Recycling of apolipoprotein(a) after PlgRKT-mediated endocytosis of lipoprotein(a)

Circulation Research

Volumn 120, Issue 7, 2017, Pages 1091-1102

  Sharma, Monika ^a   Redpath, Gregory M ^a   Williams, Michael J A ^b   McCormick, Sally P A ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

lipoprotein(a); liver; plasminogen receptor; recycling endosomes

Indexed keywords

APOLIPOPROTEIN A; ASIALOGLYCOPROTEIN RECEPTOR; LIPOPROTEIN A; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PLASMINOGEN; PLASMINOGEN RECEPTOR KT; PROTEASOME; PROTEIN ANTIBODY; RAB PROTEIN; RAB11 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; PLGRKT PROTEIN, HUMAN;

ARTICLE; CELL CYCLE; CELL FATE; CELL LYSATE; CELL MIGRATION; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FIBROBLAST CULTURE; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HEP-G2 CELL LINE; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INTERNALIZATION; INTRACELLULAR SIGNALING; INTRACELLULAR SPACE; LIPOPROTEIN SECRETION; LYSOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANS GOLGI NETWORK; WESTERN BLOTTING; METABOLISM;

APOLIPOPROTEINS A; ENDOCYTOSIS; ENDOSOMES; HEP G2 CELLS; HUMANS; LYSOSOMES; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE;

EID: 85007476918     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.310272     Document Type: Article

References (49)

1. Nordestgaard BG, Chapman MJ, Ray K, European Atherosclerosis Society Consensus Panel Lipoprotein(a) as a cardiovascular risk factor: current status. Eur Heart J 2010 31 2844 2853. doi: 10.1093/eurheartj/ehq386.
2. Utermann G, The mysteries of lipoprotein(a). Science 1989 246 904 910
3. McLean JW, Tomlinson JE, Kuang WJ, Eaton DL, Chen EY, Fless GM, Scanu AM, Lawn RM, cDNA sequence of human apolipoprotein(a) is homologous to plasminogen. Nature 1987 330 132 137. doi: 10.1038/330132a0.
4. Donate LE, Gherardi E, Srinivasan N, Sowdhamini R, Aparicio S, Blundell TL, Molecular evolution and domain structure of plasminogen-related growth factors (HGF/SF and HGF1/MSP). Protein Sci 1994 3 2378 2394. doi: 10.1002/pro.5560031222.
5. Dieplinger H, Utermann G, The seventh myth of lipoprotein(a): where and how is it assembled? Curr Opin Lipidol 1999 10 275 283
6. Bonen DK, Nassir F, Hausman AM, Davidson NO, Inhibition of N-linked glycosylation results in retention of intracellular apo[a] in hepatoma cells, although nonglycosylated and immature forms of apolipoprotein[a] are competent to associate with apolipoprotein B-100 in vitro. J Lipid Res 1998 39 1629 1640
7. Frischmann ME, Ikewaki K, Trenkwalder E, Lamina C, Dieplinger B, Soufi M, Schweer H, Schaefer JR, König P, Kronenberg F, Dieplinger H, In vivo stable-isotope kinetic study suggests intracellular assembly of lipoprotein(a). Atherosclerosis 2012 225 322 327. doi: 10.1016/j.atherosclerosis.2012.09.031.
8. Rader DJ, Cain W, Ikewaki K, Talley G, Zech LA, Usher D, Brewer HB Jr, The inverse association of plasma lipoprotein(a) concentrations with apolipoprotein(a) isoform size is not due to differences in Lp(a) catabolism but to differences in production rate. J Clin Invest 1994 93 2758 2763. doi: 10.1172/JCI117292.
9. Cain WJ, Millar JS, Himebauch AS, Tietge UJ, Maugeais C, Usher D, Rader DJ, Lipoprotein [a] is cleared from the plasma primarily by the liver in a process mediated by apolipoprotein [a]. J Lipid Res 2005 46 2681 2691. doi: 10.1194/jlr.M500249-JLR200.
10. Yang XP, Amar MJ, Vaisman B, Bocharov AV, Vishnyakova TG, Freeman LA, Kurlander RJ, Patterson AP, Becker LC, Remaley AT, Scavenger receptor-BI is a receptor for lipoprotein(a). J Lipid Res 2013 54 2450 2457. doi: 10.1194/jlr.M038877.
11. Sharma M, Von Zychlinski-Kleffmann A, Porteous CM, Jones GT, Williams MJ, McCormick SP, Lipoprotein (a) upregulates ABCA1 in liver cells via scavenger receptor-B1 through its oxidized phospholipids. J Lipid Res 2015 56 1318 1328. doi: 10.1194/jlr.M056150.
12. Krempler F, Kostner GM, Roscher A, Haslauer F, Bolzano K, Sandhofer F, Studies on the role of specific cell surface receptors in the removal of lipoprotein (a) in man. J Clin Invest 1983 71 1431 1441
13. Lingenhel A, Kraft HG, Kotze M, Peeters AV, Kronenberg F, Kruse R, Utermann G, Concentrations of the atherogenic Lp(a) are elevated in FH. Eur J Hum Genet 1998 6 50 60. doi: 10.1038/sj.ejhg.5200152.
14. Raal FJ, Giugliano RP, Sabatine MS, Koren MJ, Langslet G, Bays H, Blom D, Eriksson M, Dent R, Wasserman SM, Huang F, Xue A, Albizem M, Scott R, Stein EA, Reduction in lipoprotein(a) with PCSK9 monoclonal antibody evolocumab (AMG 145): a pooled analysis of more than 1,300 patients in 4 phase II trials. J Am Coll Cardiol 2014 63 1278 1288. doi: 10.1016/j.jacc.2014.01.006.
15. Gaudet D, Kereiakes DJ, McKenney JM, Roth EM, Hanotin C, Gipe D, Du Y, Ferrand AC, Ginsberg HN, Stein EA, Effect of alirocumab, a monoclonal proprotein convertase subtilisin/kexin 9 antibody, on lipoprotein(a) concentrations (a pooled analysis of 150 mg every two weeks dosing from phase 2 trials). Am J Cardiol 2014 114 711 715. doi: 10.1016/j.amjcard.2014.05.060.
16. Romagnuolo R, Scipione CA, Boffa MB, Marcovina SM, Seidah NG, Koschinsky ML, Lipoprotein(a) catabolism is regulated by proprotein convertase subtilisin/kexin type 9 through the low density lipoprotein receptor. J Biol Chem 2015 290 11649 11662. doi: 10.1074/jbc.M114.611988.
17. Knight BL, Perombelon YF, Soutar AK, Wade DP, Seed M, Catabolism of lipoprotein(a) in familial hypercholesterolaemic subjects. Atherosclerosis 1991 87 227 237
18. Carmena R, Lussier-Cacan S, Roy M, Minnich A, Lingenhel A, Kronenberg F, Davignon J, Lp(a) levels and atherosclerotic vascular disease in a sample of patients with familial hypercholesterolemia sharing the same gene defect. Arterioscler Thromb Vasc Biol 1996 16 129 136
19. Reblin T, Niemeier A, Meyer N, Willnow TE, Kronenberg F, Dieplinger H, Greten H, Beisiegel U, Cellular uptake of lipoprotein[a] by mouse embryonic fibroblasts via the LDL receptor and the LDL receptor-related protein. J Lipid Res 1997 38 2103 2110
20. Pedersen TR, Kjekshus J, Berg K, Haghfelt T, Faergeman O, Faergeman G, Pyörälä K, Miettinen T, Wilhelmsen L, Olsson AG, Wedel H, Scandinavian Simvastatin Survival Study Group Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). 1994. Atheroscler Suppl 2004 5 81 87. doi: 10.1016/j.atherosclerosissup.2004.08.027.
21. Khera AV, Everett BM, Caulfield MP, Hantash FM, Wohlgemuth J, Ridker PM, Mora S, Lipoprotein(a) concentrations, rosuvastatin therapy, and residual vascular risk: an analysis from the JUPITER Trial (Justification for the Use of Statins in Prevention: an Intervention Trial Evaluating Rosuvastatin). Circulation 2014 129 635 642. doi: 10.1161/CIRCULATIONAHA.113.004406.
22. Argraves KM, Kozarsky KF, Fallon JT, Harpel PC, Strickland DK, The atherogenic lipoprotein Lp(a) is internalized and degraded in a process mediated by the VLDL receptor. J Clin Invest 1997 100 2170 2181. doi: 10.1172/JCI119753.
23. Niemeier A, Willnow T, Dieplinger H, Jacobsen C, Meyer N, Hilpert J, Beisiegel U, Identification of megalin/gp330 as a receptor for lipoprotein(a) in vitro. Arterioscler Thromb Vasc Biol 1999 19 552 561
24. Hrzenjak A, Frank S, Wo X, Zhou Y, Van Berkel T, Kostner GM, Galactose-specific asialoglycoprotein receptor is involved in lipoprotein (a) catabolism. Biochem J 2003 376 765 771. doi: 10.1042/BJ20030932.
25. Miles LA, Fless GM, Scanu AM, Baynham P, Sebald MT, Skocir P, Curtiss LK, Levin EG, Hoover-Plow JL, Plow EF, Interaction of Lp(a) with plasminogen binding sites on cells. Thromb Haemost 1995 73 458 465
26. Kang C, Durlach V, Soulat T, Fournier C, Anglés-Cano E, Lipoprotein(a) isoforms display differences in affinity for plasminogen-like binding to human mononuclear cells. Arterioscler Thromb Vasc Biol 1997 17 2036 2043
27. Tam SP, Zhang X, Koschinsky ML, Interaction of a recombinant form of apolipoprotein[a] with human fibroblasts and with the human hepatoma cell line HepG2. J Lipid Res 1996 37 518 533
28. Plow EF, Doeuvre L, Das R, So many plasminogen receptors: why? J Biomed Biotechnol 2012 2012 141806. doi: 10.1155/2012/141806.
29. Marcovina SM, Albers JJ, Gabel B, Koschinsky ML, Gaur VP, Effect of the number of apolipoprotein(a) kringle 4 domains on immunochemical measurements of lipoprotein(a). Clin Chem 1995 41 246 255
30. Brown MS, Goldstein JL, A receptor-mediated pathway for cholesterol homeostasis. Science 1986 232 34 47
31. Pease RJ, Milne RW, Jessup WK, Law A, Provost P, Fruchart JC, Dean RT, Marcel YL, Scott J, Use of bacterial expression cloning to localize the epitopes for a series of monoclonal antibodies against apolipoprotein B100. J Biol Chem 1990 265 553 568
32. Kirkland PA, Reuter CJ, Maupin-Furlow JA, Effect of proteasome inhibitor clasto-lactacystin-beta-lactone on the proteome of the haloarchaeon Haloferax volcanii. Microbiology 2007 153 2271 2280. doi: 10.1099/mic.0.2007/005769-0.
33. Wood SA, Park JE, Brown WJ, Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 1991 67 591 600
34. Stoorvogel W, Geuze HJ, Griffith JM, Strous GJ, The pathways of endocytosed transferrin and secretory protein are connected in the trans-Golgi reticulum. J Cell Biol 1988 106 1821 1829
35. Andronicos NM, Chen EI, Baik N, Bai H, Parmer CM, Kiosses WB, Kamps MP, Yates JR III, Parmer RJ, Miles LA, Proteomics-based discovery of a novel, structurally unique, and developmentally regulated plasminogen receptor, Plg-RKT, a major regulator of cell surface plasminogen activation. Blood 2010 115 1319 1330. doi: 10.1182/blood-2008-11-188938.
36. Villard EF, Thedrezy A, Blankenstein J, Croyaly M, Tran TT, Poirier B, Bail JL, Illiano S, Nobécourty S, Krempfy M, Blomx DJ, Maraisjj AD, Janiak P, Muslin AJ, Guillot E, Lambert G, PCSK9 modulates the secretion but not the cellular uptake of Lipoprotein (a) ex vivo: an effect blunted by alirocumab. JACC Basic Transl Sci 2016 1 419 427
37. White AL, Rainwater DL, Lanford RE, Intracellular maturation of apolipoprotein[a] and assembly of lipoprotein[a] in primary baboon hepatocytes. J Lipid Res 1993 34 509 517
38. Yang J, Chen H, Vlahov IR, Cheng JX, Low PS, Evaluation of disulfide reduction during receptor-mediated endocytosis by using FRET imaging. Proc Natl Acad Sci USA 2006 103 13872 13877. doi: 10.1073/pnas.0601455103.
39. Edelstein C, Pfaffinger D, Hinman J, Miller E, Lipkind G, Tsimikas S, Bergmark C, Getz GS, Witztum JL, Scanu AM, Lysine-phosphatidylcholine adducts in kringle V impart unique immunological and potential pro-inflammatory properties to human apolipoprotein(a). J Biol Chem 2003 278 52841 52847. doi: 10.1074/jbc.M310425200.
40. Rouy D, Koschinsky ML, Fleury V, Chapman J, Anglés-Cano E, Apolipoprotein(a) and plasminogen interactions with fibrin: a study with recombinant apolipoprotein(a) and isolated plasminogen fragments. Biochemistry 1992 31 6333 6339
41. von Zychlinski A, Kleffmann T, Williams MJ, McCormick SP, Proteomics of Lipoprotein(a) identifies a protein complement associated with response to wounding. J Proteomics 2011 74 2881 2891. doi: 10.1016/j.jprot.2011.07.008.
42. Hasty AH, Plummer MR, Weisgraber KH, Linton MF, Fazio S, Swift LL, The recycling of apolipoprotein E in macrophages: influence of HDL and apolipoprotein A-I. J Lipid Res 2005 46 1433 1439. doi: 10.1194/jlr.M400418-JLR200.
43. Fazio S, Linton MF, Swift LL, The cell biology and physiologic relevance of ApoE recycling. Trends Cardiovasc Med 2000 10 23 30
44. Jenner JL, Seman LJ, Millar JS, Lamon-Fava S, Welty FK, Dolnikowski GG, Marcovina SM, Lichtenstein AH, Barrett PH, deLuca C, Schaefer EJ, The metabolism of apolipoproteins (a) and B-100 within plasma lipoprotein (a) in human beings. Metabolism 2005 54 361 369. doi: 10.1016/j.metabol.2004.10.001.
45. Diffenderfer MR, Lamon-Fava S, Marcovina SM, Barrett PH, Lel J, Dolnikowski GG, Berglund L, Schaefer EJ, Distinct metabolism of apolipoproteins (a) and B-100 within plasma lipoprotein(a). Metabolism 2016 65 381 390. doi: 10.1016/j.metabol.2015.10.031.
46. Demant T, Seeberg K, Bedynek A, Seidel D, The metabolism of lipoprotein(a) and other apolipoprotein B-containing lipoproteins: a kinetic study in humans. Atherosclerosis 2001 157 325 339
47. Su W, Campos H, Judge H, Walsh BW, Sacks FM, Distinct metabolism of apolipoproteins (a) and B-100 within plasma lipoprotein(a). J Clin Endocrinol Metab 1998 83 3267 3276
48. Kostner KM, Maurer G, Huber K, Stefenelli T, Dieplinger H, Steyrer E, Kostner GM, Urinary excretion of apo(a) fragments. Role in apo(a) catabolism. Arterioscler Thromb Vasc Biol 1996 16 905 911
49. Tsimikas S, Viney NJ, Hughes SG, Singleton W, Graham MJ, Baker BF, Burkey JL, Yang Q, Marcovina SM, Geary RS, Crooke RM, Witztum JL, Antisense therapy targeting apolipoprotein(a): a randomised, double-blind, placebo-controlled phase 1 study. Lancet 2015 386 1472 1483. doi: 10.1016/S010-6736(15)61252-1.