Two Sets of Interacting Collagens Form Functionally Distinct Substructures within a<i>Caenorhabditis elegans</i>Extracellular Matrix

McMahon, Laura; Muriel, Joaquin M.; Roberts, Brett; Quinn, Martyn; Johnstone, Iain L.

doi:10.1091/mbc.e02-08-0479

Cited by 83 publications

(116 citation statements)

References 30 publications

(41 reference statements)

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“…This labeling pattern is consistent with the antigen being a secreted cuticle component. In similar experiments using monoclonal antiserum specific for the collagen DPY-7, McMahon et al (2003) obtained comparable results, with the difference that the DPY-7 antigen localized extracellularly to the annular furrows, not ridges.…”

Section: Resultsmentioning

confidence: 57%

The C Terminus of Collagen SQT-3 Has Complex and Essential Functions in Nematode Collagen Assembly

Novelli

Page²,

Hodgkin

2006

Genetics

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The nematode exoskeleton is a multilayered structure secreted by the underlying hypodermal cells and mainly composed of small collagens, which are encoded by a large gene family. In previous work, we reported analysis of the C. elegans dpy-31 locus, encoding a hypodermally expressed zinc-metalloprotease of the BMP-1/TOLLOID family essential for viability and cuticle deposition. We have generated a large set of extragenic suppressors of dpy-31 lethality, most of which we show here to be allelic to the cuticle collagen genes sqt-3 and dpy-17. We analyzed the interaction among dpy-31, sqt-3, and dpy-17 using a SQT-3-specific antiserum, which was employed in immunofluorescence experiments. Our results support a role for DPY-31 in SQT-3 extracellular processing and suggest that the SQT-3 C-terminal nontrimeric region serves multiple roles during SQT-3 assembly. Different missense mutations of this region have diverse phenotypic consequences, including cold-sensitive lethality. Furthermore, the biochemical and genetic data indicate that the extracellular assemblies of DPY-17 and SQT-3 are interdependent, most likely because the collagens are incorporated into the same cuticular substructure. We find that absence of DPY-17 causes extensive intracellular retention of SQT-3, indicating that formation of the SQT-3-DPY-17 polymer could begin in the intracellular environment before secretion.

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Section: Resultsmentioning

confidence: 57%

The C Terminus of Collagen SQT-3 Has Complex and Essential Functions in Nematode Collagen Assembly

Novelli

Page²,

Hodgkin

2006

Genetics

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“…During larval development, nematodes synthesize a new cuticle before each of four molts (45). During cuticle synthesis, circumferential bundles of actin filaments form in the hypodermis underneath each furrow and are hypothesized to function as anchoring points for furrow formation (75,92). Taken together, these data suggest that a yet to be identified osmotic sensor complex is formed in or between the hypodermis and cuticle, possibly associated with annular furrows.…”

Section: Extracellular Signaling Controls Organic Osmolytes and Osmosmentioning

confidence: 85%

“…1, E and F). Mutations in five dpy collagens were shown to disrupt furrow formation, and at least three of these (dpy-7, dpy-8, and dpy-10) are known to also activate glycerol accumulation (61,75,118). DPY-7 and DPY-10 proteins have been localized to annular furrows (Fig.…”

Section: Extracellular Signaling Controls Organic Osmolytes and Osmosmentioning

confidence: 99%

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Physiological and molecular mechanisms of salt and water homeostasis in the nematodeCaenorhabditis elegans

Choe

2013

American Journal of Physiology-Regulatory, Integrative and Comp

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Choe KP. Physiological and molecular mechanisms of salt and water homeostasis in the nematode Caenorhabditis elegans. Am J Physiol Regul Integr Comp Physiol 305: R175-R186, 2013. First published June 5, 2013 doi:10.1152/ajpregu.00109.2013.-Intracellular salt and water homeostasis is essential for all cellular life. Extracellular salt and water homeostasis is also important for multicellular organisms. Many fundamental mechanisms of compensation for osmotic perturbations are well defined and conserved. Alternatively, molecular mechanisms of detecting salt and water imbalances and regulating compensatory responses are generally poorly defined for animals. Throughout the last century, researchers studying vertebrates and vertebrate cells made critical contributions to our understanding of osmoregulation, especially mechanisms of salt and water transport and organic osmolyte accumulation. Researchers have more recently started using invertebrate model organisms with defined genomes and well-established methods of genetic manipulation to begin defining the genes and integrated regulatory networks that respond to osmotic stress. The nematode Caenorhabditis elegans is well suited to these studies. Here, I introduce osmoregulatory mechanisms in this model, discuss experimental advantages and limitations, and review important findings. Key discoveries include defining genetic mechanisms of osmolarity sensing in neurons, identifying protein damage as a sensor and principle determinant of hypertonic stress resistance, and identification of a putative sensor for hypertonic stress associated with the extracellular matrix. Many of these processes and pathways are conserved and, therefore, provide new insights into salt and water homeostasis in other animals, including mammals. osmoregulation; cell volume; ion; organic osmolyte; protein homeostasis; model organism SALT AND WATER HOMEOSTASIS is a fundamental requirement for metazoan life. Ion and water transport mechanisms that compensate for changes in composition and volume of intracellular and extracellular compartments have been generally well defined using vertebrate cell and in vivo models (38). Alternatively, the upstream molecular mechanisms that animal cells use to sense deviations in salt and water balance and regulate compensatory responses are still poorly characterized (20). Studies in brewer's yeast demonstrate that osmotic signal detection and transduction within a single eukaryotic cell can be highly complex with numerous components, acting in parallel pathways, that often cross-talk with other processes (40,55). Osmotic signal detection and transduction are likely to be even more complex in metazoans, which require homeostasis of both the extracellular and intracellular compartments and integration of responses between cells. Genetics is an extremely powerful approach for identifying and characterizing genes and proteins that function in complex biological processes but has been underutilized in the field of osmosensing and signal transduction in metazoans. In...

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“…In invertebrates, collagens also play a crucial role. For example, Caenorhabditis elegans has more than 150 genes for collagenous proteins, mostly for cuticle collagens (8). Annelid cuticle collagen has 4(R)Hyp residues in the Xaa position and galactosylated threonine residues in the Yaa position of the repeated -Gly-XaaYaa-sequences, which are not found in vertebrates (9).…”

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confidence: 99%

Hydroxylation-induced Stabilization of the Collagen Triple Helix

Mizuno

Hayashi

Peyton

et al. 2004

Journal of Biological Chemistry

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The collagen triple helix is one of the most abundant protein motifs in animals. The structural motif of collagen is the triple helix formed by the repeated sequence of -Gly-Xaa-Yaa-. Previous reports showed that H-(Pro-4(R)Hyp-Gly) 10 -OH (where '4(R)Hyp' is (2S,4R)-4-hydroxyproline) forms a trimeric structure, whereas H-(4(R)Hyp-Pro-Gly) 10 -OH does not form a triple helix. Compared with H-(Pro-Pro-Gly) 10 -OH, the melting temperature of H-(Pro-4(R)Hyp-Gly) 10 -OH is higher, suggesting that 4(R)Hyp in the Yaa position has a stabilizing effect. The inability of triple helix formation of H-(4(R)Hyp-Pro-Gly) 10 -OH has been explained by a stereoelectronic effect, but the details are unknown. In this study, we synthesized a peptide that contains 4(R)Hyp in both the Xaa and the Yaa positions, that is, Ac-(Gly-4(R)Hyp-4(R)Hyp) 10 -NH 2 and compared it to Ac-(GlyPro-4(R)Hyp) 10 -NH 2 , and Ac-(Gly-4(R)Hyp-Pro) 10 -NH 2 . Ac-(Gly-4(R)Hyp-4(R)Hyp) 10 -NH 2 showed a polyproline II-like circular dichroic spectrum in water. The thermal transition temperatures measured by circular dichroism and differential scanning calorimetry were slightly higher than the values measured for Ac-(Gly-Pro-4(R)Hyp) 10 -NH 2 under the same conditions. For Ac-(Gly-4(R)Hyp-4(R)Hyp) 10 -NH 2 , the calorimetric and the van't Hoff transition enthalpy ⌬H were significantly smaller than that of Ac-(Gly-Pro-4(R)Hyp) 10 -NH 2 . We postulate that the denatured states of the two peptides are significantly different, with Ac-(Gly-4(R)Hyp-4(R)Hyp) 10 -NH 2 forming a more polyproline II-like structure instead of a random coil. Two-dimensional nuclear Overhauser effect spectroscopy suggests that the triple helical structure of Ac-(Gly-4(R)Hyp-4(R)Hyp) 10 -NH 2 is more flexible than that of Ac-(Gly-Pro-4(R)Hyp) 10 -NH 2 . This is confirmed by the kinetics of amide 1 H exchange with solvent deuterium of Ac-(Gly-4(R)Hyp-4(R)Hyp) 10 -NH 2 , which is faster than that of Ac-(Gly-Pro-4(R)Hyp) 10 -NH 2 . The higher transition temperature of Ac-(Gly-4(R)Hyp-4(R)Hyp) 10 -NH 2 , can be explained by the higher trans/cis ratio of the Gly-4(R)Hyp peptide bonds than that of the Gly-Pro bonds, and this ratio compensates for the weaker interchain hydrogen bonds.The collagen triple helix is one of the most abundant protein motifs in animals. Each of the three polypeptide chains forms a polyproline-II like structure, and these structures twist around each other to form a right-handed superhelix (1, 2). To form this structure, a sequence with Gly in every third position is required. The general sequence is -Gly-Xaa-Yaa-, and the Xaa and Yaa positions contain a high content of proline and hydroxyproline. Twenty-seven types of collagens and more than fifteen proteins that form a triple helix, but are not named collagens such as collectins, ficolins, and scavenger receptors (3-5), occur in humans. In vertebrates, most of the proline residues in the Yaa position of the -Gly-Xaa-Yaa-repeated sequence are post-translationally modified to 4(R)Hyp 1 by prolyl 4-hydroxylase (EC 1.14.1...

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Two Sets of Interacting Collagens Form Functionally Distinct Substructures within aCaenorhabditis elegansExtracellular Matrix

Cited by 83 publications

References 30 publications

The C Terminus of Collagen SQT-3 Has Complex and Essential Functions in Nematode Collagen Assembly

The C Terminus of Collagen SQT-3 Has Complex and Essential Functions in Nematode Collagen Assembly

Physiological and molecular mechanisms of salt and water homeostasis in the nematodeCaenorhabditis elegans

Hydroxylation-induced Stabilization of the Collagen Triple Helix

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