A Conserved LIM Protein That Affects Muscular Adherens Junction Integrity and Mechanosensory Function in Caenorhabditis elegans

We describe here the molecular and functional characterization of the Caenorhabditis elegans unc-97 gene, whose gene product constitutes a novel component of muscular adherens junctions. UNC-97 and homologues from several other species define the PINCH family, a family of LIM proteins whose modular composition of five LIM domains implicates them as potential adapter molecules. unc-97 expression is restricted to tissue types that attach to the hypodermis, specifically body wall muscles, vulval muscles, and mechanosensory neurons. In body wall muscles, the UNC-97 protein colocalizes with the β-integrin PAT-3 to the focal adhesion-like attachment sites of muscles. Partial and complete loss-of-function studies demonstrate that UNC-97 affects the structural integrity of the integrin containing muscle adherens junctions and contributes to the mechanosensory functions of touch neurons. The expression of a Drosophila homologue of unc-97 in two integrin containing cell types, muscles, and muscle-attached epidermal cells, suggests that unc-97 function in adherens junction assembly and stability has been conserved across phylogeny. In addition to its localization to adherens junctions UNC-97 can also be detected in the nucleus, suggesting multiple functions for this LIM domain protein.

• Publication year

  1999

• Venue

  Journal of Cell Biology

• Publication date

  1999-01-11

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1083/JCB.144.1.45PMID 9885243PMCID 2148118
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• The uric-86 Gene Product Couples Cell Lineage and Cell Identity in C . elegans

  2003cited by this paper
• The LIM-Only Protein PINCH Directly Interacts with Integrin-Linked Kinase and Is Recruited to Integrin-Rich Sites in Spreading Cells

  1999influential reference
• Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans

  1998cited by this paper
• Structure and function in the nucleus.

  1998cited by this paper
• LIM Protein KyoT2 Negatively Regulates Transcription by Association with the RBP-J DNA-Binding Protein

  1998cited by this paper
• LIM domains: multiple roles as adapters and functional modifiers in protein interactions.

  1998influential reference
• Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants.

  1997cited by this paper
• Comparison of Three Members of the Cysteine-rich Protein Family Reveals Functional Conservation and Divergent Patterns of Gene Expression*

  1997cited by this paper
• Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD

  1997influential reference
• Actinin-associated LIM Protein: Identification of a Domain Interaction between PDZ and Spectrin-like Repeat Motifs

  1997cited by this paper
• Muscle: Structure, Function, and Development

  1997cited by this paper
• The LIM‐only protein Lmo2 is a bridging molecule assembling an erythroid, DNA‐binding complex which includes the TAL1, E47, GATA‐1 and Ldb1/NLI proteins

  1997cited by this paper
• MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure.

  1997cited by this paper
• Nuclear–Cytoplasmic Shuttling of the Focal Contact Protein, Zyxin: A Potential Mechanism for Communication between Sites of Cell Adhesion and the Nucleus

  1997cited by this paper
• Cloning and characterization of the

  1996cited by this paper
• Cell autonomous expression of perlecan and plasticity of cell shape in embryonic muscle of Caenorhabditis elegans.

  1996cited by this paper
• Two muscle-specific LIM proteins in Drosophila

  1996influential reference
• Talin requires beta-integrin, but not vinculin, for its assembly into focal adhesion-like structures in the nematode Caenorhabditis elegans.

  1996cited by this paper
• Specificity of single LIM motifs in targeting and LIM/LIM interactions in situ.

  1996cited by this paper
• Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase

  1996cited by this paper
• Characterization of beta pat-3 heterodimers, a family of essential integrin receptors in C. elegans

  1995influential reference
• Integrins and signal transduction pathways: the road taken.

  1995cited by this paper
• Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family

  1995cited by this paper
• In situ hybridization to RNA.

  1994cited by this paper
• The LIM domain is a modular protein-binding interface.

  1994cited by this paper
• Molecular biology of muscle development.

  1994cited by this paper
• Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans

  1994cited by this paper
• Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations

  1994cited by this paper
• Biochemical and molecular characterization of the chicken cysteine-rich protein, a developmentally regulated LIM-domain protein that is associated with the actin cytoskeleton

  1994cited by this paper
• The LIM/double zinc-finger motif functions as a protein dimerization domain.

  1994cited by this paper
• The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development.

  1994cited by this paper
• A new LIM protein containing an autoepitope homologous to "senescent cell antigen".

  1994influential reference
• Cloning and characterization of αPS1, a novel Drosophila melanogaster integrin

  1993cited by this paper
• Myosin and paramyosin of Caenorhabditis elegans embryos assemble into nascent structures distinct from thick filaments and multi-filament assemblages

  1993influential reference
• Cloning and characterization of alpha PS1, a novel Drosophila melanogaster integrin.

  1993cited by this paper
• Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan.

  1993cited by this paper
• Zyxin and cCRP: two interactive LIM domain proteins associated with the cytoskeleton

  1992cited by this paper
• Vinculin is essential for muscle function in the nematode

  1991influential reference
• Muscle cell attachment in Caenorhabditis elegans

  1991cited by this paper
• A role for integrin in the formation of sarcomeric cytoarchitecture.

  1990cited by this paper
• Paxillin: a new vinculin-binding protein present in focal adhesions

  1990influential reference
• The function of PS integrins during Drosophila embryogenesis.

  1989cited by this paper
• mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans.

  1988cited by this paper
• The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localized to muscle attachments.

  1987cited by this paper
• Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization

  1985influential reference
• The neural circuit for touch sensitivity in Caenorhabditis elegans

  1985cited by this paper
• The embryonic cell lineage of the nematode Caenorhabditis elegans.

  1983cited by this paper
• Identification of genetic elements associated with muscle structure in the nematode Caenorhabditis elegans.

  1980cited by this paper
• Mutants with altered muscle structure of Caenorhabditis elegans.

  1980cited by this paper
• The phenogenetics of the embryonic mutant, lethal myospheroid, in Drosophila melanogaster.

  1960cited by this paper

• Mechanism of (+)-Isoaltholactone from Goniothalamus griffithii with Excellent Nematicidal Activity against Meloidogyne incognita.

  2025cites this paper
• The β integrin modulates serotonin sensitivity via NPxY motifs to regulate egg laying and mechanosensation behaviors in C. elegans

  2025cites this paper
• The ILK–PINCH–parvin complex: a conserved primary adhesome regulating biological processes

  2025cites this paper
• Microfluidic approach to correlate C. elegans neuronal functional aging and underlying changes of gene expression in mechanosensation

  2024cites this paper
• Sequences in the myosin A rod interact with UNC‐89/obscurin and the zinc‐finger protein UNC‐98 during thick filament assembly and M‐line formation in C. elegans striated muscle

  2024cites this paper
• Forkhead transcription factor FKH-8 cooperates with RFX in the direct regulation of sensory cilia in Caenorhabditis elegans

  2023cites this paper
• The Muscleblind-like protein MBL-1 regulates microRNA expression in Caenorhabditis elegans through an evolutionarily conserved autoregulatory mechanism

  2023cites this paper
• The role of crm-1 in ionizing radiation-induced nervous system dysfunction in Caenorhabditis elegans

  2022cites this paper
• Pinch2 is a novel regulator of myelination in the Central Nervous System

  2022cites this paper
• Neuron-epidermal attachment protects hyper-fragile axons from mechanical strain.

  2022cites this paper
• The role of Actopaxin in tumor metastasis.

  2022cites this paper
• Genetic analysis suggests a surface of PAT-4 (ILK) that interacts with UNC-112 (kindlin)

  2022cites this paper
• Characterisation of a nucleo-adhesome

  2022cites this paper
• Forkhead transcription factor FKH-8 is a master regulator of primary cilia in C. elegans

  2021cites this paper
• The Doublesex/Mab-3 domain transcription factor DMD-10 regulates ASH-dependent behavioral responses

  2021cites this paper
• Multiple Molecular Mechanisms Rescue mtDNA Disease in C. Multiple Molecular Mechanisms Rescue mtDNA Disease in C. elegans Let us know how access to this document benefits you.

  2021cites this paper
• Cisplatin-induced neurotoxicity involves the disruption of serotonergic neurotransmission.

  2021cites this paper
• The RGD (Arg-Gly-Asp) is a potential cell-binding motif of UNC-52/PERLECAN.

  2021cites this paper
• Crk and Crkl have shared functions in neural crest cells for cardiac outflow tract septation and vascular smooth muscle differentiation.

  2021cites this paper
• Characterisation of a nucleo-adhesome

  2021cites this paper
• Fatty acids impact sarcomere integrity through myristoylation and ER homeostasis

  2021cites this paper
• Requirement for PINCH in skeletal myoblast differentiation

  2021cites this paper
• PINCH-1 regulates mitochondrial dynamics to promote proline synthesis and tumor growth

  2020cites this paper
• Construction of a Five-Super-Enhancer-Associated-Genes Prognostic Model for Osteosarcoma Patients

  2020cites this paper
• Inflammation-induced PINCH expression leads to actin depolymerization and mitochondrial mislocalization in neurons

  2020cites this paper
• RSU-1 interaction with prohibitin-2 links cell–extracellular matrix detachment to downregulation of ERK signaling

  2020cites this paper
• LDB1 and the SWI/SNF complex participate in both transcriptional activation and repression by Caenorhabditis elegans BLIMP1/PRDM1.

  2020cites this paper
• RSU-1 interaction with prohibitin-2 links cell-extracellular matrix detachment to down-regulation of extracellular signal-regulated kinase signalling.

  2020cites this paper
• Signaling by AWC Olfactory Neurons Is Necessary for Caenorhabditis elegans’ Response to Prenol, an Odor Associated with Nematode-Infected Insects

  2020cites this paper
• An autism-causing calcium channel variant functions with selective autophagy to alter axon targeting and behavior

  2019cites this paper
• LIMS1 Promotes Pancreatic Cancer Cell Survival under Oxygen–Glucose Deprivation Conditions by Enhancing HIF1A Protein Translation

  2019cites this paper
• Swim exercise in C. elegans extends neuromuscular and intestinal healthspan, enhances learning ability, and protects against neurodegeneration

  2019cites this paper
• Purine Homeostasis Is Necessary for Developmental Timing, Germline Maintenance and Muscle Integrity in Caenorhabditis elegans

  2019cites this paper
• Gap junctions in the C. elegans nervous system regulate ageing and lifespan

  2019cites this paper
• Multiple Molecular Mechanisms Rescue mtDNA Disease in C. elegans

  2018cites this paper
• FBI-1 mRNA in normal mucosa is an independent prognostic factor in colorectal cancer patients.

  2018cites this paper
• Caenorhabditis elegans SORB-1 localizes to integrin adhesion sites and is required for organization of sarcomeres and mitochondria in myocytes

  2017cites this paper
• High‐resolution imaging of muscle attachment structures in Caenorhabditis elegans

  2017influential citation
• let-7 miRNA controls CED-7 homotypic adhesion and EFF-1–mediated axonal self-fusion to restore touch sensation following injury

  2017cites this paper
• Forces applied during classical touch assays for Caenorhabditis elegans

  2017cites this paper
• Neurexin controls plasticity of a mature, sexually dimorphic neuron

  2017cites this paper
• Preventing Illegitimate Extrasynaptic Acetylcholine Receptor Clustering Requires the RSU-1 Protein

  2016influential citation
• A Caenorhabditis elegans Model Elucidates a Conserved Role for TRPA1-Nrf Signaling in Reactive α-Dicarbonyl Detoxification.

  2016cites this paper
• MEC-10 and MEC-19 Reduce the Neurotoxicity of the MEC-4(d) DEG/ENaC Channel in Caenorhabditis elegans

  2016cites this paper
• Establishing the C. elegans uterine seam cell (utse) as a novel model for studying cell behavior

  2015cites this paper
• The C. elegans UNC-23 protein, a member of the BCL-2-associated athanogene (BAG) family of chaperone regulators, interacts with HSP-1 to regulate cell attachment and maintain hypodermal integrity

  2015cites this paper
• Identification of Nonviable Genes Affecting Touch Sensitivity in Caenorhabditis elegans Using Neuronally Enhanced Feeding RNA Interference

  2015cites this paper
• MicroRNAs Protect the Robustness of Distal Tip Cell Migrations from Temperature Changes in Caenorhabditis elegans: A Dissertation

  2015cites this paper
• PTRN-1, a microtubule minus end-binding CAMSAP homolog, promotes microtubule function in Caenorhabditis elegans neurons

  2014cites this paper
• Suppressor Mutations Suggest a Surface on PAT-4 (Integrin-linked Kinase) That Interacts with UNC-112 (Kindlin)*

  2014cites this paper
• Rsu1 contributes to cell adhesion and spreading in MCF10A cells via effects on P38 map kinase signaling

  2014cites this paper
• BLMP-1/Blimp-1 Regulates the Spatiotemporal Cell Migration Pattern in C. elegans

  2014cites this paper
• Mechanotransduction in C. elegans morphogenesis and tissue function.

  2014cites this paper
• Assaying mechanosensation.

  2014cites this paper
• Extracellular Matrix Regulates UNC-6 (Netrin) Axon Guidance by Controlling the Direction of Intracellular UNC-40 (DCC) Outgrowth Activity

  2014cites this paper
• The integrin-adhesome is required to maintain muscle structure, mitochondrial ATP production, and movement forces in Caenorhabditis elegans

  2014cites this paper
• Modulation of C. elegans Touch Sensitivity Is Integrated at Multiple Levels

  2014cites this paper
• CPNA-1, a copine domain protein, is located at integrin adhesion sites and is required for myofilament stability in Caenorhabditis elegans

  2013influential citation
• Rsu1 contributes to regulation of cell adhesion and spreading by PINCH1-dependent and - independent mechanisms

  2013cites this paper
• Calcium/Calmodulin dependent protein kinase II signaling and IGFR signaling are courter-balanced to regulate protein degradation in C. elegans muscle

  2013cites this paper
• Modulation of touch sensitivity in Caenorhabditis elegans

  2013influential citation
• C. elegans PAT-9 is a nuclear zinc finger protein critical for the assembly of muscle attachments

  2012cites this paper
• Calpains Mediate Integrin Attachment Complex Maintenance of Adult Muscle in Caenorhabditis elegans

  2012cites this paper
• Removal of Polycomb repressive complex 2 makes C. elegans germ cells susceptible to direct conversion into specific somatic cell types.

  2012cites this paper
• Finding the weakest link – exploring integrin-mediated mechanical molecular pathways

  2012cites this paper
• Dissertation zur Erlangung des Doktorgrades der Fakultät für Chemie und Pharmazie der Ludwig-Maximilians-Universität München Functional characterization of PINCH-1 in embryoid bodies and keratinocytes and identification of new interaction partners

  2012cites this paper
• Role of PINCH during early Xenopus embryogenesis

  2012cites this paper
• A Novel Mutation in β Integrin Reveals an Integrin-Mediated Interaction between the Extracellular Matrix and cki-1/p27KIP1

  2012influential citation
• PINCH Expression and Its Clinicopathological Significance in Gastric Adenocarcinoma

  2012cites this paper
• Caenorhabditis elegans muscle: a genetic and molecular model for protein interactions in the heart.

  2011cites this paper
• Impact of PINCH expression on survival in colorectal cancer patients

  2011cites this paper
• PINCH mRNA overexpression in colorectal carcinomas correlated with VEGF and FAS mRNA expression.

  2011cites this paper
• Determining the Sub-Cellular Localization of Proteins within Caenorhabditis elegans Body Wall Muscle

  2011cites this paper
• Analysis of the association between Pristionchus and beetles with emphasis on the special case of P. uniformis

  2011cites this paper
• The myosin-interacting protein SMYD1 is essential for sarcomere organization

  2011cites this paper
• The DEG/ENaC Protein MEC-10 Regulates the Transduction Channel Complex in Caenorhabditis elegans Touch Receptor Neurons

  2011cites this paper
• Host-finding behaviour in the nematode Pristionchus pacificus

  2011cites this paper
• MADD-2, a Homolog of the Opitz Syndrome Protein MID1, Regulates Guidance to the Midline in Caenorhabditis elegans

  2011cites this paper
• PINCH: More than just an adaptor protein in cellular response

  2011cites this paper
• Molecular and genetic approaches for the analysis of C. elegans neuronal development.

  2011cites this paper
• The Caenorhabditis elegans paxillin orthologue, PXL-1, is required for pharyngeal muscle contraction and for viability

  2011cites this paper
• Topological Cluster Analysis Reveals the Systemic Organization of the Caenorhabditis elegans Connectome

  2011cites this paper
• Determination of the mobility of novel and established Caenorhabditis elegans sarcomeric proteins in vivo.

  2010cites this paper
• Characterization of C. elegans PAT-9 and FRG-1, genes critical for body wall muscle development

  2010cites this paper
• A Global Analysis of Synthetic Genetic Interactions & a Genetic Analysis of Muscle Arm Development in Caenorhabditis elegans

  2010cites this paper
• Molecular Structure of Sarcomere-to-Membrane Attachment at M-Lines in C. elegans Muscle

  2010cites this paper
• DISSECTION OF NOVEL PATHWAYS LEADING TO PODOCYTE DYSFUNCTION AND PROTEINURIA

  2010cites this paper
• Neural crest cell-specific deletion of Rac1 results in defective cell-matrix interactions and severe craniofacial and cardiovascular malformations.

  2010cites this paper
• The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase!

  2010cites this paper
• CSN-5, a component of the COP9 signalosome complex, regulates the levels of UNC-96 and UNC-98, two components of M-lines in Caenorhabditis elegans muscle.

  2009cites this paper
• Integrin-linked kinase is required for radial sorting of axons and Schwann cell remyelination in the peripheral nervous system

  2009cites this paper
• Integrins mediate their unconventional, mechanical-stress-induced secretion via RhoA and PINCH in Drosophila

  2009cites this paper
• An Integrated Strategy to Study Muscle Development and Myofilament Structure in Caenorhabditis elegans

  2009cites this paper
• Particularly Interesting Cysteine- and Histidine-Rich Protein in Cardiac Development and Remodeling

  2009cites this paper
• An UNC-40 pathway directs postsynaptic membrane extension in Caenorhabditis elegans

  2009influential citation
• Targeted Ablation of PINCH1 and PINCH2 From Murine Myocardium Results in Dilated Cardiomyopathy and Early Postnatal Lethality

  2009cites this paper
• A new trick for an old dogma: ENaC proteins as mechanotransducers in vascular smooth muscle.

  2008cites this paper
• Roles of PINCH-2 in regulation of glomerular cell shape change and fibronectin matrix deposition.

  2008cites this paper
• PINCH-1 Regulates the ERK-Bim Pathway and Contributes to Apoptosis Resistance in Cancer Cells*

  2008cites this paper
• Functional analysis of the aquaporin gene family in Caenorhabditis elegans.

  2007cites this paper