Host Defence Cryptides from Human Apolipoproteins: Applications in Medicinal Chemistry

Author(s): Rosa Gaglione, Elio Pizzo, Eugenio Notomista, Cesar de la Fuente-Nunez, Angela Arciello*

Journal Name: Current Topics in Medicinal Chemistry

Volume 20 , Issue 14 , 2020


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Graphical Abstract:


Abstract:

Several eukaryotic proteins with defined physiological roles may act as precursors of cryptic bioactive peptides released upon protein cleavage by the host and/or bacterial proteases. Based on this, the term “cryptome” has been used to define the unique portion of the proteome encompassing proteins with the ability to generate bioactive peptides (cryptides) and proteins (crypteins) upon proteolytic cleavage. Hence, the cryptome represents a source of peptides with potential pharmacological interest. Among eukaryotic precursor proteins, human apolipoproteins play an important role, since promising bioactive peptides have been identified and characterized from apolipoproteins E, B, and A-I sequences. Human apolipoproteins derived peptides have been shown to exhibit antibacterial, anti-biofilm, antiviral, anti-inflammatory, anti-atherogenic, antioxidant, or anticancer activities in in vitro assays and, in some cases, also in in vivo experiments on animal models. The most interesting Host Defence Peptides (HDPs) identified thus far in human apolipoproteins are described here with a focus on their biological activities applicable to biomedicine. Altogether, reported evidence clearly indicates that cryptic peptides represent promising templates for the generation of new drugs and therapeutics against infectious diseases.

Keywords: Host defence peptides, Human apolipoproteins, Bioactive cryptides, Synergistic effects, Bacterial biofilm, Combinatorial therapy.

[1]
Ueki, N.; Someya, K.; Matsuo, Y.; Wakamatsu, K.; Mukai, H. Cryptides: functional cryptic peptides hidden in protein structures. Biopolymers, 2007, 88(2), 190-198.
[http://dx.doi.org/10.1002/bip.20687] [PMID: 17245751]
[2]
Mukai, H.; Hokari, Y.; Seki, T.; Takao, T.; Kubota, M.; Matsuo, Y.; Tsukagoshi, H.; Kato, M.; Kimura, H.; Shimonishi, Y.; Kiso, Y.; Nishi, Y.; Wakamatsu, K.; Munekata, E. Discovery of mitocryptide-1, a neutrophil-activating cryptide from healthy porcine heart. J. Biol. Chem., 2008, 283(45), 30596-30605.
[http://dx.doi.org/10.1074/jbc.M803913200] [PMID: 18768476]
[3]
Mukai, H.; Seki, T.; Nakano, H.; Hokari, Y.; Takao, T.; Kawanami, M.; Tsukagoshi, H.; Kimura, H.; Kiso, Y.; Shimonishi, Y.; Nishi, Y.; Munekata, E. Mitocryptide-2: purification, identification, and characterization of a novel cryptide that activates neutrophils. J. Immunol., 2009, 182(8), 5072-5080.
[http://dx.doi.org/10.4049/jimmunol.0802965] [PMID: 19342687]
[4]
Hokari, Y.; Seki, T.; Nakano, H.; Matsuo, Y.; Fukamizu, A.; Munekata, E.; Kiso, Y.; Mukai, H. Isolation and identification of novel neutrophil-activating cryptides hidden in mitochondrial cytochrome C. Protein Pept. Lett., 2012, 19(6), 680-687.
[http://dx.doi.org/10.2174/092986612800494048] [PMID: 22519541]
[5]
Iavarone, F.; Desiderio, C.; Vitali, A.; Messana, I.; Martelli, C.; Castagnola, M.; Cabras, T. Cryptides: latent peptides everywhere. Crit. Rev. Biochem. Mol. Biol., 2018, 53(3), 246-263.
[http://dx.doi.org/10.1080/10409238.2018.1447543] [PMID: 29564928]
[6]
Liepke, C.; Zucht, H.D.; Forssmann, W.G.; Ständker, L. Purification of novel peptide antibiotics from human milk. J. Chromatogr. B Biomed. Sci. Appl., 2001, 752(2), 369-377.
[http://dx.doi.org/10.1016/S0378-4347(00)00516-8] [PMID: 11270874]
[7]
Oddy, W.H. Breastfeeding protects against illness and infection in infants and children: a review of the evidence. Breastfeed. Rev., 2001, 9(2), 11-18.
[PMID: 11550600]
[8]
Hosea Blewett, H.J.; Cicalo, M.C.; Holland, C.D.; Field, C.J. The immunological components of human milk. Adv. Food Nutr. Res., 2008, 54, 45-80.
[http://dx.doi.org/10.1016/S1043-4526(07)00002-2] [PMID: 18291304]
[9]
Messana, I.; Cabras, T.; Iavarone, F.; Vincenzoni, F.; Urbani, A.; Castagnola, M. Unraveling the different proteomic platforms. J. Sep. Sci., 2013, 36(1), 128-139.
[http://dx.doi.org/10.1002/jssc.201200830] [PMID: 23212829]
[10]
Messana, I.; Cabras, T.; Pisano, E.; Sanna, M.T.; Olianas, A.; Manconi, B.; Pellegrini, M.; Paludetti, G.; Scarano, E.; Fiorita, A.; Agostino, S.; Contucci, A.M.; Calò, L.; Picciotti, P.M.; Manni, A.; Bennick, A.; Vitali, A.; Fanali, C.; Inzitari, R.; Castagnola, M. Trafficking and postsecretory events responsible for the formation of secreted human salivary peptides: a proteomics approach. Mol. Cell. Proteomics, 2008, 7(5), 911-926.
[http://dx.doi.org/10.1074/mcp.M700501-MCP200] [PMID: 18187409]
[11]
Autelitano, D.J.; Rajic, A.; Smith, A.I.; Berndt, M.C.; Ilag, L.L.; Vadas, M. The cryptome: a subset of the proteome, comprising cryptic peptides with distinct bioactivities. Drug Discov. Today, 2006, 11(7-8), 306-314.
[http://dx.doi.org/10.1016/j.drudis.2006.02.003] [PMID: 16580972]
[12]
Pimenta, D.C.; Lebrun, I. Cryptides: buried secrets in proteins. Peptides, 2007, 28(12), 2403-2410.
[http://dx.doi.org/10.1016/j.peptides.2007.10.005] [PMID: 18023928]
[13]
Gelman, J.S.; Sironi, J.; Castro, L.M.; Ferro, E.S.; Fricker, L.D. Hemopressins and other hemoglobin-derived peptides in mouse brain: comparison between brain, blood, and heart peptidome and regulation in Cpefat/fat mice. J. Neurochem., 2010, 113(4), 871-880.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06653.x] [PMID: 20202081]
[14]
Gomes, I.; Dale, C.S.; Casten, K.; Geigner, M.A.; Gozzo, F.C.; Ferro, E.S.; Heimann, A.S.; Devi, L.A. Hemoglobin-derived peptides as novel type of bioactive signaling molecules. AAPS J., 2010, 12(4), 658-669.
[http://dx.doi.org/10.1208/s12248-010-9217-x] [PMID: 20811967]
[15]
Ng, J.H.; Ilag, L.L. Cryptic protein fragments as an emerging source of peptide drugs. IDrugs, 2006, 9(5), 343-346.
[PMID: 16676270]
[16]
Hancock, R.E.W.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol., 2006, 24(12), 1551-1557.
[http://dx.doi.org/10.1038/nbt1267] [PMID: 17160061]
[17]
Fjell, C.D.; Hiss, J.A.; Hancock, R.E.W.; Schneider, G. Designing antimicrobial peptides: form follows function. Nat. Rev. Drug Discov., 2011, 11(1), 37-51.
[http://dx.doi.org/10.1038/nrd3591] [PMID: 22173434]
[18]
Wang, G.; Li, X.; Wang, Z. APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res., 2016, 44(D1), D1087-D1093.
[http://dx.doi.org/10.1093/nar/gkv1278] [PMID: 26602694]
[19]
Hancock, R.E.W.; Haney, E.F.; Gill, E.E. The immunology of host defence peptides: beyond antimicrobial activity. Nat. Rev. Immunol., 2016, 16(5), 321-334.
[http://dx.doi.org/10.1038/nri.2016.29] [PMID: 27087664]
[20]
Lai, Y.; Gallo, R.L. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol., 2009, 30(3), 131-141.
[http://dx.doi.org/10.1016/j.it.2008.12.003] [PMID: 19217824]
[21]
Ghosh, C.; Sarkar, P.; Issa, R.; Haldar, J. Alternatives to Conventional Antibiotics in the Era of Antimicrobial Resistance. Trends Microbiol., 2019, 27(4), 323-338.
[http://dx.doi.org/10.1016/j.tim.2018.12.010] [PMID: 30683453]
[22]
Monserrat-Martinez, A.; Gambin, Y.; Sierecki, E. Thinking Outside the Bug: Molecular Targets and Strategies to Overcome Antibiotic Resistance. Int. J. Mol. Sci., 2019, 20(6)E1255
[http://dx.doi.org/10.3390/ijms20061255] [PMID: 30871132]
[23]
Marr, A.K.; Gooderham, W.J.; Hancock, R.E.W. Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr. Opin. Pharmacol., 2006, 6(5), 468-472.
[http://dx.doi.org/10.1016/j.coph.2006.04.006] [PMID: 16890021]
[24]
Vlieghe, P.; Lisowski, V.; Martinez, J.; Khrestchatisky, M. Synthetic therapeutic peptides: science and market. Drug Discov. Today, 2010, 15(1-2), 40-56.
[http://dx.doi.org/10.1016/j.drudis.2009.10.009] [PMID: 19879957]
[25]
Gaglione, R.; Pane, K.; Dell’Olmo, E.; Cafaro, V.; Pizzo, E.; Olivieri, G.; Notomista, E.; Arciello, A. Cost-effective production of recombinant peptides in Escherichia coli. N. Biotechnol., 2019, 51, 39-48.
[http://dx.doi.org/10.1016/j.nbt.2019.02.004] [PMID: 30790718]
[26]
Bolouri, H.; Sävman, K.; Wang, W.; Thomas, A.; Maurer, N.; Dullaghan, E.; Fjell, C.D.; Ek, C.J.; Hagberg, H.; Hancock, R.E.; Brown, K.L.; Mallard, C. Innate defense regulator peptide 1018 protects against perinatal brain injury. Ann. Neurol., 2014, 75(3), 395-410.
[http://dx.doi.org/10.1002/ana.24087] [PMID: 24339166]
[27]
Brunetti, J.; Falciani, C.; Roscia, G.; Pollini, S.; Bindi, S.; Scali, S.; Arrieta, U.C.; Gómez-Vallejo, V.; Quercini, L.; Ibba, E.; Prato, M.; Rossolini, G.M.; Llop, J.; Bracci, L.; Pini, A. In vitro and in vivo efficacy, toxicity, bio-distribution and resistance selection of a novel antibacterial drug candidate. Sci. Rep., 2016, 6, 26077.
[http://dx.doi.org/10.1038/srep26077] [PMID: 27169671]
[28]
Roversi, D.; Luca, V.; Aureli, S.; Park, Y.; Mangoni, M.L.; Stella, L. How many antimicrobial peptide molecules kill a bacterium? The case of PMAP-23. ACS Chem. Biol., 2014, 9(9), 2003-2007.
[http://dx.doi.org/10.1021/cb500426r] [PMID: 25058470]
[29]
McGregor, D.P. Discovering and improving novel peptide therapeutics. Curr. Opin. Pharmacol., 2008, 8(5), 616-619.
[http://dx.doi.org/10.1016/j.coph.2008.06.002] [PMID: 18602024]
[30]
Haney, E.F.; Mansour, S.C.; Hilchie, A.L.; de la Fuente-Núñez, C.; Hancock, R.E.W. High throughput screening methods for assessing antibiofilm and immunomodulatory activities of synthetic peptides. Peptides, 2015, 71, 276-285.
[http://dx.doi.org/10.1016/j.peptides.2015.03.015] [PMID: 25836992]
[31]
Ganz, T. Extracellular release of antimicrobial defensins by human polymorphonuclear leukocytes. Infect. Immun., 1987, 55(3), 568-571.
[http://dx.doi.org/10.1128/IAI.55.3.568-571.1987] [PMID: 3643886]
[32]
Ayabe, T.; Satchell, D.P.; Wilson, C.L.; Parks, W.C.; Selsted, M.E.; Ouellette, A.J. Secretion of microbicidal α-defensins by intestinal Paneth cells in response to bacteria. Nat. Immunol., 2000, 1(2), 113-118.
[http://dx.doi.org/10.1038/77783] [PMID: 11248802]
[33]
Vandamme, D.; Landuyt, B.; Luyten, W.; Schoofs, L. A comprehensive summary of LL-37, the factotum human cathelicidin peptide. Cell. Immunol., 2012, 280(1), 22-35.
[http://dx.doi.org/10.1016/j.cellimm.2012.11.009] [PMID: 23246832]
[34]
Nijnik, A.; Hancock, R.E.W. The roles of cathelicidin LL-37 in immune defences and novel clinical applications. Curr. Opin. Hematol., 2009, 16(1), 41-47.
[http://dx.doi.org/10.1097/MOH.0b013e32831ac517] [PMID: 19068548]
[35]
Méndez-Samperio, P. The human cathelicidin hCAP18/LL-37: a multifunctional peptide involved in mycobacterial infections. Peptides, 2010, 31(9), 1791-1798.
[http://dx.doi.org/10.1016/j.peptides.2010.06.016] [PMID: 20600427]
[36]
Pachón-Ibáñez, M.E.; Smani, Y.; Pachón, J.; Sánchez-Céspedes, J. Perspectives for clinical use of engineered human host defense antimicrobial peptides. FEMS Microbiol. Rev., 2017, 41(3), 323-342.
[http://dx.doi.org/10.1093/femsre/fux012] [PMID: 28521337]
[37]
Fruitwala, S.; El-Naccache, D.W.; Chang, T.L. Multifaceted immune functions of human defensins and underlying mechanisms. Semin. Cell Dev. Biol., 2019, 88, 163-172.
[http://dx.doi.org/10.1016/j.semcdb.2018.02.023] [PMID: 29501617]
[38]
Grönberg, A.; Mahlapuu, M.; Ståhle, M.; Whately-Smith, C.; Rollman, O. Treatment with LL-37 is safe and effective in enhancing healing of hard-to-heal venous leg ulcers: a randomized, placebo-controlled clinical trial. Wound Repair Regen., 2014, 22(5), 613-621.
[http://dx.doi.org/10.1111/wrr.12211] [PMID: 25041740]
[39]
Barter, P.J.; Nicholls, S.; Rye, K.A.; Anantharamaiah, G.M.; Navab, M.; Fogelman, A.M. Antiinflammatory Properties of HDL. Circ Res.,, 2004, 95764e72
[http://dx.doi.org/10.1161/01.RES.0000146094.59640.13]
[40]
Ma, J.; Liao, X.; Lou, B.; Wu, M.P. Role of Apolipoprotein A-I in Protecting against Endotoxin Toxicity. Acta Biochim Biophys Sin.,, 2004, 36419e24.
[http://dx.doi.org/10.1093/abbs/36.6.419]
[41]
Tada, N.; Sakamoto, T.; Kamgami, A.; Mochizuki, K.; Kurosaka, K. Antimicrobial activity of lipoprotein particles containing apolipoprotein A-l. Mol Cell Biochem.,, 1993, 119 171e8.
[http://dx.doi.org/10.1007/978-1-4615-3078-7_23]
[42]
Liao, X.; Lou, B.; Ma, J.; Wu, M. Neutrophil activation can be diminished by apolipoprotein A-I. Life Sci.,, 2005, 77325e35.
[http://dx.doi.org/10.1016/j.lfs.2004.10.066]
[43]
Mineo, C.; Deguchi, H.; Griffin, J.H.; Shaul, P.W. Endothelial and antithrombotic actions of HDL. . Circ Res., 2006, 98 1352e64.
[http://dx.doi.org/10.1161/01.RES.0000225982.01988.93]
[44]
Wadham, C.; Albanese, N.; Roberts, J.; Wang, L.; Bagley, C.J.; Gamble, J.R.; Rye, K.A.; Barter, P.J.; Vadas, M.A.; Xia, P. High density lipoproteins neutralize C-reactive protein proinflammatory activity. Circulation,, 2004, 1092116e22.
[http://dx.doi.org/10.1161/01.CIR.0000127419.45975.26]
[45]
Gomaraschi, M.; Basilico, N.; Sisto, F.; Taramelli, D.; Eligini, S.; Colli, S.; Sirtori, C.R.; Franceschini, G.; Calabresi, L. High-density lipoproteins attenuate interleukin-6 production in endothelial cells exposed to pro-inflammatory stimuli. Biochim Biophys Acta.,, 2005, 1736136e43.
[http://dx.doi.org/10.1016/j.bbalip.2005.08.003]
[46]
Rezaee, F.; Casetta, B.; Levels, J.H.; Speijer, D.; Meijers, J.C. Proteomic analysis of high density lipoprotein. Proteomics.,, 2006,, 6,721e30.
[http://dx.doi.org/10.1002/pmic.200500191]
[47]
Shiflett, A.M.; Bishop, J.R.; Pahwa, A.; Hajduk, S.L. Human high density lipoproteins are platforms for the assembly of multi-component innate immune complexes. J Biol Chem.,, 2005, 28032578e85.
[http://dx.doi.org/10.1074/jbc.M503510200]
[48]
Kelly, B.A.; Harrison, I.; McKnight, A.; Dobson, C.B. Anti-infective activity of apolipoprotein domain derived peptides in vitro: identification of novel antimicrobial peptides related to apolipoprotein B with anti-HIV activity. BMC Immunol., 2010, 11, 13.
[http://dx.doi.org/10.1186/1471-2172-11-13] [PMID: 20298574]
[49]
Bhakdi, S.; Tranum-Jensen, J.; Utermann, G.; Füssle, R. Binding and partial inactivation of Staphylococcus aureus alpha-toxin by human plasma low density lipoprotein. J. Biol. Chem., 1983, 258(9), 5899-5904.
[PMID: 6853557]
[50]
Han, R. Plasma lipoproteins are important components of the immune system. Microbiol. Immunol., 2010, 54(4), 246-253.
[http://dx.doi.org/10.1111/j.1348-0421.2010.00203.x] [PMID: 20377753]
[51]
Omae, Y.; Hanada, Y.; Sekimizu, K.; Kaito, C. Silkworm apolipophorin protein inhibits hemolysin gene expression of Staphylococcus aureus via binding to cell surface lipoteichoic acids. J. Biol. Chem., 2013, 288(35), 25542-25550.
[http://dx.doi.org/10.1074/jbc.M113.495051] [PMID: 23873929]
[52]
Hanada, Y.; Sekimizu, K.; Kaito, C. Silkworm apolipophorin protein inhibits Staphylococcus aureus virulence. J. Biol. Chem., 2011, 286(45), 39360-39369.
[http://dx.doi.org/10.1074/jbc.M111.278416] [PMID: 21937431]
[53]
Thaveeratitham, P.; Plengpanich, W.; Naen-Udorn, W.; Patumraj, S.; Khovidhunkit, W. Effects of human apolipoprotein A-I on endotoxin-induced leukocyte adhesion on endothelial cells in vivo and on the growth of Escherichia coli in vitro. J. Endotoxin Res., 2007, 13(1), 58-64.
[http://dx.doi.org/10.1177/0968051907078611] [PMID: 17621547]
[54]
Sigel, S.; Bunk, S.; Meergans, T.; Doninger, B.; Stich, K.; Stulnig, T.; Derfler, K.; Hoffmann, J.; Deininger, S.; von Aulock, S.; Knapp, S. Apolipoprotein B100 is a suppressor of Staphylococcus aureus-induced innate immune responses in humans and mice. Eur. J. Immunol., 2012, 42(11), 2983-2989.
[http://dx.doi.org/10.1002/eji.201242564] [PMID: 22806614]
[55]
Harris, H.W.; Grunfeld, C.; Feingold, K.R.; Rapp, J.H. Human very low density lipoproteins and chylomicrons can protect against endotoxin-induced death in mice. J. Clin. Invest., 1990, 86(3), 696-702.
[http://dx.doi.org/10.1172/JCI114765] [PMID: 2394827]
[56]
Dobson, C.B.; Itzhaki, R.F. Herpes simplex virus type 1 and Alzheimer’s disease. Neurobiol. Aging, 1999, 20(4), 457-465.
[http://dx.doi.org/10.1016/S0197-4580(99)00055-X] [PMID: 10604441]
[57]
Papareddy, P.; Rydengård, V.; Pasupuleti, M.; Walse, B.; Mörgelin, M.; Chalupka, A.; Malmsten, M.; Schmidtchen, A. Proteolysis of human thrombin generates novel host defense peptides. PLoS Pathog., 2010, 6(4)e1000857
[http://dx.doi.org/10.1371/journal.ppat.1000857] [PMID: 20421939]
[58]
Kasetty, G.; Papareddy, P.; Kalle, M.; Rydengård, V.; Walse, B.; Svensson, B.; Mörgelin, M.; Malmsten, M.; Schmidtchen, A. The C-terminal sequence of several human serine proteases encodes host defense functions. J. Innate Immun., 2011, 3(5), 471-482.
[http://dx.doi.org/10.1159/000327016] [PMID: 21576923]
[59]
Andersson, E.; Rydengård, V.; Sonesson, A.; Mörgelin, M.; Björck, L.; Schmidtchen, A. Antimicrobial activities of heparin-binding peptides. Eur. J. Biochem., 2004, 271(6), 1219-1226.
[http://dx.doi.org/10.1111/j.1432-1033.2004.04035.x] [PMID: 15009200]
[60]
Misra, U.K.; Adlakha, C.L.; Gawdi, G.; McMillian, M.K.; Pizzo, S.V.; Laskowitz, D.T. Apolipoprotein E and mimetic peptide initiate a calcium-dependent signaling response in macrophages. J. Leukoc. Biol., 2001, 70(4), 677-683.
[PMID: 11590206]
[61]
Lynch, J.R.; Tang, W.; Wang, H.; Vitek, M.P.; Bennett, E.R.; Sullivan, P.M.; Warner, D.S.; Laskowitz, D.T. APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response. J. Biol. Chem., 2003, 278(49), 48529-48533.
[http://dx.doi.org/10.1074/jbc.M306923200] [PMID: 14507923]
[62]
Azevedo, O.G.; Oliveira, R.A.; Oliveira, B.C.; Zaja-Milatovic, S.; Araújo, C.V.; Wong, D.V.; Costa, T.B.; Lucena, H.B.; Lima, R.C., Jr; Ribeiro, R.A.; Warren, C.A.; Lima, A.Â.; Vitek, M.P.; Guerrant, R.L.; Oriá, R.B. Apolipoprotein E COG 133 mimetic peptide improves 5-fluorouracil-induced intestinal mucositis. BMC Gastroenterol., 2012, 12, 35.
[http://dx.doi.org/10.1186/1471-230X-12-35] [PMID: 22524518]
[63]
Laskowitz, D.T.; Fillit, H.; Yeung, N.; Toku, K.; Vitek, M.P. Apolipoprotein E-derived peptides reduce CNS inflammation: implications for therapy of neurological disease. Acta Neurol. Scand. Suppl., 2006, 185, 15-20.
[http://dx.doi.org/10.1111/j.1600-0404.2006.00680.x] [PMID: 16866906]
[64]
Fjell, C.D.; Jenssen, H.; Hilpert, K.; Cheung, W.A.; Panté, N.; Hancock, R.E.; Cherkasov, A. Identification of novel antibacterial peptides by chemoinformatics and machine learning. J. Med. Chem., 2009, 52(7), 2006-2015.
[http://dx.doi.org/10.1021/jm8015365] [PMID: 19296598]
[65]
Juretić, D.; Vukičević, D.; Petrov, D.; Novković, M.; Bojović, V.; Lučić, B.; Ilić, N.; Tossi, A. Knowledge-based computational methods for identifying or designing novel, non-homologous antimicrobial peptides. Eur. Biophys. J., 2011, 40(4), 371-385.
[http://dx.doi.org/10.1007/s00249-011-0674-7] [PMID: 21274708]
[66]
Fernandes, F.C.; Rigden, D.J.; Franco, O.L. Prediction of antimicrobial peptides based on the adaptive neuro-fuzzy inference system application. Biopolymers, 2012, 98(4), 280-287.
[http://dx.doi.org/10.1002/bip.22066] [PMID: 23193592]
[67]
Torrent, M.; Di Tommaso, P.; Pulido, D.; Nogués, M.V.; Notredame, C.; Boix, E.; Andreu, D. AMPA: an automated web server for prediction of protein antimicrobial regions. Bioinformatics, 2012, 28(1), 130-131.
[http://dx.doi.org/10.1093/bioinformatics/btr604] [PMID: 22053077]
[68]
Niarchou, A.; Alexandridou, A.; Athanasiadis, E.; Spyrou, G. C-PAmP: large scale analysis and database construction containing high scoring computationally predicted antimicrobial peptides for all the available plant species. PLoS One, 2013, 8(11)e79728
[http://dx.doi.org/10.1371/journal.pone.0079728] [PMID: 24244550]
[69]
Brand, G.D.; Magalhães, M.T.; Tinoco, M.L.; Aragão, F.J.; Nicoli, J.; Kelly, S.M.; Cooper, A.; Bloch, C., Jr Probing protein sequences as sources for encrypted antimicrobial peptides. PLoS One, 2012, 7(9)e45848
[http://dx.doi.org/10.1371/journal.pone.0045848] [PMID: 23029273]
[70]
Ramada, M.H.S.; Brand, G.D.; Abrão, F.Y.; Oliveira, M.; Filho, J.L.C.; Galbieri, R.; Gramacho, K.P.; Prates, M.V.; Bloch, C., Jr Encrypted antimicrobial peptides from plant proteins. Sci. Rep., 2017, 7(1), 13263.
[http://dx.doi.org/10.1038/s41598-017-13685-6] [PMID: 29038449]
[71]
Pane, K.; Durante, L.; Crescenzi, O.; Cafaro, V.; Pizzo, E.; Varcamonti, M.; Zanfardino, A.; Izzo, V.; Di Donato, A.; Notomista, E. Antimicrobial potency of cationic antimicrobial peptides can be predicted from their amino acid composition: Application to the detection of “cryptic” antimicrobial peptides. J. Theor. Biol., 2017, 419, 254-265.
[http://dx.doi.org/10.1016/j.jtbi.2017.02.012] [PMID: 28216428]
[72]
Pane, K.; Sgambati, V.; Zanfardino, A.; Smaldone, G.; Cafaro, V.; Angrisano, T.; Pedone, E.; Di Gaetano, S.; Capasso, D.; Haney, E.F.; Izzo, V.; Varcamonti, M.; Notomista, E.; Hancock, R.E.; Di Donato, A.; Pizzo, E. A new cryptic cationic antimicrobial peptide from human apolipoprotein E with antibacterial activity and immunomodulatory effects on human cells. FEBS J., 2016, 283(11), 2115-2131.
[http://dx.doi.org/10.1111/febs.13725] [PMID: 27028511]
[73]
Zanfardino, A.; Bosso, A.; Gallo, G.; Pistorio, V.; Di Napoli, M.; Gaglione, R.; Dell’Olmo, E.; Varcamonti, M.; Notomista, E.; Arciello, A.; Pizzo, E. Human apolipoprotein E as a reservoir of cryptic bioactive peptides: The case of ApoE 133-167. J. Pept. Sci., 2018, 24(7)e3095
[http://dx.doi.org/10.1002/psc.3095] [PMID: 29900637]
[74]
Gaglione, R.; Dell’Olmo, E.; Bosso, A.; Chino, M.; Pane, K.; Ascione, F.; Itri, F.; Caserta, S.; Amoresano, A.; Lombardi, A.; Haagsman, H.P.; Piccoli, R.; Pizzo, E.; Veldhuizen, E.J.A.; Notomista, E.; Arciello, A. Novel human bioactive peptides identified in Apolipoprotein B: Evaluation of their therapeutic potential. Biochem. Pharmacol., 2017, 130, 34-50.
[http://dx.doi.org/10.1016/j.bcp.2017.01.009] [PMID: 28131846]
[75]
Gaglione, R.; Cesaro, A.; Dell’Olmo, E.; Della Ventura, B.; Casillo, A.; Di Girolamo, R.; Velotta, R.; Notomista, E.; Veldhuizen, E.J.A.; Corsaro, M.M.; De Rosa, C.; Arciello, A. Effects of human antimicrobial cryptides identified in apolipoprotein B depend on specific features of bacterial strains. Sci. Rep., 2019, 9(1), 6728.
[http://dx.doi.org/10.1038/s41598-019-43063-3] [PMID: 31040323]
[76]
Mahley, R.W.; Apolipoprotein, E. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science, 1988, 240(4852), 622-630.
[http://dx.doi.org/10.1126/science.3283935] [PMID: 3283935]
[77]
Phillips, M.C. Apolipoprotein E isoforms and lipoprotein metabolism. IUBMB Life, 2014, 66(9), 616-623.
[http://dx.doi.org/10.1002/iub.1314] [PMID: 25328986]
[78]
Sofat, R.; Cooper, J.A.; Kumari, M.; Casas, J.P.; Mitchell, J.P.; Acharya, J.; Thom, S.; Hughes, A.D.; Humphries, S.E.; Hingorani, A.D. Circulating apolipoprotein e concentration and cardiovascular disease risk: meta-analysis of results from three studies. PLoS Med., 2016, 13(10)e1002146
[http://dx.doi.org/10.1371/journal.pmed.1002146] [PMID: 27755538]
[79]
Dafnis, I.; Argyri, L.; Sagnou, M.; Tzinia, A.; Tsilibary, E.C.; Stratikos, E.; Chroni, A. The ability of apolipoprotein E fragments to promote intraneuronal accumulation of amyloid beta peptide 42 is both isoform and size-specific. Sci. Rep., 2016, 6, 30654.
[http://dx.doi.org/10.1038/srep30654] [PMID: 27476701]
[80]
Liu, C.C.; Liu, C.C.; Kanekiyo, T.; Xu, H.; Bu, G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol., 2013, 9(2), 106-118.
[http://dx.doi.org/10.1038/nrneurol.2012.263] [PMID: 23296339]
[81]
Hashimoto, T.; Serrano-Pozo, A.; Hori, Y.; Adams, K.W.; Takeda, S.; Banerji, A.O.; Mitani, A.; Joyner, D.; Thyssen, D.H.; Bacskai, B.J.; Frosch, M.P.; Spires-Jones, T.L.; Finn, M.B.; Holtzman, D.M.; Hyman, B.T. Apolipoprotein E, especially apolipoprotein E4, increases the oligomerization of amyloid β peptide. J. Neurosci., 2012, 32(43), 15181-15192.
[http://dx.doi.org/10.1523/JNEUROSCI.1542-12.2012] [PMID: 23100439]
[82]
Mahley, R.W. Apolipoprotein E: from cardiovascular disease to neurodegenerative disorders. J. Mol. Med. (Berl.), 2016, 94(7), 739-746.
[http://dx.doi.org/10.1007/s00109-016-1427-y] [PMID: 27277824]
[83]
Baitsch, D.; Bock, H.H.; Engel, T.; Telgmann, R.; Müller-Tidow, C.; Varga, G.; Bot, M.; Herz, J.; Robenek, H.; von Eckardstein, A.; Nofer, J.R. Apolipoprotein E induces antiinflammatory phenotype in macrophages. Arterioscler. Thromb. Vasc. Biol., 2011, 31(5), 1160-1168.
[http://dx.doi.org/10.1161/ATVBAHA.111.222745] [PMID: 21350196]
[84]
Curtiss, L.K.; Forte, T.M.; Davis, P.A. Cord blood plasma lipoproteins inhibit mitogen-stimulated lymphocyte proliferation. J. Immunol., 1984, 133(3), 1379-1384.
[PMID: 6430997]
[85]
Tenger, C.; Zhou, X. Apolipoprotein E modulates immune activation by acting on the antigen-presenting cell. Immunology, 2003, 109(3), 392-397.
[http://dx.doi.org/10.1046/j.1365-2567.2003.01665.x] [PMID: 12807485]
[86]
Riddell, D.R.; Graham, A.; Owen, J.S. Apolipoprotein E inhibits platelet aggregation through the L-arginine:nitric oxide pathway. Implications for vascular disease. J. Biol. Chem., 1997, 272(1), 89-95.
[http://dx.doi.org/10.1074/jbc.272.1.89] [PMID: 8995232]
[87]
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.; Besra, G.S.; Kent, S.C.; Moody, D.B.; Brenner, M.B. Apolipoprotein-mediated pathways of lipid antigen presentation. Nature, 2005, 437(7060), 906-910.
[http://dx.doi.org/10.1038/nature04001] [PMID: 16208376]
[88]
Marques, M.A.; Owens, P.A.; Crutcher, K.A. Progress toward identification of protease activity involved in proteolysis of apolipoprotein e in human brain. J. Mol. Neurosci., 2004, 24(1), 73-80.
[http://dx.doi.org/10.1385/JMN:24:1:073] [PMID: 15314253]
[89]
Elliott, D.A.; Tsoi, K.; Holinkova, S.; Chan, S.L.; Kim, W.S.; Halliday, G.M.; Rye, K.A.; Garner, B. Isoform-specific proteolysis of apolipoprotein-E in the brain. Neurobiol. Aging, 2011, 32(2), 257-271.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.02.006] [PMID: 19278755]
[90]
Clay, M.A.; Anantharamaiah, G.M.; Mistry, M.J.; Balasubramaniam, A.; Harmony, J.A. Localization of a domain in apolipoprotein E with both cytostatic and cytotoxic activity. Biochemistry, 1995, 34(35), 11142-11151.
[http://dx.doi.org/10.1021/bi00035a020] [PMID: 7669772]
[91]
Datta, G.; Chaddha, M.; Garber, D.W.; Chung, B.H.; 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(1), 213-220.
[http://dx.doi.org/10.1021/bi991209w] [PMID: 10625496]
[92]
Dobson, C.B.; Sales, S.D.; Hoggard, P.; Wozniak, M.A.; Crutcher, K.A. The receptor-binding region of human apolipoprotein E has direct anti-infective activity. J. Infect. Dis., 2006, 193(3), 442-450.
[http://dx.doi.org/10.1086/499280] [PMID: 16388493]
[93]
Forbes, S.; McBain, A.J.; Felton-Smith, S.; Jowitt, T.A.; Birchenough, H.L.; Dobson, C.B. Comparative surface antimicrobial properties of synthetic biocides and novel human apolipoprotein E derived antimicrobial peptides. Biomaterials, 2013, 34(22), 5453-5464.
[http://dx.doi.org/10.1016/j.biomaterials.2013.03.087] [PMID: 23623325]
[94]
Wilson, C.; Wardell, M.R.; Weisgraber, K.H.; Mahley, R.W.; Agard, D.A. Three-dimensional structure of the LDL receptor-binding domain of human apolipoprotein E. Science, 1991, 252(5014), 1817-1822.
[http://dx.doi.org/10.1126/science.2063194] [PMID: 2063194]
[95]
Raussens, V.; Slupsky, C.M.; Ryan, R.O.; Sykes, B.D. NMR structure and dynamics of a receptor-active apolipoprotein E peptide. J. Biol. Chem., 2002, 277(32), 29172-29180.
[http://dx.doi.org/10.1074/jbc.M204043200] [PMID: 12036962]
[96]
Futamura, M.; Dhanasekaran, P.; Handa, T.; Phillips, M.C.; Lund-Katz, S.; Saito, H. Two-step mechanism of binding of apolipoprotein E to heparin: implications for the kinetics of apolipoprotein E-heparan sulfate proteoglycan complex formation on cell surfaces. J. Biol. Chem., 2005, 280(7), 5414-5422.
[http://dx.doi.org/10.1074/jbc.M411719200] [PMID: 15583000]
[97]
Azuma, M.; Kojimab, T.; Yokoyama, I.; Tajiri, H.; Yoshikawa, K.; Saga, S.; Del Carpio, C.A. A synthetic peptide of human apoprotein E with antibacterial activity. Peptides, 2000, 21(3), 327-330.
[http://dx.doi.org/10.1016/S0196-9781(00)00165-0] [PMID: 10793212]
[98]
Kojima, T.; Fujimitsu, Y.; Kojima, H. Anti-tumor activity of an antibiotic peptide derived from apoprotein E. In Vivo, 2005, 19(1), 261-264.
[PMID: 15796184]
[99]
Laskowitz, D.T.; Thekdi, A.D.; Thekdi, S.D.; Han, S.K.; Myers, J.K.; Pizzo, S.V.; Bennett, E.R. Downregulation of microglial activation by apolipoprotein E and apoE-mimetic peptides. Exp. Neurol., 2001, 167(1), 74-85.
[http://dx.doi.org/10.1006/exnr.2001.7541] [PMID: 11161595]
[100]
Sarantseva, S.; Timoshenko, S.; Bolshakova, O.; Karaseva, E.; Rodin, D.; Schwarzman, A.L.; Vitek, M.P. Apolipoprotein E-mimetics inhibit neurodegeneration and restore cognitive functions in a transgenic Drosophila model of Alzheimer’s disease. PLoS One, 2009, 4(12)e8191
[http://dx.doi.org/10.1371/journal.pone.0008191] [PMID: 19997607]
[101]
Wu, Y.; Pang, J.; Peng, J.; Cao, F.; Vitek, M.P.; Li, F.; Jiang, Y.; Sun, X. An apoE-derived mimic peptide, COG1410, alleviates early brain injury via reducing apoptosis and neuroinflammation in a mouse model of subarachnoid hemorrhage. Neurosci. Lett., 2016, 627, 92-99.
[http://dx.doi.org/10.1016/j.neulet.2016.05.058] [PMID: 27241720]
[102]
Wang, X.; Luebbe, P.; Gruenstein, E.; Zemlan, F.; Apolipoprotein, E. Apolipoprotein E (ApoE) peptide regulates tau phosphorylation via two different signaling pathways. J. Neurosci. Res., 1998, 51(5), 658-665.
[http://dx.doi.org/10.1002/(SICI)1097-4547(19980301)51:5<658:AID-JNR13>3.0.CO;2-Z] [PMID: 9512010]
[103]
Bhattacharjee, P.S.; Neumann, D.M.; Foster, T.P.; Clement, C.; Singh, G.; Thompson, H.W.; Kaufman, H.E.; Hill, J.M. Effective treatment of ocular HSK with a human apolipoprotein E mimetic peptide in a mouse eye model. Invest. Ophthalmol. Vis. Sci., 2008, 49(10), 4263-4268.
[http://dx.doi.org/10.1167/iovs.08-2077] [PMID: 18515564]
[104]
Kelly, B.A.; Neil, S.J.; McKnight, A.; Santos, J.M.; Sinnis, P.; Jack, E.R.; Middleton, D.A.; Dobson, C.B. Apolipoprotein E-derived antimicrobial peptide analogues with altered membrane affinity and increased potency and breadth of activity. FEBS J., 2007, 274(17), 4511-4525.
[http://dx.doi.org/10.1111/j.1742-4658.2007.05981.x] [PMID: 17681018]
[105]
Rossignol, T.; Kelly, B.; Dobson, C.; d’Enfert, C. Endocytosis-mediated vacuolar accumulation of the human ApoE apolipoprotein-derived ApoEdpL-W antimicrobial peptide contributes to its antifungal activity in Candida albicans. Antimicrob. Agents Chemother., 2011, 55(10), 4670-4681.
[http://dx.doi.org/10.1128/AAC.00319-11] [PMID: 21807970]
[106]
Wang, C.Q.; Yang, C.S.; Yang, Y.; Pan, F.; He, L.Y.; Wang, A.M. An apolipoprotein E mimetic peptide with activities against multidrug-resistant bacteria and immunomodulatory effects. J. Pept. Sci., 2013, 19(12), 745-750.
[http://dx.doi.org/10.1002/psc.2570] [PMID: 24243597]
[107]
Zhao, W.; Du, F.; Zhang, M.; Sun, S.; Yu, H.; Fan, D. A new recombinant human apolipoprotein E mimetic peptide with high-density lipoprotein binding and function enhancing activity. Exp. Biol. Med. (Maywood), 2011, 236(12), 1468-1476.
[http://dx.doi.org/10.1258/ebm.2011.011169] [PMID: 22087021]
[108]
Hafiane, A.; Bielicki, J.K.; Johansson, J.O.; Genest, J. Novel Apo E-Derived ABCA1 Agonist Peptide (CS-6253) Promotes Reverse Cholesterol Transport and Induces Formation of preβ-1 HDL In Vitro. PLoS One, 2015, 10(7)e0131997
[http://dx.doi.org/10.1371/journal.pone.0131997] [PMID: 26207756]
[109]
Liu, S.; McCormick, K.D.; Zhao, W.; Zhao, T.; Fan, D.; Wang, T. Human apolipoprotein E peptides inhibit hepatitis C virus entry by blocking virus binding. Hepatology, 2012, 56(2), 484-491.
[http://dx.doi.org/10.1002/hep.25665] [PMID: 22334503]
[110]
Xu, Y.; Liu, H.; Liu, M.; Li, F.; Liu, L.; Du, F.; Fan, D.; Yu, H. A human apolipoprotein E mimetic peptide reduces atherosclerosis in aged apolipoprotein E null mice. Am. J. Transl. Res., 2016, 8(8), 3482-3492.
[PMID: 27648138]
[111]
Shih, I.L.; Lees, R.S.; Chang, M.Y.; Lees, A.M. Focal accumulation of an apolipoprotein B-based synthetic oligopeptide in the healing rabbit arterial wall. Proc. Natl. Acad. Sci. USA, 1990, 87(4), 1436-1440.
[http://dx.doi.org/10.1073/pnas.87.4.1436] [PMID: 2304909]
[112]
Law, A.; Scott, J. A cross-species comparison of the apolipoprotein B domain that binds to the LDL receptor. J. Lipid Res., 1990, 31(6), 1109-1120.
[PMID: 2373961]
[113]
Zeng, Z.; Cao, B.; Guo, X.; Li, W.; Li, S.; Chen, J.; Zhou, W.; Zheng, C.; Wei, Y. Apolipoprotein B-100 peptide 210 antibody inhibits atherosclerosis by regulation of macrophages that phagocytize oxidized lipid. Am. J. Transl. Res., 2018, 10(6), 1817-1828.
[PMID: 30018722]
[114]
Chen, S.H.; Yang, C.Y.; Chen, P.F.; Setzer, D.; Tanimura, M.; Li, W.H.; Gotto, A.M., Jr; Chan, L. The complete cDNA and amino acid sequence of human apolipoprotein B-100. J. Biol. Chem., 1986, 261(28), 12918-12921.
[PMID: 3759943]
[115]
Yang, C.Y.; Gu, Z.W.; Weng, S.A.; Kim, T.W.; Chen, S.H.; Pownall, H.J.; Sharp, P.M.; Liu, S.W.; Li, W.H.; Gotto, A.M., Jr Structure of apolipoprotein B-100 of human low density lipoproteins. Arteriosclerosis, 1989, 9(1), 96-108.
[http://dx.doi.org/10.1161/01.ATV.9.1.96] [PMID: 2912424]
[116]
Tillotson, G.S.; Dorrian, I.; Blondeau, J. Fluoroquinolone resistance: mechanisms and epidemiology. J. Med. Microbiol., 1997, 46(6), 457-461.
[PMID: 9379475]
[117]
Torres, M.D.T.; Sothiselvam, S.; Lu, T.K.; de la Fuente-Nunez, C. Peptide Design Principles for Antimicrobial Applications. J. Mol. Biol., 2019, 431(18), 3547-3567.
[http://dx.doi.org/10.1016/j.jmb.2018.12.015] [PMID: 30611750]
[118]
de la Fuente-Nunez, C.; Torres, M.D.; Mojica, F.J.; Lu, T.K. Next-generation precision antimicrobials: towards personalized treatment of infectious diseases. Curr. Opin. Microbiol., 2017, 37, 95-102.
[http://dx.doi.org/10.1016/j.mib.2017.05.014] [PMID: 28623720]
[119]
de la Fuente-Núñez, C.; Cardoso, M.H.; de Souza Cândido, E.; Franco, O.L.; Hancock, R.E. Synthetic antibiofilm peptides. Biochim. Biophys. Acta, 2016, 1858(5), 1061-1069.
[http://dx.doi.org/10.1016/j.bbamem.2015.12.015] [PMID: 26724202]
[120]
Pane, K.; Cafaro, V.; Avitabile, A.; Torres, M.T.; Vollaro, A.; De Gregorio, E.; Catania, M.R.; Di Maro, A.; Bosso, A.; Gallo, G.; Zanfardino, A.; Varcamonti, M.; Pizzo, E.; Di Donato, A.; Lu, T.K.; de la Fuente-Nunez, C.; Notomista, E. Identification of Novel Cryptic Multifunctional Antimicrobial Peptides from the Human Stomach Enabled by a Computational-Experimental Platform. ACS Synth. Biol., 2018, 7(9), 2105-2115.
[http://dx.doi.org/10.1021/acssynbio.8b00084] [PMID: 30124040]
[121]
Reffuveille, F.; de la Fuente-Núñez, C.; Mansour, S.; Hancock, R.E. A broad-spectrum antibiofilm peptide enhances antibiotic action against bacterial biofilms. Antimicrob. Agents Chemother., 2014, 58(9), 5363-5371.
[http://dx.doi.org/10.1128/AAC.03163-14] [PMID: 24982074]
[122]
de la Fuente-Núñez, C.; Reffuveille, F.; Fernández, L.; Hancock, R.E. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr. Opin. Microbiol., 2013, 16(5), 580-589.
[http://dx.doi.org/10.1016/j.mib.2013.06.013] [PMID: 23880136]
[123]
de la Fuente-Núñez, C.; Korolik, V.; Bains, M.; Nguyen, U.; Breidenstein, E.B.; Horsman, S.; Lewenza, S.; Burrows, L.; Hancock, R.E. Inhibition of bacterial biofilm formation and swarming motility by a small synthetic cationic peptide. Antimicrob. Agents Chemother., 2012, 56(5), 2696-2704.
[http://dx.doi.org/10.1128/AAC.00064-12] [PMID: 22354291]
[124]
Sadovskaya, I.; Brisson, J.R.; Thibault, P.; Richards, J.C.; Lam, J.S.; Altman, E. Structural characterization of the outer core and the O-chain linkage region of lipopolysaccharide from Pseudomonas aeruginosa serotype O5. Eur. J. Biochem., 2000, 267(6), 1640-1650.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01156.x] [PMID: 10712594]
[125]
Biedzka-Sarek, M.; Metso, J.; Kateifides, A.; Meri, T.; Jokiranta, T.S.; Muszyński, A.; Radziejewska-Lebrecht, J.; Zannis, V.; Skurnik, M.; Jauhiainen, M. Apolipoprotein A-I exerts bactericidal activity against Yersinia enterocolitica serotype O:3. J. Biol. Chem., 2011, 286(44), 38211-38219.
[http://dx.doi.org/10.1074/jbc.M111.249482] [PMID: 21896489]
[126]
Singh, I.P.; Chopra, A.K.; Coppenhaver, D.H.; Ananatharamaiah, G.M.; Baron, S. Innate antiviral defenses in body fluids and tissues. Antiviral Res., 1999, 42, 211-218.
[http://dx.doi.org/10.1016/S0166-3542(99)00032-7] [PMID: 10443533]
[127]
Pérez-Morga, D.; Vanhollebeke, B.; Paturiaux-Hanocq, F.; Nolan, D.P.; Lins, L.; Homblé, F.; Vanhamme, L.; Tebabi, P.; Pays, A.; Poelvoorde, P.; Jacquet, A.; Brasseur, R.; Pays, E. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science, 2005, 309(5733), 469-472.
[http://dx.doi.org/10.1126/science.1114566] [PMID: 16020735]
[128]
Hubsch, A.P.; Casas, A.T.; Doran, J.E. Protective effects of reconstituted high-density lipoprotein in rabbit gram-negative bacteremia models. J. Lab. Clin. Med., 1995, 126(6), 548-558.
[PMID: 7490514]
[129]
Ulevitch, R.J.; Johnston, A.R.; Weinstein, D.B. New function for high density lipoproteins. Isolation and characterization of a bacterial lipopolysaccharide-high density lipoprotein complex formed in rabbit plasma. J. Clin. Invest., 1981, 67(3), 827-837.
[http://dx.doi.org/10.1172/JCI110100] [PMID: 7204557]
[130]
Sammalkorpi, K.; Valtonen, V.; Kerttula, Y.; Nikkilä, E.; Taskinen, M.R. Changes in serum lipoprotein pattern induced by acute infections. Metabolism, 1988, 37(9), 859-865.
[http://dx.doi.org/10.1016/0026-0495(88)90120-5] [PMID: 3419323]
[131]
Mendall, M.A.; Goggin, P.M.; Molineaux, N.; Levy, J.; Toosy, T.; Strachan, D.; Camm, A.J.; Northfield, T.C. Relation of Helicobacter pylori infection and coronary heart disease. Br. Heart J., 1994, 71(5), 437-439.
[http://dx.doi.org/10.1136/hrt.71.5.437] [PMID: 8011406]
[132]
Navab, M.; Anantharamaiah, G.M.; Reddy, S.T.; Fogelman, A.M. Apolipoprotein A-I mimetic peptides and their role in atherosclerosis prevention. Nat. Clin. Pract. Cardiovasc. Med., 2006, 3(10), 540-547.
[http://dx.doi.org/10.1038/ncpcardio0661] [PMID: 16990839]
[133]
Van Lenten, B.J.; Wagner, A.C.; Navab, M.; Anantharamaiah, G.M.; Hui, E.K.; Nayak, D.P.; Fogelman, A.M. D-4F, an apolipoprotein A-I mimetic peptide, inhibits the inflammatory response induced by influenza A infection of human type II pneumocytes. Circulation, 2004, 110(20), 3252-3258.
[http://dx.doi.org/10.1161/01.CIR.0000147232.75456.B3] [PMID: 15533864]
[134]
Srinivas, R.V.; Birkedal, B.; Owens, R.J.; Anantharamaiah, G.M.; Segrest, J.P.; Compans, R.W. Antiviral effects of apolipoprotein A-I and its synthetic amphipathic peptide analogs. Virology, 1990, 176(1), 48-57.
[http://dx.doi.org/10.1016/0042-6822(90)90229-K] [PMID: 2158697]
[135]
Srinivas, R.V.; Venkatachalapathi, Y.V.; Rui, Z.; Owens, R.J.; Gupta, K.B.; Srinivas, S.K.; Anantharamaiah, G.M.; Segrest, J.P.; Compans, R.W. Inhibition of virus-induced cell fusion by apolipoprotein A-I and its amphipathic peptide analogs. J. Cell. Biochem., 1991, 45(2), 224-237.
[http://dx.doi.org/10.1002/jcb.240450214] [PMID: 1647394]
[136]
Balestrieri, M.; Cigliano, L.; Simone, M.L.; Dale, B.; Abrescia, P. Haptoglobin inhibits lecithin-cholesterol acyltransferase in human ovarian follicular fluid. Mol. Reprod. Dev., 2001, 59(2), 186-191.
[http://dx.doi.org/10.1002/mrd.1021] [PMID: 11389553]
[137]
Spagnuolo, M.S.; Cigliano, L.; Abrescia, P. The binding of haptoglobin to apolipoprotein AI: influence of hemoglobin and concanavalin A. Biol. Chem., 2003, 384(12), 1593-1596.
[http://dx.doi.org/10.1515/BC.2003.176] [PMID: 14719801]
[138]
Giblett, E.R. The haptoglobin system. Ser. Haematol., 1968, 1, 3-20.
[139]
Nagel, R.L.; Gibson, Q.H. The binding of hemoglobin to haptoglobin and its relation to subunit dissociation of hemoglobin. J. Biol. Chem., 1971, 246(1), 69-73.
[PMID: 5541775]
[140]
Langlois, M.R.; Delanghe, J.R. Biological and clinical significance of haptoglobin polymorphism in humans. Clin. Chem., 1996, 42(10), 1589-1600.
[http://dx.doi.org/10.1093/clinchem/42.10.1589] [PMID: 8855140]
[141]
Kristiansen, M.; Graversen, J.H.; Jacobsen, C.; Sonne, O.; Hoffman, H.J.; Law, S.K.; Moestrup, S.K. Identification of the haemoglobin scavenger receptor. Nature, 2001, 409(6817), 198-201.
[http://dx.doi.org/10.1038/35051594] [PMID: 11196644]
[142]
Gutteridge, J.M.C. The antioxidant activity of haptoglobin towards haemoglobin-stimulated lipid peroxidation. Biochim. Biophys. Acta, 1987, 917(2), 219-223.
[http://dx.doi.org/10.1016/0005-2760(87)90125-1] [PMID: 2879568]
[143]
Alayash, A.I. Redox biology of blood. Antioxid. Redox Signal., 2004, 6(6), 941-943.
[PMID: 15548891]
[144]
Salvatore, A.; Cigliano, L.; Bucci, E.M.; Corpillo, D.; Velasco, S.; Carlucci, A.; Pedone, C.; Abrescia, P. Haptoglobin binding to apolipoprotein A-I prevents damage from hydroxyl radicals on its stimulatory activity of the enzyme lecithin-cholesterol acyl-transferase. Biochemistry, 2007, 46(39), 11158-11168.
[http://dx.doi.org/10.1021/bi7006349] [PMID: 17824618]
[145]
Cigliano, L.; Pugliese, C.R.; Spagnuolo, M.S.; Palumbo, R.; Abrescia, P. Haptoglobin binds the antiatherogenic protein apolipoprotein E - impairment of apolipoprotein E stimulation of both lecithin:cholesterol acyltransferase activity and cholesterol uptake by hepatocytes. FEBS J., 2009, 276(21), 6158-6171.
[http://dx.doi.org/10.1111/j.1742-4658.2009.07319.x] [PMID: 19758344]
[146]
Sorci-Thomas, M.G.; Curtiss, L.; Parks, J.S.; Thomas, M.J.; Kearns, M.W.; Landrum, M. The hydrophobic face orientation of apolipoprotein A-I amphipathic helix domain 143-164 regulates lecithin:cholesterol acyltransferase activation. J. Biol. Chem., 1998, 273(19), 11776-11782.
[http://dx.doi.org/10.1074/jbc.273.19.11776] [PMID: 9565601]
[147]
Spagnuolo, M.S.; Cigliano, L.; D’Andrea, L.D.; Pedone, C.; Abrescia, P. Assignment of the binding site for haptoglobin on apolipoprotein A-I. J. Biol. Chem., 2005, 280(2), 1193-1198.
[http://dx.doi.org/10.1074/jbc.M411390200] [PMID: 15533931]
[148]
Spagnuolo, M.S.; Di Stasi, R.; De Rosa, L.; Maresca, B.; Cigliano, L.; D’Andrea, L.D. Analysis of the haptoglobin binding region on the apolipoprotein A-I-derived P2a peptide. J. Pept. Sci., 2013, 19(4), 220-226.
[http://dx.doi.org/10.1002/psc.2487] [PMID: 23420675]


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Article Details

VOLUME: 20
ISSUE: 14
Year: 2020
Published on: 26 April, 2020
Page: [1324 - 1337]
Pages: 14
DOI: 10.2174/1568026620666200427091454
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