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Nano Research 2018, 11(10): 5130-5143 https://doi.org/10.1007/s12274-018-2101-1
Review Article | Issue | Published: 08 June 2018

High-density lipoprotein mimetic nanotherapeutics for cardiovascular and neurodegenerative diseases

Show Author's Information Song Ih Ahn1,2,§,  Hyun-Ji Park1,§,  Jiwon Yom1,2,  Taeyoung Kim1,  YongTae Kim1,2,3,4( )
George W. Woodruff School of Mechanical EngineeringGeorgia Institute of TechnologyAtlantaGA30332USA
Parker H. Petit Institute for Bioengineering and BioscienceGeorgia Institute of TechnologyAtlantaGA30332USA
Wallace H. Coulter Department of Biomedical EngineeringGeorgia Institute of TechnologyAtlantaGA30332USA
Institute for Electronics and NanotechnologyGeorgia Institute of TechnologyAtlantaGA30332USA

§ Song Ih Ahn and Hyun-Ji Park contributed equally to this work.

Keywords:
neurodegenerative disease, high-density lipoprotein, nanotherapeutic, cardiovascular disease
Cite this article:
Ahn SI, Park H-J, Yom J, et al. High-density lipoprotein mimetic nanotherapeutics for cardiovascular and neurodegenerative diseases. Nano Research, 2018, 11(10): 5130-5143. https://doi.org/10.1007/s12274-018-2101-1
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Abstract Full text About this article

High-density lipoprotein (HDL) serves as a natural nanoparticle with compositional and functional heterogeneity and contributes to the maintenance of lipid metabolism and various biological functions. HDL also transports endogenous microRNAs, vitamins, hormones, and proteins through blood and interstitial fluids to various organs. These unique and diverse features of HDL have encouraged its applications for the transport of therapeutics and diagnostic reagents in the last decade. In this review, we describe the heterogeneous characteristics and biological functions of HDL and highlight HDL mimetic approaches, including apolipoprotein mimetic peptides and reconstituted HDL nanoparticles. Given the potential of HDL as a nanocarrier delivering various therapeutic agents, we discuss the current representative studies of HDL mimetic nanotherapeutics for cardiovascular and neurodegenerative diseases and analyze the current challenges and future perspective.


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About this article

High-density lipoprotein mimetic nanotherapeutics for cardiovascular and neurodegenerative diseases

Show Author's information Song Ih Ahn1,2,§, Hyun-Ji Park1,§, Jiwon Yom1,2, Taeyoung Kim1, YongTae Kim1,2,3,4( )
George W. Woodruff School of Mechanical EngineeringGeorgia Institute of TechnologyAtlantaGA30332USA
Parker H. Petit Institute for Bioengineering and BioscienceGeorgia Institute of TechnologyAtlantaGA30332USA
Wallace H. Coulter Department of Biomedical EngineeringGeorgia Institute of TechnologyAtlantaGA30332USA
Institute for Electronics and NanotechnologyGeorgia Institute of TechnologyAtlantaGA30332USA

§ Song Ih Ahn and Hyun-Ji Park contributed equally to this work.

Abstract

High-density lipoprotein (HDL) serves as a natural nanoparticle with compositional and functional heterogeneity and contributes to the maintenance of lipid metabolism and various biological functions. HDL also transports endogenous microRNAs, vitamins, hormones, and proteins through blood and interstitial fluids to various organs. These unique and diverse features of HDL have encouraged its applications for the transport of therapeutics and diagnostic reagents in the last decade. In this review, we describe the heterogeneous characteristics and biological functions of HDL and highlight HDL mimetic approaches, including apolipoprotein mimetic peptides and reconstituted HDL nanoparticles. Given the potential of HDL as a nanocarrier delivering various therapeutic agents, we discuss the current representative studies of HDL mimetic nanotherapeutics for cardiovascular and neurodegenerative diseases and analyze the current challenges and future perspective.

Keywords: neurodegenerative disease, high-density lipoprotein, nanotherapeutic, cardiovascular disease

References(98)

1

Mahley, R. W.; Innerarity, T. L.; Rall, S. C., Jr.; Weisgraber, K. H. Plasma lipoproteins: Apolipoprotein structure and function. J. Lipid Res. 1984, 25, 1277–1294.
DOI Google Scholar
2

Oram, J. F. The cholesterol mobilizing transporter ABCA1 as a new therapeutic target for cardiovascular disease. Trends Cardiovas. Med. 2002, 12, 170–175.
DOI Google Scholar
3

Kontush, A.; Chapman, M. J. Functionally defective high-density lipoprotein: A new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol. Rev. 2006, 58, 342–374.
DOI Google Scholar
4

Mulder, W. J. M.; van Leent, M. M. T.; Lameijer, M.; Fisher, E. A.; Fayad, Z. A.; Pérez-Medina, C. High-density lipoprotein nanobiologics for precision medicine. Acc. Chem. Res. 2018, 51, 127–137.
DOI Google Scholar
5

Goldbourt, U.; Yaari, S.; Medalie, J. H. Isolated low HDL cholesterol as a risk factor for coronary heart disease mortality: A 21-year follow-up of 8, 000 men. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 107–113.
DOI Google Scholar
6

Kontush, A.; Lindahl, M.; Lhomme, M.; Calabresi, L.; Chapman, J. M.; Davidson, W. S. Structure of HDL: Particle subclasses and molecular components. High Density Lipoproteins 2015, 224, 3–51.
Google Scholar
7

Deane, R.; Zlokovic, B. V. Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 2007, 4, 191–197.
DOI Google Scholar
8

Musiek, E. S.; Holtzman, D. M. Three dimensions of the amyloid hypothesis: Time, space and 'wingmen'. Nat. Neurosci. 2015, 18, 800–806.
DOI Google Scholar
9

Rosenblum, W. I. Why Alzheimer trials fail: Removing soluble oligomeric beta amyloid is essential, inconsistent, and difficult. Neurobiol. Aging 2014, 35, 969–974.
DOI Google Scholar
10

Vitali, C.; Wellington, C. L.; Calabresi, L. HDL and cholesterol handling in the brain. Cardiovasc. Res. 2014, 103, 405–413.
DOI Google Scholar
11

Chetty, P. S.; Nguyen, D.; Nickel, M.; Lund-Katz, S.; Mayne, L.; Englander, S. W.; Phillips, M. C. Comparison of apoA-I helical structure and stability in discoidal and spherical HDL particles by HX and mass spectrometry. J. Lipid Res. 2013, 54, 1589–1597.
DOI Google Scholar
12

Silva, R. A. G. D.; Huang, R.; Morris, J.; Fang, J. W.; Gracheva, E. O.; Ren, G.; Kontush, A.; Jerome, W. G.; Rye, K. A.; Davidson, W. S. Structure of apolipoprotein A-I in spherical high density lipoproteins of different sizes. Proc. Natl. Acad. Sci. USA 2008, 105, 12176–12181.
DOI Google Scholar
13

Franceschini, G. Apolipoprotein function in health and disease: Insights from natural mutations. Eur. J. Clin. Invest. 1996, 26, 733–746.
DOI Google Scholar
14

Li, W. H.; Tanimura, M.; Luo, C. C.; Datta, S.; Chan, L. The apolipoprotein multigene family: Biosynthesis, structure, structure-function relationships, and evolution. J. Lipid Res. 1988, 29, 245–271.
DOI Google Scholar
15

Law, A.; Scott, J. A cross-species comparison of the apolipoprotein-B domain that binds to the LDL receptor. J. Lipid Res. 1990, 31, 1109–1120.
DOI Google Scholar
16

DeKroon, R. M.; Mihovilovic, M.; Goodger, Z. V.; Robinette, J. B.; Sullivan, P. M.; Saunders, A. M.; Strittmatter, W. J. ApoE genotype-specific inhibition of apoptosis. J. Lipid Res. 2003, 44, 1566–1573.
DOI Google Scholar
17

Mikolasevic, I.; Žutelija, M.; Mavrinac, V.; Orlic, L. Dyslipidemia in patients with chronic kidney disease: Etiology and management. Int. J. Nephrol. Renovasc. Dis. 2017, 10, 35–45.
DOI Google Scholar
18

Cohn, J. S.; Batal, R.; Tremblay, M.; Jacques, H.; Veilleux, L.; Rodriguez, C.; Mamer, O.; Davignon, J. Plasma turnover of HDL apoC-I, apoC-Ⅲ, and apoE in humans: In vivo evidence for a link between HDL apoC-Ⅲ and apoA-I metabolism. J. Lipid Res. 2003, 44, 1976–1983.
DOI Google Scholar
19

Kingwell, B. A.; Chapman, M. J.; Kontush, A.; Miller, N. E. HDL-targeted therapies: Progress, failures and future. Nat. Rev. Drug Discov. 2014, 13, 445–464.
DOI Google Scholar
20

Linton, M. F.; Tao, H.; Linton, E. F.; Yancey, P. G. SR-BI: A multifunctional receptor in cholesterol homeostasis and atherosclerosis. Trends Endocrinol. Metab. 2017, 28, 461–472.
DOI Google Scholar
21

Yvan-Charvet, L.; Wang, N.; Tall, A. R. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 139–143.
DOI Google Scholar
22

Vaughan, A. M.; Oram, J. F. ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J. Lipid Res. 2006, 47, 2433–2443.
DOI Google Scholar
23

Rinninger, F.; Heine, M.; Singaraja, R.; Hayden, M.; Brundert, M.; Ramakrishnan, R.; Heeren, J. High density lipoprotein metabolism in low density lipoprotein receptor-deficient mice. J. Lipid Res. 2014, 55, 1914–1924.
DOI Google Scholar
24

Galvani, S.; Sanson, M.; Blaho, V. A.; Swendeman, S. L.; Obinata, H.; Conger, H.; Dahlbäck, B.; Kono, M.; Proia, R. L.; Smith, J. D. et al. HDL-bound sphingosine 1-phosphate acts as a biased agonist for the endothelial cell receptor S1P1 to limit vascular inflammation. Sci. Signal. 2015, 8, ra79.
DOI Google Scholar
25

Rhainds, D.; Brissette, L. The role of scavenger receptor class B type I (SR-BI) in lipid trafficking: Defining the rules for lipid traders. Int. J. Biochem. Cell Biol. 2004, 36, 39–77.
DOI Google Scholar
26

Tall, A. R.; Yvan-Charvet, L.; Terasaka, N.; Pagler, T.; Wang, N. HDL, ABC transporters, and cholesterol efflux: Implications for the treatment of atherosclerosis. Cell Metab. 2008, 7, 365–375.
DOI Google Scholar
27

Litvinov, D.; Mahini, H.; Garelnabi, M. Antioxidant and anti-inflammatory role of paraoxonase 1: Implication in arteriosclerosis diseases. N. Am. J. Med. Sci. 2012, 4, 523– 532.
DOI Google Scholar
28

Aharoni, S.; Aviram, M.; Fuhrman, B. Paraoxonase 1 (PON1) reduces macrophage inflammatory responses. Atherosclerosis 2013, 228, 353–361.
DOI Google Scholar
29

Speer, T.; Rohrer, L.; Blyszczuk, P.; Shroff, R.; Kuschnerus, K.; Kränkel, N.; Kania, G.; Zewinger, S.; Akhmedov, A.; Shi, Y. et al. Abnormal high-density lipoprotein induces endothelial dysfunction via activation of Toll-like receptor-2. Immunity 2013, 38, 754–768.
DOI Google Scholar
30

Han, C. Y.; Tang, C. R.; Guevara, M. E.; Wei, H.; Wietecha, T.; Shao, B. H.; Subramanian, S.; Omer, M.; Wang, S. R.; O'Brien, K. D. et al. Serum amyloid A impairs the antiinflammatory properties of HDL. J. Clin. Invest. 2016, 126, 266–281.
Google Scholar
31

Röhrl, C.; Stangl, H. HDL endocytosis and resecretion. Biochim. Biophys. Acta 2013, 1831, 1626–1633.
DOI Google Scholar
32

Kowal, R. C.; Herz, J.; Goldstein, J. L.; Esser, V.; Brown, M. S. Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc. Natl. Acad. Sci. USA 1989, 86, 5810–5814.
DOI Google Scholar
33

Mooberry, L. K.; Sabnis, N. A.; Panchoo, M.; Nagarajan, B.; Lacko, A. G. Targeting the SR-B1 receptor as a gateway for cancer therapy and imaging. Front. Pharmacol. 2016, 7, 466.
Google Scholar
34

Rodrigueza, W. V.; Thuahnai, S. T.; Temel, R. E.; Lund-Katz, S.; Phillips, M. C.; Williams, D. L. Mechanism of scavenger receptor class B type I-mediated selective uptake of cholesteryl esters from high density lipoprotein to adrenal cells. J. Biol. Chem. 1999, 274, 20344–20350.
DOI Google Scholar
35

Shahzad, M. M. K.; Mangala, L. S.; Han, H. D.; Lu, C. H.; Bottsford-Miller, J.; Nishimura, M.; Mora, E. M.; Lee, J. W.; Stone, R. L.; Pecot, C. V. et al. Targeted delivery of small interfering RNA using reconstituted high-density lipoprotein nanoparticles. Neoplasia 2011, 13, 309–319.
DOI Google Scholar
36

Zheng, Y.; Liu, Y. Y.; Jin, H. L.; Pan, S. T.; Qian, Y.; Huang, C.; Zeng, Y. X.; Luo, Q. M.; Zeng, M. S.; Zhang, Z. H. Scavenger receptor B1 is a potential biomarker of human nasopharyngeal carcinoma and its growth is inhibited by HDL-mimetic nanoparticles. Theranostics 2013, 3, 477–486.
DOI Google Scholar
37

Zhang, Z. H.; Chen, J.; Ding, L. L.; Jin, H. L.; Lovell, J. F.; Corbin, I. R.; Cao, W. G.; Lo, P. C.; Yang, M.; Tsao, M. S. et al. HDL-mimicking peptide-lipid nanoparticles with improved tumor targeting. Small 2010, 6, 430–437.
DOI Google Scholar
38

Chen, W.; Jarzyna, P. A.; van Tilborg, G. A. F.; Nguyen, V. A.; Cormode, D. P.; Klink, A.; Griffioen, A. W.; Randolph, G. J.; Fisher, E. A.; Mulder, W. J. M. et al. RGD peptide functionalized and reconstituted high-density lipoprotein nanoparticles as a versatile and multimodal tumor targeting molecular imaging probe. FASEB J. 2010, 24, 1689–1699.
DOI Google Scholar
39

Molino, Y.; David, M.; Varini, K.; Jabes, F.; Gaudin, N.; Fortoul, A.; Bakloul, K.; Masse, M.; Bernard, A.; Drobecq, L. et al. Use of LDL receptor-targeting peptide vectors for in vitro and in vivo cargo transport across the blood-brain barrier. FASEB J. 2017, 31, 1807–1827.
DOI Google Scholar
40

Blaho, V. A.; Galvani, S.; Engelbrecht, E.; Liu, C.; Swendeman, S. L.; Kono, M.; Proia, R. L.; Steinman, L.; Han, M. H.; Hla, T. HDL-bound sphingosine-1-phosphate restrains lymphopoiesis and neuroinflammation. Nature 2015, 523, 342–346.
DOI Google Scholar
41

Hatch, F. T.; Lees, R. S. Practical methods for plasma lipoprotein analysis. Adv. Lipid Res. 1968, 6, 1–68.
Google Scholar
42

Havel, R. J.; Eder, H. A.; Bragdon, J. H. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 1955, 34, 1345–1353.
DOI Google Scholar
43

Patsch, J. R.; Sailer, S.; Kostner, G.; Sandhofer, F.; Holasek, A.; Braunsteiner, H. Separation of the main lipoprotein density classes from human plasma by rate-zonal ultracentrifugation. J. Lipid Res. 1974, 15, 356–366.
DOI Google Scholar
44

McVicar, J. P.; Kunitake, S. T.; Hamilton, R. L.; Kane, J. P. Characteristics of human lipoproteins isolated by selected-affinity immunosorption of apolipoprotein A-I. Proc. Natl. Acad. Sci. USA 1984, 81, 1356–1360.
DOI Google Scholar
45

Okazaki, M.; Hara, I. Analysis of cholesterol in high density lipoprotein subfractions by high performance liquid chromatography. J. Biochem. 1980, 88, 1215–1218.
DOI Google Scholar
46

Lerch, P. G.; Förtsch, V.; Hodler, G.; Bolli, R. Production and characterization of a reconstituted high density lipoprotein for therapeutic applications. Vox Sang. 1996, 71, 155–164.
DOI Google Scholar
47

Bonomo, E. A.; Swaney, J. B. A rapid method for the synthesis of protein-lipid complexes using adsorption chromatography. J. Lipid Res. 1988, 29, 380–384.
DOI Google Scholar
48

Foit, L.; Giles, F. J.; Gordon, L. I.; Thaxton, C. S. Synthetic high-density lipoprotein-like nanoparticles for cancer therapy. Expert Rev. Anticancer Ther. 2015, 15, 27–34.
DOI Google Scholar
49

Ganzetti, G. S.; Busnelli, M.; Parolini, C.; Manzini, S.; Dellera, F.; Sirtori, C. R.; Chiesa, G. Apoa-I depletion in chow-fed apoeko mice severely worsens coronary atherosclerosis development. Atherosclerosis 2016, 252, e104.
Google Scholar
50

Van Lenten, B. J.; Wagner, A. C.; Anantharamaiah, G. M.; Navab, M.; Reddy, S. T.; Buga, G. M.; Fogelman, A. M. Apolipoprotein A-I mimetic peptides. Curr. Atheroscler. Rep. 2009, 11, 52–57.
DOI Google Scholar
51

Sviridov, D.; Remaley, A. T. High-density lipoprotein mimetics: Promises and challenges. Biochem. J. 2015, 472, 249–259.
DOI Google Scholar
52

Marrache, S.; Dhar, S. Biodegradable synthetic high-density lipoprotein nanoparticles for atherosclerosis. Proc. Natl. Acad. Sci. USA 2013, 110, 9445–9450.
DOI Google Scholar
53

Zhang, Z. H.; Cao, W. G.; Jin, H. L.; Lovell, J. F.; Yang, M.; Ding, L. L.; Chen, J.; Corbin, I.; Luo, Q. M.; Zheng, G. Biomimetic nanocarrier for direct cytosolic drug delivery. Angew. Chem., Int. Ed. 2009, 48, 9171–9175.
DOI Google Scholar
54

Qin, S.; Kamanna, V. S.; Lai, J. H.; Liu, T.; Ganji, S. H.; Zhang, L.; Bachovchin, W. W.; Kashyap, M. L. Reverse D4F, an apolipoprotein-AI mimetic peptide, inhibits atherosclerosis in ApoE-null mice. J. Cardiovasc. Pharmacol. Ther. 2012, 17, 334–343.
DOI Google Scholar
55

Park, H. J.; Kuai, R.; Jeon, E. J.; Seo, Y.; Jung, Y.; Moon, J. J.; Schwendeman, A.; Cho, S. W. High-density lipoprotein-mimicking nanodiscs carrying peptide for enhanced therapeutic angiogenesis in diabetic hindlimb ischemia. Biomaterials 2018, 161, 69–80.
DOI Google Scholar
56

Amar, M. J. A.; D'Souza, W.; Turner, S.; Demosky, S.; Sviridov, D.; Stonik, J.; Luchoomun, J.; Voogt, J.; Hellerstein, M.; Sviridov, D. et al. 5A apolipoprotein mimetic peptide promotes cholesterol efflux and reduces atherosclerosis in mice. J. Pharmacol. Exp. Ther. 2010, 334, 634–641.
DOI Google Scholar
57

Sviridov, D. O.; Andrianov, A. M.; Anishchenko, I. V.; Stonik, J. A.; Amar, M. J. A.; Turner, S.; Remaley, A. T. Hydrophobic amino acids in the hinge region of the 5A apolipoprotein mimetic peptide are essential for promoting cholesterol efflux by the ABCA1 transporter. J. Pharmacol. Exp. Ther. 2013, 344, 50–58.
DOI Google Scholar
58

Datta, G.; White, C. R.; Dashti, N.; Chaddha, M.; Palgunachari, M. N.; Gupta, H.; Handattu, S. P.; Garber, D. W.; Anantharamaiah, G. M. Anti-inflammatory and recycling properties of an apolipoprotein mimetic peptide, Ac-hE18A-NH2. Atherosclerosis 2010, 208, 134–141.
DOI Google Scholar
59

Miles, J.; Khan, M.; Painchaud, C.; Lalwani, N.; Drake, S.; Dasseux, J. L. Single-dose tolerability, pharmacokinetics, and cholesterol mobilization in HDL-C fraction following intravenous administration of ETC-642, a 22-mer ApoA-I analogue and phospholipids complex, in atherosclerosis patients. Arterioscler. Thromb. Vasc. Biol. 2004, 24, e19.
Google Scholar
60

Di Bartolo, B. A.; Nicholls, S. J.; Bao, S. S.; Rye, K. A.; Heather, A. K.; Barter, P. J.; Bursill, C. The apolipoprotein A-I mimetic peptide ETC-642 exhibits anti-inflammatory properties that are comparable to high density lipoproteins. Atherosclerosis 2011, 217, 395–400.
DOI Google Scholar
61

Sethi, A. A.; Amar, M.; Shamburek, R. D.; Remaley, A. T. Apolipoprotein AI mimetic peptides: Possible new agents for the treatment of atherosclerosis. Curr. Opin. Investig. Drugs 2007, 8, 201–212.
Google Scholar
62

Datta, G.; Chaddha, M.; Garber, D. W.; Chung, B. L.; Tytler, E. M.; Dashti, N.; Bradley, W. A.; Gianturco, S. H.; Anantharamaiah, G. M. The receptor binding domain of apolipoprotein E, linked to a model class A amphipathic helix, enhances internalization and degradation of LDL by fibroblasts. Biochemistry 2000, 39, 213–220.
DOI Google Scholar
63

Scanu, A. Binding of human serum high density lipoprotein apoprotein with aqueous dispersions of phospholipids. J. Biol. Chem. 1967, 242, 711–719.
DOI Google Scholar
64

Scanu, A.; Cump, E.; Toth, J.; Koga, S.; Stiller, E.; Albers, L. Degradation and reassembly of a human serum high-density lipoprotein. Evidence for differences in lipid affinity among three classes of polypeptide chains. Biochemistry 1970, 9, 1327–1335.
DOI Google Scholar
65

van den Elzen, P.; Garg, S.; León, L.; Brigl, M.; Leadbetter, E. A.; Gumperz, J. E.; Dascher, C. C.; Cheng, T. Y.; Sacks, F. M.; Illarionov, P. A. et al. Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 2005, 437, 906–910.
DOI Google Scholar
66

Tall, A. R. Studies on the transfer of phosphatidylcholine from unilamellar vesicles into plasma high density lipoproteins in the rat. J. Lipid Res. 1980, 21, 354–363.
DOI Google Scholar
67

Kim, Y.; Fay, F.; Cormode, D. P.; Sanchez-Gaytan, B. L.; Tang, J.; Hennessy, E. J.; Ma, M. M.; Moore, K.; Farokhzad, O. C.; Fisher, E. A. et al. Single step reconstitution of multifunctional high-density lipoprotein-derived nanomaterials using microfluidics. ACS Nano 2013, 7, 9975–9983.
DOI Google Scholar
68

Toth, M. J.; Kim, T.; Kim, Y. Robust manufacturing of lipid-polymer nanoparticles through feedback control of parallelized swirling microvortices. Lab Chip 2017, 17, 2805–2813.
DOI Google Scholar
69

Ahn, J.; Sei, Y. J.; Jeon, N. L.; Kim, Y. Probing the effect of bioinspired nanomaterials on angiogenic sprouting with a microengineered vascular system. IEEE Trans. Nanotechnol. 2018, 17, 393–397.
DOI Google Scholar
70

Sei, Y. J.; Ahn, J.; Kim, T.; Shin, E.; Santiago-Lopez, A. J.; Jang, S. S.; Jeon, N. L.; Jang, Y. C.; Kim, Y. Detecting the functional complexities between high-density lipoprotein mimetics. Biomaterials 2018, 170, 58–69.
DOI Google Scholar
71

Kim, Y. T.; Chung, B. L.; Ma, M. M.; Mulder, W. J. M.; Fayad, Z. A.; Farokhzad, O. C.; Langer, R. Mass production and size control of lipid-polymer hybrid nanoparticles through controlled microvortices. Nano Lett. 2012, 12, 3587–3591.
DOI Google Scholar
72

Sanchez-Gaytan, B. L.; Fay, F.; Lobatto, M. E.; Tang, J.; Ouimet, M.; Kim, Y.; van der Staay, S. E. M.; van Rijs, S. M.; Priem, B.; Zhang, L. F. et al. HDL-mimetic PLGA nanoparticle to target atherosclerosis plaque macrophages. Bioconjug. Chem. 2015, 26, 443–451.
DOI Google Scholar
73

Benjamin, E. J.; Virani, S. S.; Callaway, C. W.; Chang, A. R.; Cheng, S. S.; Chiuve, S. E.; Cushman, M.; Delling, F. N.; Deo, R.; de Ferranti, S. D. et al. Heart disease and stroke statistics—2018 update: A report from the American heart association. Circulation 2018, 137, e67–e492.
Google Scholar
74

Hu, C. M. J.; Fang, R. H.; Wang, K. C.; Luk, B. T.; Thamphiwatana, S.; Dehaini, D.; Nguyen, P.; Angsantikul, P.; Wen, C. H.; Kroll, A. V. et al. Nanoparticle biointerfacing by platelet membrane cloaking. Nature 2015, 526, 118–121.
DOI Google Scholar
75

Tang, J. N.; Su, T.; Huang, K.; Dinh, P. U.; Wang, Z. G.; Vandergriff, A.; Hensley, M. T.; Cores, J.; Allen, T.; Li, T. S. et al. Targeted repair of heart injury by stem cells fused with platelet nanovesicles. Nat. Biomed. Eng. 2018, 2, 17–26.
DOI Google Scholar
76

Nguyen, M. M.; Carlini, A. S.; Chien, M. P.; Sonnenberg, S.; Luo, C.; Braden, R. L.; Osborn, K. G.; Li, Y. W.; Gianneschi, N. C.; Christman, K. L. Enzyme-responsive nanoparticles for targeted accumulation and prolonged retention in heart tissue after myocardial infarction. Adv. Mater. 2015, 27, 5547–5552.
DOI Google Scholar
77

Korin, N.; Kanapathipillai, M.; Matthews, B. D.; Crescente, M.; Brill, A.; Mammoto, T.; Ghosh, K.; Jurek, S.; Bencherif, S. A.; Bhatta, D. et al. Shear-activated nanotherapeutics for drug targeting to obstructed blood vessels. Science 2012, 337, 738–742.
DOI Google Scholar
78

Michael Gibson, C.; Korjian, S.; Tricoci, P.; Daaboul, Y.; Yee, M.; Jain, P.; Alexander, J. H.; Steg, P. G.; Lincoff, A. M.; Kastelein, J. J. P. et al. Safety and tolerability of CSL112, a reconstituted, infusible, plasma-derived apolipoprotein A-I, after acute myocardial infarction: The AEGIS-I trial (ApoA-I event reducing in ischemic syndromes I). Circulation 2016, 134, 1918–1930.
DOI Google Scholar
79

Hovingh, G. K.; Smits, L. P.; Stefanutti, C.; Soran, H.; Kwok, S.; de Graaf, J.; Gaudet, D.; Keyserling, C. H.; Klepp, H.; Frick, J. et al. The effect of an apolipoprotein A-I-containing high-density lipoprotein-mimetic particle (CER-001) on carotid artery wall thickness in patients with homozygous familial hypercholesterolemia: The Modifying Orphan Disease Evaluation (MODE) study. Am. Heart. J. 2015, 169, 736–742. e1.
DOI Google Scholar
80

Tabet, F.; Vickers, K. C.; Cuesta Torres, L. F.; Wiese, C. B.; Shoucri, B. M.; Lambert, G.; Catherinet, C.; Prado-Lourenco, L.; Levin, M. G.; Thacker, S. et al. HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells. Nat. Commun. 2014, 5, 3292.
DOI Google Scholar
81

Duivenvoorden, R.; Tang, J.; Cormode, D. P.; Mieszawska, A. J.; Izquierdo-Garcia, D.; Ozcan, C.; Otten, M. J.; Zaidi, N.; Lobatto, M. E.; van Rijs, S. M. et al. A statin-loaded reconstituted high-density lipoprotein nanoparticle inhibits atherosclerotic plaque inflammation. Nat. Commun. 2014, 5, 3065.
DOI Google Scholar
82

Argraves, K. M.; Gazzolo, P. J.; Groh, E. M.; Wilkerson, B. A.; Matsuura, B. S.; Twal, W. O.; Hammad, S. M.; Argraves, W. S. High density lipoprotein-associated sphingosine 1-phosphate promotes endothelial barrier function. J. Biol. Chem. 2008, 283, 25074–25081.
DOI Google Scholar
83

Nanjee, M. N.; Doran, J. E.; Lerch, P. G.; Miller, N. E. Acute effects of intravenous infusion of ApoA1/phosphatidylcholine discs on plasma lipoproteins in humans. Arterioscler. Thromb. Vasc. Biol. 1999, 19, 979–989.
DOI Google Scholar
84

Tardif, J. C.; Grégoire, J.; L'Allier, P. L.; Ibrahim, R.; Lespérance, J.; Heinonen, T. M.; Kouz, S.; Berry, C.; Basser, R.; Lavoie, M. A. et al. Effects of reconstituted high-density lipoprotein infusions on coronary atherosclerosis: A randomized controlled trial. JAMA 2007, 297, 1675–1682.
DOI Google Scholar
85

Nasr, H.; Torsney, E.; Poston, R. N.; Hayes, L.; Gaze, D. C.; Basser, R.; Thompson, M. M.; Loftus, I. M.; Cockerill, G. W. Investigating the effect of a single infusion of reconstituted high-density lipoprotein in patients with symptomatic carotid plaques. Ann. Vasc. Surg. 2015, 29, 1380–1391.
DOI Google Scholar
86

Easton, R.; Gille, A.; D'Andrea, D.; Davis, R.; Wright, S. D.; Shear, C. A multiple ascending dose study of CSL112, an infused formulation of ApoA-I. J. Clin. Pharmacol. 2014, 54, 301–310.
DOI Google Scholar
87

Krause, B. R.; Remaley, A. T. Reconstituted HDL for the acute treatment of acute coronary syndrome. Curr. Opin. Lipidol. 2013, 24, 480–486.
DOI Google Scholar
88

Tricoci, P.; D'Andrea, D. M.; Gurbel, P. A.; Yao, Z. L.; Cuchel, M.; Winston, B.; Schott, R.; Weiss, R.; Blazing, M. A.; Cannon, L. et al. Infusion of reconstituted high-density lipoprotein, CSL112, in patients with atherosclerosis: Safety and pharmacokinetic results from a phase 2a randomized clinical trial. J. Am. Heart Assoc. 2015, 4, e002171.
Google Scholar
89

Goffinet, M.; Tardy, C.; Bluteau, A.; Boubekeur, N.; Baron, R.; Keyserling, C.; Barbaras, R.; Lalwani, N.; Dasseux, J. L. Anti-atherosclerotic effect of CER-001, an engineered HDL-mimetic, in the high-fat diet-fed LDLr knockout mice. Circulation 2012, 126, A18667.
Google Scholar
90

Tardif, J. C.; Ballantyne, C. M.; Barter, P.; Dasseux, J. L.; Fayad, Z. A.; Guertin, M. C.; Kastelein, J. J. P.; Keyserling, C.; Klepp, H.; Koenig, W. et al. Effects of the high-density lipoprotein mimetic agent CER-001 on coronary atherosclerosis in patients with acute coronary syndromes: A randomized trial. Eur. Heart J. 2014, 35, 3277–3286.
DOI Google Scholar
91

Keyserling, C. H.; Hunt, T. L.; Klepp, H. M.; Scott, R. A.; Barbaras, R.; Schwendeman, A.; Lalwani, N.; Dasseux, J. L. CER-001, a synthetic HDL-mimetic, safely mobilizes cholesterol in healthy dyslipidemic volunteers. Circulation 2011, 124, A15525.
Google Scholar
92

Vickers, K. C.; Palmisano, B. T.; Shoucri, B. M.; Shamburek, R. D.; Remaley, A. T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell. Biol. 2011, 13, 423–433.
DOI Google Scholar
93

Alzheimer's Association. 2017 Alzheimer's disease facts and figures. Alzheimers Dement. 2017, 13, 325–373.
DOI Google Scholar
94

Stukas, S.; Robert, J.; Wellington, C. L. High-density lipoproteins and cerebrovascular integrity in Alzheimer's disease. Cell Metab. 2014, 19, 574–591.
DOI Google Scholar
95

Song, Q. X.; Huang, M.; Yao, L.; Wang, X. L.; Gu, X.; Chen, J.; Chen, J.; Huang, J. L.; Hu, Q. Y.; Kang, T. et al. Lipoprotein-based nanoparticles rescue the memory loss of mice with Alzheimer's disease by accelerating the clearance of amyloid-beta. ACS Nano 2014, 8, 2345–2359.
DOI Google Scholar
96

Huang, M.; Hu, M.; Song, Q. X.; Song, H. H.; Huang, J. L.; Gu, X.; Wang, X. L.; Chen, J.; Kang, T.; Feng, X. Y. et al. GM1-modified lipoprotein-like nanoparticle: Multifunctional nanoplatform for the combination therapy of Alzheimer's disease. ACS Nano 2015, 9, 10801–10816.
DOI Google Scholar
97

Song, Q. X.; Song, H. H.; Xu, J. R.; Huang, J. L.; Hu, M.; Gu, X.; Chen, J.; Zheng, G.; Chen, H. Z.; Gao, X. L. Biomimetic ApoE-reconstituted high density lipoprotein nanocarrier for blood-brain barrier penetration and amyloid beta-targeting drug delivery. Mol. Pharm. 2016, 13, 3976– 3987.
DOI Google Scholar
98

Redondo, S.; Martínez-González, J.; Urraca, C.; Tejerina, T. Emerging therapeutic strategies to enhance HDL function. Lipids Health Dis. 2011, 10, 175.
DOI Google Scholar
Publication history
Copyright
Acknowledgements

Publication history

Received: 20 March 2018
Revised: 20 May 2018
Accepted: 21 May 2018
Published: 08 June 2018
Issue date: October 2018

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Acknowledgements

Acknowledgements

This work was supported by the National Institutes of Health Director's New Innovator Award (No. 1DP2HL142050, Y. K.) and the American Heart Association Scientist Development (No. 15SDG25080314, Y. K.).

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