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.

Williams, K.J.; Fless, G.M.; Petrie, K.A.; Snyder, M.L.; Brocia, R.W.; Swenson, T.L.

doi:10.1016/s0021-9258(18)42208-9

Cited by 205

The DOI matches its Crossref record.

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.

Williams, K.J., Fless, G.M., Petrie, K.A., Snyder, M.L., Brocia, R.W., Swenson, T.L.·1992·Journal of Biological Chemistry

DOI 10.1016/s0021-9258(18)42208-9

Open this paper in CoChat — free account

Abstract

We sought to investigate effects of lipoprotein lipase (LpL) on cellular catabolism of lipoproteins rich in apolipoprotein B-100. LpL increased cellular degradation of lipoprotein(a) (Lp(a)) and low density lipoprotein (LDL) by 277% +/- 3.8% and 32.5% +/- 4.1%, respectively, and cell association by 509% +/- 8.7% and 83.9% +/- 4.0%. The enhanced degradation was entirely lysosomal. Enhanced degradation of Lp(a) had at least two components, one LDL receptor-dependent and unaffected by heparitinase digestion of the cells, and the other LDL receptor-independent and heparitinase-sensitive. The effect of LpL on LDL degradation was entirely LDL receptor-independent, heparitinase-sensitive, and essentially absent from mutant Chinese hamster ovary cells that lack cell surface heparan sulfate proteoglycans. Enhanced cell association of Lp(a) and LDL was largely LDL receptor-independent and heparitinase-sensitive. The ability of LpL to reduce net secretion of apolipoprotein B-100 by HepG2 cells by enhancing cellular reuptake of nascent lipoproteins was also LDL receptor-independent and heparitinase-sensitive. None of these effects on Lp(a), LDL, or nascent lipoproteins required LpL enzymatic activity. We conclude that LpL promotes binding of apolipoprotein B-100-rich lipoproteins to cell surface heparan sulfate proteoglycans. LpL also enhanced the otherwise weak binding of Lp(a) to LDL receptors. The heparan sulfate proteoglycan pathway represents a novel catabolic mechanism that may all…

Integrity signals

Registry

Crossref · 10.1016/s0021-9258(18)42208-9

Cites

Statistics

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

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?

In cell culture models, HSPGs can interact directly with lipoproteins bearing apoE, Lpl, and HL and facilitate their internalization by endocytosis.
“In cell culture models, HSPGs can interact directly with lipoproteins bearing apoE, Lpl, and HL and facilitate their internalization by endocytosis (6,17,23).”
From Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members (2007) · cites this paper as [6]

No references could be resolved yet.

Research works printed but not linked: 85

Williams, 1991, Circulation, 84, 566
Editorial, 1988, Lancet, 1, 1141
Scanu, 1990, J. Clin. Invest., 85, 1709, 10.1172/JCI114625 · DOI
Editorial, 1991, Lancet, 337, 397, 10.1016/0140-6736(91)91170-Y · DOI
Goldstein, 1983, Methods Enzymol., 98, 241, 10.1016/0076-6879(83)98152-1 · DOI
Zawadzki, 1988, Biochemistry, 27, 8474, 10.1021/bi00422a027 · DOI
Miles, 1989, Nature, 339, 301, 10.1038/339301a0 · DOI
Hajjar, 1989, Nature, 339, 303, 10.1038/339303a0 · DOI
Zilversmit, 1973, Circ. Res., 33, 633, 10.1161/01.RES.33.6.633 · DOI
Zilversmit, 1979, Circulation, 60, 473, 10.1161/01.CIR.60.3.473 · DOI · Paper page
Beisiegel, 1991, Curr. Opin. Lipidol., 2, 317, 10.1097/00041433-199110000-00008 · DOI
Ishibashi, 1990, J. Biol. Chem., 265, 3040, 10.1016/S0021-9258(19)39730-3 · DOI
Catapano, 1979, J. Biol. Chem., 254, 1007, 10.1016/S0021-9258(17)34157-1 · DOI
Bradley, 1984, J. Biol. Chem., 259, 14728, 10.1016/S0021-9258(17)42663-9 · DOI
Mulder, 1991, Biochim. Biophys. Acta, 1081, 308, 10.1016/0005-2760(91)90287-R · DOI
Aviram, 1988, J. Biol. Chem., 263, 15416, 10.1016/S0021-9258(19)37604-5 · DOI
Aviram, 1988, J. Biol. Chem., 263, 16842, 10.1016/S0021-9258(18)37468-4 · DOI
Ostlund-Lindqvist, 1983, Arteriosclerosis, 3, 433, 10.1161/01.ATV.3.5.433 · DOI
Borensztajn, 1988, J. Lipid Res., 29, 1087, 10.1016/S0022-2275(20)38471-6 · DOI
Robinson, 1963, Adv. Lipid Res., 1, 133, 10.1016/B978-1-4831-9937-5.50010-7 · DOI
Felts, 1975, Biochem. Biophys. Res. Commun., 66, 1467, 10.1016/0006-291X(75)90524-0 · DOI · Paper page
Shimada, 1981, J. Clin. Invest., 68, 995, 10.1172/JCI110354 · DOI
Cisar, 1989, J. Biol. Chem., 264, 1767, 10.1016/S0021-9258(18)94253-5 · DOI
Goldberg, 1986, J. Clin. Invest., 78, 1523, 10.1172/JCI112744 · DOI
Beisiegel, 1991, Proc. Natl. Acad. Sci. U. S. A., 88, 8342, 10.1073/pnas.88.19.8342 · DOI · Paper page
Williams, 1991, J. Clin. Invest., 88, 1300, 10.1172/JCI115434 · DOI
Goldstein, 1976, Cell, 7, 85, 10.1016/0092-8674(76)90258-0 · DOI
Williams, 1990, J. Biol. Chem., 265, 16741, 10.1016/S0021-9258(17)44822-8 · DOI
Rothblat, 1977, Biochem. Biophys. Res. Commun., 78, 45, 10.1016/0006-291X(77)91219-0 · DOI
Posner, 1983, Arch. Biochem. Biophys., 226, 306, 10.1016/0003-9861(83)90297-7 · DOI
Snyder, 1992, J. Biol. Chem., 267, 339, 10.1016/S0021-9258(18)48499-2 · DOI
Fless, 1986, J. Biol. Chem., 261, 8712, 10.1016/S0021-9258(19)84439-3 · DOI
Bilheimer, 1972, Biochim. Biophys. Acta, 260, 212, 10.1016/0005-2760(72)90034-3 · DOI
Wallinder, 1984, Biochim. Biophys. Acta, 795, 513, 10.1016/0005-2760(84)90181-4 · DOI
Quinn, 1985, Biochim. Biophys. Acta, 834, 267, 10.1016/0005-2760(85)90165-1 · DOI
Bradford, 1976, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 · DOI · Paper page
Beisiegel, 1981, J. Biol. Chem., 256, 11923, 10.1016/S0021-9258(19)68494-2 · DOI · Paper page
Knowles, 1980, Science, 209, 497, 10.1126/science.6248960 · DOI
Goldstein, 1975, Proc. Natl. Acad. Sci. U. S. A., 72, 1092, 10.1073/pnas.72.3.1092 · DOI
Murphy-Ullrich, 1988, J. Biol. Chem., 263, 6400, 10.1016/S0021-9258(18)68799-X · DOI
Esko, 1991, Curr. Opin. Cell Biol., 3, 805, 10.1016/0955-0674(91)90054-3 · DOI
Capriotti, 1986, J. Tissue Culture Methods, 10, 219, 10.1007/BF01404480 · DOI
Rapraeger, 1991, Science, 252, 1705, 10.1126/science.1646484 · DOI · Paper page
Humphries, 1988, Biochem. Biophys. Res. Commun., 154, 365, 10.1016/0006-291X(88)90694-8 · DOI
Markwell, 1978, Anal. Biochem., 87, 206, 10.1016/0003-2697(78)90586-9 · DOI
Bisgaier, 1991, J. Lipid Res., 32, 21, 10.1016/S0022-2275(20)42240-0 · DOI
Bliss, 1967, 1, 213
Friedman, 1982, Biochim. Biophys. Acta, 711, 114, 10.1016/0005-2760(82)90016-9 · DOI
Faustinella, 1991, J. Biol. Chem., 266, 9481, 10.1016/S0021-9258(18)92846-2 · DOI
Seguchi, 1991, Arch. Biochem. Biophys., 284, 245, 10.1016/0003-9861(91)90292-Q · DOI
Kjellén, 1991, Annu. Rev. Biochem., 60, 443, 10.1146/annurev.bi.60.070191.002303 · DOI
Ishihara, 1987, J. Biol. Chem., 262, 4708, 10.1016/S0021-9258(18)61253-0 · DOI
Busch, 1989, J. Biol. Chem., 264, 9527, 10.1016/S0021-9258(18)60563-0 · DOI
Bosner, 1988, Proc. Natl. Acad. Sci. U. S. A., 85, 7438, 10.1073/pnas.85.20.7438 · DOI
Zolfaghari, 1989, Proc. Natl. Acad. Sci. U. S. A., 86, 6913, 10.1073/pnas.86.18.6913 · DOI
Stein, 1984, Biochim. Biophys. Acta, 795, 47, 10.1016/0005-2760(84)90103-6 · DOI
Camejo, 1990, Curr. Opin. Lipidol., 1, 431, 10.1097/00041433-199010000-00006 · DOI
Grundy, 1987, Arteriosclerosis, 7, 203
Babirak, 1989, Arteriosclerosis, 9, 326, 10.1161/01.ATV.9.3.326 · DOI
Babirak, 1989, Circulation, 80, 79
Wilson, 1990, J. Clin. Invest., 86, 735, 10.1172/JCI114770 · DOI
Emi, 1990, J. Biol. Chem., 265, 5910, 10.1016/S0021-9258(19)39449-9 · DOI
Lund-Katz, 1991, J. Biol. Chem., 266, 2701, 10.1016/S0021-9258(18)49900-0 · DOI
Brown, 1991, Curr. Opin. Lipidol., 2, 65, 10.1097/00041433-199104000-00002 · DOI
Kjellén, 1981, Proc. Natl. Acad. Sci. U. S. A., 78, 5371, 10.1073/pnas.78.9.5371 · DOI
Brandan, 1989, J. Biol. Chem., 264, 10520, 10.1016/S0021-9258(18)81652-0 · DOI
Chan, 1988, Science, 241, 1670, 10.1126/science.2843987 · DOI
Chajek-Shaul, 1989, Biochim. Biophys. Acta, 1014, 178, 10.1016/0167-4889(89)90031-1 · DOI
Klinger, 1985, J. Biol. Chem., 260, 4082, 10.1016/S0021-9258(18)89234-1 · DOI
Saxena, 1991, J. Biol. Chem., 266, 17516, 10.1016/S0021-9258(19)47402-4 · DOI · Paper page
Kern, 1990, J. Lipid Res., 31, 17, 10.1016/S0022-2275(20)42756-7 · DOI
Peterson, 1985, Biochim. Biophys. Acta, 837, 262, 10.1016/0005-2760(85)90049-9 · DOI
Vilaro, 1988, Biochim. Biophys. Acta, 959, 106, 10.1016/0005-2760(88)90021-5 · DOI · Paper page
Camps, 1991, J. Lipid Res., 32, 1877, 10.1016/S0022-2275(20)41891-7 · DOI
Howard, 1971, Atherosclerosis, 14, 17, 10.1016/0021-9150(71)90035-9 · DOI
Jonasson, 1987, J. Lipid Res., 28, 437, 10.1016/S0022-2275(20)38694-6 · DOI
Ylä-Herttuala, 1991, Circulation, 84, 258
Wiklund, 1991, Circulation, 84, 258
Pitas, 1990, J. Biol. Chem., 265, 12722, 10.1016/S0021-9258(19)38404-2 · DOI
Wolfbauer, 1986, Proc. Natl. Acad. Sci. U. S. A., 83, 7760, 10.1073/pnas.83.20.7760 · DOI
Xu, 1991, J. Biol. Chem., 266, 24849, 10.1016/S0021-9258(18)54306-4 · DOI
Williams, 1988, Proc. Natl. Acad. Sci. U. S. A., 85, 242, 10.1073/pnas.85.1.242 · DOI
Shirai, 1981, Biochim. Biophys. Acta, 665, 504, 10.1016/0005-2760(81)90264-2 · DOI
Weisweiler, 1990, Circulation, 82, 6
Jones, 1991, Circulation, 84, 483

Sorted by citations

The Response-to-Retention Hypothesis of Early Atherogenesis
Williams, K. J., & Tabas, I. (1995) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.15.5.551 · Cited by 1,413
Self-citation
Subendothelial Lipoprotein Retention as the Initiating Process in Atherosclerosis: Update and Therapeutic Implications
Tabas, I., Williams, K. J., & Borén, J. (2007) · Circulation · doi:10.1161/circulationaha.106.676890 · Cited by 1,399
Self-citation
Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E
Mahley, R. W., & Ji, Z.-S. (1999) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)33334-4 · Cited by 693
Osteoprotegerin is bound, internalized, and degraded by multiple myeloma cells.
Standal, T., Seidel, C., Hjertner, Ø., Plesner, T., Sanderson, R. D., Waage, A., Borset, M., & Sundan, A. (2002) · Blood · doi:10.1182/blood-2002-04-1190 · Cited by 244
Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice
Stanford, K. I., Bishop, J. R., Foley, E. M., Gonzales, J. C., Niesman, I. R., Witztum, J. L., & Esko, J. D. (2009) · Journal of Clinical Investigation · doi:10.1172/jci38251 · Cited by 226
Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members
MacArthur, J. M., Bishop, J. R., Stanford, K. I., Wang, L., Bensadoun, A., Witztum, J. L., & Esko, J. D. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29154 · Cited by 216
Low density lipoprotein receptor internalizes low density and very low density lipoproteins that are bound to heparan sulfate proteoglycans via lipoprotein lipase
Mulder, M., Lombardi, P., Jansen, H., van Berkel, T. J., Frants, R. R., & Havekes, L. M. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)98359-6 · Cited by 214
Postprandial hypertriglyceridemia as a coronary risk factor
Borén, J., Matikainen, N., Adiels, M., & Taskinen, M.-R. (2014) · Clinica Chimica Acta · doi:10.1016/j.cca.2014.01.015 · Cited by 182
Lipoprotein lipase mass and activity in plasma and their increase after heparin are separate parameters with different relations to plasma lipoproteins
Tornvall, P., Olivecrona, G., Karpe, F., Hamsten, A., & Olivecrona, T. (1995) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.15.8.1086 · Cited by 172
Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing
Mahley, R. W., & Huang, Y. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30889 · Cited by 159
Differential Cellular Accumulation/Retention of Apolipoprotein E Mediated by Cell Surface Heparan Sulfate Proteoglycans
Ji, Z.-S., Pitas, R. E., & Mahley, R. W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.22.13452 · Cited by 134
Presecretory oxidation, aggregation, and autophagic destruction of apoprotein-B: A pathway for late-stage quality control
Pan, M., Maitin, V., Parathath, S., Andreo, U., Lin, S. X., Germain, C. S., Yao, Z., Maxfield, F. R., Williams, K. J., & Fisher, E. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707460104 · Cited by 128
Self-citation
ApoC-III content of apoB-containing lipoproteins is associated with binding to the vascular proteoglycan biglycan
Olin-Lewis, K., Krauss, R. M., La Belle, M., Blanche, P. J., Barrett, P. H. R., Wight, T. N., & Chait, A. (2002) · Journal of Lipid Research · doi:10.1194/jlr.m200322-jlr200 · Cited by 114
Phospholipid Transfer Protein Deficiency Impairs Apolipoprotein-B Secretion from Hepatocytes by Stimulating a Proteolytic Pathway through a Relative Deficiency of Vitamin E and an Increase in Intracellular Oxidants
Jiang, X.-C., Li, Z., Liu, R., Yang, X. P., Pan, M., Lagrost, L., Fisher, E. A., & Williams, K. J. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m500007200 · Cited by 102
Self-citation
Recent insights into factors affecting remnant lipoprotein uptake
Williams, K. J., & Chen, K. (2010) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328338cabc · Cited by 91
Self-citation
Hepatic remnant lipoprotein clearance by heparan sulfate proteoglycans and low-density lipoprotein receptors depend on dietary conditions in mice
Foley, E. M., Gordts, P. L. S. M., Stanford, K. I., Gonzales, J. C., Lawrence, R., Stoddard, N., & Esko, J. D. (2013) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.113.301637 · Cited by 77
Lipoprotein Lipase Up‐regulation in Hepatic Stellate Cells Exacerbates Liver Fibrosis in Nonalcoholic Steatohepatitis in Mice
Teratani, T., Tomita, K., Furuhashi, H., Sugihara, N., Higashiyama, M., Nishikawa, M., Irie, R., Takajo, T., Wada, A., Horiuchi, K., et al. (2019) · Hepatology Communications · doi:10.1002/hep4.1383 · Cited by 56
Activated Cyclin-Dependent Kinase 5 Promotes Microglial Phagocytosis of Fibrillar β-Amyloid by Up-regulating Lipoprotein Lipase Expression
Ma, Y., Bao, J., Zhao, X., Shen, H., Lv, J., Ma, S., Zhang, X., Li, Z., Wang, S., Wang, Q., et al. (2013) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m112.026864 · Cited by 60
Serum lipoprotein lipase mass: Clinical significance of its measurement
Kobayashi, J., Nohara, A., Kawashiri, M.-A., Inazu, A., Koizumi, J., Nakajima, K., & Mabuchi, H. (2007) · Clinica Chimica Acta · doi:10.1016/j.cca.2006.12.003 · Cited by 35
Dominant expression of type III hyperlipoproteinemia. Pathophysiological insights derived from the structural and kinetic characteristics of ApoE-1 (Lys146-->Glu).
Mann, W. A., Lohse, P., Gregg, R. E., Ronan, R., Hoeg, J. M., Zech, L. A., & Brewer, H. B. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118096 · Cited by 28

Authors: Williams, K. J., Fless, G. M., Petrie, K. A., Snyder, M. L., Brocia, R. W., & Swenson, T. L.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 1992-07
Volume: 267
Issue: 19
Pages: 13284-13292
ISSN: 0021-9258
DOI: 10.1016/s0021-9258(18)42208-9
Cited by: 205
References: 0
Language: en
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 10332 d)

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

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.

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Metadata

Record

About these checks