LPS Regulates Apolipoprotein E and Aβ Interactionswith Effects on Acute Phase Proteins and Amyloidosis

Abstract

Interactions between apolipoprotein E (apo E) and amyloid beta (Aβ) are associated with the peripheral clearance of Aβ and are important to the development of neurodegenerative diseases. Interests in acute phase proteins (APP) as biomarkers for the early progression of Alzheimer’s disease indicate that the peripheral Aβ metabolism is perturbed and the role of nutritional diets are important to reduce APPs to maintain peripheral Aβ clearance with relevance to hepatic cholesterol homeostasis and brain amyloidosis. The role of nutriproteomic diets that reverse the effects of high fat diets are associated with the reduction in APPs, cholesterol homeostasis and improved clearance of Aβ. Nutritional diets that reduce the increase in plasma endotoxins (gut microbiotica) such as lipopolysaccarides (LPS) reduce the effects of LPS on cell membranes and increase the cellular uptake of Aβ by interactions with apo E. LPS alter hepatic lipid metabolism with an increase hepatic cytokines and APPs in plasma. Interactions between apo E and Aβ are altered by LPS with increased binding of LPS to apo E with effects on electrostatic alterations in Aβ oligomers. The role of LPS in neurodegenerative diseases includes the effects of LPS on alpha-synuclein metabolism with relevance to Parkinson’s disease and Alzheimer’s disease

Share and Cite:

Martins, I. (2015) LPS Regulates Apolipoprotein E and Aβ Interactionswith Effects on Acute Phase Proteins and Amyloidosis. Advances in Aging Research, 4, 69-77. doi: 10.4236/aar.2015.42009.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Tremblay, J.C., Phivilay, C.A., Berthiaume, L., Emond, V., Julien, P. and Calon, F. (2010) High-Fat Diet Aggravates Amyloid-Beta and Tau Pathologies in the 3xTg-AD Mouse Model. Neurobiology of Aging, 9, 1516-1531.
[2] Maesako, M., Uemura, K., Kubota, M., Kuzuya, A., Sasaki, K. and Hayashida, N. (2012) Exercise Is More Effective than Diet Control in Preventing High Fat Diet-Induced β-Amyloid Deposition and Memory Deficit in Amyloid Precursor Protein Transgenic Mice. Journal of Biological Chemistry, 287, 23024-23033.
http://dx.doi.org/10.1074/jbc.M112.367011
[3] Martins, I.J., Gupta, V., Wilson, A.C., Fuller, S.J. and Martins, R.N. (2014) Interactions between Apo E and Amyloid Beta and Their Relationship to Nutriproteomics and Neurodegeneration. Current Pro-teomics, 11, 171-183.
http://dx.doi.org/10.2174/157016461103140922163729
[4] Martins, I.J. (2015) Diabetes and Cholesterol Dyshomeostasis Involves Abnormal α-Synuclein and Amyloid Beta Transport in Neurodegenerative Diseases. Austin Alzheimer’s and Parkinson’s Disease, in Press.
[5] Van Oosten, M., Rensen, P.C., Van Amersfoort, E.S., Van Eck, M., Van Dam, A.M. and Breve, J.J. (2001) Apolipoprotein E Protects against Bacterial Lipopolysaccharide-Induced Lethality. A New Therapeutic Approach to Treat Gram-Negative Sepsis. Journal of Biological Chemistry, 276, 8820-8824.
http://dx.doi.org/10.1074/jbc.M009915200
[6] Laskowitz, D.T., Matthew, W.D., Bennett, E.R., Schmechel, D., Herbstreith, M.H. and Goel, S. (1998) Endogenous Apolipoprotein E Suppresses LPS-Stimulated Microglial Nitric Oxide Production. Neuroreport, 9, 615-618.
http://dx.doi.org/10.1097/00001756-199803090-00010
[7] de Bont, N., Netea, M.G., Demacker, P.N., Verschueren, I., Kullberg, B.J. and van Dijk, K.W. (1999) Apolipoprotein E Knock-Out Mice Are Highly Susceptible to Endotoxemia and Klebsiella pneumoniae Infection. Journal of Lipid Research, 40, 680-685.
[8] Saura, J., Petegnief, V., Wu, X., Liang, Y. and Paul, S.M. (2003) Microglial Apolipoprotein E and Astroglial Apolipoprotein J Expression in Vitro: Opposite Effects of Lipopolysaccharide. Journal of Neurochemistry, 85, 1455-1467.
http://dx.doi.org/10.1046/j.1471-4159.2003.01788.x
[9] Zaiou, M., Arnold, K.S., Newhouse, Y.M., Innerarity, T.L., Weisgraber, K.H. and Segall, M.L. (2000) Apolipoprotein E-Low Density Lipoprotein Receptor Interaction: Influences of Basic Residue and Amphipathic a-Helix Organization in the Ligand. Journal of Lipid Research, 4, 1087-1095.
[10] Lee, J.Y., Lee, YK. Yuk, D.Y., Choi, D.Y., Ban, S.B. and Oh, K.W. (2008) Neuro-Inflammation Induced by Lipo-polysaccharide Causes Cognitive Impairment through Enhancement of Beta-Amyloid Generation. Journal of Neuroinflammation, 5, 1-14.
[11] Spitzer, P., Herrmann, M., Klafki, H.W., Smirnov, A., Lewczuk, P. and Kornhuber, J. (2010) Phagocytosis and LPS Alter the Maturation State of β-Amyloid Precursor Protein and Induce Different Aβ Peptide Release Signatures in Human Mononuclear Phagocytes. Journal of Neuroinflammation, 7, 59.
http://dx.doi.org/10.1186/1742-2094-7-59
[12] Bitting, L., Naidu, A., Cordell, B. and Murphy, G.M. (1996) Beta-Amyloid Peptide Secretion by a Microglial Cell Line Is Induced by Beta-Amyloid-(25-35) and Lipopolysaccharide. Journal of Biological Chemistry, 271, 16084-16089.
http://dx.doi.org/10.1074/jbc.271.27.16084
[13] Chen, X., Dings, R.P., Nesmelova, I., Debbert, S., Haseman, J.R. and Maxwell, J. (2006) Topomimetics of Amphipathic Beta-Sheet and Helix-Forming Bactericidal Peptides Neutralize Lipopolysaccharide Endotoxins. Journal of Medicinal Chemistry, 49, 7754-7765.
http://dx.doi.org/10.1021/jm0610447
[14] Bommineni, Y.R., Dai, H., Gong, Y.X., Soulages, J.L., Fernando, S.C. and Desilva, U. (2007) Fowlicidin-3 Is an Alpha-Helical Cationic Host Defense Peptide with Potent Antibacterial and Lipopolysaccharide-Neutralizing Activities. FEBS Journal, 274, 418-428.
http://dx.doi.org/10.1111/j.1742-4658.2006.05589.x
[15] Scott, M.G., Rosenberger, C.M., Gold, M.R., Finlay, B.B. and Hancock, R.E. (2000) An Alpha-Helical Cationic Antimicrobial Peptide Selectively Modulates Macrophage Responses to Lipopolysaccharide and Directly Alters Macrophage Gene Expression. Journal of Immunology, 165, 3358-3365.
http://dx.doi.org/10.4049/jimmunol.165.6.3358
[16] Mazuski, J.E., Tolman, K. and Shapiro, M.J. (1997) Effects of Cytokine Antagonists on the Hepatic Acute-Phase Response. Journal of Surgery Research, 68, 161-169.
http://dx.doi.org/10.1006/jsre.1997.4999
[17] Fang, C., Yoon, S., Tindberg, N., Jarvelainen, H.A., Lindros, K.O. and Ingelman-Sundberg, M. (2004) Hepatic Expression of Multiple Acute Phase Proteins and Down-Regulation of Nuclear Receptors after Acute Endotoxin Exposure. Biochemical Pharmacology, 67, 1389-1397.
http://dx.doi.org/10.1016/j.bcp.2003.12.012
[18] Hardardóttir, I., Kunitake, S.T., Moser, A.H., Doerrler, W.T., Rapp, J.H. and Grünfeld, C. (1994) Endotoxin and Cytokines Increase Hepatic Messenger RNA Levels and Serum Concentrations of Apolipoprotein J (Clusterin) in Syrian Hamsters. Journal of Clinical Investigation, 94, 1304-1309.
http://dx.doi.org/10.1172/JCI117449
[19] Haziot, A., Lin, X.Y., Zhang, F. and Goert S.M. (1998) Cutting Edge: The Induction of Acute Phase Proteins by Lipopolysaccharide Uses a Novel Pathway That Is CD14-Independent. Journal of Immunology, 160, 2570-2572.
[20] Bucki, R., Georges, P.C., Espinassous, Q., Funaki, M., Pastore, J.J. and Chaby, R. (2005) Inactivation of Endotoxin by Human Plasma Gelsolin. Biochemistry, 44, 9590-9597.
http://dx.doi.org/10.1021/bi0503504
[21] Vreugdenhil, A.C., Dentener, M.A., Snoek, A.M., Greve, J.W. and Buurman, W.A. (1999) Lipopolysaccharide Binding Protein and Serum Amyloid A Secretion by Human Intestinal Epithelial Cells during the Acute Phase Response. Journal of Immunology, 163, 2792-2798.
[22] de Haas, C.J., van der Zee, R., Benaissa-Trouw, B., van Kessel, K.P., Verhoef, J. and van Strijp, J.A. (1999) Lipopolysaccharide (LPS)-Binding Synthetic Peptides Derived from Serum Amyloid P Component Neutralize LPS. Infection and Immunity, 67, 2790-2796.
[23] Argüelles, S., Venero, J.L., García-Rodriguez, S., Tomas-Camardiel, M., Ayala, A. and Cano, J. (2010) Use of Haptoglobin and Transthyretin as Potential Biomarkers for the Preclinical Diagnosis of Parkinson’s Disease. Neurochemistry International, 57, 227-234.
http://dx.doi.org/10.1016/j.neuint.2010.05.014
[24] Lamari, F.N., Gioldassi, X.M., Mitropoulou, T.N. and Karamanos, N.K. (2002) Structure Analysis of Lipoglycans and Lipoglycan-Derived Carbohydrates by Capillary Electrophoresis and Mass Spectrometry. Biomedical Chromatography, 16, 116-126.
http://dx.doi.org/10.1002/bmc.149
[25] Clifton, L.A., Skoda. M.W.A., Daulton, E.L., Hughes, A.V., Le Brun, A.P. and Lakey J.H. (2013) Asymmetric Phospholipid: Lipopolysaccharide Bilayers; a Gram-Negative Bacterial Outer Membrane Mimic. Journal of the Royal Society Interface, 10, Article ID: 20130810.
http://dx.doi.org/10.1098/rsif.2013.0810
[26] Liu, M. and Bing, G. (2011) Lipopolysaccharide Animal Models for Parkinson’s Disease. Parkinson’s Disease, 2011, Article ID: 327089.
http://dx.doi.org/10.4061/2011/327089
[27] Zanoni, I., Ostuni, R., Marek, L.R., Barresi S., Barbalat, R. and Barton, G.M. (2011) CD14 Controls the LPS-Induced Endocytosis of Toll-Like Receptor 4. Cell, 147, 868-880.
http://dx.doi.org/10.1016/j.cell.2011.09.051
[28] Haziot, A., Lin, X.Y., Zhang, F. and Goyert, S.M. (1998) The Induction of Acute Phase Proteins by Lipopolysaccharide Uses a Novel Pathway That Is CD14-Independent. Journal of Immunology, 160, 2570-2572.
[29] Bas, S., Gauthier, B.R., Spenato, U., Stingelin, S. and Gabay, C. (2004) CD14 Is an Acute-Phase Protein. Journal of Immunology, 172, 4470-4479.
http://dx.doi.org/10.4049/jimmunol.172.7.4470
[30] Liu, Y., Walter, S., Stagi, M., Cherny, D., Letiembre, M. and Schulz-Schaeffer, W. (2005) LPS Receptor (CD14): A Receptor for Phagocytosis of Alzheimer’s Amyloid Peptide. Brain, 128, 1778-1789.
http://dx.doi.org/10.1093/brain/awh531
[31] Ogawa, Y., Imajo, K., Yoneda. M., Kessoku, T., Tomeno, W. and Shinohara, Y. (2013) Soluble CD14 Levels Reflect Liver Inflammation in Patients with Nonalcoholic Steatohepatitis. PLOS ONE, 8, e65211.
http://dx.doi.org/10.1371/journal.pone.0065211
[32] Kovalchuk, I., Walz, P., Thomas, J. and Kovalchuk, O. (2013) Genomic Instability in Liver Cells. PLOS ONE, 8, e67342.
http://dx.doi.org/10.1371/journal.pone.0067342
[33] Fenton, M.J. and Golenbock, D.T. (1998) LPS-Binding Proteins and Receptors. Journal of Leukocyte Biology, 64, 25- 32.
[34] Asai, Y., Iwamoto, K. and Watanabe, S. (1998) The Effect of the Lipid A Analog E5531 on Phospholipid Membrane Properties. FEBS Letters, 438, 15-20.
http://dx.doi.org/10.1016/S0014-5793(98)01262-9
[35] Ciesielski, F., Griffin, D.C., Rittig, M., Moriyón, I. and Bonev, B.B. (2013) Interactions of Lipopolysaccharide with Lipid Membranes, Raft Models—A Solid State NMR Study. Biochimica et Biophysica Acta, 1828, 1731-1742.
http://dx.doi.org/10.1016/j.bbamem.2013.03.029
[36] Ciesielski, F., Davis, B., Rittig, M., Bonev, B.B. and O’Shea, P. (2012) Receptor-Independent Interaction of Bacterial Lipopolysaccharide with Lipid and Lymphocyte Membranes; the Role of Cholesterol. PLOS ONE, 7, e38677.
http://dx.doi.org/10.1371/journal.pone.0038677
[37] Harte, A.L., da Silva, N.F., Creely, S.J., McGee, K.C., Billyard, T. and Youssef-Elabd, E.M. (2010) Elevated Endotoxin Levels in Non-Alcoholic Fatty Liver Disease. Journal of Inflammation, 7, 15.
http://dx.doi.org/10.1186/1476-9255-7-15
[38] Huang, H., Liu, T., Rose, J.L., Stevens, R.L. and Hoyt, D.G. (2007) Sensitivity of Mice to Lipopolysaccharide Is Increased by a High Saturated Fat and Cholesterol Diet. Journal of Inflammation, 4, 22.
http://dx.doi.org/10.1186/1476-9255-4-22
[39] Kim, K-A., Gu, W., Lee, I-A., Joh, E-H. and Kim, D-H. (2012) High Fat Diet-Induced Gut Microbiota Exacerbates Inflammation and Obesity in Mice via the TLR4 Signaling Pathway. PLOS ONE, 7, e47713.
http://dx.doi.org/10.1371/journal.pone.0047713
[40] Lee, C.Y. (2013) The Effect of High-Fat Diet-Induced Pathophysiological Changes in the Gut on Obesity: What Should Be the Ideal Treatment? Clinical and Translational Gastroenterology, 4, e39.
http://dx.doi.org/10.1038/ctg.2013.11
[41] Feingold, K.R., Staprans, I., Memon, R.A., Moser, A.H., Shigenaga, J.K. and Doerrler, W. (1992) Endotoxin Rapidly Induces Changes in Lipid Metabolism That Produce Hypertriglyceridemia: Low Doses Stimulate Hepatic Triglyceride Production While High Doses Inhibit Clearance. Journal of Lipid Research, 33, 1765-1776.
[42] Miele, L., Marrone, G., Lauritano, C., Cefalo, C., Gasbarrini, A. and Day, C. (2013) Gut-Liver Axis and Microbiota in NAFLD: Insight Pathophysiology for Novel Therapeutic Target. Current Pharmaceutical Design, 19, 5314-5324.
http://dx.doi.org/10.2174/1381612811319290011
[43] Le Roy, T., Llopis, M., Lepage, P., Bruneau, A., Rabot, S. and Bevilacqua, C. (2013) Intestinal Microbiota Determines Development of Non-Alcoholic Fatty Liver Disease in Mice. Gut, 62, 1787-1794.
http://dx.doi.org/10.1136/gutjnl-2012-303816
[44] Alisi, A., Ceccarelli, S., Panera, N. and Nobili, V. (2012) Causative Role of Gut Microbiota in Non-Alcoholic Fatty Liver Disease Pathogenesis. Frontiers in Cellular Infection Microbiology, 2, 132.
[45] Duseja, A. and Chawla, Y.K. (2014) Obesity and NAFLD: The Role of Bacteria and Microbiota. Clinical Liver Disease, 18, 59-71.
http://dx.doi.org/10.1016/j.cld.2013.09.002
[46] Memon, R.A., Holleran, W.M., Moser, A.H., Seki, T., Uchida, Y. and Fuller, J. (1998) Endotoxin and Cytokines Increase Hepatic Sphingolipid Biosynthesis and Produce Lipoproteins Enriched in Ceramides and Sphingomyelin. Arteriosclerosis, Thrombosis, and Vascular Biology, 18, 1257-1265.
http://dx.doi.org/10.1161/01.ATV.18.8.1257
[47] Gourine, A.V., Gourine, V.N., Tesfaigzi, Y., Caluwaerts, N., Van Leuven, F. and Kluger, M.J. (2002) Role of α2 -Macroglobulin in Fever and Cytokine Responses Induced by Lipopolysaccharide in Mice. American Journal of Physiology Regulation Integrative Comparative Physiology, 283, R218-R226.
http://dx.doi.org/10.1152/ajpregu.00746.2001
[48] Ng, P.M., Jin, Z., Tan, S.S., Ho, B. and Ding, J.L. (2004) C-Reactive Protein: A Predominant LPS-Binding Acute Phase Protein Responsive to Pseudomonas Infection. Innate Immunity, 10, 163-174.
http://dx.doi.org/10.1177/09680519040100030301
[49] Mold, C., Rodriguez, W., Rodic-Polic, B. and Du Clos, T.W. (2002) C-Reactive Protein Mediates Protection from Lipopolysaccharide through Interactions with FcγR. Journal of Immunology, 169, 7019-7025.
http://dx.doi.org/10.4049/jimmunol.169.12.7019
[50] Jangula, A. and Murphy, E.J. (2013) Lipopolysaccharide-Induced Blood Brain Barrier Permeability Is Enhanced by Alpha-Synuclein Expression. Neuroscience Letters, 551, 23-27.
http://dx.doi.org/10.1016/j.neulet.2013.06.058
[51] Ballou, S.P., Lozanski, G.B., Hodder, S., Rzewnicki, D.L., Mion, L.C. and Sipe, J.D. (1996) Quantitative and Qualitative Alterations of Acute-Phase Proteins in Healthy Elderly Persons. Age and Ageing, 25, 224-230.
http://dx.doi.org/10.1093/ageing/25.3.224
[52] Martins, I.J. and Fernando, W.M.A.D. (2014) High Fibre Diets and Alzheimer’s Disease. Food and Nutrition Sciences (Diet and Disease), 5, 410-424.
http://dx.doi.org/10.4236/fns.2014.54049
[53] Martins, I.J. (2014) Induction of NAFLD with Increased Risk of Obesity and Chronic Diseases in Developed Countries. Open Journal of Endocrine and Metabolic Diseases, 4, 90-110.
http://dx.doi.org/10.4236/ojemd.2014.44011
[54] Martins, I.J. (2014) The Global Obesity Epidemic Is Related to Stroke, Dementia and Alzheimer’s Disease. JSM Alzheimer’s Disease Related Dementia, 1, 1010.
[55] Martins, I.J. (2013) Increased Risk for Obesity and Diabetes with Neurodegeneration in Developing Countries. Journal of Molecular Genetic Medicine, 1, Article ID: 001.
[56] Lira, F.S., Rosa J.C., Pimentel, G.D., Seelaender, M., Damaso, A.R. and Oyama LM. (2012) Both Adiponectin and Interleukin-10 Inhibit LPS-Induced Activation of the NF-κB Pathway in 3T3-L1 Adipocytes. Cytokine, 57, 98-106.
http://dx.doi.org/10.1016/j.cyto.2011.10.001
[57] Ajuwon, K.M. and Spurlock, M.E. (2005) Adiponectin Inhibits LPS-Induced NF-κB Activation and IL-6 Production and Increases PPARγ2 Expression in Adipocytes. American Journal of Physiology, Regulatory, Integrative and Comparative Physiology, 288, R1220-R1225.
http://dx.doi.org/10.1152/ajpregu.00397.2004
[58] Taira, R., Yamaguchi, S., Shimizu, K., Nakamura, K., Ayabe, T. and Taira, T. (2015) Bacterial Cell Wall Components Regulate Adipokine Secretion from Visceral Adipocytes. Journal of Clinical Biochemistry and Nutrition, 1, 1-6.
[59] O’Bryan, C.A., Pak, D., Crandall, P.G., Lee, S.O. and Ricke, S.C. (2013) The Role of Prebiotics and Probiotics in Human Health. Journal of Probiotics and Health, 1, 108.
[60] Kotzampassi, K., Giamarellos-Bourboulis, E.J. and Stavrou, G. (2014) Obesity as a Consequence of Gut Bacteria and diet Interactions. International Scholarly Research Notices Obesity, 2014, Article ID: 651895.
[61] Thompson, P.A., Gauthier, K.C., Varley, A.W. and Kitchens, R.L. (2010) ABCA1 Promotes the Efflux of Bacterial LPS from Macrophages and Accelerates Recovery from LPS-Induced Tolerance. Journal of Lipid Research, 51, 2672-2685.
http://dx.doi.org/10.1194/jlr.M007435
[62] Karunaratne, D.N. (2012) Polysaccharide-Protein Interactions and Their Relevance in Food Colloids, Chapter 14. In: Amit, P.B. and Desiree, N., Eds., The Complex World of Polysaccharides. Biochemistry, Genetics and Molecular Biology. InTech Journals.
[63] Everett, D.W. and McLeod, R.E. (2005) Interactions of Polysaccharide Stabilisers with Casein Aggregates in Stirred Skim-Milk Yoghurt. International Dairy Journal, 15, 1175-1183.
http://dx.doi.org/10.1016/j.idairyj.2004.12.004
[64] Neemann, S., Rosenberger, F., Jefferson, B. and McAdam, E.J. (2013) Non-Covalent Protein-Polysaccharide Interactions and Their Influence on Membrane Fouling. Journal of Molecular Science, 446, 310-317.

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.