Expression and recovery of biologically active recombinant Apolipoprotein AIMilano from transgenic safflower (Carthamus tinctorius) seeds

Plant Biotechnology Journal

Volumn 9, Issue 2, 2011, Pages 250-263

  Nykiforuk, Cory L ^a   Shen, Yin ^a   Murray, Elizabeth W ^a   Boothe, Joseph G ^a   Busseuil, David ^b   Rhéaume, Eric ^b   Tardif, Jean Claude ^b   Reid, Alexandra ^c   Moloney, Maurice M ^a  

^a SemBioSys Genetics Inc   (Canada)

^b MONTREAL HEART INSTITUTE   (Canada)

^c YORK UNIVERSITY   (Canada)

Author keywords

Apolipoprotein AIMilano; Atherosclerosis; Recombinant protein; Safflower

Indexed keywords

1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; APOLIPOPROTEIN A1; CHOLESTEROL; HYBRID PROTEIN; PHOSPHATIDYLCHOLINE;

ANIMAL; ARTICLE; BLOOD; C57BL MOUSE; GENETICS; LIPID METABOLISM; METABOLISM; MOUSE; PLANT SEED; SAFFLOWER; TRANSGENIC PLANT;

ANIMALS; APOLIPOPROTEIN A-I; CARTHAMUS TINCTORIUS; CHOLESTEROL; LIPID METABOLISM; MICE; MICE, INBRED C57BL; PHOSPHATIDYLCHOLINES; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; SEEDS;

CARTHAMUS TINCTORIUS;

EID: 78650956114     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2010.00546.x     Document Type: Article

References (65)

1. Abrahamsen, L., Holmgren, E., Kalderen, C., Lake, M., Mikaelsson, A. and Sejlitz, T. (1998) Expression system for producing Apolipoprotein AI-M. United States Patent 5, 721, 144.
2. Adorni, M.P., Zimetti, F., Billheimer, J.T., Wang, N., Rader, D.J., Phillips, M.C. and Rothblat, G.H. (2007) The roles of different pathways in the release of cholesterol from macrophages. J. Lipid Res., 48, 2453-2462.
3. Badimon, J.J., Badimon, L. and Fuster, V. (1990) Regression of atherosclerotic lesions by high density lipoprotein plasma fraction in the cholesterol-fed rabbit. J. Clin. Invest., 85, 1234-1241.
4. Barter, P.J. and Rye, K.A. (1996) Molecular mechanisms of reverse cholesterol transport. Curr. Opin. Lipidol., 7, 82-87.
5. Milano transgenic mice. J. Lipid Res., 38, 2314-2321.
6. Boothe, J., Nykiforuk, C., Shen, Y., Zaplachinski, S., Szarka, S., Kuhlman, P., Murray, E., Morck, D. and Moloney, M.M. (2010) Seed-based expression systems for plant molecular farming. Plant Biotechnol. J., 8, 588-606.
7. Busseuil, D., Shi, Y., Mecteau, M., Brand, G., Kernaleguen, A.-E., Thorin, E., Latour, J.-G., Rhéaume, E. and Tardif, J.-C. (2008) Regression of aortic valve stenosis by ApoA-I mimetic peptide infusions in rabbits. Br. J. Pharmacol., 154, 765-773.
8. Calabresi, L., Vecchio, G., Frigerio, F., Vavassori, L., Sirtori, C.R. and Franceschini, G. (1997) Reconstituted high-density lipoproteins with a disulfide-linked apolipoprotein A-I dimer: evidence for restricted particle size heterogeneity. Biochemistry., 36, 12428-12433.
9. Calabresi, L., Sirtori, C.R., Paoletti, R. and Franceschini, G. (2006) Recombinant apolipoprotein A-Imilano for the treatment of cardiovascular diseases. Curr. Atheroscler. Rep., 8, 163-167.
10. Castelli, W.P., Garrison, R.J., Wilson, P.W., Abbott, R.D., Kalousdian, S. and Kannel, W.B. (1986) Incidence of coronary heart disease and lipoprotein cholesterol levels. The Framingham Study. J. Am. Med. Assoc., 256, 2835-2838.
11. Cho, K.-H., Durbin, D.M. and Jonas, A. (2001) Role of individual amino acids of apolipoprotein A-I in the activation of lecithin:cholesterol acyltransferase and in HDL rearrangements. J. Lipid Res., 42, 379-389.
12. Davidson, W.S. and Thompson, T.B. (2007) The structure of Apolipoprotein A-I in high density lipoproteins. J. Biol. Chem., 31, 22249-22253.
13. Deckers, H., Moloney, M.M. and Baum, A. (1999) The case for recombinant production of pharmaceutical proteins in plants. Annu. Rep. Med. Chem., 34, 237-245.
14. Favari, E., Calabresi, L., Adorni, M.P., Jessup, W., Simonelli, S., Franceschini, G. and Bernini, F. (2009) Small discoidal Pre-β1 HDL particles are efficient acceptors of cell cholesterol via ABCA1 and ABCG1. Biochemistry, 48, 11067-11074.
15. Franceschini, G., Sirtori, C.R., Capurso, A., Weisgraber, K.H. and Mahley, R.W. (1980) Decreased high density lipoprotein cholesterol levels with significant lipoprotein modifications and without clinical atherosclerosis in an Italian family. J. Clin. Invest., 66, 892-899.
16. Franceschini, G., Maderna, P. and Sirtori, C.R. (1991) Reverse cholesterol transport: physiology and pharmacology. Atherosclerosis, 88, 99-107.
17. Gavel, P. and von Heijne, G. (1990) Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng., 3, 433-442.
18. Gordon, T., Castelli, W.P., Hjortland, M.C., Kannel, W.B. and Dawber, T.R. (1977) High density lipoprotein as a protective factor against coronary heart disease. The Framingham Study. Am. J. Med., 62, 707-714.
19. Ho, S.V., McLaughlin, J.K., Thomas, K.E., Suda, E., Herberg, J.T., Dufield, R.L. and Hunter, A.K. (2009) Reaction kinetics and optimization of the copper-catalyzed oxidation of ApoA-1M. Chem. Eng. Sci., 64, 2623-2630.
20. Hunter, A.K., Wang, X., Suda, E.J., Herberg, J.T., Shell, R.E., Thomas, K.E., Dufield, R.L., Gustafson, M.E., Mozier, N.M. and Ho, S.V. (2009) Separation of product associating E. coli host cell proteins OppA and DppA from recombinant Apolipoprotein A-Imilano in an industrial HIC unit operation. Biotechnol. Prog., 25, 446-457.
21. Ibanez, B., Vilajur, G., Cimmino, G., Speidl, W.S., Pinero, A., Choi, B.G., Zafar, M.U., Santos-Gallego, C.G., Krause, B., Badimon, L., Fuster, V. and Badimon, J.J. (2008) Rapid change in plaque size, composition, and molecular footprint after recombinant apolipoprotein A-I Milano (ETC.-216) administration: magnetic resonance imaging study ina an experimental model of atherosclerosis. J. Am. Coll. Cardiol., 51, 1104-1109.
22. Kannel, W.B., Neaton, J.D., Wnetworth, D., Thomas, H.E., Stramler, J., Hulley, S.B. and Kjelsberg, M.O. (1986) Overall and coronary heart disease mortality rates in relation to major risk factors in 325, 348 men screened for the MRFIT. Am. Heart J., 112, 825-836.
23. Milano reduces atherosclerosis in hypercholesterolemic Apolipoprotein E (-/-) mice. J. Am. Coll. Cardiol., 55, A50.
24. Li, M., Zhao, H.L., Xue, C., Zhang, W., Zhang, S.M. and Liu, Z.M. (2005) Soluble expression of recombinant human apolipoprotein A-I-Milano in Escherichia coli. Sheng Wu Gong Cheng Xue Bao, 21, 354-359.
25. Liu, A.C., Lawn, R.M., Verstuyft, J.G. and Rubin, E.M. (1994) Human apolipoprotein A-1 prevents atherosclerosis associated with apolipoprotein a in transgenic mice. J. Lipid Res., 35, 2263-2267.
26. Lorenzetti, R., Sidoli, A., Palomba, R., Monaco, L., Martineau, D., Lappi, D.A. and Soria, M. (1986) Expression of the human apolipoprotein AI gene fused to the E. coli gene for beta-galactosidase. FEBS Lett., 194, 343-346.
27. Ma, J.K., Drake, P.M.W. and Christou, P. (2003) The production of recombinant Pharmaceutical proteins in plants. Nat. Rev. Gen., 4, 794-805.
28. Mallory, J.B., Kushner, P.J., Protter, A.A., Cofer, C.L., Appleby, V.L., Lau, K., Schilling, J.W. and Vigne, J.L. (1987) Expression and characterization of human apolipoprotein A-I in Chinese hamster ovary cells. J. Biol. Chem., 262, 4241-4247.
29. Marchesi, M., Booth, E.A., Davis, T., Bisgaier, C.L. and Lucchesi, B.R. (2004) Apolipoprotein A-IMilano and 1-Palmitoyl-2-oleoyl Phosphatidylcholine Comples (ETC.-216) Protects the in Vivo Rabbit Heart from Regional Ischemia-Reperfusion Injury. J. Pharmacol. Exp. Ther., 311, 1023-1031.
30. Marchesi, M., Booth, E.A., Rossoni, G., Farcia, R.A., Hill, K.R., Sirtori, C.R., Bisgaier, C.L. and Lucchesi, B.R. (2008) Apolipoprotein A-IMilano/POPC complex attenuates post-isechemic ventricular dysfunction in the isolated rabbit heart. Atherosclerosis, 197, 572-578.
31. Markley, N., Nykiforuk, C., Boothe, J. and Moloney, M. (2006) Producing proteins using transgenic oilbody oleosin technology. BioPharm Int., 19, 34-47.
32. Miyazaki, A., Sakuma, S., Morikawa, W., Takiue, T., Miake, F., Terano, T., Sakai, M., Hakamata, H., Sakamoto, Y., Natio, M., Ruan, Y.M., Takahashi, K., Ohta, T. and Horiuchi, S. (1995) Intravenous injection of rabbit apolipoprotein A-1 inhibits the progression of atherosclerosis in cholesterol-fed rabbits. Arterioscler. Thromb. Vasc. Biol., 15, 1882-1888.
33. Moguilevsky, N., Roobol, C., Loriau, R., Guillaume, J.P., Jacobs, P., Cravador, A., Herzog, A., Brouwers, L., Scarso, A., Gilles, P., Holmquist, L., Carlson, L.A. and Bollen, A. (1989) Production of Human recombinant proapolipoprotein A-I in Escherichia coli: purification and biochemical characterization. DNA, 8, 429-436.
34. Monaco, L., Bond, H.M., Howell, K.E. and Cortese, R. (1987) A recombinant apoA-I-protein A hybrid reproduces the binding parameters of HDL to its receptor. EMBO J., 6, 3253-3260.
35. Nissen, S.E., Tsunoda, T., Tuzcu, E.M., Schoenhagen, P., Cooper, C.J., Yasin, M., Eaton, G.M., Lauer, M.A., Sheldon, W.S., Grines, C.L., Halpern, S., Crowe, T., Blankenship, J.C. and Kerensky, R. (2003) Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes. A randomized controlled trial. J. Am. Med. Assoc., 290, 2292-2300.
36. Nykiforuk, C.L., Boothe, J.G., Murray, E.W., Keon, R.G., Goren, H.J., Markley, N.A. and Moloney, M.M. (2006) Transgenic expression and recovery of biologically active recombinant human insulin from Arabidopsis thaliana seeds. Plant Biotechnol. J., 4, 77-85.
37. Parolini, C., Marchesi, M., Lorenzon, P., Castano, M., Balconi, E., Miragoli, L., Chaabane, L., Morisetti, A., Lorusso, V., Martin, B.J., Bisgaier, C.L., Krause, B., Newton, R.S., Sirtori, C.R. and Chisea, G. (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 intracascular ultrasound and magnetic resonance imaging. J. Am. Coll. Cardiol., 51, 1098-1103.
38. Paszty, C., Maeda, N., Verstuyft, J. and Rubin, E.M. (1994) Apolipoprotein A-1 transgene corrects apolipoprotein E deficiency-induced atherosclerosis in mice. J. Clin. Invest., 94, 899-903.
39. Pisano, A., Redmond, J.W., Williams, K.L. and Gooley, A.A. (1993) Glycosylation sites identified by solid-phase Edman degradation: O-linked glycosylation motifs on human glycophorin A. Glycobiology, 3, 429-435.
40. Pyle, L.E., Barton, P., Fujiwara, Y., Mitchell, A. and Fidge, N. (1995) Secretion of biologically active human proapolipoprotein A-I in a Baculovirus-insect cell system: protection from degradation by protease inhibitors. J. Lipid Res., 36, 2355-2361.
41. Pyle, L.E., Fidge, N.H., Barton, P.A., Luong, A. and Sviridov, D. (1997) Production of mature human apolipoprotein A-I in a baculovirus-insect cell system: propeptide is not essential for intracellular processing but may assist rapid secretion. Anal. Biochem., 253, 253-258.
42. Roosbeek, S., Vanloo, B., Duverger, N., Caster, H., Breyne, J., De Beun, I., Patel, H., Vandekerckhove, J., Shoulders, C., Rosseneu, M. and Peelman, F. (2001) Three arginine residues in apolipoprotein A-I are critical for activation of lecithin:cholesterol acyltransferase. J. Lipid Res., 42, 31-40.
43. Rothblat, G.H., de la Llera-Moya, M., Atger, V., Kellner-Weibel, G., Williams, D.L. and Phillips, M.C. (1999) Cell cholesterol efflux: integration of old and new observations provides new insights. J. Lipid Res., 40, 781-796.
44. Rubin, E.M., Krauss, R.M., Spangler, E.A., Verstuyft, J.G. and Clift, S.M. (1991) Inhibition of early atherogenesis in transgenic mice by human apolipoprotein A-1. Nature, 353, 265-267.
45. Ryan, R.O., Forte, T.M. and Oda, M.N. (2003) Optimized bacterial expression of human apolipoprotein A-I. Protein Expr. Purif., 27, 98-103.
46. Schmidt, H.H., Genschel, J., Haas, R., Buttner, C. and Manns, M.P. (1997) Expression and purification of recombinant human apolipoprotein A-I in Chinese hamster ovary cells. Protein Expr. Purif., 10, 226-236.
47. Seon, J.H., Szarka, S.J. and Moloney, M.M. (2002) A unique strategy for recovering recombinant proteins from molecular farming in affinity capture on engineered oilbodies. J. Plant Biotechnol., 4, 95-101.
48. Shah, P.K., Nilsson, J., Kaul, S., Fishbein, M.C., Ageland, H., Hamsten, A., Johansson, J., Karpe, F. and Cercek, B. (1998) Effects of recombinant Apolipoprotein A-IMilano on aortic atherosclerosis in Apolipoprotein E-deficient mice. Circulation, 97, 780-785.
49. Shah, P.K., Kaul, S., Nilsson, J. and Cercek, B. (2001a) Exploiting the vascular protective effects of high-density lipoprotein and its apolipoproteins: an idea whose time for testing is coming, Part I. Circulation, 104, 2376-2383.
50. Shah, P.K., Yano, J., Reyes, O., Chyu, K.Y., Kaul, S., Bisgaier, C.L., Drake, S. and Cercek, B. (2001b) High-dose recombinant apolipoprotein A-I(milano) mobilizes tissue cholesterol and rapidly reduces plaque lipid and macrophage content in apolipoprotein e-deficient mice. Potential implications for acute plaque stabilization. Circulation, 103, 3047-3050.
51. Sidoli, A., Baralle, F., Sirtori, C. and Franceschini, G. (1994) Expression of Human apolipoproteins AI-Milano in yeast. European Patent Specification Number 0 469 017 B1.
52. Sirtori, C., Franceschini, G., Abrahmsen, L., Holmgren, E., Lake, M., Bilsoson, B., Chmielewska, J. and Lind, P. (2003) Dimer of molecular variant of Apolipoprotein and processes for the production thereof. United States Patent 6, 617, 134 B1.
53. Slightom, J.L., Sun, S.M. and Hall, T.C. (1983) Complete nucleotide sequence of a French bean storage protein gene: phaseolin. Proc. Natl Acad. Sci. USA, 80, 1897-1901.
54. Sorci-Thomas, M.G., Curtiss, L., Parks, J.S., Thomas, M.J., Kearns, M.W. and Landrum, M. (1998) The hydrophobic face orientation of apolipoprotein A-I amphipathic helix domain 143-164 regulates lecithin:cholesterol acyltransferase activation. J. Biol. Chem., 273, 11776-11782.
55. Sourrouille, C., Marchall, B., Liénard, D. and Faye, L. (2008) From Neanderthal to Nanobiotech: from plant potions to pharming with plant factories. Methods Mol. Biol. Recomb. Prot. Plants, 483, 1-23.
56. Spady, D.K. (1999) Reverse cholesterol transport and atherosclerosis regression. Circulation, 100, 576-578.
57. Stein, O. and Stein, Y. (1999) Atheroprotective mechanisms of HDL. Atherosclerosis, 144, 285-301.
58. Sviridov, D., Luong, A., Pyle, L. and Fidge, N. (1999) Effectivity of expression of mature forms of mutant human Apolipoprotein A-I. Protein Expr. Purif., 17, 231-238.
59. Sviridov, D., Pyle, L.E., Jauhiainen, M., Ehnholm, C. and Fidge, N.H. (2000) Deletion of the propeptide of paolipoprotein A-1 reduces protein expression but stimulates effective conversion of preβ-high density lipoprotein to α-high density lipoprotein. J. Lipid Res., 41, 1872-1882.
60. Twyman, R.M., Stoger, E., Schillberg, S., Christou, P. and Fischer, R. (2003) Molecular farming in plants: host systems and expression technology. Trends Biotechnol., 21, 570-578.
61. Valente, M.T., Chiaiese, P., Galante, V., Di Gaitano, S., Piccoli, R., Monti, L. and Filippone, E. (2004) In planta expression of a human apolipoprotein. Proceedings of the XLVIII Italian Society of Agricultural Genetics. SIFV-SIGA Joint Meeting Leece, Italy. ISBN 88-900622-5-8.
62. Van Rooijen, G.J.H. and Moloney, M.M. (1995) Plant seed oil-bodies as carriers for foreign proteins. Bio/Technology, 13, 72-77.
63. Wang, L., Sharifi, B.G., Pan, T., Song, L., Yukht, A. and Shah, P.K. (2006) Bone marrow transplantation shows superior atheroprotective effects of gene therapy with Apolipoprotein A-I Milano compared with wild-type Apolipoprotein A-I in hyperlipidemic mice. J. Am. Coll. Cardiol., 48, 1459-1468.
64. Weisgraber, K.H., Bersot, T.P., Mahley, R.W., Franceschini, G. and Sirtori, C.R. (1980) Isolation and characterization of a cysteine-containing variant of the A-I apoprotein from human high density lipoproteins. J. Clin. Invest., 66, 901-907.
65. Milano detection of normal A-I in affected subjects and evidence for a cysteine for arginine substitution in the variant A-I. J. Biol. Chem., 258, 2508-2513.