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Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article

Immune and Metabolic Interactions of Human Erythrocytes: A Molecular Perspective

Author(s): Charalampos Papadopoulos, Maria Panopoulou, Konstantinos Anagnostopoulos* and Ioannis Tentes

Volume 21, Issue 5, 2021

Published on: 04 November, 2020

Page: [843 - 853] Pages: 11

DOI: 10.2174/1871530320666201104115016

Price: $65

Abstract

Apart from their main function as oxygen carriers in vertebrates, erythrocytes are also involved in immune regulation. By circulating throughout the body, the erythrocytes are exposed and interact with tissues that are damaged as a result of a disease. In this study, we summarize the literature regarding the contribution of erythrocytes to immune regulation and metabolism. Under the circumstances of a disease state, the erythrocytes may lose their antioxidant capacity and release Damage Associated Molecular Patterns, resulting in the regulation of innate and adaptive immunity. In addition, the erythrocytes scavenge and affect the levels of chemokines, circulating cell-free mtDNA, and C3b attached immune complexes. Furthermore, through surface molecules, erythrocytes control the function of T lymphocytes, macrophages, and dendritic cells. Through an array of enzymes, red blood cells contribute to the pool of blood’s bioactive lipids. Finally, the erythrocytes contribute to reverse cholesterol transport through various mechanisms. Our study is highlighting overlooked molecular interactions between erythrocytes and immunity and metabolism, which could lead to the discovery of potent therapeutic targets for immunometabolic diseases.

Keywords: Erythrocytes, immunity, metabolism, lipid signaling, reverse cholesterol transport, cytokine signaling, DAMP binding, DAMP release, cellular interactions.

Graphical Abstract
[1]
Chen, L.; Deng, H.; Cui, H.; Fang, J.; Zuo, Z.; Deng, J. Inflammatory responses and inflammation-associated diseases in organs. Vol. 9. Oncotarget. Impact Journals, 2018, LLC, 7204-7218.
[http://dx.doi.org/10.18632/oncotarget.23208]
[2]
Anderson, H.L.; Brodsky, I.E.; Mangalmurti, N.S. The Evolving Erythrocyte: Red Blood Cells as Modulators of Innate Immunity. J. Immunol., 2018, 201(5), 1343-1351.
[http://dx.doi.org/10.4049/jimmunol.1800565] [PMID: 30127064]
[3]
Buttari, B.; Profumo, E.; Riganò, R. Crosstalk between red blood cells and the immune system and its impact on atherosclerosis. BioMed Res. Int., 2015, 2015616834
[http://dx.doi.org/10.1155/2015/616834] [PMID: 25722984]
[4]
Barnett, K.C.; Kagan, J.C. Lipids that directly regulate innate immune signal transduction. Innate Immun., 2020, 26(1), 4-14.
[http://dx.doi.org/10.1177/1753425919852695] [PMID: 31180799]
[5]
Dodge, J.T.; Mitchell, C.; Hanahan, D.J. The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes. Arch. Biochem. Biophys., 1963, 100(1), 119-130.
[http://dx.doi.org/10.1016/0003-9861(63)90042-0] [PMID: 14028302]
[6]
Nikolić, M.; Stanić, D.; Antonijević, N.; Niketić, V. Cholesterol bound to hemoglobin in normal human erythrocytes: a new form of cholesterol in circulation? Clin. Biochem., 2004, 37(1), 22-26.
[http://dx.doi.org/10.1016/j.clinbiochem.2003.10.002] [PMID: 14675558]
[7]
Dmitry, Y. Lipids that directly regulate innate immune signal transduction Innate Immunity , 2018, 26 (1 ), 4 -14 .
[8]
Dushianthan, A; Cusack, R; Koster , G.; Grocott, M.; Postle, A. Insight into erythrocyte phospholipid molecular flux in healthy humans and in patients with acute respiratory distress syndrome PLOS ONE, 2019, 14(8), 02215959.
[http://dx.doi.org/10.1161/ATVBAHA.112.248971] [PMID: 22499994]
[9]
Hung, KT; Berisha, SZ; Ritchey, BM; Santore, J; Smith, JD Red Blood Cells Play a Role in Reverse Cholesterol Transport Arterioscler Thromb Vasc Biol., 2012, 32(6), 1460-5.
[10]
Minetti, M.; Agati, L.; Malorni, W. The microenvironment can shift erythrocytes from a friendly to a harmful behavior: pathogenetic implications for vascular diseases. Cardiovasc. Res., 2007, 75(1), 21-28.
[http://dx.doi.org/10.1016/j.cardiores.2007.03.007] [PMID: 17412313]
[11]
Rifkind, J.M.; Nagababu, E. Hemoglobin redox reactions and red blood cell aging. Antioxid. Redox Signal., 2013, 18(17), 2274-2283.
[http://dx.doi.org/10.1089/ars.2012.4867] [PMID: 23025272]
[12]
Lutz, H.U.; Bogdanova, A. Mechanisms tagging senescent red blood cells for clearance in healthy humans. Front. Physiol., 2013, 4, 387.
[http://dx.doi.org/10.3389/fphys.2013.00387] [PMID: 24399969]
[13]
Ghashghaeinia, M.; Cluitmans, J.C.A.; Akel, A.; Dreischer, P.; Toulany, M.; Köberle, M.; Skabytska, Y.; Saki, M.; Biedermann, T.; Duszenko, M.; Lang, F.; Wieder, T.; Bosman, G.J. The impact of erythrocyte age on eryptosis. Br. J. Haematol., 2012, 157(5), 606-614.
[http://dx.doi.org/10.1111/j.1365-2141.2012.09100.x] [PMID: 22429222]
[14]
Liese, A.M.; Siddiqi, M.Q.; Siegel, J.H.; Denny, T.; Spolarics, Z. Augmented TNF-alpha and IL-10 production by primed human monocytes following interaction with oxidatively modified autologous erythrocytes. J. Leukoc. Biol., 2001, 70(2), 289-296.
[PMID: 11493622]
[15]
Aoshiba, K.; Nakajima, Y.; Yasui, S.; Tamaoki, J.; Nagai, A. Red blood cells inhibit apoptosis of human neutrophils. Blood, 1999, 93(11), 4006-4010.
[http://dx.doi.org/10.1182/blood.V93.11.4006] [PMID: 10339510]
[16]
Fonseca, A.M.; Porto, G.; Uchida, K.; Arosa, F.A. Red blood cells inhibit activation-induced cell death and oxidative stress in human peripheral blood T lymphocytes. Blood, 2001, 97(10), 3152-3160.
[http://dx.doi.org/10.1182/blood.V97.10.3152] [PMID: 11342443]
[17]
Jeney, V.; Balla, G.; Balla, J. Red blood cell, hemoglobin and heme in the progression of atherosclerosis. Front. Physiol., 2014, 5, 379.
[http://dx.doi.org/10.3389/fphys.2014.00379] [PMID: 25324785]
[18]
Wagener, F.A.D.T.G.; Feldman, E.; de Witte, T.; Abraham, N.G. Heme induces the expression of adhesion molecules ICAM-1, VCAM-1, and E selectin in vascular endothelial cells. Proc. Soc. Exp. Biol. Med., 1997, 216(3), 456-463.
[http://dx.doi.org/10.3181/00379727-216-44197] [PMID: 9402154]
[19]
Silva, G.; Jeney, V.; Chora, A.; Larsen, R.; Balla, J.; Soares, M.P. Oxidized hemoglobin is an endogenous proinflammatory agonist that targets vascular endothelial cells. J. Biol. Chem., 2009, 284(43), 29582-29595.
[http://dx.doi.org/10.1074/jbc.M109.045344] [PMID: 19700768]
[20]
Monteiro, A.P.; Pinheiro, C.S.; Luna-Gomes, T.; Alves, L.R.; Maya-Monteiro, C.M.; Porto, B.N.; Barja-Fidalgo, C.; Benjamim, C.F.; Peters-Golden, M.; Bandeira-Melo, C.; Bozza, M.T.; Canetti, C. Leukotriene B4 mediates neutrophil migration induced by heme. J. Immunol., 2011, 186(11), 6562-6567.
[http://dx.doi.org/10.4049/jimmunol.1002400] [PMID: 21536805]
[21]
Belcher, J.D.; Chen, C.; Nguyen, J.; Milbauer, L.; Abdulla, F.; Alayash, A.I.; Smith, A.; Nath, K.A.; Hebbel, R.P.; Vercellotti, G.M. Heme triggers TLR4 signaling leading to endothelial cell activation and vaso-occlusion in murine sickle cell disease. Blood, 2014, 123(3), 377-390.
[http://dx.doi.org/10.1182/blood-2013-04-495887] [PMID: 24277079]
[22]
Buttari, B.; Profumo, E.; Di Cristofano, C.; Pietraforte, D.; Lionetti, V.; Capoano, R.; Salvati, B.; Businaro, R.; Di Giammarco, G.; Riganò, R. Haemoglobin triggers chemotaxis of human monocyte-derived dendritic cells: possible role in atherosclerotic lesion instability. Atherosclerosis, 2011, 215(2), 316-322.
[http://dx.doi.org/10.1016/j.atherosclerosis.2010.12.032] [PMID: 21333994]
[23]
Sikora, J.; Orlov, S.N.; Furuya, K.; Grygorczyk, R. Hemolysis is a primary ATP-release mechanism in human erythrocytes. Blood, 2014, 124(13), 2150-2157.
[http://dx.doi.org/10.1182/blood-2014-05-572024] [PMID: 25097178]
[24]
Sáez, P.J.; Vargas, P.; Shoji, K.F.; Harcha, P.A.; Lennon-Duménil, A-M.; Sáez, J.C. ATP promotes the fast migration of dendritic cells through the activity of pannexin 1 channels and P2X7 receptors. Sci. Signal., 2017, 10(506)eaah7107
[http://dx.doi.org/10.1126/scisignal.aah7107] [PMID: 29162744]
[25]
Trabanelli, S.; Ocadlíková, D.; Gulinelli, S.; Curti, A.; Salvestrini, V.; Vieira, R.P.; Idzko, M.; Di Virgilio, F.; Ferrari, D.; Lemoli, R.M. Extracellular ATP exerts opposite effects on activated and regulatory CD4+ T cells via purinergic P2 receptor activation. J. Immunol., 2012, 189(3), 1303-1310.
[http://dx.doi.org/10.4049/jimmunol.1103800] [PMID: 22753942]
[26]
Cauwels, A.; Rogge, E.; Vandendriessche, B.; Shiva, S.; Brouckaert, P. Extracellular ATP drives systemic inflammation, tissue damage and mortality. Cell Death Dis., 2014, 5(3), e1102-e1102.
[http://dx.doi.org/10.1038/cddis.2014.70] [PMID: 24603330]
[27]
Awojoodu, A.O.; Keegan, P.M.; Lane, A.R.; Zhang, Y.; Lynch, K.R.; Platt, M.O.; Botchwey, E.A. Acid sphingomyelinase is activated in sickle cell erythrocytes and contributes to inflammatory microparticle generation in SCD. Blood, 2014, 124(12), 1941-1950.
[http://dx.doi.org/10.1182/blood-2014-01-543652] [PMID: 25075126]
[28]
Sadallah, S.; Eken, C.; Schifferli, J.A. Erythrocyte-derived ectosomes have immunosuppressive properties. J. Leukoc. Biol., 2008, 84(5), 1316-1325.
[http://dx.doi.org/10.1189/jlb.0108013] [PMID: 18685086]
[29]
Danesh, A.; Inglis, H.C.; Jackman, R.P.; Wu, S.; Deng, X.; Muench, M.O.; Heitman, J.W.; Norris, P.J. Exosomes from red blood cell units bind to monocytes and induce proinflammatory cytokines, boosting T-cell responses in vitro. Blood, 2014, 123(5), 687-696.
[http://dx.doi.org/10.1182/blood-2013-10-530469] [PMID: 24335232]
[30]
Belizaire, R.M.; Prakash, P.S.; Richter, J.R.; Robinson, B.R.; Edwards, M.J.; Caldwell, C.C.; Lentsch, A.B.; Pritts, T.A. Microparticles from stored red blood cells activate neutrophils and cause lung injury after hemorrhage and resuscitation. J. Am. Coll. Surg., 2012, 214(4), 648-655.
[http://dx.doi.org/10.1016/j.jamcollsurg.2011.12.032] [PMID: 22342784]
[31]
Liew, F.Y.; Girard, J.P.; Turnquist, H.R. Interleukin-33 in health and disease.Nature Reviews Immunology; Nature Publishing Group, 2016, 16, pp. 676-689.
[32]
Wei, J.; Zhao, J.; Schrott, V.; Zhang, Y.; Gladwin, M.; Bullock, G.; Zhao, Y. Red Blood Cells Store and Release Interleukin-33. J. Investig. Med., 2015, 63(6), 806-810.
[http://dx.doi.org/10.1097/JIM.0000000000000213] [PMID: 26107423]
[33]
Karsten, E.; Breen, E.; Herbert, B.R. Red blood cells are dynamic reservoirs of cytokines. Sci. Rep., 2018, 8(1), 3101.
[http://dx.doi.org/10.1038/s41598-018-21387-w] [PMID: 29449599]
[34]
Darbonne, W.C.; Rice, G.C.; Mohler, M.A.; Apple, T.; Hébert, C.A.; Valente, A.J.; Baker, J.B. Red blood cells are a sink for interleukin 8, a leukocyte chemotaxin. J. Clin. Invest., 1991, 88(4), 1362-1369.
[http://dx.doi.org/10.1172/JCI115442] [PMID: 1918386]
[35]
Hansell, CA; Hurson, CE; Nibbs, RJ. DARC and D6: silent partners in chemokine regulation? Immunol Cell Biol., 2011, 89(2), 197-206.
[http://dx.doi.org/10.7754/Clin.Lab.2016.161027] [PMID: 28397469]
[36]
Yamamoto, A.; Saito, N.; Ogasawara, S.; Shiratori, T.; Kondo, J.; Itoga, M. Intracellular Storage of Duffy Antigen-Binding Chemokines by Duffy-Positive Red Blood Cells. Clin Lab, 2017, 63(4), 717-23.
[37]
Mangalmurti, N.S.; Xiong, Z.; Hulver, M.; Ranganathan, M.; Liu, X.H.; Oriss, T.; Fitzpatrick, M.; Rubin, M.; Triulzi, D.; Choi, A.; Lee, J.S. Loss of red cell chemokine scavenging promotes transfusion-related lung inflammation. Blood, 2009, 113(5), 1158-1166.
[http://dx.doi.org/10.1182/blood-2008-07-166264] [PMID: 19064726]
[38]
Reutershan, J.; Harry, B.; Chang, D.; Bagby, G.J.; Ley, K. DARC on RBC limits lung injury by balancing compartmental distribution of CXC chemokines. Eur. J. Immunol., 2009, 39(6), 1597-1607.
[http://dx.doi.org/10.1002/eji.200839089] [PMID: 19499525]
[39]
Kanda, A.; Adachi, T.; Kayaba, H.; Yamada, Y.; Ueki, S.; Yamaguchi, K.; Hamada, K.; Fujita, M.; Chihara, J. Red blood cells regulate eosinophil chemotaxis by scavenging RANTES secreted from endothelial cells. Clin. Exp. Allergy, 2004, 34(10), 1621-1626.
[http://dx.doi.org/10.1111/j.1365-2222.2004.02073.x] [PMID: 15479279]
[40]
Kirch, H.J.; Moyes, R.B.; Chiarantini, L.; DeLoach, J.R. Effect of targeted erythrocytes coated with recombinant human interleukin 2 on T-lymphocyte proliferation in vitro. Biotechnol. Appl. Biochem., 1994, 19(3), 331-340.
[PMID: 8031507]
[41]
Moyes, R.B.; DeLoach, J.R. Binding of human recombinant interleukin 2 to murine erythrocytes is erythropoietin receptor mediated. Comp. Haematol. Int., 1996, 6(3), 134-140.
[http://dx.doi.org/10.1007/BF00368456]
[42]
Moyes, R.B.; Kirch, H.; DeLoach, J.R. Enhanced biological activity of human recombinant interleukin 2 coupled to mouse red blood cells as evaluated using the mouse Meth A sarcoma model. Biotechnol. Appl. Biochem., 1996, 23(1), 29-36.
[PMID: 8867894]
[43]
Wagner, H. The immunobiology of the TLR9 subfamily Trends in Immunology , 2004, 25 , 381 -6 .
[44]
Hotz, M.J.; Qing, D.; Shashaty, M.G.S.; Zhang, P.; Faust, H.; Sondheimer, N.; Rivella, S.; Worthen, G.S.; Mangalmurti, N.S. Red Blood Cells Homeostatically Bind Mitochondrial DNA through TLR9 to Maintain Quiescence and to Prevent Lung Injury. Am. J. Respir. Crit. Care Med., 2018, 197(4), 470-480.
[http://dx.doi.org/10.1164/rccm.201706-1161OC] [PMID: 29053005]
[45]
Pascual, M; Schifferli, JA Erythrocyte CR1 receptor: binding and transport of immune complexes in the blood circulation. Schweiz Med Wochenschr , 1993, 123 (3 ), 39 -43 .
[46]
Miyaike, J.; Iwasaki, Y.; Takahashi, A.; Shimomura, H.; Taniguchi, H.; Koide, N.; Matsuura, K.; Ogura, T.; Tobe, K.; Tsuji, T. Regulation of circulating immune complexes by complement receptor type 1 on erythrocytes in chronic viral liver diseases. Gut, 2002, 51(4), 591-596.
[http://dx.doi.org/10.1136/gut.51.4.591] [PMID: 12235086]
[47]
Oldenborg, P-A. CD47: A Cell Surface Glycoprotein Which Regulates Multiple Functions of Hematopoietic Cells in Health and Disease. ISRN Hematol., 2013, 2013614619
[http://dx.doi.org/10.1155/2013/614619] [PMID: 23401787]
[48]
Burger, P.; Hilarius-Stokman, P.; de Korte, D.; van den Berg, T.K.; van Bruggen, R. CD47 functions as a molecular switch for erythrocyte phagocytosis. Blood, 2012, 119(23), 5512-5521.
[http://dx.doi.org/10.1182/blood-2011-10-386805] [PMID: 22427202]
[49]
Schäkel, K.; von Kietzell, M.; Hänsel, A.; Ebling, A.; Schulze, L.; Haase, M.; Semmler, C.; Sarfati, M.; Barclay, A.N.; Randolph, G.J.; Meurer, M.; Rieber, E.P. Human 6-sulfo LacNAc-expressing dendritic cells are principal producers of early interleukin-12 and are controlled by erythrocytes. Immunity, 2006, 24(6), 767-777.
[http://dx.doi.org/10.1016/j.immuni.2006.03.020] [PMID: 16782032]
[50]
Buttari, B.; Profumo, E.; Cuccu, B.; Straface, E.; Gambardella, L.; Malorni, W.; Genuini, I.; Capoano, R.; Salvati, B.; Riganò, R. Erythrocytes from patients with carotid atherosclerosis fail to control dendritic cell maturation. Int. J. Cardiol., 2012, 155(3), 484-486.
[http://dx.doi.org/10.1016/j.ijcard.2011.12.068] [PMID: 22265585]
[51]
Lizcano, A.; Secundino, I.; Döhrmann, S.; Corriden, R.; Rohena, C.; Diaz, S.; Ghosh, P.; Deng, L.; Nizet, V.; Varki, A. Erythrocyte sialoglycoproteins engage Siglec-9 on neutrophils to suppress activation. Blood, 2017, 129(23), 3100-3110.
[http://dx.doi.org/10.1182/blood-2016-11-751636] [PMID: 28416510]
[52]
Lutz, H.U.; Fehr, J. Total sialic acid content of glycophorins during senescence of human red blood cells. J. Biol. Chem., 1979, 254(22), 11177-11180.
[PMID: 500635]
[53]
Boas, F.E.; Forman, L.; Beutler, E. Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc. Natl. Acad. Sci. USA, 1998, 95(6), 3077-3081.
[http://dx.doi.org/10.1073/pnas.95.6.3077] [PMID: 9501218]
[54]
Franco, R.S.; Puchulu-Campanella, M.E.; Barber, L.A.; Palascak, M.B.; Joiner, C.H.; Low, P.S.; Cohen, R.M. Changes in the properties of normal human red blood cells during in vivo aging. Am. J. Hematol., 2013, 88(1), 44-51.
[http://dx.doi.org/10.1002/ajh.23344] [PMID: 23115087]
[55]
Dinkla, S.; Wessels, K.; Verdurmen, W.P.R.; Tomelleri, C.; Cluitmans, J.C.A.; Fransen, J.; Fuchs, B.; Schiller, J.; Joosten, I.; Brock, R.; Bosman, G.J. Functional consequences of sphingomyelinase-induced changes in erythrocyte membrane structure. Cell Death Dis., 2012, 3(10), e410-e410.
[http://dx.doi.org/10.1038/cddis.2012.143] [PMID: 23076218]
[56]
van Zwieten, R.; Bochem, A.E.; Hilarius, P.M.; van Bruggen, R.; Bergkamp, F.; Hovingh, G.K.; Verhoeven, A.J. The cholesterol content of the erythrocyte membrane is an important determinant of phosphatidylserine exposure. Biochim. Biophys. Acta, 2012, 1821(12), 1493-1500.
[http://dx.doi.org/10.1016/j.bbalip.2012.08.008] [PMID: 22960544]
[57]
Straat, M.; van Bruggen, R.; de Korte, D.; Juffermans, N.P. Red blood cell clearance in inflammation. Transfus. Med. Hemother., 2012, 39(5), 353-361.
[http://dx.doi.org/10.1159/000342229] [PMID: 23801928]
[58]
Otogawa, K.; Kinoshita, K.; Fujii, H.; Sakabe, M.; Shiga, R.; Nakatani, K.; Ikeda, K.; Nakajima, Y.; Ikura, Y.; Ueda, M.; Arakawa, T.; Hato, F.; Kawada, N. Erythrophagocytosis by liver macrophages (Kupffer cells) promotes oxidative stress, inflammation, and fibrosis in a rabbit model of steatohepatitis: implications for the pathogenesis of human nonalcoholic steatohepatitis. Am. J. Pathol., 2007, 170(3), 967-980.
[http://dx.doi.org/10.2353/ajpath.2007.060441] [PMID: 17322381]
[59]
Nagahashi, M.; Abe, M.; Sakimura, K.; Takabe, K.; Wakai, T. The role of sphingosine-1-phosphate in inflammation and cancer progressionCancer Science; Blackwell Publishing Ltd, 2018, 109, pp. 3671-8.
[60]
Hänel, P.; Andréani, P.; Gräler, M.H. Erythrocytes store and release sphingosine 1-phosphate in blood. FASEB J., 2007, 21(4), 1202-1209.
[http://dx.doi.org/10.1096/fj.06-7433com] [PMID: 17215483]
[61]
Pappu, R.; Schwab, S.R.; Cornelissen, I.; Pereira, J.P.; Regard, J.B.; Xu, Y.; Camerer, E.; Zheng, Y.W.; Huang, Y.; Cyster, J.G.; Coughlin, S.R. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science, 2007, 316(5822), 295-298.
[http://dx.doi.org/10.1126/science.1139221] [PMID: 17363629]
[62]
Xu, R.; Sun, W.; Jin, J.; Obeid, L.M.; Mao, C. Role of alkaline ceramidases in the generation of sphingosine and its phosphate in erythrocytes. FASEB J., 2010, 24(7), 2507-2515.
[http://dx.doi.org/10.1096/fj.09-153635] [PMID: 20207939]
[63]
Sun, K.; Zhang, Y.; Bogdanov, M.V.; Wu, H.; Song, A.; Li, J.; Dowhan, W.; Idowu, M.; Juneja, H.S.; Molina, J.G.; Blackburn, M.R.; Kellems, R.E.; Xia, Y. Elevated adenosine signaling via adenosine A2B receptor induces normal and sickle erythrocyte sphingosine kinase 1 activity. Blood, 2015, 125(10), 1643-1652.
[http://dx.doi.org/10.1182/blood-2014-08-595751] [PMID: 25587035]
[64]
Knapp, M.; Lisowska, A.; Zabielski, P.; Musiał, W.; Baranowski, M. Sustained decrease in plasma sphingosine-1-phosphate concentration and its accumulation in blood cells in acute myocardial infarction. Prostaglandins Other Lipid Mediat., 2013, 106, 53-61.
[http://dx.doi.org/10.1016/j.prostaglandins.2013.10.001] [PMID: 24120760]
[65]
Bode, C.; Sensken, S-C.; Peest, U.; Beutel, G.; Thol, F.; Levkau, B.; Li, Z.; Bittman, R.; Huang, T.; Tölle, M.; van der Giet, M.; Gräler, M.H. Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J. Cell. Biochem., 2010, 109(6), 1232-1243.
[http://dx.doi.org/10.1002/jcb.22507] [PMID: 20186882]
[66]
Christensen, P.M.; Bosteen, M.H.; Hajny, S.; Nielsen, L.B.; Christoffersen, C. Apolipoprotein M mediates sphingosine-1-phosphate efflux from erythrocytes. Sci. Rep., 2017, 7(1), 14983.
[http://dx.doi.org/10.1038/s41598-017-15043-y] [PMID: 29118354]
[67]
Vu, T.M.; Ishizu, A-N.; Foo, J.C.; Toh, X.R.; Zhang, F.; Whee, D.M.; Torta, F.; Cazenave-Gassiot, A.; Matsumura, T.; Kim, S.; Toh, S.E.S.; Suda, T.; Silver, D.L.; Wenk, M.R.; Nguyen, L.N. Mfsd2b is essential for the sphingosine-1-phosphate export in erythrocytes and platelets. Nature, 2017, 550(7677), 524-528.
[http://dx.doi.org/10.1038/nature24053] [PMID: 29045386]
[68]
Kurano, M.; Nishikawa, M.; Kuma, H.; Jona, M.; Yatomi, Y. Involvement of Band3 in the efflux of sphingosine 1-phosphate from erythrocytes.PLoS One; Gerós H, editor, 2017, 12, pp. 5-0177543.
[69]
Kobayashi, N.; Kobayashi, N.; Yamaguchi, A.; Nishi, T. Characterization of the ATP-dependent sphingosine 1-phosphate transporter in rat erythrocytes. J. Biol. Chem., 2009, 284(32), 21192-21200.
[http://dx.doi.org/10.1074/jbc.M109.006163] [PMID: 19531471]
[70]
Xiang, H; Lu, Y; Shao, M; Wu, T. Lysophosphatidic acid receptors: Biochemical and clinical implications in different diseases Journal of Cancer. , 2020, 11 , 3519 -35 .
[71]
Cripps, M.W.; Soupene, E.; Harken, A.; Kuypers, F. Erythrocytes contain a membrane lysophosphatidic acid acyltransferase that modulates serum lysophosphatidic acid concentration. J. Am. Coll. Surg., 2007, 205(3), S34.
[http://dx.doi.org/10.1016/j.jamcollsurg.2007.06.287]
[72]
Neidlinger, N.A.; Larkin, S.K.; Bhagat, A.; Victorino, G.P.; Kuypers, F.A. Hydrolysis of phosphatidylserine-exposing red blood cells by secretory phospholipase A2 generates lysophosphatidic acid and results in vascular dysfunction. J. Biol. Chem., 2006, 281(2), 775-781.
[http://dx.doi.org/10.1074/jbc.M505790200] [PMID: 16278219]
[73]
Cripps, M.W.; Ereso, A.Q.; Victorino, G.P.; Harken, A.H.; Soupene, E.; Kuypers, F. Lysophosphatidic acid formation in old packed red blood cells causes post transfusion vascular leak. J. Am. Coll. Surg., 2008, 207(3), S37.
[http://dx.doi.org/10.1016/j.jamcollsurg.2008.06.072]
[74]
Aoki, J.; Taira, A.; Takanezawa, Y.; Kishi, Y.; Hama, K.; Kishimoto, T.; Mizuno, K.; Saku, K.; Taguchi, R.; Arai, H. Serum lysophosphatidic acid is produced through diverse phospholipase pathways. J. Biol. Chem., 2002, 277(50), 48737-48744.
[http://dx.doi.org/10.1074/jbc.M206812200] [PMID: 12354767]
[75]
Macdonald, D.J.; Boyle, R.M.; Glen, A.C.A.; Horrobin, D.F. Cytosolic phospholipase A2 type IVA is present in human red cells. Blood, 2004, 103(9), 3562-3564.
[http://dx.doi.org/10.1182/blood-2002-09-2698] [PMID: 14726390]
[76]
Wu, H.; Bogdanov, M.; Zhang, Y.; Sun, K.; Zhao, S.; Song, A.; Luo, R.; Parchim, N.F.; Liu, H.; Huang, A.; Adebiyi, M.G.; Jin, J.; Alexander, D.C.; Milburn, M.V.; Idowu, M.; Juneja, H.S.; Kellems, R.E.; Dowhan, W.; Xia, Y. Hypoxia-mediated impaired erythrocyte Lands’ Cycle is pathogenic for sickle cell disease. Sci. Rep., 2016, 6, 29637.
[http://dx.doi.org/10.1038/srep29637] [PMID: 27436223]
[77]
McGee, J.E.; Fitzpatrick, F.A. Erythrocyte-Neutrophil Interactions: Formation of Leukotriene B4 by Transcellular Biosynthesis Proceedings of the National Academy of Sciences, 1986, 83, pp. 1349-53.
[http://dx.doi.org/10.1073/pnas.83.5.1349]
[78]
Oonishi, T.; Sakashita, K.; Ishioka, N.; Suematsu, N.; Shio, H.; Uyesaka, N. Production of prostaglandins E1 and E2 by adult human red blood cells. Prostaglandins Other Lipid Mediat., 1998, 56(2-3), 89-101.
[http://dx.doi.org/10.1016/S0090-6980(98)00045-8] [PMID: 9785380]
[79]
Lang, P.A.; Kempe, D.S.; Tanneur, V.; Eisele, K.; Klarl, B.A.; Myssina, S.; Jendrossek, V.; Ishii, S.; Shimizu, T.; Waidmann, M.; Hessler, G.; Huber, S.M.; Lang, F.; Wieder, T. Stimulation of erythrocyte ceramide formation by platelet-activating factor. J. Cell Sci., 2005, 118(Pt 6), 1233-1243.
[http://dx.doi.org/10.1242/jcs.01730] [PMID: 15741229]
[80]
Spector, AA; Norris, AW Action of epoxyeicosatrienoic acids on cellular function American Journal of Physiology - Cell Physiology , 2007, 292 , 996 -1012 .
[81]
Jiang, H.; Zhu, A.G.; Mamczur, M.; Falck, J.R.; Lerea, K.M.; McGiff, J.C. Stimulation of rat erythrocyte P2X7 receptor induces the release of epoxyeicosatrienoic acids. Br. J. Pharmacol., 2007, 151(7), 1033-1040.
[http://dx.doi.org/10.1038/sj.bjp.0707311] [PMID: 17558440]
[82]
Shin, H.S.; Chin, M.R.; Kim, J.S.; Chung, J.H.; Ryu, C.K.; Jung, S.Y.; Kim, D.K. Purification and characterization of a cytosolic, 42-kDa and Ca2+-dependent phospholipase A2 from bovine red blood cells: its involvement in Ca2+-dependent release of arachidonic acid from mammalian red blood cells. J. Biol. Chem., 2002, 277(23), 21086-21094.
[http://dx.doi.org/10.1074/jbc.M200203200] [PMID: 11909855]
[83]
Starke, D.W.; Blisard, K.S.; Mieyal, J.J. Substrate specificity of the monooxygenase activity of hemoglobin. Mol. Pharmacol., 1984, 25(3), 467-475.
[PMID: 6727868]
[84]
Jiang, H.; Quilley, J.; Reddy, L.M.; Falck, J.R.; Wong, P.Y.K.; McGiff, J.C. Red blood cells: reservoirs of cis- and trans-epoxyeicosatrienoic acids. Prostaglandins Other Lipid Mediat., 2005, 75(1-4), 65-78.
[http://dx.doi.org/10.1016/j.prostaglandins.2004.10.003] [PMID: 15789616]
[85]
Jiang, H.; Zhu, A.G.; Mamczur, M.; Morisseau, C.; Hammock, B.D.; Falck, J.R.; McGiff, J.C. Hydrolysis of cis- and trans-epoxyeicosatrienoic acids by rat red blood cells. J. Pharmacol. Exp. Ther., 2008, 326(1), 330-337.
[http://dx.doi.org/10.1124/jpet.107.134858] [PMID: 18445784]
[86]
Kobayashi, T.; Levine, L. Arachidonic acid metabolism by erythrocytes J. Biol. Chem., 1983, 258(15), 9116-9121.
[PMID: 6409900]
[87]
Shumilina, E.; Kiedaisch, V.; Akkel, A.; Lang, P.; Hermle, T.; Kempe, D.S.; Huber, S.M.; Wieder, T.; Laufer, S.; Lang, F. Stimulation of suicidal erythrocyte death by lipoxygenase inhibitor Bay-Y5884. Cell. Physiol. Biochem., 2006, 18(4-5), 233-242.
[http://dx.doi.org/10.1159/000097670] [PMID: 17167228]
[88]
Turner, S.; Voogt, J.; Davidson, M.; Glass, A.; Killion, S.; Decaris, J.; Mohammed, H.; Minehira, K.; Boban, D.; Murphy, E.; Luchoomun, J.; Awada, M.; Neese, R.; Hellerstein, M. Measurement of reverse cholesterol transport pathways in humans: in vivo rates of free cholesterol efflux, esterification, and excretion. J. Am. Heart Assoc., 2012, 1(4), e001826-e001826.
[http://dx.doi.org/10.1161/JAHA.112.001826] [PMID: 23130164]
[89]
Chung, B.H.; Franklin, F.; Cho, B.H.; Segrest, J.P.; Hart, K.; Darnell, B.E. Potencies of lipoproteins in fasting and postprandial plasma to accept additional cholesterol molecules released from cell membranes. Arterioscler. Thromb. Vasc. Biol., 1998, 18(8), 1217-1230.
[http://dx.doi.org/10.1161/01.ATV.18.8.1217] [PMID: 9714128]
[90]
Chung, B.H.; Liang, P.; Doran, S.; Cho, B.H.S.; Franklin, F. Postprandial chylomicrons: potent vehicles for transporting cholesterol from endogenous LDL+HDL and cell membranes to the liver via LCAT and CETP. J. Lipid Res., 2004, 45(7), 1242-1255.
[http://dx.doi.org/10.1194/jlr.M300350-JLR200] [PMID: 15102891]
[91]
Klop, B.; van de Geijn, G.J.M.; Bovenberg, S.A.; van der Meulen, N.; Elte, J.W.F.; Birnie, E.; Njo, T.L.; Janssen, H.W.; van Miltenburg, A.; Jukema, J.W.; Cabezas, M.C. Erythrocyte-bound apolipoprotein B in relation to atherosclerosis, serum lipids and ABO blood group. PLoS One, 2013, 8(9)e75573
[http://dx.doi.org/10.1371/journal.pone.0075573] [PMID: 24069429]
[92]
Kuypers, F.A.; Larkin, S.; Beckstead, J.; Oda, M.; Ueda, K.; Ryan, R.O. Red Blood Cells Facilitate Reverse Cholesterol Transport. Blood, 2004, 104(11), 1589-1589.
[http://dx.doi.org/10.1182/blood.V104.11.1589.1589]
[93]
Lai, S.J.; Ohkawa, R.; Horiuchi, Y.; Kubota, T.; Tozuka, M. Red blood cells participate in reverse cholesterol transport by mediating cholesterol efflux of high-density lipoprotein and apolipoprotein A-I from THP-1 macrophages. Biol. Chem., 2019, 400(12), 1593-1602.
[http://dx.doi.org/10.1515/hsz-2019-0244] [PMID: 31188743]

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