Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues
The role of the cellular microenvironment in enabling metazoan tissue genesis remains obscure. Ctenophora has recently emerged as one of the earliest-branching extant animal phyla, providing a unique opportunity to explore the evolutionary role of the cellular microenvironment in tissue genesis. Her...
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Format: | Article |
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eLife Sciences Publications Ltd
2017-04-01
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Series: | eLife |
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Online Access: | https://elifesciences.org/articles/24176 |
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doaj-e19f2cf7fd724dce8e52fab510ae0f42 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Aaron L Fidler Carl E Darris Sergei V Chetyrkin Vadim K Pedchenko Sergei P Boudko Kyle L Brown W Gray Jerome Julie K Hudson Antonis Rokas Billy G Hudson |
spellingShingle |
Aaron L Fidler Carl E Darris Sergei V Chetyrkin Vadim K Pedchenko Sergei P Boudko Kyle L Brown W Gray Jerome Julie K Hudson Antonis Rokas Billy G Hudson Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues eLife Ctenophora Basement Membrane Collagen IV epithelial cells |
author_facet |
Aaron L Fidler Carl E Darris Sergei V Chetyrkin Vadim K Pedchenko Sergei P Boudko Kyle L Brown W Gray Jerome Julie K Hudson Antonis Rokas Billy G Hudson |
author_sort |
Aaron L Fidler |
title |
Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues |
title_short |
Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues |
title_full |
Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues |
title_fullStr |
Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues |
title_full_unstemmed |
Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues |
title_sort |
collagen iv and basement membrane at the evolutionary dawn of metazoan tissues |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2017-04-01 |
description |
The role of the cellular microenvironment in enabling metazoan tissue genesis remains obscure. Ctenophora has recently emerged as one of the earliest-branching extant animal phyla, providing a unique opportunity to explore the evolutionary role of the cellular microenvironment in tissue genesis. Here, we characterized the extracellular matrix (ECM), with a focus on collagen IV and its variant, spongin short-chain collagens, of non-bilaterian animal phyla. We identified basement membrane (BM) and collagen IV in Ctenophora, and show that the structural and genomic features of collagen IV are homologous to those of non-bilaterian animal phyla and Bilateria. Yet, ctenophore features are more diverse and distinct, expressing up to twenty genes compared to six in vertebrates. Moreover, collagen IV is absent in unicellular sister-groups. Collectively, we conclude that collagen IV and its variant, spongin, are primordial components of the extracellular microenvironment, and as a component of BM, collagen IV enabled the assembly of a fundamental architectural unit for multicellular tissue genesis. |
topic |
Ctenophora Basement Membrane Collagen IV epithelial cells |
url |
https://elifesciences.org/articles/24176 |
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doaj-e19f2cf7fd724dce8e52fab510ae0f422021-05-05T13:24:54ZengeLife Sciences Publications LtdeLife2050-084X2017-04-01610.7554/eLife.24176Collagen IV and basement membrane at the evolutionary dawn of metazoan tissuesAaron L Fidler0https://orcid.org/0000-0002-2519-8864Carl E Darris1Sergei V Chetyrkin2Vadim K Pedchenko3Sergei P Boudko4Kyle L Brown5W Gray Jerome6Julie K Hudson7Antonis Rokas8https://orcid.org/0000-0002-7248-6551Billy G Hudson9https://orcid.org/0000-0002-5420-4100Department of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United States; Aspirnaut Program, Vanderbilt University Medical Center, Nashville, United States; Department of Biological Sciences, Tennessee State University, Nashville, United StatesDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United StatesDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United States; Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, United StatesDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United States; Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, United StatesDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United States; Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, United StatesDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United States; Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, United States; Center for Structural Biology, Vanderbilt University Medical Center, Nashville, United StatesDepartment of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, United StatesAspirnaut Program, Vanderbilt University Medical Center, Nashville, United States; Department of Medical Education and Administration, Vanderbilt University Medical Center, Nashville, United StatesDepartment of Biological Sciences, Vanderbilt University Medical Center, Nashville, United StatesDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United States; Aspirnaut Program, Vanderbilt University Medical Center, Nashville, United States; Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, United States; Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, United States; Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, United States; Department of Biochemistry, Vanderbilt University Medical Center, Nashville, United States; Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, United States; Vanderbilt Institute of Chemical Biology, Vanderbilt University Medical Center, Nashville, United StatesThe role of the cellular microenvironment in enabling metazoan tissue genesis remains obscure. Ctenophora has recently emerged as one of the earliest-branching extant animal phyla, providing a unique opportunity to explore the evolutionary role of the cellular microenvironment in tissue genesis. Here, we characterized the extracellular matrix (ECM), with a focus on collagen IV and its variant, spongin short-chain collagens, of non-bilaterian animal phyla. We identified basement membrane (BM) and collagen IV in Ctenophora, and show that the structural and genomic features of collagen IV are homologous to those of non-bilaterian animal phyla and Bilateria. Yet, ctenophore features are more diverse and distinct, expressing up to twenty genes compared to six in vertebrates. Moreover, collagen IV is absent in unicellular sister-groups. Collectively, we conclude that collagen IV and its variant, spongin, are primordial components of the extracellular microenvironment, and as a component of BM, collagen IV enabled the assembly of a fundamental architectural unit for multicellular tissue genesis.https://elifesciences.org/articles/24176CtenophoraBasement MembraneCollagen IVepithelial cells |