Heparan Sulfate: A Regulator of White Adipocyte Differentiation and of Vascular/Adipocyte Interactions

Overview

Journal Biomedicines

Specialty Biomedical Engineering

Date 2022 Sep 23

PMID 36140217

Authors

J Michael Sorrell

Arnold I Caplan

Affiliations

Soon will be listed here.

Abstract

White adipose tissues are major endocrine organs that release factors, termed adipokines, which affect other major organ systems. The development and functions of adipose tissues depend largely upon the glycosaminoglycan heparan sulfate. Heparan sulfate proteoglycans (HSPGs) surround both adipocytes and vascular structures and facilitate the communication between these two components. This communication mediates the continued export of adipokines from adipose tissues. Heparan sulfates regulate cellular physiology and communication through a sulfation code that ionically interacts with heparan-binding regions on a select set of proteins. Many of these proteins are growth factors and chemokines that regulate tissue function and inflammation. Cells regulate heparan sulfate sulfation through the release of heparanases and sulfatases. It is now possible to tissue engineer vascularized adipose tissues that express heparan sulfate proteoglycans. This makes it possible to use these tissue constructs to study the role of heparan sulfates in the regulation of adipokine production and release. It is possible to regulate the production of heparanases and sulfatases in order to fine-tune experimental studies.

References

Aratani Y, Kitagawa Y . Enhanced synthesis and secretion of type IV collagen and entactin during adipose conversion of 3T3-L1 cells and production of unorthodox laminin complex. J Biol Chem. 1988; 263(31):16163-9. View

Tavassoli M . Ultrastructural development of bone marrow adipose cell. Acta Anat (Basel). 1976; 94(1):65-77. DOI: 10.1159/000144545. View

Arita Y, Kihara S, Ouchi N, Maeda K, Kuriyama H, Okamoto Y . Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation. 2002; 105(24):2893-8. DOI: 10.1161/01.cir.0000018622.84402.ff. View

Iozzo R . Heparan sulfate proteoglycans: intricate molecules with intriguing functions. J Clin Invest. 2001; 108(2):165-7. PMC: 203034. DOI: 10.1172/JCI13560. View

Marinkovich M, Keene D, Rimberg C, Burgeson R . Cellular origin of the dermal-epidermal basement membrane. Dev Dyn. 1993; 197(4):255-67. DOI: 10.1002/aja.1001970404. View

Ramakrishnan V, Boyd N . The Adipose Stromal Vascular Fraction as a Complex Cellular Source for Tissue Engineering Applications. Tissue Eng Part B Rev. 2017; 24(4):289-299. PMC: 6080106. DOI: 10.1089/ten.TEB.2017.0061. View

Tran-Lundmark K, Tran P, Paulsson-Berne G, Friden V, Soininen R, Tryggvason K . Heparan sulfate in perlecan promotes mouse atherosclerosis: roles in lipid permeability, lipid retention, and smooth muscle cell proliferation. Circ Res. 2008; 103(1):43-52. PMC: 2765377. DOI: 10.1161/CIRCRESAHA.108.172833. View

Frerich B, Winter K, Scheller K, Braumann U . Comparison of different fabrication techniques for human adipose tissue engineering in severe combined immunodeficient mice. Artif Organs. 2011; 36(3):227-37. DOI: 10.1111/j.1525-1594.2011.01346.x. View

Yamashita Y, Nakada S, Yoshihara T, Nara T, Furuya N, Miida T . Perlecan, a heparan sulfate proteoglycan, regulates systemic metabolism with dynamic changes in adipose tissue and skeletal muscle. Sci Rep. 2018; 8(1):7766. PMC: 5958100. DOI: 10.1038/s41598-018-25635-x. View

10.

Langford R, Hurrion E, Dawson P . Genetics and pathophysiology of mammalian sulfate biology. J Genet Genomics. 2017; 44(1):7-20. DOI: 10.1016/j.jgg.2016.08.001. View

11.

Kolset S, Salmivirta M . Cell surface heparan sulfate proteoglycans and lipoprotein metabolism. Cell Mol Life Sci. 2001; 56(9-10):857-70. PMC: 11146903. DOI: 10.1007/s000180050031. View

12.

Traktuev D, Prater D, Merfeld-Clauss S, Sanjeevaiah A, Saadatzadeh M, Murphy M . Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res. 2009; 104(12):1410-20. DOI: 10.1161/CIRCRESAHA.108.190926. View

13.

Recinella L, Orlando G, Ferrante C, Chiavaroli A, Brunetti L, Leone S . Adipokines: New Potential Therapeutic Target for Obesity and Metabolic, Rheumatic, and Cardiovascular Diseases. Front Physiol. 2020; 11:578966. PMC: 7662468. DOI: 10.3389/fphys.2020.578966. View

14.

van Wijk X, van Kuppevelt T . Heparan sulfate in angiogenesis: a target for therapy. Angiogenesis. 2013; 17(3):443-62. DOI: 10.1007/s10456-013-9401-6. View

15.

Zhu S, Li J, Loka R, Song Z, Vlodavsky I, Zhang K . Modulating Heparanase Activity: Tuning Sulfation Pattern and Glycosidic Linkage of Oligosaccharides. J Med Chem. 2020; 63(8):4227-4255. PMC: 7376576. DOI: 10.1021/acs.jmedchem.0c00156. View

16.

Berthod F, Germain L, Tremblay N, Auger F . Extracellular matrix deposition by fibroblasts is necessary to promote capillary-like tube formation in vitro. J Cell Physiol. 2006; 207(2):491-8. DOI: 10.1002/jcp.20584. View

17.

Pessentheiner A, Ducasa G, Gordts P . Proteoglycans in Obesity-Associated Metabolic Dysfunction and Meta-Inflammation. Front Immunol. 2020; 11:769. PMC: 7248225. DOI: 10.3389/fimmu.2020.00769. View

18.

Nielsen M, Brejning J, Garcia R, Zhang H, Hayden M, Vilaro S . Segments in the C-terminal folding domain of lipoprotein lipase important for binding to the low density lipoprotein receptor-related protein and to heparan sulfate proteoglycans. J Biol Chem. 1997; 272(9):5821-7. DOI: 10.1074/jbc.272.9.5821. View

19.

Sillat T, Saat R, Pollanen R, Hukkanen M, Takagi M, Konttinen Y . Basement membrane collagen type IV expression by human mesenchymal stem cells during adipogenic differentiation. J Cell Mol Med. 2011; 16(7):1485-95. PMC: 3823217. DOI: 10.1111/j.1582-4934.2011.01442.x. View

20.

Weng X, Maxwell-Warburton S, Hasib A, Ma L, Kang L . The membrane receptor CD44: novel insights into metabolism. Trends Endocrinol Metab. 2022; 33(5):318-332. DOI: 10.1016/j.tem.2022.02.002. View