CoChat
Sign Up
Cited by 49

The DOI matches its Crossref record; 13 of the 13 references it cites were found in a registry or an index.

Heparan sulfate proteoglycans and triglyceride-rich lipoprotein metabolism

Bishop, Joseph R, Stanford, Kristin I, Esko, Jeffrey D·2008·Current Opinion in Lipidology
DOI 10.1097/mol.0b013e3282feec2d
Open this paper in CoChat — free account

Abstract

Purpose of review Clearance of triglyceride-rich lipoprotein remnants by the liver is a key step in preventing hypertriglyceridemia, an independent risk factor for cardiovascular disease. We review recent genetic evidence that heparan sulfate proteoglycans work in concert with the LDL receptor in the liver to facilitate binding and clearance of both triglyceride and cholesterol-rich lipoproteins from the circulation. Recent findings Partial reduction of sulfation of liver heparan sulfate using the Cre-loxP system caused accumulation of hepatic and dietary triglyceride-rich lipoprotein particles due to delayed clearance. Compounding the mutation with LDL receptor deficiency caused enhanced accumulation of both cholesterol and triglyceride-rich particles compared with mice lacking only LDL receptors. These findings provide the first genetic evidence that hepatic heparan sulfate proteoglycans play a central role in the clearance of lipoproteins by the liver and work independently of LDL receptors. Summary A role for hepatocyte heparan sulfate in lipoprotein metabolism has now been genetically established in mice. Given this finding, mild, but clinically relevant, hyperlipidemias in human patients may be a result of alterations in heparan sulfate structure or possible genetic polymorphisms in the relevant biosynthetic genes.

Overview

Integrity signals

Registry

Crossref · 10.1097/mol.0b013e3282feec2d

Cites

13 of 13 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • TRLs arising from LPL-mediated lipolysis are cleared by multiple hepatic receptors, including LDLR, LRP1, and syndecan-1 (SDC).

    “TRLs arising from LPL-mediated lipolysis are cleared by multiple hepatic receptors, including LDL receptor (LDLR), LDLR-related protein 1 (LRP1), and syndecan-1 (SDC), the predominant hepatic heparin sulfate proteoglycan (HSPG) (Bishop et al., 2008; Foley et al., 2013; MacArthur et al., 2007; Stanford et al., 2009).”

    From γ-secretase inhibition lowers plasma triglyceride-rich lipoproteins by stabilizing the LDL receptor (2018) · cites this paper as Bishop et al., 2008

  • In mice, diminished sulfation of heparan sulfate in hepatocytes alters hepatic lipoprotein clearance via heparan sulfate proteoglycans and can cause accumulation of triglyceride-rich lipoproteins.

    “In mice, accumulation of triglyceride-rich lipoproteins can occur if sulfation of heparan sulfate in hepatocytes is diminished, as this alters hepatic lipoprotein clearance via heparan sulfate proteoglycans (HSPGs).”

    From Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice (2009) · cites this paper as [10]

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 57

  1. Havel, 2004, Hepatic catabolism of remnant lipoproteins: where the action is, Arterioscler Thromb Vasc Biol, 24, 213, 10.1161/01.ATV.0000115382.53810.24 · DOI
  2. Weiss, 1989, The asialoglycoprotein receptor: properties and modulation by ligand, Prog Clin Biol Res, 300, 169
  3. Woodworth, 2001, The man/GalNAc-4-SO4-receptor has multiple specificities and functions, Results Probl Cell Differ, 33, 123, 10.1007/978-3-540-46410-5_7 · DOI
  4. Weigel, 2002, Glycans as endocytosis signals: the cases of the asialoglycoprotein and hyaluronan/chondroitin sulfate receptors, Biochim Biophys Acta Gen Subj, 1572, 341, 10.1016/S0304-4165(02)00318-5 · DOI · Paper page
  5. Brown, 1981, Regulation of plasma cholesterol by lipoprotein receptors, Science, 212, 628, 10.1126/science.6261329 · DOI · Paper page
  6. Brown, 1986, A receptor-mediated pathway for cholesterol homeostasis, Science, 232, 34, 10.1126/science.3513311 · DOI · Paper page
  7. Herz, 2001, LRP: a multifunctional scavenger and signaling receptor, J Clin Invest, 108, 779, 10.1172/JCI200113992 · DOI · Paper page
  8. Tacken, 2001, Living up to a name: the role of the VLDL receptor in lipid metabolism, Curr Opin Lipidol, 12, 275, 10.1097/00041433-200106000-00006 · DOI
  9. Fujino, 2003, Low-density lipoprotein receptor-related protein 5 (LRP5) is essential for normal cholesterol metabolism and glucose-induced insulin secretion, Proc Natl Acad Sci U S A, 100, 229, 10.1073/pnas.0133792100 · DOI · Paper page
  10. Williams, 1997, Cell-surface heparan sulfate proteoglycans: dynamic molecules mediating ligand catabolism, Curr Opin Lipidol, 8, 253, 10.1097/00041433-199710000-00003 · DOI · Paper page
  11. Mahley, 1999, Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E, J Lipid Res, 40, 1, 10.1016/S0022-2275(20)33334-4 · DOI · Paper page
  12. Ji, 1995, Intravenous heparinase inhibits remnant lipoprotein clearance from the plasma and uptake by the liver: in vivo role of heparan sulfate proteoglycans, J Lipid Res, 36, 583, 10.1016/S0022-2275(20)39892-8 · DOI
  13. Cortes, 2007, Liver heparan sulfate proteoglycans: old molecules provide new insights on lipoprotein metabolism, Hepatology, 45, 1078, 10.1002/hep.21647 · DOI
  14. Esko, 2001, Molecular diversity of heparan sulfate, J Clin Invest, 108, 169, 10.1172/JCI200113530 · DOI
  15. Oldberg, 1979, Cell-surface heparan sulfate. Isolation and characterization of a proteoglycan from rat liver membranes, J Biol Chem, 254, 8505, 10.1016/S0021-9258(19)86920-X · DOI
  16. Lyon, 1994, Liver heparan sulfate structure. A novel molecular design, J Biol Chem, 269, 11208, 10.1016/S0021-9258(19)78112-5 · DOI · Paper page
  17. Zhang, 1994, Amino acid determinants that drive heparan sulfate assembly in a proteoglycan, J Biol Chem, 269, 19295, 10.1016/S0021-9258(17)32166-X · DOI
  18. Zhang, 1995, Repetitive Ser-Gly sequences enhance heparan sulfate assembly in proteoglycans, J Biol Chem, 270, 27127, 10.1074/jbc.270.45.27127 · DOI
  19. Hacker, 2005, Heparan sulphate proteoglycans: the sweet side of development, Nat Rev Mol Cell Biol, 6, 530, 10.1038/nrm1681 · DOI
  20. Bulow, 2006, The molecular diversity of glycosaminoglycans shapes animal development, Annu Rev Cell Dev Biol, 22, 375, 10.1146/annurev.cellbio.22.010605.093433 · DOI
  21. Coppi, 2007, Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells, Cell Host Microbe, 2, 316, 10.1016/j.chom.2007.10.002 · DOI
  22. Vongchan, 2005, Structural characterization of human liver heparan sulfate, Biochim Biophys Acta, 1721, 1, 10.1016/j.bbagen.2004.09.007 · DOI · Paper page
  23. Horie, 1992, The functional characteristics of a human apolipoprotein E variant (cysteine at residue 142) may explain its association with dominant expression of type III hyperlipoproteinemia, J Biol Chem, 267, 1962, 10.1016/S0021-9258(18)46040-1 · DOI · Paper page
  24. Ji, 1994, Variable heparan sulfate proteoglycan binding of apolipoprotein E variants may modulate the expression of type III hyperlipoproteinemia, J Biol Chem, 269, 13421, 10.1016/S0021-9258(17)36849-7 · DOI · Paper page
  25. Mann, 1995, Apolipoprotein E isoforms and rare mutations: parallel reduction in binding to cells and to heparin reflects severity of associated type III hyperlipoproteinemia, J Lipid Res, 36, 517, 10.1016/S0022-2275(20)39885-0 · DOI · Paper page
  26. Minnich, 1995, Identification and characterization of a novel apolipoprotein E variant, apolipoprotein E3′ (Arg136–>His): association with mild dyslipidemia and double prebeta very low density lipoproteins, J Lipid Res, 36, 57, 10.1016/S0022-2275(20)39754-6 · DOI · Paper page
  27. Marz, 1998, Apolipoprotein E2 (Arg136–> Cys) mutation in the receptor binding domain of apoE is not associated with dominant type III hyperlipoproteinemia, J Lipid Res, 39, 658, 10.1016/S0022-2275(20)33303-4 · DOI
  28. Goldberg, 1998, The NH2-terminal region of apolipoprotein B is sufficient for lipoprotein association with glycosaminoglycans, J Biol Chem, 273, 35355, 10.1074/jbc.273.52.35355 · DOI
  29. Borén, 1998, Identification of the principal proteoglycan-binding site in LDL: a single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding, J Clin Invest, 101, 2658, 10.1172/JCI2265 · DOI
  30. Flood, 2002, Identification of the proteoglycan binding site in apolipoprotein B48, J Biol Chem, 277, 32228, 10.1074/jbc.M204053200 · DOI
  31. Wong, 2007, Characterization of apolipoprotein A-V structure and mode of plasma triacylglycerol regulation, Curr Opin Lipidol, 18, 319, 10.1097/MOL.0b013e328133856c · DOI
  32. Goldberg, 2001, Lipoprotein lipase: physiology, biochemistry, and molecular biology, Front Biosci, 6, D388
  33. Parthasarathy, 1994, Oligosaccharide sequences of endothelial cell surface heparan sulfate proteoglycan with affinity for lipoprotein lipase, J Biol Chem, 269, 22391, 10.1016/S0021-9258(17)31802-1 · DOI · Paper page
  34. Spillmann, 2006, Isolation and characterization of low sulfated heparan sulfate sequences with affinity for lipoprotein lipase, J Biol Chem, 281, 23405, 10.1074/jbc.M604702200 · DOI · Paper page
  35. Anfinsen, 1952, The role of heparin in lipoprotein metabolism, Science, 115, 583, 10.1126/science.115.2996.583 · DOI
  36. Beigneux, 2007, Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons, Cell Metab, 5, 279, 10.1016/j.cmet.2007.02.002 · DOI · Paper page
  37. Young, 2007, GPIHBP1: an endothelial cell molecule important for the lipolytic processing of chylomicrons, Curr Opin Lipidol, 18, 389, 10.1097/MOL.0b013e3281527914 · DOI
  38. Wallinder, 1984, Hepatic and extrahepatic uptake of intravenously injected lipoprotein lipase, Biochim Biophys Acta, 795, 513, 10.1016/0005-2760(84)90181-4 · DOI
  39. Olivecrona, 1993, Lipoprotein lipase and hepatic lipase, Curr Opin Lipidol, 4, 187, 10.1097/00041433-199306000-00003 · DOI
  40. Williams, 1992, Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein(a), low density lipoprotein, and nascent lipoproteins. Roles for low density lipoprotein receptors and heparan sulfate proteoglycans, J Biol Chem, 267, 13284, 10.1016/S0021-9258(18)42208-9 · DOI · Paper page
  41. Aikawa, 2001, Multiple isozymes of heparan sulfate/heparin GlcNAc N-deacetylase/N-sulfotransferase: structure and activity of the fourth member, NDST4, J Biol Chem, 276, 5876, 10.1074/jbc.M009606200 · DOI
  42. Postic, 2000, DNA excision in liver by an albumin-Cre transgene occurs progressively with age, Genesis, 26, 149, 10.1002/(SICI)1526-968X(200002)26:2<149::AID-GENE16>3.0.CO;2-V · DOI
  43. Condac, 2007, Polycystic disease caused by deficiency in xylosyltransferase 2, an initiating enzyme of glycosaminoglycan biosynthesis, Proc Natl Acad Sci U S A, 104, 9416, 10.1073/pnas.0700908104 · DOI
  44. Fuki, 1997, The syndecan family of proteoglycans. Novel receptors mediating internalization of atherogenic lipoproteins in vitro, J Clin Invest, 100, 1611, 10.1172/JCI119685 · DOI · Paper page
  45. Zeng, 1998, Chylomicron remnant uptake is regulated by the expression and function of heparan sulfate proteoglycan in hepatocytes, J Lipid Res, 39, 845, 10.1016/S0022-2275(20)32571-2 · DOI · Paper page
  46. Wilsie, 2006, Syndecan-1 mediates internalization of apoE-VLDL through a low density lipoprotein receptor-related protein (LRP)-independent, nonclathrin-mediated pathway, Lipids Health Dis, 5, 23, 10.1186/1476-511X-5-23 · DOI · Paper page
  47. Cortes, 2007, Adenovirus-mediated hepatic syndecan-1 overexpression induces hepatocyte proliferation and hyperlipidaemia in mice, Liver Int, 27, 569, 10.1111/j.1478-3231.2007.01442.x · DOI
  48. Tkachenko, 2005, Syndecans: new kids on the signaling block, Circ Res, 96, 488, 10.1161/01.RES.0000159708.71142.c8 · DOI
  49. Yanagishita, 1992, Cell surface heparan sulfate proteoglycans, J Biol Chem, 267, 9451, 10.1016/S0021-9258(19)50108-9 · DOI
  50. Takeuchi, 1992, Recycling of transferrin receptors and heparan sulfate proteoglycans in a rat parathyroid cell line, J Biol Chem, 267, 14685, 10.1016/S0021-9258(18)42095-9 · DOI
  51. Fransson, 2004, Novel aspects of glypican glycobiology, Cell Mol Life Sci, 61, 1016, 10.1007/s00018-004-3445-0 · DOI
  52. Zimmermann, 2005, Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6, Dev Cell, 9, 377, 10.1016/j.devcel.2005.07.011 · DOI
  53. Truong, 2000, Analysis of low-density lipoprotein catabolism by primary cultures of hepatic cells from normal and low-density lipoprotein receptor knockout mice, Biochim Biophys Acta, 1484, 307, 10.1016/S1388-1981(00)00023-8 · DOI
  54. Auger, 2001, Low and high density lipoprotein metabolism in primary cultures of hepatic cells from normal and apolipoprotein E knockout mice, Eur J Biochem, 268, 2322, 10.1046/j.1432-1327.2001.02115.x · DOI
  55. Payne, 2007, Internalization and trafficking of cell surface proteoglycans and proteoglycan-binding ligands, Traffic, 8, 389, 10.1111/j.1600-0854.2007.00540.x · DOI
  56. Shimano, 1994, Secretion-recapture process of apolipoprotein E in hepatic uptake of chylomicron remnants in transgenic mice, J Clin Invest, 93, 2215, 10.1172/JCI117218 · DOI
  57. Rodriguez-Lee, 2007, Fatty acid-induced atherogenic changes in extracellular matrix proteoglycans, Curr Opin Lipidol, 18, 546, 10.1097/MOL.0b013e3282ef534f · DOI

Cited by

Sorted by citations

Metadata

Authors
Bishop, J. R., Stanford, K. I., & Esko, J. D.
Venue
Current Opinion in Lipidology
Publisher
Ovid Technologies (Wolters Kluwer Health)
Published
2008-06
Volume
19
Issue
3
Pages
307-313
ISSN
0957-9672
DOI
10.1097/mol.0b013e3282feec2d
Cited by
49
References
13
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review