scholarly journals The Caenorhabditis elegans unc-78 Gene Encodes a Homologue of Actin-Interacting Protein 1 Required for Organized Assembly of Muscle Actin Filaments

2001 ◽  
Vol 152 (6) ◽  
pp. 1313-1320 ◽  
Author(s):  
Shoichiro Ono
Keyword(s):  
Caenorhabditis Elegans ◽  
Actin Filament ◽  
Actin Filaments ◽  
Body Wall ◽  
Point Mutations ◽  
The Body ◽  
Body Wall Muscle ◽  
Dynamic Regulation ◽  
Interacting Protein ◽  
Actin Organization

Assembly and maintenance of myofibrils require dynamic regulation of the actin cytoskeleton. In Caenorhabditis elegans, UNC-60B, a muscle-specific actin depolymerizing factor (ADF)/cofilin isoform, is required for proper actin filament assembly in body wall muscle (Ono, S., D.L. Baillie, and G.M. Benian. 1999. J. Cell Biol. 145:491–502). Here, I show that UNC-78 is a homologue of actin-interacting protein 1 (AIP1) and functions as a novel regulator of actin organization in myofibrils. In unc-78 mutants, the striated organization of actin filaments is disrupted, and large actin aggregates are formed in the body wall muscle cells, resulting in defects in their motility. Point mutations in unc-78 alleles change conserved residues within different WD repeats of the UNC-78 protein and cause less severe phenotypes than a deletion allele, suggesting that these mutations partially impair the function of UNC-78. UNC-60B is normally localized in the diffuse cytoplasm and to the myofibrils in wild type but mislocalized to the actin aggregates in unc-78 mutants. Similar Unc-78 phenotypes are observed in both embryonic and adult muscles. Thus, AIP1 is an important regulator of actin filament organization and localization of ADF/cofilin during development of myofibrils.

scholarly journals The two actin-interacting protein 1 genes have overlapping and essential function for embryonic development in Caenorhabditis elegans

2011 ◽  
Vol 22 (13) ◽  
pp. 2258-2269 ◽  
Author(s):  
Shoichiro Ono ◽  
Kazumi Nomura ◽  
Sadae Hitosugi ◽  
Domena K. Tu ◽  
Jocelyn A. Lee ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Actin Filament ◽  
Actin Filaments ◽  
Body Wall ◽  
The Body ◽  
Body Wall Muscle ◽  
Interacting Protein ◽  
Adult Muscle ◽  
Essential Function

Disassembly of actin filaments by actin-depolymerizing factor (ADF)/cofilin and actin-interacting protein 1 (AIP1) is a conserved mechanism to promote reorganization of the actin cytoskeleton. We previously reported that unc-78, an AIP1 gene in the nematode Caenorhabditis elegans, is required for organized assembly of sarcomeric actin filaments in the body wall muscle. unc-78 functions in larval and adult muscle, and an unc-78–null mutant is homozygous viable and shows only weak phenotypes in embryos. Here we report that a second AIP1 gene, aipl-1 (AIP1-like gene-1), has overlapping function with unc-78, and that depletion of the two AIP1 isoforms causes embryonic lethality. A single aipl-1–null mutation did not cause a detectable phenotype. However, depletion of both unc-78 and aipl-1 arrested development at late embryonic stages due to severe disorganization of sarcomeric actin filaments in body wall muscle. In vitro, both AIPL-1 and UNC-78 preferentially cooperated with UNC-60B, a muscle-specific ADF/cofilin isoform, in actin filament disassembly but not with UNC-60A, a nonmuscle ADF/cofilin. AIPL-1 is expressed in embryonic muscle, and forced expression of AIPL-1 in adult muscle compensated for the function of UNC-78. Thus our results suggest that enhancement of actin filament disassembly by ADF/cofilin and AIP1 proteins is critical for embryogenesis.

scholarly journals Two Caenorhabditis elegans calponin-related proteins have overlapping functions to maintain cytoskeletal integrity and are essential for reproduction

2020 ◽  
Author(s):  
Shoichiro Ono ◽  
Kanako Ono
Keyword(s):  
Caenorhabditis Elegans ◽  
Actin Filaments ◽  
Body Wall ◽  
The Body ◽  
Body Wall Muscle ◽  
Related Protein ◽  
Somatic Gonad ◽  
Related Proteins

AbstractMulticellular organisms have multiple genes encoding calponins and calponin-related proteins, and some of these are known to regulate actin cytoskeletal dynamics and contractility. However, functional similarities and differences among these proteins are largely unknown. In the nematode Caenorhabditis elegans, UNC-87 is a calponin-related protein with seven calponin-like (CLIK) motifs and is required for maintenance of contractile apparatuses in muscle cells. Here, we report that CLIK-1, another calponin-related protein that also contains seven CLIK motifs, has an overlapping function with UNC-87 to maintain actin cytoskeletal integrity in vivo and has both common and different actin-regulatory activities in vitro. CLIK-1 is predominantly expressed in the body wall muscle and somatic gonad, where UNC-87 is also expressed. unc-87 mutation causes cytoskeletal defects in the body wall muscle and somatic gonad, whereas clik-1 depletion alone causes no detectable phenotypes. However, simultaneous depletion of clik-1 and unc-87 caused sterility due to ovulation failure by severely affecting the contractile actin networks in the myoepithelial sheath of the somatic gonad. In vitro, UNC-87 bundles actin filaments. However, CLIK-1 binds to actin filaments without bundling them and is antagonistic to UNC-87 in filament bundling. UNC-87 and CLIK-1 share common functions to inhibit cofilin binding and allow tropomyosin binding to actin filaments, suggesting that both proteins stabilize actin filaments. Thus, partially redundant functions of UNC-87 and CLIK-1 in ovulation is likely mediated by their common actin-regulatory activities, but their distinct activities in actin bundling suggest that they also have different biological functions.

scholarly journals Two Caenorhabditis elegans calponin-related proteins have overlapping functions that maintain cytoskeletal integrity and are essential for reproduction

2020 ◽  
Vol 295 (34) ◽  
pp. 12014-12027
Author(s):  
Shoichiro Ono ◽  
Kanako Ono
Keyword(s):  
Caenorhabditis Elegans ◽  
Actin Filaments ◽  
Body Wall ◽  
The Body ◽  
Body Wall Muscle ◽  
Related Protein ◽  
Somatic Gonad ◽  
Related Proteins

Multicellular organisms have multiple genes encoding calponins and calponin-related proteins, some of which are known to regulate actin cytoskeletal dynamics and contractility. However, the functional similarities and differences among these proteins are largely unknown. In the nematode Caenorhabditis elegans, UNC-87 is a calponin-related protein with seven calponin-like (CLIK) motifs and is required for maintenance of contractile apparatuses in muscle cells. Here, we report that CLIK-1, another calponin-related protein that also contains seven CLIK motifs, functionally overlaps with UNC-87 in maintaining actin cytoskeletal integrity in vivo and has both common and different actin-regulatory activities in vitro. We found that CLIK-1 is predominantly expressed in the body wall muscle and somatic gonad in which UNC-87 is also expressed. unc-87 mutation caused cytoskeletal defects in the body wall muscle and somatic gonad, whereas clik-1 depletion alone caused no detectable phenotypes. However, simultaneous clik-1 and unc-87 depletion caused sterility because of ovulation failure by severely affecting the contractile actin networks in the myoepithelial sheath of the somatic gonad. In vitro, UNC-87 bundled actin filaments, whereas CLIK-1 bound to actin filaments without bundling them and antagonized UNC-87–mediated filament bundling. We noticed that UNC-87 and CLIK-1 share common functions that inhibit cofilin binding and allow tropomyosin binding to actin filaments, suggesting that both proteins stabilize actin filaments. In conclusion, partially redundant functions of UNC-87 and CLIK-1 in ovulation are likely mediated by their common actin-regulatory activities, but their distinct actin-bundling activities suggest that they also have different biological functions.

scholarly journals A screen for genetic loci required for body-wall muscle development during embryogenesis in Caenorhabditis elegans.

Genetics ◽  
1994 ◽  
Vol 137 (2) ◽  
pp. 483-498
Author(s):  
J Ahnn ◽  
A Fire
Keyword(s):  
Caenorhabditis Elegans ◽  
Myosin Heavy Chain ◽  
Muscle Cell ◽  
Heavy Chain ◽  
Body Wall ◽  
Muscle Development ◽  
Contractile Function ◽  
The Body ◽  
Body Wall Muscle ◽  
Genetic Loci

Abstract We have used available chromosomal deficiencies to screen for genetic loci whose zygotic expression is required for formation of body-wall muscle cells during embryogenesis in Caenorhabditis elegans. To test for muscle cell differentiation we have assayed for both contractile function and the expression of muscle-specific structural proteins. Monoclonal antibodies directed against two myosin heavy chain isoforms, the products of the unc-54 and myo-3 genes, were used to detect body-wall muscle differentiation. We have screened 77 deficiencies, covering approximately 72% of the genome. Deficiency homozygotes in most cases stain with antibodies to the body-wall muscle myosins and in many cases muscle contractile function is observed. We have identified two regions showing distinct defects in myosin heavy chain gene expression. Embryos homozygous for deficiencies removing the left tip of chromosome V fail to accumulate the myo-3 and unc-54 products, but express antigens characteristic of hypodermal, pharyngeal and neural development. Embryos lacking a large region on chromosome III accumulate the unc-54 product but not the myo-3 product. We conclude that there exist only a small number of loci whose zygotic expression is uniquely required for adoption of a muscle cell fate.

scholarly journals α spectrin is essential for morphogenesis and body wall muscle formation in Caenorhabditis elegans

2002 ◽  
Vol 157 (4) ◽  
pp. 665-677 ◽  
Author(s):  
Kenneth R. Norman ◽  
Donald G. Moerman
Keyword(s):  
Caenorhabditis Elegans ◽  
Cell Membrane ◽  
Body Wall ◽  
Longitudinal Axis ◽  
The Body ◽  
Body Wall Muscle ◽  
Cell Stage ◽  
Muscle Formation ◽  
Spectrin Cytoskeleton ◽  
Caenorhabditis Elegans Genome

Acommon feature of multicellular animals is the ubiquitous presence of the spectrin cytoskeleton. Although discovered over 30 yr ago, the function of spectrin in nonerythrocytes has remained elusive. We have found that the spc-1 gene encodes the only α spectrin gene in the Caenorhabditis elegans genome. During embryogenesis, α spectrin localizes to the cell membrane in most if not all cells, starting at the first cell stage. Interestingly, this localization is dependent on β spectrin but not βHeavy spectrin. Furthermore, analysis of spc-1 mutants indicates that β spectrin requires α spectrin to be stably recruited to the cell membrane. Animals lacking functional α spectrin fail to complete embryonic elongation and die just after hatching. These mutant animals have defects in the organization of the hypodermal apical actin cytoskeleton that is required for elongation. In addition, we find that the process of elongation is required for the proper differentiation of the body wall muscle. Specifically, when compared with myofilaments in wild-type animals the myofilaments of the body wall muscle in mutant animals are abnormally oriented relative to the longitudinal axis of the embryo, and the body wall muscle cells do not undergo normal cell shape changes.

scholarly journals The ALP-Enigma Protein ALP-1 Functions in Actin Filament Organization to Promote Muscle Structural Integrity in Caenorhabditis elegans

2009 ◽  
Vol 20 (9) ◽  
pp. 2361-2370 ◽  
Author(s):  
Hsiao-Fen Han ◽  
Mary C. Beckerle
Keyword(s):  
Caenorhabditis Elegans ◽  
Actin Filament ◽  
Actin Filaments ◽  
Body Wall ◽  
Structural Integrity ◽  
Mechanical Stability ◽  
Single Gene ◽  
Cardiac Diseases ◽  
C Elegans ◽  
Dense Bodies

Mutations that affect the Z-disk–associated ALP-Enigma proteins have been linked to human muscular and cardiac diseases. Despite their clear physiological significance for human health, the mechanism of action of ALP-Enigma proteins is largely unknown. In Caenorhabditis elegans, the ALP-Enigma protein family is encoded by a single gene, alp-1; thus C. elegans provides an excellent model to study ALP-Enigma function. Here we present a molecular and genetic analysis of ALP-Enigma function in C. elegans. We show that ALP-1 and α-actinin colocalize at dense bodies where actin filaments are anchored and that the proper localization of ALP-1 at dense bodies is dependent on α-actinin. Our analysis of alp-1 mutants demonstrates that ALP-1 functions to maintain actin filament organization and participates in muscle stabilization during contraction. Reducing α-actinin activity enhances the actin filament phenotype of the alp-1 mutants, suggesting that ALP-1 and α-actinin function in the same cellular process. Like α-actinin, alp-1 also interacts genetically with a connectin/titin family member, ketn-1, to provide mechanical stability for supporting body wall muscle contraction. Taken together, our data demonstrate that ALP-1 and α-actinin function together to stabilize actin filaments and promote muscle structural integrity.

scholarly journals Mutations in the sup-38 gene of Caenorhabditis elegans suppress muscle-attachment defects in unc-52 mutants.

Genetics ◽  
1992 ◽  
Vol 132 (2) ◽  
pp. 431-442 ◽  
Author(s):  
E J Gilchrist ◽  
D G Moerman
Keyword(s):  
Caenorhabditis Elegans ◽  
Body Wall ◽  
Muscle Cells ◽  
The Body ◽  
Body Wall Muscle ◽  
Variable Degree ◽  
Loss Of Function ◽  
Uterine Muscle ◽  
Somatic Gonad ◽  
Class 1

Abstract Mutations in the unc-52 locus of Caenorhabditis elegans have been classified into three different groups based on their complex pattern of complementation. These mutations result in progressive paralysis (class 1 mutations) or in lethality (class 2 and 3 mutations). The paralysis exhibited by animals carrying class 1 mutations is caused by disruption of the myofilaments at their points of attachment to the cell membrane in the body wall muscle cells. We have determined that mutations of this class also have an effect on the somatic gonad, and this may be due to a similar disruption in the myoepithelial sheath cells of the uterus, or in the uterine muscle cells. Mutations that suppress the body wall muscle defects of the class 1 unc-52 mutations have been isolated, and they define a new locus, sup-38. Only the muscle disorganization of the Unc-52 mutants is suppressed; the gonad abnormalities are not, and the suppressors do not rescue the lethal phenotype of the class 2 and class 3 mutations. The suppressor mutations on their own exhibit a variable degree of gonad and muscle disorganization. Putative null sup-38 mutations cause maternal-effect lethality which is rescued by a wild-type copy of the locus in the zygote. These loss-of-function mutations have no effect on the body wall muscle structure.

scholarly journals Caenorhabditis elegans Kettin, a Large Immunoglobulin-like Repeat Protein, Binds to Filamentous Actin and Provides Mechanical Stability to the Contractile Apparatuses in Body Wall Muscle

2006 ◽  
Vol 17 (6) ◽  
pp. 2722-2734 ◽  
Author(s):  
Kanako Ono ◽  
Robinson Yu ◽  
Kurato Mohri ◽  
Shoichiro Ono
Keyword(s):  
Caenorhabditis Elegans ◽  
Actin Filaments ◽  
Body Wall ◽  
Mechanical Stability ◽  
Functional Characterization ◽  
Body Wall Muscle ◽  
Actin Binding ◽  
Filamentous Actin ◽  
Thin Filaments ◽  
Dense Bodies

Kettin is a large actin-binding protein with immunoglobulin-like (Ig) repeats, which is associated with the thin filaments in arthropod muscles. Here, we report identification and functional characterization of kettin in the nematode Caenorhabditis elegans. We found that one of the monoclonal antibodies that were raised against C. elegans muscle proteins specifically reacts with kettin (Ce-kettin). We determined the entire cDNA sequence of Ce-kettin that encodes a protein of 472 kDa with 31 Ig repeats. Arthropod kettins are splice variants of much larger connectin/titin-related proteins. However, the gene for Ce-kettin is independent of other connectin/titin-related genes. Ce-kettin localizes to the thin filaments near the dense bodies in both striated and nonstriated muscles. The C-terminal four Ig repeats and the adjacent non-Ig region synergistically bind to actin filaments in vitro. RNA interference of Ce-kettin caused weak disorganization of the actin filaments in body wall muscle. This phenotype was suppressed by inhibiting muscle contraction by a myosin mutation, but it was enhanced by tetramisole-induced hypercontraction. Furthermore, Ce-kettin was involved in organizing the cytoplasmic portion of the dense bodies in cooperation with α-actinin. These results suggest that kettin is an important regulator of myofibrillar organization and provides mechanical stability to the myofibrils during contraction.

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