Teething during sleep: Ultrastructural analysis of pharyngeal muscle and cuticular grinder during the molt in Caenorhabditis elegans.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2020
Historique:
received: 05 02 2020
accepted: 27 04 2020
entrez: 21 5 2020
pubmed: 21 5 2020
medline: 1 8 2020
Statut: epublish

Résumé

Complex extracellular structures exist throughout phylogeny, but the dynamics of their formation and dissolution are often opaque. One example is the pharyngeal grinder of the nematode Caenorhabditis elegans, an extracellular structure that ruptures bacteria during feeding. During each larval transition stage, called lethargus, the grinder is replaced with one of a larger size. Here, we characterize at the ultrastructural level the deconstruction of the larval grinder and the construction of the adult grinder during the fourth larval stage (L4)-to-adult transition. Early in L4 lethargus, pharyngeal muscle cells trans-differentiate from contractile to secretory cells, as evidenced by the appearance of clear and dense core vesicles and disruptions in sarcomere organization. This is followed, within minutes, by the dissolution of the L4 grinder and the formation and maturation of the adult grinder. Components of the nascent adult grinder are deposited basally, and are separated from the dissolving larval grinder by a visible apical layer. The complete grinder is a lamellated extracellular matrix comprised of five layers. Following grinder formation, pharyngeal muscle cells regain ultrastructural contractile properties, and muscle contractions resume. Our findings add to our understanding of how complex extracellular structures assemble and dissemble.

Identifiants

pubmed: 32433687
doi: 10.1371/journal.pone.0233059
pii: PONE-D-20-03428
pmc: PMC7239488
doi:

Substances chimiques

Caenorhabditis elegans Proteins 0
Metalloendopeptidases EC 3.4.24.-

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0233059

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS088432
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS107969
Pays : United States
Organisme : NIGMS NIH HHS
ID : R15 GM122058
Pays : United States
Organisme : NIH HHS
ID : P40 OD010440
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

J Neurosci. 2015 Oct 28;35(43):14571-84
pubmed: 26511247
Cold Spring Harb Perspect Biol. 2011 Dec 01;3(12):
pubmed: 21917992
Protein Sci. 1995 Jul;4(7):1247-61
pubmed: 7670368
Nat Neurosci. 2007 Oct;10(10):1300-7
pubmed: 17891142
Nature. 2010 Jan 28;463(7280):485-92
pubmed: 20110992
Cold Spring Harb Perspect Biol. 2012 Jan 01;4(1):a004903
pubmed: 21937732
Mol Cell. 2014 Feb 6;53(3):380-92
pubmed: 24440504
Methods Cell Biol. 2012;107:93-149
pubmed: 22226522
Evol Dev. 2002 Jan-Feb;4(1):16-27
pubmed: 11871396
BMC Dev Biol. 2015 Jun 12;15:26
pubmed: 26066484
Dev Biol. 2005 Sep 15;285(2):330-9
pubmed: 16098962
J Mol Biol. 1969 May 14;41(3):459-72
pubmed: 4896022
Proc Natl Acad Sci U S A. 2009 Nov 24;106(47):20093-6
pubmed: 19903886
Worm. 2017 May 17;6(1):e1330246
pubmed: 28702275
J Neurosci. 1995 Dec;15(12):8408-18
pubmed: 8613772
Nat Rev Mol Cell Biol. 2014 Dec;15(12):786-801
pubmed: 25415508
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Trends Biochem Sci. 2007 May;32(5):217-24
pubmed: 17412596
Bioessays. 1994 Mar;16(3):171-8
pubmed: 8166670
PLoS One. 2013;8(1):e53419
pubmed: 23301069
Genetics. 2002 Jul;161(3):1101-12
pubmed: 12136014
Biol Open. 2014 Oct 31;3(11):1139-49
pubmed: 25361578
Philos Trans R Soc Lond B Biol Sci. 2008 Apr 27;363(1496):1529-37
pubmed: 18192181
BMC Dev Biol. 2010 Jan 28;10:14
pubmed: 20109220
PLoS One. 2008 Jul 30;3(7):e2821
pubmed: 18665238
Eur J Biochem. 2003 Dec;270(24):4909-20
pubmed: 14653817
Tissue Cell. 1979;11(4):643-53
pubmed: 524341
J Morphol. 2017 Dec;278(12):1656-1666
pubmed: 28898441
J Cell Sci. 2010 Dec 15;123(Pt 24):4195-200
pubmed: 21123617
Nature. 2008 Jan 31;451(7178):569-72
pubmed: 18185515
Genetics. 1995 Dec;141(4):1365-82
pubmed: 8601480
Philos Trans R Soc Lond B Biol Sci. 1976 Aug 10;275(938):299-325
pubmed: 8805
J Exp Biol. 2006 Jan;209(Pt 1):89-102
pubmed: 16354781
J Exp Biol. 2015 May;218(Pt 9):1306-13
pubmed: 25767144

Auteurs

Alessandro P Sparacio (AP)

Department of Biology, Saint Joseph's University, Philadelphia, Pennsylvania, United States of America.

Nicholas F Trojanowski (NF)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.
Department of Biology, Brandeis University, Waltham, Massachusetts, United States of America.

Karen Snetselaar (K)

Department of Biology, Saint Joseph's University, Philadelphia, Pennsylvania, United States of America.

Matthew D Nelson (MD)

Department of Biology, Saint Joseph's University, Philadelphia, Pennsylvania, United States of America.

David M Raizen (DM)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America.

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Classifications MeSH