4.6 Review

Why Argonaute is needed to make microRNA target search fast and reliable

Journal

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY
Volume 65, Issue -, Pages 20-28

Publisher

ACADEMIC PRESS LTD- ELSEVIER SCIENCE LTD
DOI: 10.1016/j.semcdb.2016.05.017

Keywords

Argonaute; miRNA; Target Search; Lateral diffusion; Single molecule; FRET; Free-energy landscape; Theoretical model; RNA silencing; Search stability paradox; MicroRNA target prediction

Funding

  1. European Research Council [309509]
  2. TU Delft start up
  3. Netherlands Organization for Scientific Research (NWO/OCW)
  4. European Research Council (ERC) [309509] Funding Source: European Research Council (ERC)

Ask authors/readers for more resources

MicroRNA (miRNA) interferes with the translation of cognate messenger RNA (mRNA) by finding, preferentially binding, and marking it for degradation. To facilitate the search process, Argonaute (Ago) proteins come together with miRNA, forming a dynamic search complex. In this review we use the language of free-energy landscapes to discuss recent single-molecule and high-resolution structural data in the light of theoretical work appropriated from the study of transcription-factor search. We suggest that experimentally observed internal states of the Ago-miRNA search complex may have the explicit biological function of speeding up search while maintaining specificity. (C) 2016 The Authors. Published by Elsevier Ltd.

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

mRNA structural dynamics shape Argonaute-target interactions

Suzan Ruijtenberg, Stijn Sonneveld, Tao Ju Cui, Ive Logister, Dion de Steenwinkel, Yao Xiao, Ian J. MacRae, Chirlmin Joo, Marvin E. Tanenbaum

NATURE STRUCTURAL & MOLECULAR BIOLOGY (2020)

Review Biochemistry & Molecular Biology

Small RNA-directed DNA elimination: the molecular mechanism and its potential for genome editing

Carolien Bastiaanssen, Chirlmin Joo

Summary: Tetrahymena uniquely deals with transposable elements by having separate somatic and germline genomes in a single cell. During sexual reproduction, a small RNA directed system compares the two genomes to identify and process transposable elements. The chromatin context in Tetrahymena allows for potential advantages in genome editing and gene therapy compared to the CRISPR-Cas9 system.

RNA BIOLOGY (2021)

Article Biochemistry & Molecular Biology

Targeting G-quadruplex Forming Sequences with Cas9

Hamza Balci, Viktorija Globyte, Chirlmin Joo

Summary: The structural characteristics of the complex formed by CRISPR-Cas9 and target DNA are influenced by the stability of GQ and the position of PQS, leading to variations in conformational states and dynamics. The presence of PQS in the target or nontarget strand results in different structural heterogeneity within the target dsDNA and the R-loop, impacting Cas9 activity.

ACS CHEMICAL BIOLOGY (2021)

Article Chemistry, Multidisciplinary

High-Resolution Single-Molecule FRET via DNA eXchange (FRET X)

Mike Filius, Sung Hyun Kim, Ivo Severins, Chirlmin Joo

Summary: The research team introduced a new method that allows for determining multiple distances between FRET pairs in a single object by resolving the FRET efficiency of multiple fluorophore pairs through transient binding of short DNA strands. This FRET X technology is expected to be a tool for high-resolution analysis of biomolecules and nanostructures.

NANO LETTERS (2021)

Review Biology

FRET-based dynamic structural biology: Challenges, perspectives and an appeal for open-science practices

Eitan Lerner, Anders Barth, Jelle Hendrix, Benjamin Ambrose, Victoria Birkedal, Scott C. Blanchard, Richard Boerner, Hoi Sung Chung, Thorben Cordes, Timothy D. Craggs, Ashok A. Deniz, Jiajia Diao, Jingyi Fei, Ruben L. Gonzalez, Irina Gopich, Taekjip Ha, Christian A. Hanke, Gilad Haran, Nikos S. Hatzakis, Sungchul Hohng, Seok-Cheol Hong, Thorsten Hugel, Antonino Ingargiola, Chirlmin Joo, Achillefs N. Kapanidis, Harold D. Kim, Ted Laurence, Nam Ki Lee, Tae-Hee Lee, Edward A. Lemke, Emmanuel Margeat, Jens Michaelis, Xavier Michalet, Sua Myong, Daniel Nettels, Thomas-Otavio Peulen, Evelyn Ploetz, Yair Razvag, Nicole C. Robb, Benjamin Schuler, Hamid Soleimaninejad, Chun Tang, Reza Vafabakhsh, Don C. Lamb, Claus A. M. Seidel, Shimon Weiss

Summary: Single-molecule FRET (smFRET) has become a mainstream technique for studying biomolecular structural dynamics, with significant progress being made in sample preparation, measurement procedures, data analysis, algorithms, and documentation. Efforts have been made to streamline experiments and analyze results for obtaining quantitative information. Open science practices are strongly encouraged for further progress in this field.

ELIFE (2021)

Article Biophysics

FRETboard: Semisupervised classification of FRET traces

Carlos Victor de Lannoy, Mike Filius, Sung Hyun Kim, Chirlmin Joo, Dick de Ridder

Summary: FRET is a useful phenomenon in biomolecular investigations for nanoscale measurements, and a semisupervised approach with the web tool FRETboard has been proposed to fit models more intuitively. This approach accurately reproduces ground truth FRET statistics in simulated scenarios and retrieves parameters in vitro data in a fraction of the time required for manual classification. Additionally, FRETboard is designed to easily adapt to future developments in FRET measurement and analysis by being extendable to other models.

BIOPHYSICAL JOURNAL (2021)

Article Biochemical Research Methods

The emerging landscape of single-molecule protein sequencing technologies

Javier Antonio Alfaro, Peggy Bohlander, Mingjie Dai, Mike Filius, Cecil J. Howard, Xander F. van Kooten, Shilo Ohayon, Adam Pomorski, Sonja Schmid, Aleksei Aksimentiev, Eric V. Anslyn, Georges Bedran, Chan Cao, Mauro Chinappi, Etienne Coyaud, Cees Dekker, Gunnar Dittmar, Nicholas Drachman, Rienk Eelkema, David Goodlett, Sebastien Hentz, Umesh Kalathiya, Neil L. Kelleher, Ryan T. Kelly, Zvi Kelman, Sung Hyun Kim, Bernhard Kuster, David Rodriguez-Larrea, Stuart Lindsay, Giovanni Maglia, Edward M. Marcotte, John P. Marino, Christophe Masselon, Michael Mayer, Patroklos Samaras, Kumar Sarthak, Lusia Sepiashvili, Derek Stein, Meni Wanunu, Mathias Wilhelm, Peng Yin, Amit Meller, Chirlmin Joo

Summary: Single-cell profiling methods have greatly impacted the understanding of cellular heterogeneity, although proteome profiling at the single-cell level is still in the early stages. The development of new technologies, such as single-molecule protein sequencing and innovations in mass spectrometry, will eventually enable broad sequence coverage in single-cell proteomics, leading to new biological discoveries and opportunities for ultra-sensitive disease diagnostics.

NATURE METHODS (2021)

Correction Biochemistry & Molecular Biology

mRNA structural dynamics shape Argonaute-target interactions (vol 27, pg 790, 2020)

Suzan Ruijtenberg, Stijn Sonneveld, Tao Ju Cui, Ive Logister, Dion de Steenwinkel, Yao Xiao, Ian J. MacRae, Chirlmin Joo, Marvin E. Tanenbaum

NATURE STRUCTURAL & MOLECULAR BIOLOGY (2021)

Article Optics

Drift correction in localization microscopy using entropy minimization

Jelmer Cnossen, Tao Ju Cui, Chirlmin Joo, Carlas Smith

Summary: The study introduces a new algorithm for drift estimation in localization microscopy, showing a 5x improvement in precision over the widely used RCC algorithm. The algorithm operates directly on fluorophore localizations and is tested on simulated and experimental datasets in 2D and 3D.

OPTICS EXPRESS (2021)

Review Biochemistry & Molecular Biology

Completing the canvas: advances and challenges for DNA-PAINT super-resolution imaging

Raman van Wee, Mike Filius, Chirlmin Joo

Summary: Single-molecule localization microscopy (SMLM) is a powerful tool for examining biological systems with unprecedented resolution. DNA-based point accumulation for imaging in nanoscale topography (DNA-PAINT) has faced challenges such as low throughput, long acquisition time, and difficulty integrating with live-cell imaging, but recent advances are addressing these issues and expanding its applications. The current state of DNA-PAINT is reviewed in light of these advancements, with consideration for further developments needed to achieve live-cell imaging.

TRENDS IN BIOCHEMICAL SCIENCES (2021)

Editorial Material Multidisciplinary Sciences

Leaders of the field: What does the future hold for single molecule technology?

Chirlmin Joo, Amit Meller

ISCIENCE (2021)

Article Multidisciplinary Sciences

Evaluation of FRET X for single-molecule protein fingerprinting

Carlos Victor de Lannoy, Mike Filius, Raman van Wee, Chirlmin Joo, Dick de Ridder

Summary: The study introduces a method called FRET X fingerprinting for single-molecule protein identification, which aims to create fingerprints for proteins. Through simulations and experimental validation, the effectiveness of the method was demonstrated, successfully identifying complex mixtures including multiple proteins, providing a new analysis tool for targeted proteomics.

ISCIENCE (2021)

Article Engineering, Electrical & Electronic

Classifiable Limiting Mass Change Detection in a Graphene Resonator Using Applied Machine Learning

Miri Seo, Eunseo Yang, Dong Hoon Shin, Yugyeong Je, Chirlmin Joo, Kookjin Lee, Sang Wook Lee

Summary: In this study, we successfully reduced noise interference and improved the accuracy of mass detection in suspended graphene-based nanomechanical resonators using machine learning techniques.

ACS APPLIED ELECTRONIC MATERIALS (2022)

Article Computer Science, Artificial Intelligence

AutoStepfinder: A fast and automated step detection method for single-molecule analysis

Luuk Loeff, Jacob W. J. Kerssemakers, Chirlmin Joo, Cees Dekker

Summary: Single-molecule techniques allow visualization of molecular dynamics with high resolution. AutoStepfinder is a fast, automated, bias-free step detection method that can be used for a wide variety of experimental traces, providing a robust and user-friendly analysis procedure.

PATTERNS (2021)

Article Biochemistry & Molecular Biology

Voices of chemical biology

Benjamin Davis, Keri Backus, Georg Winter, Roberto Chica, Dan Li, Sang Yup Lee, Chuan He, Amy Weeks, Christopher Overall, Shinya Hagihara, Ben Thuronyi, Siddhesh Kamat, Ling-Ling Chen, Ramon Hurtado Guerrero, Shao Yao, Lara K. Mahal, Christopher Voigt, Christina Woo, Erick Strauss, Kazuya Kikuchi, Timothy Dore, Sheena Radford, Xiang David Li, Won Do Heo, Giulio Superti-Furga, Tara Deans, Vsevolod Belousov, Megan Matthews, Colin Jackson, Shiva Malek, Herbert Waldmann, Anna Rising, Michael Jewett, Dimitrios Stamou, Emily Parker, Mario Murakami, Karen Polizzi, Itaru Hamachi, Tobias Erb, Chirlmin Joo, Motonari Uesugi, Rab Prinjha, Gidi Rechavi, Roberto Solano, Brenda Schulman, Yael David, Rob Oslund

Summary: In the last five years, the most exciting research achievements or technological innovations in chemical biology have garnered attention from many chemical biologists.

NATURE CHEMICAL BIOLOGY (2021)

Review Cell Biology

Composition and function of stress granules and P-bodies in plants

Alyssa Kearly, Andrew D. L. Nelson, Aleksandra Skirycz, Monika Chodasiewicz

Summary: Stress Granules (SGs) and Processing-bodies (P-bodies) are important biomolecular condensates that play crucial roles in maintaining mRNA balance and regulating stress responses. They are composed of proteins and RNAs involved in translation, protein folding, and energy metabolism.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Calvin cycle and guard cell metabolism impact stomatal function

P. Lemonnier, T. Lawson

Summary: Stomatal conductance plays a crucial role in determining CO2 uptake and water loss in plants, affecting overall water status and productivity. However, the signals coordinating mesophyll demands for CO2, the role of chloroplasts in stomatal function, and other GC metabolic processes in stomatal function remain poorly understood.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Perspectives on improving crop Rubisco by directed evolution

Matteo Gionfriddo, Timothy Rhodes, Spencer M. Whitney

Summary: Rubisco is a key enzyme that facilitates the entry of CO2 into the biosphere, but its catalytic properties are slow and error-prone. More effective Rubisco variants have been discovered in certain algae, offering the potential to significantly improve crop productivity. However, incompatibilities in protein folding have hindered the transplantation of these variants into plants. Directed evolution is now being explored to enhance Rubisco catalysis.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Natural variation in metabolism of the Calvin-Benson cycle

Vittoria Clapero, Stephanie Arrivault, Mark Stitt

Summary: The Calvin-Benson cycle has undergone massive selection and co-evolution with carbon-concentrating mechanisms due to changing environmental factors. Metabolite profiling reveals species-specific variations in the operation of the cycle, indicating the influence of different modes of photosynthesis. Connectivity analysis identifies constraints and driving factors for cross-species diversity in the cycle.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Emerging functions of thrombospondin-1 in immunity

Sukhbir Kaur, David D. Roberts

Summary: Thrombospondin-1 modulates cell behavior by interacting with components of the extracellular matrix and cell surface receptors. Its release and expression are influenced by injuries and various diseases, while its sustained presence in the extracellular space is regulated by receptor-mediated clearance. Thrombospondin-1 plays important roles in immune responses.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Molecular evolution of the Thrombospondin superfamily

Richard P. Tucker, Josephine C. Adams

Summary: Thrombospondins (TSPs) play diverse roles in animals and have been found to belong to a superfamily that includes different subgroups such as mega-TSPs, sushi-TSPs, and poriferan-TSPs. Invertebrates encode a greater diversity of TSP superfamily members than vertebrates.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Thrombospondins in the tumor microenvironment

James Petrik, Sylvia Lauks, Bianca Garlisi, Jack Lawler

Summary: Many cancers start with a small nest of transformed cells that can remain dormant. Thrombospondin-1 (TSP-1) initially promotes dormancy by suppressing angiogenesis, but over time, factors promoting angiogenesis become dominant and recruit various cells to form a complex tumor microenvironment. TSPs play a role in the proliferation, migration, and invasion of cells in the tumor microenvironment, as well as influencing the immune characteristics and phenotype of tumor-associated macrophages.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

The implications of physiological biomolecular condensates in amyotrophic lateral sclerosis

Hana Fakim, Christine Vande Velde

Summary: There has been increasing attention to the role of phase-separated biomolecular condensates, specifically stress granules, in neurodegenerative diseases like ALS. ALS-associated mutations in genes involved in stress granule assembly have been found, and stress granule proteins have been detected in pathological inclusions in ALS patient neurons. However, protein components of stress granules are also present in other physiological biomolecular condensates, which have not been adequately discussed in relation to ALS. This review explores the functions of TDP-43 and FUS in physiological condensates occurring in the nucleus and neurites beyond stress granules, and discusses the impact of ALS-linked mutations on their ability to phase separate and perform their functions in stress-independent biomolecular condensates.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Developmental heterogeneity of vascular cells: Insights into cellular plasticity in atherosclerosis?

Alexander Lin, Yogambha Ramaswamy, Ashish Misra

Summary: Smooth muscle cells, endothelial cells, and macrophages in blood vessels display remarkable heterogeneity, and their developmental origins may influence their plasticity. Unbiased single cell whole transcriptome analysis techniques are revolutionizing the understanding of cellular diversity and plasticity, providing insights for therapeutic research.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

The Calvin Benson cycle in bacteria: New insights from systems biology

Elton P. Hudson

Summary: The Calvin Benson cycle plays a crucial role in the ecological and biotechnological aspects of bacteria. Recent studies have shed light on the regulation of this cycle in bacteria, with post-transcriptional and post-translational regulation being important in phototrophic bacteria, and transcriptional regulation being prominent in chemolithoautotrophic bacteria. Understanding the regulation of the Calvin Benson cycle has implications for enhancing CO2 fixation and improving the synthesis of desired products. Non-canonical cycles may offer potential benefits for industrial applications.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Mechanisms controlling metabolite concentrations of the Calvin

Xin-Guang Zhu, Haim Treves, Honglong Zhao

Summary: This paper discusses the major regulatory mechanisms over the Calvin Benson Cycle (CBC) that maintain homeostasis of metabolite levels. These mechanisms include redox regulation of enzymes, metabolite regulations (especially allosteric regulations), and balanced activities of enzymes. These regulatory mechanisms are crucial for maintaining high flux and photosynthetic efficiency in CBC.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

The antagonistic relationship between apoptosis and polyploidy in development and cancer

Hunter C. Herriage, Yi-Ting Huang, Brian R. Calvi

Summary: Apoptosis prevents the inappropriate acquisition of extra copies of the genome, known as polyploidy, but the polyploid state can suppress apoptosis. The mechanisms linking apoptosis and polyploid cell cycles are still largely unknown, and studying the regulation of apoptosis in development and cancer could lead to more effective therapies.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

The mechanisms and roles of mitochondrial dynamics in C. elegans

Daniel Campbell, Steven Zuryn

Summary: Mitochondrial dynamics play a crucial role in regulating cellular and organismal homeostasis, impacting various aspects of an organism's healthspan. By studying the nematode Caenorhabditis elegans, a comprehensive understanding of the impact of mitochondrial dynamics on homeostasis over a lifetime can be obtained.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Vagal pathways for systemic regulation of glucose metabolism

Diba Borgmann, Henning Fenselau

Summary: Maintaining blood glucose at an appropriate physiological level requires coordination of multiple organs and tissues, with the vagus nerve playing a key role in central control. Recent studies have revealed the cellular identity, neuroanatomical organization, and functional contributions of vagal neurons in the regulation of systemic glucose metabolism. These findings provide new insights into the precise roles of vagal neurons in coordinating glucose levels and offer potential avenues for treating glucose metabolism disorders.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)

Review Cell Biology

Molecular cell types as functional units of the efferent vagus nerve

Tatiana C. Coverdell, Stephen B. G. Abbott, John N. Campbell

Summary: In this article, we review how genetic technology and single-cell genomics are revealing the organizational principles of the efferent vagus in unprecedented detail.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2024)