased microbiota abundance and shifted composition in aged flies. The findings suggest that immune effectors, known for resistance against pathogens, also influence the beneficial gut community composition.
Article Microbiology

The Drosophila Baramicin polypeptide gene protects against fungal infection

Mark Austin Hanson, Lianne B. Cohen, Alice Marra, Igor Iatsenko, Steven A. Wasserman, Bruno Lemaitre

Summary: The fruit fly Drosophila melanogaster produces a variety of effector peptides to combat microbial infection, including a novel antifungal peptide gene named Baramicin A. This gene is strongly induced in the fat body downstream of the Toll pathway and plays a key role in the antimicrobial response of the fruit fly.

PLOS PATHOGENS (2021)

Article Genetics & Heredity

Cecropins contribute to Drosophila host defense against a subset of fungal and Gram-negative bacterial infection

Alexia L. Carboni, Mark A. Hanson, Scott A. Lindsay, Steven A. Wasserman, Bruno Lemaitre

Summary: Cecropins are small helical secreted peptides with antimicrobial activity that play an important role in host defense. Experimental studies have shown that Cecropins play a role in defense against Gram-negative bacteria and fungi in fruit flies.

GENETICS (2022)

Article Multidisciplinary Sciences

The wall-less bacterium Spiroplasma poulsonii builds a polymeric cytoskeleton composed of interacting MreB isoforms

Florent Masson, Xavier Pierrat, Bruno Lemaitre, Alexandre Persat

Summary: A rigid cell wall defines bacteria morphology, but wall-less Spiroplasma have five homologs of MreB. Research shows that these homologs play a key role in forming a polymeric cytoskeleton in shaping the cell.

ISCIENCE (2021)

Article Multidisciplinary Sciences

Disproportionate investment in Spiralin B production limits in-host growth and favors the vertical transmission of Spiroplasma insect endosymbionts

Florent Masson, Samuel Rommelaere, Fanny Schupfer, Jean-Philippe Boquete, Bruno Lemaitre

Summary: The abundance and amino acid composition of a protein called Spiralin B (SpiB) plays a crucial role in the nutritional interactions between insects and their endosymbionts. Increasing SpiB levels disrupts the localization of endosymbionts in insect eggs and decreases vertical transmission. This protein ensures the durability of the interaction in a variable environment.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2022)

Article Biology

Drosophila immunity: the Drosocin gene encodes two host defence peptides with pathogen-specific roles

M. A. Hanson, S. Kondo, B. Lemaitre

Summary: Antimicrobial peptides (AMPs) play a crucial role in defending against infection in plants and animals. A study on Drosophila has revealed that the Drosocin gene encodes two prominent host defense peptides with different specificities against distinct pathogens.

PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES (2022)

Article Genetics & Heredity

Repeated truncation of a modular antimicrobial peptide gene for neural context

Mark Hanson, Bruno Lemaitre

Summary: Antimicrobial peptides (AMPs) are host-encoded antibiotics that not only combat invading pathogens, but also have roles in neurological contexts. The evolutionary history of Baramicin genes reveals how they have adapted for either immune-specific or neurological roles, providing a case study for how AMP-encoding genes might play dual roles in both immune and non-immune processes via their multiple peptide products.

PLOS GENETICS (2022)

Article Cell Biology

Antimicrobial peptides do not directly contribute to aging in Drosophila, but improve lifespan by preventing dysbiosis

Mark A. Hanson, Bruno Lemaitre

Summary: Antimicrobial peptides (AMPs) play important roles in host defense and have been implicated in the clearance of aberrant cells and neurodegenerative syndromes. AMPs are produced in Drosophila downstream of Toll and Imd NF-κB pathways and have antimicrobial properties. Aging leads to upregulation of AMPs, potentially contributing to age-associated inflammatory diseases. However, the individual effects of AMPs on lifespan have been inconclusive. In this study, the researchers found no significant effect of individual AMPs on lifespan, except for Defensin. However, flies lacking seven AMP gene families displayed a reduced lifespan due to microbiome dysbiosis, and germ-free conditions extended their lifespan. Overall, AMPs collectively impact lifespan by preventing dysbiosis during aging.

DISEASE MODELS & MECHANISMS (2023)

Article Multidisciplinary Sciences

Ecology-relevant bacteria drive the evolution of host antimicrobial peptides in Drosophila

M. A. Hanson, L. Grollmus, B. Lemaitre

Summary: Antimicrobial peptides, encoded by the host, play a crucial role in combating pathogens and shaping the microbiome in plants and animals. This study focuses on the Diptericin antimicrobial peptide family of Diptera and reveals the specific roles of DptA and DptB in Drosophila melanogaster, demonstrating how they interact with different bacteria. The findings also highlight the correlation between the presence of DptA- or DptB-like genes and the presence of specific bacteria across Diptera.

SCIENCE (2023)

No Data Available