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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Main Authors: 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
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/24176
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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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spelling 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