Fibulin-1 is Required During Cardiac Ventricular Morphogenesis for Versican Cleavage, Suppression of ErbB2 and Erk1/2 Activation, and to Attenuate Trabecular Cardiomyocyte Proliferation

Overview

Journal Dev Dyn

Publisher Wiley

Specialty Anatomy & Histology

Date 2011 Dec 21

PMID 22183742

Citations 19

Authors

Marion A Cooley

Victor M Fresco

Margaret E Dorlon

Waleed O Twal

Nathan V Lee

Jeremy L Barth

Christine B Kern

M Luisa Iruela-Arispe

W Scott Argraves

Affiliations

Soon will be listed here.

Abstract

Background: Trabeculation is an integral component of cardiac ventricular morphogenesis and is dependent on the matrix metalloproteinase, ADAMTS1. A substrate of ADAMTS1 is the proteoglycan versican which is expressed in the developing ventricle and which has been implicated in trabeculation. Fibulin-1 is a versican and ADAMTS1-binding extracellular matrix protein required for ventricular morphogenesis. Here we investigated the involvement of fibulin-1 in ADAMTS1-mediated cleavage of versican in vitro, and the involvement of fibulin-1 in versican cleavage in ventricular morphogenesis.

Results: We show that fibulin-1 is a cofactor for ADAMTS1-dependent in vitro cleavage of versican V1, yielding a 70-kDa amino-terminal fragment. Furthermore, fibulin-1-deficiency in mice was found to cause a significant reduction (>90%) in ventricular levels of the 70-kDa versican V1 cleavage product and a 2-fold increase in trabecular cardiomyocyte proliferation. Decreased versican V1 cleavage and augmented trabecular cardiomyocyte proliferation in fibulin-1 null hearts is accompanied by increased ventricular activation of ErbB2 and Erk1/2. By contrast, versican deficiency was found to lead to decreased cardiomyocyte proliferation and reduced ventricular trabeculation.

Conclusion: We conclude that fibulin-1 regulates versican-dependent events in ventricular morphogenesis by promoting ADAMTS1 cleavage of versican leading to suppression of trabecular cardiomyocyte proliferation mediated by the ErbB2-Map kinase pathway.

Citing Articles

Fibulin-1 promotes intimal hyperplasia after venous stent implantation through ACE mediated angiotensin II signaling.

Gao Y, Chen T, Hong L Heliyon. 2024; 10(7):e27626.

PMID: 38560238 PMC: 10979058. DOI: 10.1016/j.heliyon.2024.e27626.

Exploring the cardiac ECM during fibrosis: A new era with next-gen proteomics.

Sarohi V, Chakraborty S, Basak T Front Mol Biosci. 2022; 9:1030226.

PMID: 36483540 PMC: 9722982. DOI: 10.3389/fmolb.2022.1030226.

Defining the versican interactome in lung health and disease.

Tang F, Brune J, Chang M, Reeves S, Altemeier W, Frevert C Am J Physiol Cell Physiol. 2022; 323(2):C249-C276.

PMID: 35649251 PMC: 9291419. DOI: 10.1152/ajpcell.00162.2022.

ADAMTS Proteins and Vascular Remodeling in Aortic Aneurysms.

Mougin Z, Huguet Herrero J, Boileau C, Le Goff C Biomolecules. 2022; 12(1).

PMID: 35053160 PMC: 8773774. DOI: 10.3390/biom12010012.

Targeting cardiomyocyte proliferation as a key approach of promoting heart repair after injury.

Li S, Ma W, Cai B Mol Biomed. 2022; 2(1):34.

PMID: 35006441 PMC: 8607366. DOI: 10.1186/s43556-021-00047-y.

References

Kern C, Wessels A, McGarity J, Dixon L, Alston E, Argraves W . Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol. 2010; 29(4):304-16. PMC: 2862783. DOI: 10.1016/j.matbio.2010.01.005. View

Aspberg A, Adam S, Kostka G, Timpl R, Heinegard D . Fibulin-1 is a ligand for the C-type lectin domains of aggrecan and versican. J Biol Chem. 1999; 274(29):20444-9. DOI: 10.1074/jbc.274.29.20444. View

Nakamura T, Colbert M, Krenz M, Molkentin J, Hahn H, Dorn 2nd G . Mediating ERK 1/2 signaling rescues congenital heart defects in a mouse model of Noonan syndrome. J Clin Invest. 2007; 117(8):2123-32. PMC: 1913487. DOI: 10.1172/JCI30756. View

Porter S, Clark I, Kevorkian L, Edwards D . The ADAMTS metalloproteinases. Biochem J. 2004; 386(Pt 1):15-27. PMC: 1134762. DOI: 10.1042/BJ20040424. View

King T, Bland Y, Webb S, Barton S, Brown N . Expression of Peg1 (Mest) in the developing mouse heart: involvement in trabeculation. Dev Dyn. 2002; 225(2):212-5. DOI: 10.1002/dvdy.10142. View

Takeuchi T, Kojima M, Nakajima K, Kondo S . jumonji gene is essential for the neurulation and cardiac development of mouse embryos with a C3H/He background. Mech Dev. 1999; 86(1-2):29-38. DOI: 10.1016/s0925-4773(99)00100-8. View

Sedmera D, Pexieder T, Hu N, Clark E . Developmental changes in the myocardial architecture of the chick. Anat Rec. 1997; 248(3):421-32. DOI: 10.1002/(SICI)1097-0185(199707)248:3<421::AID-AR15>3.0.CO;2-R. View

Argraves W, Dickerson K, Burgess W, Ruoslahti E . Fibulin, a novel protein that interacts with the fibronectin receptor beta subunit cytoplasmic domain. Cell. 1989; 58(4):623-9. DOI: 10.1016/0092-8674(89)90097-4. View

Somerville R, Longpre J, Jungers K, Engle J, Ross M, Evanko S . Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol Chem. 2003; 278(11):9503-13. DOI: 10.1074/jbc.M211009200. View

10.

Kuno K, Okada Y, Kawashima H, Nakamura H, Miyasaka M, Ohno H . ADAMTS-1 cleaves a cartilage proteoglycan, aggrecan. FEBS Lett. 2000; 478(3):241-5. DOI: 10.1016/s0014-5793(00)01854-8. View

11.

Shou W, Aghdasi B, Armstrong D, Guo Q, Bao S, Charng M . Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature. 1998; 391(6666):489-92. DOI: 10.1038/35146. View

12.

Zhao S, Fernald R . Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol. 2005; 12(8):1047-64. PMC: 2716216. DOI: 10.1089/cmb.2005.12.1047. View

13.

Godyna S, Mann D, Argraves W . A quantitative analysis of the incorporation of fibulin-1 into extracellular matrix indicates that fibronectin assembly is required. Matrix Biol. 1995; 14(6):467-77. DOI: 10.1016/0945-053x(95)90004-7. View

14.

Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R . Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature. 1995; 378(6555):390-4. DOI: 10.1038/378390a0. View

15.

Sedmera D, Pexieder T, Vuillemin M, Thompson R, Anderson R . Developmental patterning of the myocardium. Anat Rec. 2000; 258(4):319-37. DOI: 10.1002/(SICI)1097-0185(20000401)258:4<319::AID-AR1>3.0.CO;2-O. View

16.

Xiang Y, Dong H, Wan Y, Li J, Yee A, Yang B . Versican G3 domain regulates neurite growth and synaptic transmission of hippocampal neurons by activation of epidermal growth factor receptor. J Biol Chem. 2006; 281(28):19358-68. DOI: 10.1074/jbc.M512980200. View

17.

Kern C, Norris R, Thompson R, Argraves W, Fairey S, Reyes L . Versican proteolysis mediates myocardial regression during outflow tract development. Dev Dyn. 2007; 236(3):671-83. PMC: 1828600. DOI: 10.1002/dvdy.21059. View

18.

Nakajima K, Inagawa M, Uchida C, Okada K, Tane S, Kojima M . Coordinated regulation of differentiation and proliferation of embryonic cardiomyocytes by a jumonji (Jarid2)-cyclin D1 pathway. Development. 2011; 138(9):1771-82. DOI: 10.1242/dev.059295. View

19.

Ong L, Kim N, Mima T, Cohen-Gould L, Mikawa T . Trabecular myocytes of the embryonic heart require N-cadherin for migratory unit identity. Dev Biol. 1998; 193(1):1-9. DOI: 10.1006/dbio.1997.8775. View

20.

Matsumoto K, Shionyu M, Go M, Shimizu K, Shinomura T, Kimata K . Distinct interaction of versican/PG-M with hyaluronan and link protein. J Biol Chem. 2003; 278(42):41205-12. DOI: 10.1074/jbc.M305060200. View