Heterogeneity of Red Blood Cell Deformability Caused by Lipopolysaccharide based on a Microfluidic Chip

Page: [1795 - 1802] Pages: 8

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Abstract

Introduction: Alterations in red blood cell deformability (RBC-df) provide important information for the diagnosis of various diseases.

Aim: We evaluated individual differences of lipopolysaccharide (LPS)-induced oxidative damage of RBC-df and analyzed the correlation between RBC-df and biochemical parameters.

Methods: A microfluidic chip was developed to detect inter-individual variability of different concentrations of LPS-induced oxidative damage of RBC-df in 9 healthy volunteers. The relationships between various biochemical indicators (Na+-K+-ATPase activity, lipid peroxide (LPO) content, glutathione peroxidase (GSH-PX) activity, catalase (CAT) activity, superoxide dismutase (SOD) activity, adenosine triphosphate (ATP) content, and hemoglobin (HB) content) and RBCsdf were investigated.

Results: The obvious inter-individual variability of LPS-induced oxidative damage of RBC-df was revealed. The Na+-K+-ATPase activity, LPO content, GSH-PX activity, and CAT activity of RBCs showed significant correlations with RBC-df (P < 0.05).

Conclusion: Oxidative damage and energy metabolism are the critical factors of RBC-df impairment induced by LPS, and the individual dependence on RBC-df is an important indicator for the treatment of infection-associated sepsis since antibiotics can kill pathogenic bacteria, which results in the release of LPS from the cell wall.

Graphical Abstract

[1]
Tandon, P.; Garcia-Tsao, G. Bacterial infections, sepsis, and multiorgan failure in cirrhosis. Semin. Liver Dis., 2008, 28(1), 026-042.
[http://dx.doi.org/10.1055/s-2008-1040319]
[2]
Velkov, T.; Thompson, P.E.; Nation, R.L.; Li, J. Structure-activity relationships of polymyxin antibiotics. J. Med. Chem., 2010, 53(5), 1898-1916.
[http://dx.doi.org/10.1021/jm900999h] [PMID: 19874036]
[3]
Foit, L.; Thaxton, C.S. Synthetic high-density lipoprotein-like nanoparticles potently inhibit cell signaling and production of inflammatory mediators induced by lipopolysaccharide binding Toll-like receptor 4. Biomaterials, 2016, 100, 67-75.
[http://dx.doi.org/10.1016/j.biomaterials.2016.05.021] [PMID: 27244690]
[4]
Hernández, G.; Teboul, J.L. Is the macrocirculation really dissociated from the microcirculation in septic shock? Intensive Care Med., 2016, 42(10), 1621-1624.
[http://dx.doi.org/10.1007/s00134-016-4416-2] [PMID: 27289357]
[5]
Piagnerelli, M.; Zouaoui Boudjeltia, K.; Piro, P.; Brohee, D.; Vanhaeverbeek, M.; Vincent, J.L. Effects of sample temperature on red blood cell shape in septic patients. Clin. Hemorheol. Microcirc., 2004, 30(3-4), 463-466.
[PMID: 15258388]
[6]
Forst, T.; Weber, M.M.; Löbig, M.; Lehmann, U.; Müller, J.; Hohberg, C.; Friedrich, C.; Fuchs, W.; Pfützner, A. Pioglitazone in addition to metformin improves erythrocyte deformability in patients with Type 2 diabetes mellitus. Clin. Sci., 2010, 119(8), 345-351.
[http://dx.doi.org/10.1042/CS20100161] [PMID: 20509857]
[7]
Ramdani, G.; Naissant, B.; Thompson, E.; Breil, F.; Lorthiois, A.; Dupuy, F.; Cummings, R.; Duffier, Y.; Corbett, Y.; Mercereau-Puijalon, O.; Vernick, K.; Taramelli, D.; Baker, D.A.; Langsley, G.; Lavazec, C. cAMP-signalling regulates gametocyte-infected erythrocyte deformability required for malaria parasite transmission. PLoS Pathog., 2015, 11(5), e1004815.
[http://dx.doi.org/10.1371/journal.ppat.1004815] [PMID: 25951195]
[8]
Jain, S.A.; Basu, H.; Prabhu, P.S.; Soni, U.; Joshi, M.D.; Mathur, D.; Patravale, V.B.; Pathak, S.; Sharma, S. Parasite impairment by targeting Plasmodium-infected RBCs using glyceryl-dilaurate nanostructured lipid carriers. Biomaterials, 2014, 35(24), 6636-6645.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.058] [PMID: 24818881]
[9]
Glenister, F.K.; Coppel, R.L.; Cowman, A.F.; Mohandas, N.; Cooke, B.M. Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood, 2002, 99(3), 1060-1063.
[http://dx.doi.org/10.1182/blood.V99.3.1060] [PMID: 11807013]
[10]
Piagnerelli, M.; Boudjeltia, K.Z.; Vanhaeverbeek, M.; Vincent, J.L. Red blood cell rheology in sepsis. Intensive Care Med., 2003, 29(7), 1052-1061.
[http://dx.doi.org/10.1007/s00134-003-1783-2] [PMID: 12802488]
[11]
Dyson, A.; Cone, S.; Singer, M.; Ackland, G.L. Microvascular and macrovascular flow are uncoupled in early polymicrobial sepsis. Br. J. Anaesth., 2012, 108(6), 973-978.
[http://dx.doi.org/10.1093/bja/aes093] [PMID: 22466820]
[12]
Singer, M. The role of mitochondrial dysfunction in sepsis-induced multi-organ failure. Virulence, 2014, 5(1), 66-72.
[http://dx.doi.org/10.4161/viru.26907] [PMID: 24185508]
[13]
Bone, R.C. The pathogenesis of sepsis. Ann. Intern. Med., 1991, 115(6), 457-469.
[http://dx.doi.org/10.7326/0003-4819-115-6-457] [PMID: 1872494]
[14]
Moriguchi, T.; Takasugi, N.; Itakura, Y. The effects of aged garlic extract on lipid peroxidation and the deformability of erythrocytes. J. Nutr., 2001, 131(3), 1016S-1019S.
[http://dx.doi.org/10.1093/jn/131.3.1016S] [PMID: 11238808]
[15]
Kalfa, T.A.; Pushkaran, S.; Mohandas, N.; Hartwig, J.H.; Fowler, V.M.; Johnson, J.F.; Joiner, C.H.; Williams, D.A.; Zheng, Y. Rac GTPases regulate the morphology and deformability of the erythrocyte cytoskeleton. Blood, 2006, 108(12), 3637-3645.
[http://dx.doi.org/10.1182/blood-2006-03-005942] [PMID: 16882712]
[16]
Hebbel, R.P.; Leung, A.; Mohandas, N. Oxidation-induced changes in microrheologic properties of the red blood cell membrane. Blood, 1990, 76(5), 1015-1020.
[http://dx.doi.org/10.1182/blood.V76.5.1015.1015] [PMID: 2393710]
[17]
Dulińska, I.; Targosz, M.; Strojny, W.; Lekka, M.; Czuba, P.; Balwierz, W.; Szymoński, M. Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. J. Biochem. Biophys. Methods, 2006, 66(1-3), 1-11.
[http://dx.doi.org/10.1016/j.jbbm.2005.11.003] [PMID: 16443279]
[18]
Dao, M.; Lim, C.T.; Suresh, S. Mechanics of the human red blood cell deformed by optical tweezers [Journal of the Mechanics and Physics of Solids, 51 (2003) 2259-2280]. J. Mech. Phys. Solids, 2005, 53(2), 493-494.
[http://dx.doi.org/10.1016/j.jmps.2004.10.003]
[19]
Skoutelis, A.T.; Kaleridis, V.; Athanassiou, G.M.; Kokkinis, K.I.; Missirlis, Y.F.; Bassaris, H.P. Neutrophil deformability in patients with sepsis, septic shock, and adult respiratory distress syndrome. Crit. Care Med., 2000, 28(7), 2355-2359.
[http://dx.doi.org/10.1097/00003246-200007000-00029] [PMID: 10921564]
[20]
Betticher, D.C.; Keller, H.; Maly, F.E.; Reinhart, W.H. The effect of endotoxin and tumour necrosis factor on erythrocyte and leucocyte deformability in vitro. Br. J. Haematol., 1993, 83(1), 130-137.
[http://dx.doi.org/10.1111/j.1365-2141.1993.tb04643.x] [PMID: 8435320]
[21]
Qiu, X.; Westerhof, T.M.; Karunaratne, A.A.; Werner, E.M.; Pourfard, P.P.; Nelson, E.L.; Hui, E.E.; Haun, J.B. Microfluidic device for rapid digestion of tissues into cellular suspensions. Lab Chip, 2017, 17(19), 3300-3309.
[http://dx.doi.org/10.1039/C7LC00575J] [PMID: 28850139]
[22]
Agustini, D.; Bergamini, M.F.; Marcolino-Junior, L.H. Low cost microfluidic device based on cotton threads for electroanalytical application. Lab Chip, 2016, 16(2), 345-352.
[http://dx.doi.org/10.1039/C5LC01348H] [PMID: 26659997]
[23]
Lachaux, J.; Alcaine, C.; Gómez-Escoda, B.; Perrault, C.M.; Duplan, D.O.; Wu, P.Y.J.; Ochoa, I.; Fernandez, L.; Mercier, O.; Coudreuse, D.; Roy, E. Thermoplastic elastomer with advanced hydrophilization and bonding performances for rapid (30 s) and easy molding of microfluidic devices. Lab Chip, 2017, 17(15), 2581-2594.
[http://dx.doi.org/10.1039/C7LC00488E] [PMID: 28656191]
[24]
Liu, L.; Huang, S.; Xu, X.; Han, J. Study of individual erythrocyte deformability susceptibility to INFeD and ethanol using a microfluidic chip. Sci. Rep., 2016, 6(1), 22929.
[http://dx.doi.org/10.1038/srep22929] [PMID: 26964754]
[25]
Marinaro, G.; Accardo, A.; De Angelis, F.; Dane, T.; Weinhausen, B.; Burghammer, M.; Riekel, C. A superhydrophobic chip based on SU-8 photoresist pillars suspended on a silicon nitride membrane. Lab Chip, 2014, 14(19), 3705-3709.
[http://dx.doi.org/10.1039/C4LC00750F] [PMID: 25111677]
[26]
D’ Amico, M.; Di Filippo, C.; La, M.; Solito, E.; McLean, P.G. JFlower, R.J.; Oliani, S.M.; Perretti, M. Lipocortin 1 reduces myocardial ischemia‐reperfusion injury by affecting local leukocyte recruitment. FASEB J., 2000, 14(13), 1867-1869.
[http://dx.doi.org/10.1096/fj.99-0602fje] [PMID: 11023969]
[27]
Safeukui, I.; Buffet, P.A.; Deplaine, G.; Perrot, S.; Brousse, V.; Ndour, A.; Nguyen, M.; Mercereau-Puijalon, O.; David, P.H.; Milon, G.; Mohandas, N. Quantitative assessment of sensing and sequestration of spherocytic erythrocytes by the human spleen. Blood, 2012, 120(2), 424-430.
[http://dx.doi.org/10.1182/blood-2012-01-404103] [PMID: 22510876]
[28]
Lavazec, C. Molecular mechanisms of deformability of Plasmodium-infected erythrocytes. Curr. Opin. Microbiol., 2017, 40, 138-144.
[http://dx.doi.org/10.1016/j.mib.2017.11.011] [PMID: 29175339]
[29]
Stuart, J.; Nash, G.B. Red cell deformability and haematological disorders. Blood Rev., 1990, 4(3), 141-147.
[http://dx.doi.org/10.1016/0268-960X(90)90041-P] [PMID: 2245249]
[30]
Hod, E.A.; Zhang, N.; Sokol, S.A.; Wojczyk, B.S.; Francis, R.O.; Ansaldi, D.; Francis, K.P.; Della-Latta, P.; Whittier, S.; Sheth, S.; Hen-drickson, J.E.; Zimring, J.C.; Brittenham, G.M.; Spitalnik, S.L. Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood, 2010, 115(21), 4284-4292.
[http://dx.doi.org/10.1182/blood-2009-10-245001] [PMID: 20299509]
[31]
Yang, X.; Zhou, L.; Hao, Y.; Zhou, B.; Yang, P. Erythrocytes-based quartz crystal microbalance cytosensor for in situ detection of cell surface sialic acid. Analyst, 2017, 142(12), 2169-2176.
[http://dx.doi.org/10.1039/C7AN00073A] [PMID: 28524185]
[32]
Bellary, S.; Anderson, K.W.; Arden, W.A.; Butterfield, D.A. Effect of lipopolysaccharide on the physical conformation of the erythrocyte cytoskeletal proteins. Life Sci., 1995, 56(2), 91-98.
[http://dx.doi.org/10.1016/0024-3205(94)00418-R] [PMID: 7823763]
[33]
Ferrer-Martinez, A. Javier CASADO, F.; Felipe, A.; Pastor-Anglada, M. Regulation of Na+,K+-ATPase and the Na+/K+/Cl+ co-transporter in the renal epithelial cell line NBL-1 under osmotic stress. Biochem. J., 1996, 319(2), 337-342.
[http://dx.doi.org/10.1042/bj3190337] [PMID: 8912665]
[34]
Powell, R.J.; MacHiedo, G.W.; Rush, B.F., Jr; Dikdan, G. Oxygen free radicals. Crit. Care Med., 1991, 19(5), 732-735.
[http://dx.doi.org/10.1097/00003246-199105000-00022] [PMID: 2026037]
[35]
Srour; Bilto, Y.Y.; Juma, M.; Irhimeh, M.R. Exposure of human erythrocytes to oxygen radicals causes loss of deformability, increased osmotic fragility, lipid peroxidation and protein degradation. Clin. Hemorheol. Microcirc., 2000, 23(1), 13-21.
[PMID: 11214709]