Effect of repeated apoA -IMilano/POPC infusion on lipids, (apo)lipoproteins, and serum cholesterol efflux capacity in cynomolgus monkeys

Journal of Lipid Research

Volumn 54, Issue 9, 2013, Pages 2341-2353

  Kempen, Herman J ^a   Gomaraschi, Monica ^b   Bellibas, S Eralp ^c   Plassmann, Stephanie ^d   Zerler, Brad ^c   Collins, Heidi L ^e   Adelman, Steven J ^e   Calabresi, Laura ^b   Wijngaard, Peter L J ^a  

^a Medicines Company (Schweiz) GmbH   (Switzerland)

^b UNIVERSITY OF MILAN   (Italy)

^c MEDICINES COMPANY   (United States)

^d PCS Consultants   (Switzerland)

^e Vascular Strategies LLC   (United States)

Author keywords

ABCA1 mediated cholesterol efflux; Palmitoyl oleoyl phosphatidylcholine

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; ANTILIPEMIC AGENT; APOLIPOPROTEIN; APOLIPOPROTEIN A1; APOLIPOPROTEIN A1 MILANO; APOLIPOPROTEIN A2; CHOLESTEROL; GLYCEROPHOSPHOLIPID; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MDCO 216; OLEOYLPALMITOYLLECITHIN; PHOSPHOLIPID; RECOMBINANT PROTEIN; SCAVENGER RECEPTOR BI; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL ESTERIFICATION; CHOLESTEROL TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG INFUSION; DRUG MECHANISM; DRUG SAFETY; DRUG TOLERABILITY; EX VIVO STUDY; FEMALE; LIPID BLOOD LEVEL; LIPOPROTEIN BLOOD LEVEL; MACACA FASCICULARIS; MALE; NONHUMAN; PHOSPHOLIPID BLOOD LEVEL; PRIORITY JOURNAL; TOXICITY TESTING; TREATMENT DURATION;

ABCA1-MEDIATED CHOLESTEROL EFFLUX; PALMITOYL-OLEOYL-PHOSPHATIDYLCHOLINE;

ANIMALS; APOLIPOPROTEINS A; APOLIPOPROTEINS E; BIOLOGICAL TRANSPORT; CHOLESTEROL; ESTERIFICATION; FEMALE; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; MACACA FASCICULARIS; MALE; PHOSPHATIDYLCHOLINES; RECOMBINANT FUSION PROTEINS; TIME FACTORS;

EID: 84883197917     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M033779     Document Type: Article

References (61)

1. Gordon, T., W. P. Castelli, M. C. Hjortland, W. B. Kannel, and T. R. Dawber. 1977. High density lipoprotein as a protective factor against coronary heart disease. Am. J. Med. 62: 707-714.
2. Rifkind, B. M. 1990. High-density lipoprotein cholesterol and coronary artery disease: survey of the evidence. Am. J. Cardiol. 66: 3A-6A.
3. Wilson, P. W. F. 1990. High-density lipoprotein, low density lipoprotein and coronary artery disease. Am. J. Cardiol. 66: 7A-10A.
4. Glomset, J. A. 1968. The plasma lecithin:cholesterol acyltransferase reaction. J. Lipid Res. 9: 155-167.
5. Tall, A. R. 1990. Plasma high density lipoproteins: metabolism and relationship to atherogenesis. J. Clin. Invest. 86: 379-384.
6. Acton, S., A. Rigotti, K. T. Landschulz, S. Xu, H. H. Hobbs, and M. Krieger. 1996. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 271: 518-520.
7. Palgunachari, M. N., V. K. Mishra, S. Lund-Katz, M. C. Phillips, S. O. Adeyeye, S. Alluri, G. M. Anantharamaiah, and J. P. Segrest. 1996. Only the two ends of eight tandem amphipathic helical domains of human apoA-I have significant lipid affinity: implications for HDL assembly. Arterioscler. Thromb. Vasc. Biol. 16: 328-338.
8. Banka, C. L., D. J. Bonnet, A. S. Black, R. S. Smith, and L. K. Curtiss. 1991. Localization of an apolipoprotein A-I epitope critical for activation of lecithin-cholesterol acyltransferase. J. Biol. Chem. 266: 23886-23892.
9. Rothblat, G. H., F. H. Mahlberg, W. J. Johnson, and M. C. Phillips. 1992. Apolipoproteins, membrane cholesterol domains, and the regulation of cholesterol efflux. J. Lipid Res. 33: 1091-1097.
10. Sirtori, C. R., L. Calabresi, G. Franceschini, D. Baldassarre, M. Amato, J. Johansson, M. Salvetti, C. Monteduro, R. Zulli, M. L. Muiesan, et al. 2001. Cardiovascular status of carriers of the apolipoprotein a-i(milano) mutant: The Limone sul Garda study. Circulation. 103: 1949-1954.
11. Weisgraber, K. H., T. P. Bersot, R. W. Mahley, G. Franceschini, and C. R. Sirtori. 1980. A-IMilano apoprotein: isolation and characterization of a cysteine-containing variant of the A-I apoprotein from human high density lipoproteins. J. Clin. Invest. 66: 901-907.
12. Weisgraber, K. H., S. C. Rall, Jr., T. P. Bersot, R. W. Mahley, G. Franceschini, and C. R. Sirtori. 1983. Apolipoprotein A-IMilano: detection of normal apoA-I in affected subjects and evidence for a cysteine for arginine substitution in the variant A-I. J. Biol. Chem. 258: 2508-2513.
13. Franceschini, G., T. G. Frosi, C. Manzoni, G. Gianfranceschi, and C. R. Sirtori. 1982. High density lipoprotein-3 heterogeneity in subjects with the apoA-IMilano variant. J. Biol. Chem. 257: 9926-9930.
14. Franceschini, G., L. Calabresi, C. Tosi, G. Gianfranceschi, C. R. Sirtori, and A. V. Nichols. 1990. Apolipoprotein A-IMilano: disulfide-linked dimers increase high density lipoprotein stability and hinder particle interconversion in carrier plasma. J. Biol. Chem. 265: 12224-12231.
15. Calabresi, L., G. Vecchio, R. Longhi, E. Gianazza, G. Palm, H. Wadensten, A. Hammarstrom, A. Olsson, A. Karlstrom, T. Sejlitz, et al. 1994. Molecular characterization of native and recombinant apolipoprotein A-IMilano dimers: the introduction of an interchain disulfide bridge remarkably alters the physicochemical properties of apolipoprotein A-I. J. Biol. Chem. 269: 32168-32174.
16. Ameli, S., A. Hultgardh-Nilsson, B. Cercek, P. K. Shah, J. S. Forrester, H. Ageland, and J. Nilsson. 1994. Recombinant apolipoprotein A-I Milano reduces intimal thickening after balloon injury in hypercholesterolemic rabbits. Circulation. 90: 1935-1941.
17. Shah, P. K., J. Nilsson, S. Kaul, M. C. Fishbein, H. Ageland, A. Hamsten, J. Johansson, F. Karpe, and B. Cercek. 1998. Effects of recombinant apolipoprotein A-I(Milano) on aortic atherosclerosis in apolipoprotein E-deficient mice. Circulation. 97: 780-785.
18. Chiesa, G., E. Monteggia, M. Marchesi, P. Lorenzon, M. Laucello, V. Lorusso, C. Di Mario, E. Karvouni, R. S. Newton, C. L. Bisgaier, et al. 2002. Recombionant apolipoprotein A-IMilano infusion into rabbit carotid artery rapidly removes lipid from fatty streaks. Circ. Res. 90: 974-980.
19. Parolini, C., M. Marchesi, P. Lorenzon, M. Castano, E. Balconi, L. Miragoli, L. Chaabane, A. Morisetti, V. Lorusso, B. J. Martin, et al. 2008. Dose-related effects of repeated ETC-216 (recombinant apolipoprotein A-I Milano/1-palmitoyl-2-oleoyl phosphatidylcholine complexes) administrations on rabbit lipid-rich soft plaques: in vivo assessment by intravascular ultrasound and magnetic resonance imaging. J. Am. Coll. Cardiol. 51: 1098-1103.
20. Ibanez, B., G. Vilahur, G. Cimmino, W. S. Speidl, A. Pinero, B. G. Choi, M. U. Zafar, C. G. Santos-Gallego, B. Krause, L. Badimon, et al. 2008. Rapid change in plaque size, composition, and molecular footprint after recombinant apolipoprotein A-I Milano (ETC-216) administration: magnetic resonance imaging study in an experimental model of atherosclerosis. J. Am. Coll. Cardiol. 51: 1104-1109.
21. Nissen, S. E., T. Tsunoda, E. M. Tuzcu, P. Schoenhagen, C. J. Cooper, M. Yasin, G. M. Eaton, M. A. Lauer, W. S. Sheldon, C. L. Grines, et al. 2003. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes. A randomized controlled trial. JAMA. 290: 2292-2300.
22. Caparon, M. H., K. J. Rust, A. K. Hunter, J. K. McLaughlin, K. E. Thomas, J. T. Herberg, R. E. Shell, P. B. Lanter, B. F. Bishop, R. L. Dufield, et al. 2010. Integrated solution to purification challenges in the manufacture of a soluble recombinant protein in E. coli. Biotechnol. Bioeng. 105: 239-249.
23. Mweva, S., J. L. Paul, M. Cambillau, D. Goudouneche, P. Beaune, A. Simon, and N. Fournier. 2006. Comparison of different cellular models measuring in vitro the whole human serum cholesterol efflux capacity. Eur. J. Clin. Invest. 36: 552-559.
24. de la Llera-Moya, M., D. Drazul-Schrader, B. F. Asztalos, M. Cuchel, D. J. Rader, and G. H. Rothblat. 2010. The ability to promote efflux via ABCA1 determines the capacity of serum specimens with similar high-density lipoprotein cholesterol to remove cholesterol from macrophages. Arterioscler. Thromb. Vasc. Biol. 30: 796-801.
25. Sankaranarayanan, S., J. F. Oram, B. F. Asztalos, A. M. Vaughan, S. Lund-Katz, M. P. Adorni, M. C. Phillips, and G. H. Rothblat. 2009. Effects of acceptor composition and mechanism of ABCG1-mediated cellular free cholesterol efflux. J. Lipid Res. 50: 275-284.
26. Franceschini, G., M. Baio, L. Calabresi, C. R. Sirtori, and M. C. Cheung. 1990. Apolipoprotein AIMilano. Partial lecithin:cholesterol acyltransferase deficiency due to low levels of a functional enzyme. Biochim. Biophys. Acta. 1043: 1-6.
27. Franceschini, G., C. R. Sirtori, E. Bosisio, V. Gualandri, G. B. Orsini, A. M. Mogavero, and A. Capurso. 1985. Relationship of the phenotypic expression of the A-IMilano apoprotein with plasma lipid and lipoprotein patterns. Atherosclerosis. 58: 159-174.
28. Bielicki, J. K., T. M. Forte, M. McCall, L. J. Stoltzfus, G. Chiesa, C. R. Sirtori, G. Franceschini, and E. M. Rubin. 1997. High density lipoprotein particle size restriction in apolipoprotein A-I(Milano) transgenic mice. J. Lipid Res. 38: 2314-2321.
29. Calabresi, L., G. Franceschini, A. Burkybile, and A. Jonas. 1997. Activation of lecithin cholesterol acyltransferase by a disulfidelinked apolipoprotein A-I dimer. Biochem. Biophys. Res. Commun. 232: 345-349.
30. Cole, T. G., W. L. Nowatzke, C. L. Bisgaier, and B. Krause. 2002. Method-dependent changes in "HDL-cholesterol" with recombinant apolipoprotein A-I(Milano) infusion in healthy volunteers. Clin. Chem. 48: 680-681.
31. Roma, P., R. E. Gregg, M. S. Meng, R. Ronan, L. A. Zech, G. Franceschini, C. R. Sirtori, and H. B. Brewer, Jr. 1993. In vivo metabolism of a mutant form of apolipoprotein A-I, apoA-IMilano, associated with familial hypoalphalipoproteinemia. J. Clin. Invest. 91: 1445-1452.
32. Rubin, E. M., B. Y. Ishida, S. Clift, and R. M. Krauss. 1991. Expression of human apolipoprotein A-I in transgenic mice results in reduced plasma levels of murine apolipoprotein A-I and the appearance of two new high density lipoprotein size subclasses. Proc. Natl. Acad. Sci. USA. 88: 434-438.
33. Kuivenhoven, J. A., H. Pritchard, J. Hill, J. Frohlich, G. Assmann, and J. Kastelein. 1997. The molecular pathology of lecithin:cholesterol acyltransferase (LCAT) deficiency syndromes. J. Lipid Res. 38: 191-205.
34. Chiesa, G., L. J. Stoltzfus, S. Michelangoli, J. K. Bielicki, M. Santi, T. M. Forte, C. R. Sirtori, G. Franceschini, and E. M. Rubin. 1998. Elevated triglycerides and low HDL cholesterol in transgenic mice expressing human apoA-I(Milano). Atherosclerosis. 136: 139-146.
35. Stone, B. G., D. Schreiber, L. D. Alleman, and C. Y. Ho. 1987. Hepatic metabolism and secretion of a cholesterol-enriched lipoprotein fraction. J. Lipid Res. 28: 162-172.
36. Wiersma, H., N. Nijstad, T. Gautier, J. Iqbal, F. Kuipers, M. M. Hussain, and U. Tietge. 2010. Scavenger receptor B1 facilitates hepatic very low density lipoprotein production in mice. J. Lipid Res. 51: 544-553.
37. Shah, P. K., J. Yano, O. Reyes, K. Y. Chyu, S. Kaul, C. L. Bisgaier, S. Drake, and B. Cercek. 2001. High-dose recombinant apolipoprotein A-I(Milano) mobilizes tissue cholesterol and rapidly reduces plaque lipid and macrophage content in apolipoprotein E-deficient mixce. Potential applications for acute plaque stabilization. Circulation. 103: 3047-3050.
38. Wang, Y., J. F. P. Berbee, E. S. Stroes, J. W. A. Smit, L. M. Havekes, J. A. Romijn, and P. C. N. Rensen. 2011. CETP expression reverses the reconstituted HDL-induced increase in VLDL. J. Lipid Res. 52: 1533-1541.
39. Patsch, J. R., K. C. Aune, A. M. Gotto, and J. D. Morrisett. 1977. Isolation, chemical characterization and biophysical properties of three different abnormal lipoproteins: LP-X 1, Lp-X 2 and LP-X 3. J. Biol. Chem. 252: 2113-2120.
40. Chen, Z., E. O'Neill, R. D. Meurer, K. Gagen, S. Luell, S-P. Wang, M. Ichetovkin, B. Franz-Wattley, S. Eveland, A. M. Strack, et al. 2012. Reconstituted HDL elicits marked changes in plasma lipids following single-dose injection in C57Bl/6 Mice. J. Cardiovasc. Pharmacol. Ther. 17: 315-323.
41. Carballo-Jane, E., Z. Chen, E. O'Neill, J. Wang, C. Burton, C. H. Chang, X. Chen, S. Eeveland, B. Frantz-Wattley, K. Gagen, et al. 2010. ApoA-I mimetic peptides promote pre- - HDL formation in vivo causing remodeling of HDL and triglyceride accumulation at higher dose. Bioorg. Med. Chem. 18: 8669-8678.
42. Bielicki, J. K., M. R. McCall, and T. M. Forte. 1999. Apolipoprotein A-I promotes cholesterol release and apolipoprotein E recruitment from THP-1 macrophage-like foam cells. J. Lipid Res. 40: 85-92.
43. Kockx, M., K. A. Rye, K. Gaus, C. M. Quinn, J. Wright, T. Sloane, D. Sviridov, Y. Fu, D. Sullivan, J. R. Burnett, et al. 2004. Apolipoprotein A-I stimulated apolipoprotein E secretion from human macrophages is independent of cholesterol efllux. J. Biol. Chem. 279: 25966-25977.
44. Farkas, M. H., L. L. Swift, A. H. Hasty, M. F. Linton, and S. Fazio. 2003. The recycling of apolipoprotein E in primary cultures of mouse hepatocytes. Evidence for a physiologic connection to high density lipoprotein metabolism. J. Biol. Chem. 278: 9412-9417.
45. Bencharif, K., L. Hoareau, R. K. Murumalla, E. Tarnus, F. Tallet, R. G. Glerc, C. Gardes, M. Cesari, and R. Roche. 2010. Effect of apoA-I on cholesterol release and apoE secretion in human mature adipocytes. Lipids Health Dis. 9: 75-84.
46. Huang, Z. H., M. L. Fitzgerald, and T. Mazzone. 2006. Distinct cellular loci for the ABCA1-dependent and ABCA1-independent lipid efflux mediated by endogenous apolipoprtein E expression. Arterioscler. Thromb. Vasc. Biol. 26: 157-162.
47. Zannis, V. I., G. Koukos, K. Drosatos, A. Vezeridis, E. E. Zanni, K. E. Kypreos, and A. Chroni. 2008. Discrete roles of apoA-I and apoE in the biogenesis of HDL species: lessons learned from gene transfer studies in different mouse models. Ann. Med. 40: 14-28.
48. Favari, E., L. Calabresi, M. P. Adorni, W. Jessup, S. Simonelli, G. Franceschini, and F. Bernini. 2009. Small discoidal pre-beta1 HDL particles are efficient acceptors of cell cholesterol via ABCA1 and ABCG1. Biochemistry. 48: 11067-11074.
49. Favari, E., M. Gomaraschi, I. Zanotti, F. Bernini, M. Lee-Rueckert, P. T. Kovanen, C. R. Sirtori, G. Franceschini, and L. Calabresi. 2007. A unique protease-sensitive high-density lipoprotein particle containing the apolipoprotein A-I(Milano) dimer effectively promotes ATP-binding cassette A1-mediated cell cholesterol efflux. J. Biol. Chem. 282: 5125-5132.
50. Weibel, G. L., E. T. Alexander, M. R. Joshi, D. J. Rader, S. Lund-Katz, M. C. Phillips, and G. H. Rothblat. 2007. Wild-type apoA-I and the Milano variant have similar abilities to stimulate cellular lipid mobilization and efflux. Arterioscler. Thromb. Vasc. Biol. 27: 2022-2029.
51. Liadaki, K. N., T. Liu, S. Xu, B. Y. Ishida, P. N. Duchateaux, J. P. Krieger, J. Kane, M. Krieger, and V. I. Zannis. 2000. Binding of high density lipoprotein (HDL) and discoidal reconstituted HDL to the HDL receptor scavenger receptor class B type I. Effect of lipid association and apo-A-I mutations on receptor binding. J. Biol. Chem. 275: 21262-21271.
52. Liu, T., M. Krieger, H. Y. Kan, and V. I. Zannis. 2002. The effects of mutations in helices 4 and 6 of apoA-I on scavenger receptor class B type I (SR-BI)-mediated cholesterol efflux suggest that formation of a productive complex between reconstituted high density lipoprotein is required for efficient lipid transport. J. Biol. Chem. 277: 21576-21584.
53. Wang, X., H. L. Collins, M. Ranalletta, I. V. Fuki, J. T. Billheimer, G. H. Rothblat, A. R. Tall, and D. J. Rader. 2007. Macrophage ABCA1 and ABCG1, but not SR-B1, promote macrophage reverse cholesterol transport in vivo. J. Clin. Invest. 117: 2216-2224.
54. Cuchel, M., S. Lund-Katz, M. de la Llera-Moya, J. S. Millar, D. Chang, I. Fuki, G. H. Rothblat, M. C. Phillips, and D. J. Rader. 2010. Pathways by which reconstituted high-density lipoprotein mobilizes free cholesterol from whole body and from macrophages. Arterioscler. Thromb. Vasc. Biol. 30: 526-532.
55. Out, R., M. Hoekstra, R. B. Hildebrand, J. K. Kruit, I. Meurs, Z. Li, F. Kuipers, T. J. Van Berkel, and M. Van Eck. 2006. Macrophage ABC-G1 deletion disrupts lipid homeostasis in lung alveolar macrophages and moderately influences atherosclerotic lesions development in LDL-receptor deficient mice. Arterioscler. Thromb. Vasc. Biol. 26: 2295-2300.
56. Out, R., M. Hoekstra, K. Habets, I. Meurs, V. de Waard, R. B. Hildebrand, Y. Wang, G. Chimini, J. Kuiper, T. J. Van Berkel, et al. 2008. Combined deletion of macrophage ABC-A1 and ABCG1 leads to massive lipid accumulation in tissue macrophages and distinct atherosclerosis at relatively low plasma cholesterol levels. Arterioscler. Thromb. Vasc. Biol. 28: 258-264.
57. Vaughan, A. M., and J. F. Oram. 2006. ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J. Lipid Res. 47: 2433-2443.
58. Adorni, M. P., F. Zimetti, J. T. Billheimer, N. Wang, D. J. Rader, M. C. Phillips, and G. H. Rothblat. 2007. The roles of different pathways in the release of cholesterol from macrophages. J. Lipid Res. 48: 2453-2462.
59. Rodrigueza, W. V., K. J. Williams, G. H. Rothblat, and M. C. Phillips. 1997. Remodeling and shuttling. Mechanisms for the synergistic effects between different acceptor particlles in the mobilization of cellular cholesterol. Arterioscler. Thromb. Vasc. Biol. 17: 383-393.
60. Hoang, A., B. G. Drew, H. Low, A. T. Remaley, P. Nestel, B. A. Kindwell, and D. Sviridov. 2012. Mechanism of cholesterol efflux in humans after infusion of reconstituted high-density lipoprotein. Eur. Heart J. 33: 657-665.
61. Bagdade, J. D., J. D. Wagner, L. L. Rudel, and T. B. Clarkson. 1995. Accelerated cholesteryl ester transfer and altered lipoprotein composition in diabetic cynomolgus monkeys. J. Lipid Res. 36: 759-766.