An Overview of the Loading Efficacy of Cationic Lipids with Milk Proteins: A Potential Application for Lipid Delivery

Author(s): Penprapa Chanphai, Philippe Bourassa, Heidar Ali Tajmir-Riahi*

Journal Name: Current Medicinal Chemistry

Volume 27 , Issue 24 , 2020


DOI : 10.2174/0929867325666180608122439

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Abstract:

In this review, the loading efficacies of helper and Cationic Lipids Cholesterol (CHOL), 1,2-dioleoyl-3-trimethylammonium-propane (DOTAP), Dioctadecyl Dimethyl- Ammonium Bromide (DDAB) and Dioleoyl Phosphatidylethanolamine (DOPE) with milk β- lactoglobulin, α-casein and β-casein were compared in aqueous solution at physiological conditions. Structural analysis showed that lipids bind milk proteins via hydrophilic, hydrophobic and H-bonding contacts with DOTAP and DDAB forming more stable protein conjugates. Loading efficacy was 30-50% and enhanced with cationic lipids. Lipid conjugation altered protein conformation, causing a partial protein structural destabilization. Milk proteins are capable of transporting lipids in vitro.

Keywords: Milk protein, lipid, loading efficacy, spectroscopy, modeling, Cationic Lipids Cholesterol.

[1]
Saliba, A.E.; Vonkova, I.; Gavin, A.C. The systematic analysis of protein-lipid interactions comes of age. Nat. Rev. Mol. Cell Biol., 2015, 16(12), 753-761.
[http://dx.doi.org/10.1038/nrm4080] [PMID: 26507169]
[2]
Montoya, M. TALIying lipid-protein interactions. Nat. Struct. Mol. Biol., 2014, 21, 19-20.
[http://dx.doi.org/10.1038/nsmb.2761]
[3]
Gonen, T.; Cheng, Y.; Sliz, P.; Hiroaki, Y.; Fujiyoshi, Y.; Harrison, S.C.; Walz, T. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature, 2005, 438(7068), 633-638.
[http://dx.doi.org/10.1038/nature04321] [PMID: 16319884]
[4]
Hsia, C.Y.; Richards, M.J.; Daniel, S. A review of traditional and emerging methods to characterize lipid–protein interactions in biological membranes. Anal. Methods, 2015, 7, 7076-7094.
[http://dx.doi.org/10.1039/C5AY00599J]
[5]
Lee, A.G. Lipid-protein interactions. Biochem. Soc. Trans., 2011, 39(3), 761-766.
[http://dx.doi.org/10.1042/BST0390761] [PMID: 21599646]
[6]
Lee, A.G. Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta, 2003, 1612(1), 1-40.
[http://dx.doi.org/10.1016/S0005-2736(03)00056-7] [PMID: 12729927]
[7]
Smith, A.W. Lipid-protein interactions in biological membranes: a dynamic perspective. Biochim. Biophys. Acta, 2012, 1818(2), 172-177.
[http://dx.doi.org/10.1016/j.bbamem.2011.06.015] [PMID: 21763269]
[8]
Sansom, M.S.; Bond, P.J.; Deol, S.S.; Grottesi, A.; Haider, S.; Sands, Z.A. Molecular simulations and lipid-protein interactions: potassium channels and other membrane proteins. Biochem. Soc. Trans., 2005, 33(Pt 5), 916-920.
[http://dx.doi.org/10.1042/BST0330916] [PMID: 16246010]
[9]
Páli, T.; Kóta, Z. Studying lipid-protein interactions with electron paramagnetic resonance spectroscopy of spin-labeled lipids. Methods Mol. Biol., 2013, 974, 297-328.
[http://dx.doi.org/10.1007/978-1-62703-275-9_14] [PMID: 23404282]
[10]
Schuler, M.A.; Denisov, I.G.; Sligar, S.G. Nanodiscs as a new tool to examine lipid-protein interactions. Methods Mol. Biol., 2013, 974, 415-433.
[http://dx.doi.org/10.1007/978-1-62703-275-9_18] [PMID: 23404286]
[11]
Waninge, R.; Walstra, P.; Bastiaans, J.; Nieuwenhuijse, H.; Nylander, T.; Paulsson, M.; Bergenståhl, B. Competitive adsorption between β-casein or β-lactoglobulin and model milk membrane lipids at oil-water interfaces. J. Agric. Food Chem., 2005, 53(3), 716-724.
[http://dx.doi.org/10.1021/jf049267y] [PMID: 15686425]
[12]
Bertram, Y.F.; Norris, C.S.; MacGibbon, A.K.H. Protein and lipid composition of bovine milk-fat-globule membrane. Int. Dairy J., 2007, 17, 275-288.
[http://dx.doi.org/10.1016/j.idairyj.2006.05.004]
[13]
Fang, Y.; Dalgleish, D.G. Studies on interactions between phosphatidylcholine, and casein. Langmuir, 1995, 11, 75-79.
[http://dx.doi.org/10.1021/la00001a016]
[14]
Rodríguez Patino, J.M.; Sánchez, C.C.; Rodríguez Niño, M.R. Analysis of β-casein-monopalmitin mixed films at the air-water interface. J. Agric. Food Chem., 1999, 47(12), 4998-5008.
[http://dx.doi.org/10.1021/jf9902696] [PMID: 10606564]
[15]
Charbonneau, D.M.; Tajmir-Riahi, H.A. Study on the interaction of cationic lipids with bovine serum albumin. J. Phys. Chem. B, 2010, 114(2), 1148-1155.
[http://dx.doi.org/10.1021/jp910077h] [PMID: 19961210]
[16]
Charbonneau, D.; Beauregard, M.; Tajmir-Riahi, H.A. Structural analysis of human serum albumin complexes with cationic lipids. J. Phys. Chem. B, 2009, 113(6), 1777-1784.
[http://dx.doi.org/10.1021/jp8092012] [PMID: 19143492]
[17]
Dalgleish, D.G. On the structural models of bovine casein micelles- review and possible improvements. Soft Matter, 2011, 7, 2265-2272.
[http://dx.doi.org/10.1039/C0SM00806K]
[18]
McKenzie, H.A.; Sawyer, W.H. Effect of pH on β-lactoglobulins. Nature, 1967, 214(5093), 1101-1104.
[http://dx.doi.org/10.1038/2141101a0] [PMID: 6053067]
[19]
Kontopidis, G.; Holt, C.; Sawyer, L. Invited review: β-lactoglobulin: binding properties, structure, and function. J. Dairy Sci., 2004, 87(4), 785-796.
[http://dx.doi.org/10.3168/jds.S0022-0302(04)73222-1] [PMID: 15259212]
[20]
Jameson, G.B.; Adams, J.J.; Creamer, L.K. Flexibility, functionality and hydrophobicity of bovine beta-lactoglobulin. Int. Dairy J., 2002, 12, 319-329.
[http://dx.doi.org/10.1016/S0958-6946(02)00028-6]
[21]
Loch, J.I.; Bonarek, P.; Polit, A.; Świątek, S.; Czub, M.; Ludwikowska, M.; Lewiński, K. Conformational variability of goat β-lactoglobulin: crystallographic and thermodynamic studies. Int. J. Biol. Macromol., 2015, 72, 1283-1291.
[http://dx.doi.org/10.1016/j.ijbiomac.2014.10.031] [PMID: 25450833]
[22]
Hasni, I.; Bourassa, P.; Tajmir-Riahi, H.A. Binding of cationic lipids to milk β-lactoglobulin. J. Phys. Chem. B, 2011, 115(20), 6683-6690.
[http://dx.doi.org/10.1021/jp200045h] [PMID: 21542594]
[23]
Essemine, J.; Hasni, I.; Carpentier, R.; Thomas, T.J.; Tajmir-Riahi, H.A. Binding of biogenic and synthetic polyamines to β-lactoglobulin. Int. J. Biol. Macromol., 2011, 49(2), 201-209.
[http://dx.doi.org/10.1016/j.ijbiomac.2011.04.016] [PMID: 21569792]
[24]
Zúñiga, R.N.; Tolkach, A.; Kulozik, U.; Aguilera, J.M. Kinetics of formation and physicochemical characterization of thermally-induced β-lactoglobulin aggregates. J. Food Sci., 2010, 75(5), E261-E268.
[PMID: 20629872]
[25]
Bateman, L.; Ye, A.; Singh, H. In vitro digestion of β-lactoglobulin fibrils formed by heat treatment at low pH. J. Agric. Food Chem., 2010, 58(17), 9800-9808.
[http://dx.doi.org/10.1021/jf101722t] [PMID: 20684554]
[26]
Veerman, C.; Ruis, H.; Sagis, L.M.; van der Linden, E. Effect of electrostatic interactions on the percolation concentration of fibrillar beta-lactoglobulin gels. Biomacromolecules, 2002, 3(4), 869-873.
[http://dx.doi.org/10.1021/bm025533+] [PMID: 12099836]
[27]
Zappone, B.; De Santo, M.P.; Labate, C.; Rizzutia, B.; Guzzi, R. Catalytic activity of copper ions in the amyloid fibrillation of beta-lactoglobulin. Soft Matter, 2013, 9, 2412-2419.
[http://dx.doi.org/10.1039/c2sm27408f]
[28]
Lexis, M.; Willenbacher, N. Relating foam and interfacial rheological properties of β-lactoglobulin solutions. Soft Matter, 2014, 10(48), 9626-9636.
[http://dx.doi.org/10.1039/C4SM01972E] [PMID: 25363684]
[29]
Uversky, V.N. Natively unfolded proteins: a point where biology waits for physics. Protein Sci., 2002, 11(4), 739-756.
[http://dx.doi.org/10.1110/ps.4210102] [PMID: 11910019]
[30]
Curley, D.M.; Kumosinski, T.F.; Unruh, J.J.; Farrell, H.M., Jr Changes in the secondary structure of bovine casein by Fourier transform infrared spectroscopy: effects of calcium and temperature. J. Dairy Sci., 1998, 81(12), 3154-3162.
[http://dx.doi.org/10.3168/jds.S0022-0302(98)75881-3] [PMID: 9891263]
[31]
Fox, P.F.; McSweeny, P.I.H. , 2003.
[32]
Kumosinski, T.F.; Brown, E.M.; Farrell, H.M., Jr Three-dimensional molecular modeling of bovine caseins: an energy-minimized beta-casein structure. J. Dairy Sci., 1993, 76(4), 931-945.
[http://dx.doi.org/10.3168/jds.S0022-0302(93)77420-2] [PMID: 8486844]
[33]
Bourassa, P.; Bekale, L.; Tajmir-Riahi, H.A. Association of lipids with milk α- and β-caseins. Int. J. Biol. Macromol., 2014, 70, 156-166.
[http://dx.doi.org/10.1016/j.ijbiomac.2014.06.038] [PMID: 24984025]
[34]
Collini, M.; D’Alfonso, L.; Baldini, G. New insight on β-lactoglobulin binding sites by 1-anilinonaphthalene-8-sulfonate fluorescence decay. Protein Sci., 2000, 9(10), 1968-1974.
[http://dx.doi.org/10.1110/ps.9.10.1968] [PMID: 11106170]
[35]
Thorn, D.C.; Meehan, S.; Sunde, M.; Rekas, A.; Gras, S.L.; MacPhee, C.E.; Dobson, C.M.; Wilson, M.R.; Carver, J.A. Amyloid fibril formation by bovine milk κ-casein and its inhibition by the molecular chaperones alphaS- and β-casein. Biochemistry, 2005, 44(51), 17027-17036.
[http://dx.doi.org/10.1021/bi051352r] [PMID: 16363816]
[36]
Qin, B.Y.; Bewley, M.C.; Creamer, L.K.; Baker, H.M.; Baker, E.N.; Jameson, G.B. Structural basis of the Tanford transition of bovine β-lactoglobulin. Biochemistry, 1998, 37(40), 14014-14023.
[http://dx.doi.org/10.1021/bi981016t] [PMID: 9760236]
[37]
Liang, L.; Tajmir-Riahi, H.A.; Subirade, M. Interaction of β-lactoglobulin with resveratrol and its biological implications. Biomacromolecules, 2008, 9(1), 50-56.
[http://dx.doi.org/10.1021/bm700728k] [PMID: 18067252]
[38]
Liang, L.; Subirade, M. β-lactoglobulin/folic acid complexes: formation, characterization, and biological implication. J. Phys. Chem. B, 2010, 114(19), 6707-6712.
[http://dx.doi.org/10.1021/jp101096r] [PMID: 20411963]
[39]
Chakraborty, A.; Basak, S. Effect of surfactants on casein structure: a spectroscopic study. Colloids Surf. B Biointerfaces, 2008, 63(1), 83-90.
[http://dx.doi.org/10.1016/j.colsurfb.2007.11.005] [PMID: 18155889]
[40]
Chakraborty, A.; Basak, S. pH-induced structural transitions of caseins. J. Photochem. Photobiol. B, 2007, 87(3), 191-199.
[http://dx.doi.org/10.1016/j.jphotobiol.2007.04.004] [PMID: 17537643]
[41]
Dousseau, F.; Therrien, M.; Pezolet, M. On the spectral subtraction of water from the FT-IR spectra of aqueous solutions of proteins. Appl. Spectrosc., 1989, 43, 538-542.
[http://dx.doi.org/10.1366/0003702894202814]
[42]
Byler, D.M.; Susi, H. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers, 1986, 25(3), 469-487.
[http://dx.doi.org/10.1002/bip.360250307] [PMID: 3697478]
[43]
Beauchemin, R.; N’soukpoé-Kossi, C.N.; Thomas, T.J.; Thomas, T.; Carpentier, R.; Tajmir-Riahi, H.A. Polyamine analogues bind human serum albumin. Biomacromolecules, 2007, 8(10), 3177-3183.
[http://dx.doi.org/10.1021/bm700697a] [PMID: 17887793]
[44]
Lakowicz, J.R. In Principles of Fluorescence Spectroscopy, 3rd ed; Springer: New York, 2006.
[45]
Chandra, S.; Dietrich, S.; Lang, H.; Bahadur, D. Dendrimer-doxorubicin conjugate for enhanced therapeutic effects for cancer. J. Mater. Chem., 2011, 21, 5729-5737.
[http://dx.doi.org/10.1039/c0jm04198j]
[46]
Krimm, S.; Bandekar, J. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem., 1986, 38, 181-364.
[http://dx.doi.org/10.1016/S0065-3233(08)60528-8] [PMID: 3541539]
[47]
Malin, E.L.; Alaimo, M.H.; Brown, E.M.; Aramini, J.M.; Germann, M.W.; Farrell, H.M., Jr; McSweeney, P.L.; Fox, P.F. Solution structures of casein peptides: NMR, FTIR, CD, and molecular modeling studies of alphas1-casein, 1-23. J. Protein Chem., 2001, 20(5), 391-404.
[http://dx.doi.org/10.1023/A:1012232804665] [PMID: 11732691]
[48]
Chanphai, P.; Tajmir-Riahi, H.A. Trypsin and trypsin inhibitor bind milk beta-lactoglobulin: Protein-protein interactions and morphology. Int. J. Biol. Macromol., 2017, 96, 754-758.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.12.075] [PMID: 28049012]
[49]
Shukla, A.; Narayanan, T.; Zanchi, D. Structure of casein micelles and their complexation with tannins. Soft Matter, 2009, 5, 2884-2888.
[http://dx.doi.org/10.1039/b903103k]
[50]
Chanphai, P.; Bourassa, P.; Kanakis, C.D.; Tarantilis, P.A.; Polissiou, M.G.; Tajmir-Riahi, H.A. Review on the loading efficacy of dietary tea polyphenols with milk proteins. Food Hydrocoll., 2018, 77, 322-328.
[http://dx.doi.org/10.1016/j.foodhyd.2017.10.008]
[51]
Zuris, J.A.; Thompson, D.B.; Shu, Y.; Guilinger, J.P.; Bessen, J.L.; Hu, J.H.; Maeder, M.L.; Joung, J.K.; Chen, Z.Y.; Liu, D.R. Cationic lipid-mediated delivery of proteins enables efficient protein-based genome editing in vitro and in vivo. Nat. Biotechnol., 2015, 33(1), 73-80.
[http://dx.doi.org/10.1038/nbt.3081] [PMID: 25357182]
[52]
Wang, M.; Zuris, J.A.; Meng, F.; Rees, H.; Sun, S.; Deng, P.; Han, Y.; Gao, X.; Pouli, D.; Wu, Q.; Georgakoudi, I.; Liu, D.R.; Xu, Q. Efficient delivery of genome-editing proteins using bioreducible lipid nanoparticles. Proc. Natl. Acad. Sci. USA, 2016, 113(11), 2868-2873.
[http://dx.doi.org/10.1073/pnas.1520244113] [PMID: 26929348]
[53]
Ma, T.; Wang, L.; TingyuanYang, ; Wang, D.; Ma, G.; Wang, S. PLGA-lipid liposphere as a promising platform for oral delivery of proteins. Colloids Surf. B Biointerfaces, 2014, 117, 512-519.
[http://dx.doi.org/10.1016/j.colsurfb.2014.02.039] [PMID: 24698146]
[54]
Chatin, B.; Mével, M.; Devallière, J.; Dallet, L.; Haudebourg, T.; Peuziat, P.; Colombani, T.; Berchel, M.; Lambert, O.; Edelman, A.; Pitard, B. Liposome-based formulation for intracellular delivery of functional proteins. Mol. Ther. Nucleic Acids, 2015, 4e244
[http://dx.doi.org/10.1038/mtna.2015.17] [PMID: 26102064]
[55]
Puri, A.; Loomis, K.; Smith, B.; Lee, J.H.; Yavlovich, A.; Heldman, E.; Blumenthal, R. Lipid-based nanoparticles as pharmaceutical drug carriers: from concepts to clinic. Crit. Rev. Ther. Drug Carrier Syst., 2009, 26(6), 523-580.
[http://dx.doi.org/10.1615/CritRevTherDrugCarrierSyst.v26.i6.10] [PMID: 20402623]
[56]
Tavares, G.M.; Croguennec, T.; Carvalho, A.F.; Bouhallab, S. Milk proteins as encapsulation devices and delivery vehicles: applications and trends. Trends Food Sci. Technol., 2014, 37, 5-20.
[http://dx.doi.org/10.1016/j.tifs.2014.02.008]


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VOLUME: 27
ISSUE: 24
Year: 2020
Published on: 06 July, 2020
Page: [4109 - 4117]
Pages: 9
DOI: 10.2174/0929867325666180608122439
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