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Elife. 2017 Apr 18;6. pii: e24176. doi: 10.7554/eLife.24176.

Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues.

Author information

1
Department of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, United States.
2
Aspirnaut Program, Vanderbilt University Medical Center, Nashville, United States.
3
Department of Biological Sciences, Tennessee State University, Nashville, United States.
4
Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, United States.
5
Center for Structural Biology, Vanderbilt University Medical Center, Nashville, United States.
6
Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, United States.
7
Department of Medical Education and Administration, Vanderbilt University Medical Center, Nashville, United States.
8
Department of Biological Sciences, Vanderbilt University Medical Center, Nashville, United States.
9
Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, United States.
10
Department of Biochemistry, Vanderbilt University Medical Center, Nashville, United States.
11
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, United States.
12
Vanderbilt Institute of Chemical Biology, Vanderbilt University Medical Center, Nashville, United States.

Abstract

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.

KEYWORDS:

Basement Membrane; Collagen IV; Ctenophora; developmental biology; epithelial cells; evolutionary biology; genomics; stem cells

PMID:
28418331
PMCID:
PMC5395295
DOI:
10.7554/eLife.24176
[Indexed for MEDLINE]
Free PMC Article

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