ArticleThe Journal of cell biology2016
Extracellular chloride signals collagen IV network assembly during basement membrane formation.
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Article in The Journal of cell biology, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 46 papers.
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46citing papers in PubMed
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46 citing papers in PubMed, 75 citations in OpenAlex.
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- Collagen IV of basement membrane: V. Bromide-mediated sulfilimine bonds interlock the quaternary structure of NC1-hexamer of scaffolds enabling metazoan evolution.bioRxiv : the preprint server for biology · 2026Article
- Mesenchymal stem cell-derived extracellular matrix for musculoskeletal tissue regeneration.Communications biology · 2026Review
- Basement membrane structure and function: Relating biology to mechanics.Matrix biology : journal of the International Society for Matrix Biology · 2025Review
- Collagen IV in Gould syndrome and Alport syndrome.Nature reviews. Nephrology · 2025Review
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- Collagen IV biosynthesis: Intracellular choreography of post-translational modifications.Matrix biology : journal of the International Society for Matrix Biology · 2025Review
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- A collagen IV fluorophore knock-in toolkit reveals trimer diversity in C. elegans basement membranes.The Journal of cell biology · 2025Article
- Decoding collagen's thermally induced unfolding and refolding pathways.Proceedings of the National Academy of Sciences of the United States of America · 2025Article
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- Kidney resident macrophages have distinct subsets and multifunctional roles.Matrix biology : journal of the International Society for Matrix Biology · 2024Article
- Peroxidasin is required for full viability in development and for maintenance of tissue mechanics in adults.Matrix biology : journal of the International Society for Matrix Biology · 2024Article
- Tissue Morphogenesis Through Dynamic Cell and Matrix Interactions.Annual review of cell and developmental biology · 2023Review
- Spatial composition and turnover of the main molecules in the adult glomerular basement membrane.Tissue barriers · 2023Review
- Identification of unique α4 chain structure and conserved antiangiogenic activity of α3NC1 type IV collagen in zebrafish.Developmental dynamics : an official publication of the American Association of Anatomists · 2023Article
- Gene therapy for pediatric genetic kidney diseases.Pediatric discovery · 2023Review
- Molecular Dynamics Investigation on the Effects of Protonation and Lysyl Hydroxylation on Sulfilimine Cross-links in Collagen IV.ACS omega · 2022Article
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Authors and funding
19 authors at 2 institutions in 2 countries.
Christopher F CummingsDepartment of Biochemistry, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Vadim PedchenkoDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Kyle L BrownDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Structural Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Selene ColonDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Aspirnaut Program, Vanderbilt University Medical Center, Nashville, TN 37232.
Mohamed RafiDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Celestial Jones-ParisAspirnaut Program, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232.
Elena PokydeshavaDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Min LiuSchool of Life Sciences, Tsinghua University, Beijing 100084, China.
Jose C Pastor-ParejaSchool of Life Sciences, Tsinghua University, Beijing 100084, China.
Cody StothersDepartment of Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Aspirnaut Program, Vanderbilt University Medical Center, Nashville, TN 37232.
Isi A Ero-TolliverDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Aspirnaut Program, Vanderbilt University Medical Center, Nashville, TN 37232.
A Scott McCallDepartment of Pharmacology, Vanderbilt University Medical Center, Nashville, TN 37232.
Roberto VanacoreDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Gautam BhaveDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Samuel SantoroDepartment of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232.
Timothy S BlackwellDepartment of Medicine, Division of Allergy, Pulmonary, and Critical Care Medicine, Vanderbilt University Medical Center, Nashville, TN 37232.
Roy ZentDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Cancer Biology, Vanderbilt University Medical Center, Nashville, TN 37232.
Ambra PozziDepartment of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Cancer Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Molecular Physiology and Biophysics, Vanderbilt University Medical Center, Nashville, TN 37232.
Billy G HudsonDepartment of Biochemistry, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Medicine, Division of Nephrology and Hypertension, Vanderbilt University Medical Center, Nashville, TN 37232 Center for Matrix Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Aspirnaut Program, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232 Department of Cell and Developmental Biology, Vanderbilt University Medical Center, Nashville, TN 37232 Vanderbilt Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN 37232 Vanderbilt Institute of Chemical Biology, Vanderbilt University Medical Center, Nashville, TN 37232 billy.hudson@vanderbilt.edu.
Vanderbilt University Medical Center · USTsinghua University · CN
Funding
MEDICAL SCIENTIST TRAINING PROGRAMT32GM007347 · NIGMS · VANDERBILT UNIVERSITY · PI WILLIAMS, CHRISTOPHER S. · 1985 to 2023
$26.3MTYPE IV COLLAGEN, LAMININS, AND INTEGRINS IN NORMAL AND DISEASED GLOMERULIP01DK065123 · NIDDK · VANDERBILT UNIVERSITY · PI HUDSON, BILLY GERALD · 2003 to 2012
$12.9MSTUDIES ON THE STRUCTURE OF BASEMENT MEMBRANESR01DK018381 · NIDDK · VANDERBILT UNIVERSITY MEDICAL CENTER · PI Sergey Petrovich Budko, BILLY GERALD HUDSON · 1986 to 2026
$12.4MVanderbilt/Meharry Initiative for Minority Student DvptR25GM062459 · NIGMS · VANDERBILT UNIVERSITY · PI VELEZ EDWARDS, DIGNA R · 2002 to 2020
$10.4MInterdisciplinary Training Program in Lung ResearchT32HL094296 · NHLBI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI Ray Stokes Peebles · 2008 to 2026
$6.3MGlucose Modifications of Proteins in Diabetic NephropathyR01DK065138 · NIDDK · VANDERBILT UNIVERSITY MEDICAL CENTER · PI HUDSON, BILLY GERALD, VOZIYAN, PAUL A · 2003 to 2020
$6.3MThe role of lysyl oxidase like-2 in chronic kidney diseaseR01DK099467 · NIDDK · VANDERBILT UNIVERSITY MEDICAL CENTER · PI VANACORE, ROBERTO MARCELO · 2013 to 2023
$3.8MUndergraduate Research Internships in Pathobiology of Diabetic NephropathyR25DK096999 · NIDDK · VANDERBILT UNIVERSITY MEDICAL CENTER · PI BILLY GERALD HUDSON · 2012 to 2026
$1.6MIntegrin/TGF-beta Axis in Tubulointerstitial FibrosisR01DK095761 · NIDDK · VANDERBILT UNIVERSITY MEDICAL CENTER · PI POZZI, AMBRA · 2013 to 2016
$1.4MRole of Peroxidasin in Glomerular Matrix HomeostasisK08DK097306 · NIDDK · VANDERBILT UNIVERSITY MEDICAL CENTER · PI BHAVE, GAUTAM · 2013 to 2017
$739kThe role of peroxidasin in Goodpasture's diseaseF30DK100094 · NIDDK · VANDERBILT UNIVERSITY · PI MCCALL, ABRAHAM SCOTT · 2013 to 2016
$153kRole of Collagen Binding Receptors in GlomerulosclerosisI01BX002025 · VA · VETERANS HEALTH ADMINISTRATION · PI AMBRA POZZI · 2013 to 2026
–BLRD VA I01 BX002025NHLBI NIH HHS T32 HL094296NIDDK NIH HHS F30 DK100094NIDDK NIH HHS K08 DK097306NIDDK NIH HHS P01 DK065123NIDDK NIH HHS R01 DK018381NIDDK NIH HHS R01 DK065138NIDDK NIH HHS R01 DK095761NIDDK NIH HHS R01 DK099467NIDDK NIH HHS R25 DK096999NIGMS NIH HHS R25 GM062459NIGMS NIH HHS T32 GM007347
Abstract
Basement membranes are defining features of the cellular microenvironment; however, little is known regarding their assembly outside cells. We report that extracellular Cl(-) ions signal the assembly of collagen IV networks outside cells by triggering a conformational switch within collagen IV noncollagenous 1 (NC1) domains. Depletion of Cl(-) in cell culture perturbed collagen IV networks, disrupted matrix architecture, and repositioned basement membrane proteins. Phylogenetic evidence indicates this conformational switch is a fundamental mechanism of collagen IV network assembly throughout Metazoa. Using recombinant triple helical protomers, we prove that NC1 domains direct both protomer and network assembly and show in Drosophila that NC1 architecture is critical for incorporation into basement membranes. These discoveries provide an atomic-level understanding of the dynamic interactions between extracellular Cl(-) and collagen IV assembly outside cells, a critical step in the assembly and organization of basement membranes that enable tissue architecture and function. Moreover, this provides a mechanistic framework for understanding the molecular pathobiology of NC1 domains.
Indexed as
Amino Acid SequenceAnimalsBasement MembraneCattleCell Line, TumorChloridesCollagen Type IVHumansPhylogenyProtein ConformationProtein Structure, TertiaryProtein SubunitsChloridesCollagen Type IVProtein Subunits
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