Mechanical clearance of red blood cells by the human spleen: Potential therapeutic applications of a biomimetic RBC filtration method

Transfusion Clinique et Biologique

Volumn 22, Issue 3, 2015, Pages 151-157

  Duez, J ^a,b,c,d   Holleran, J P ^d   Ndour, P A ^a,b   Pionneau, C ^a   Diakite S ^a,b   Roussel, C ^b,e,f   Dussiot, M ^b,e,f   Amireault, P ^b,e,f   Avery, V M ^d   Buffet, P A ^a,b  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b Boulevard du Montparnasse   (France)

^c Laboratoire HRA Pharma   (France)

^d GRIFFITH UNIVERSITY   (Australia)

^e IMAGINE INSTITUTE   (France)

^f INSTITUT NATIONAL DE LA TRANSFUSION SANGUINE   (France)

Author keywords

Applications; Deformability; Erythrocyte; Filtration; Malaria; Microspheres; Spleen; Transfusion

Indexed keywords

ARTEMISININ DERIVATIVE; PRIMAQUINE; ANTIMALARIAL AGENT; MICROSPHERE;

BIOMECHANICS; BLOOD SAFETY; DRUG POTENCY; DRUG SCREENING; ERYTHROCYTE COUNT; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE FILTERABILITY; ERYTHROCYTE KINETICS; ERYTHROCYTE STRUCTURE; ERYTHROCYTE TRANSFUSION; HEMATOLOGICAL PROCEDURE; HUMAN; LIGAND BINDING; MALARIA; MALARIA CONTROL; MALARIA FALCIPARUM; MICROFLUIDICS; MICROPLATE BASED MICROSPHILTRATION; NONHUMAN; PARASITE SURVIVAL; PARASITE TRANSMISSION; PATHOPHYSIOLOGY; PHAGOCYTOSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); SHORT SURVEY; SPLEEN; SPLEEN BLOOD FLOW; VACUUM ASPIRATION; ADVERSE EFFECTS; BIOMIMETICS; BLOOD; BLOOD STORAGE; BLOOD TRANSFUSION; DEVICES; DRUG EFFECTS; EQUIPMENT DESIGN; ERYTHROCYTE; ERYTHROCYTE DISORDER; ERYTHROCYTE LIFESPAN; FILTRATION; GROWTH, DEVELOPMENT AND AGING; MEAN CORPUSCULAR VOLUME; PARASITEMIA; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM; PRECLINICAL STUDY; PROCEDURES;

ANTIMALARIALS; BIOMIMETICS; BLOOD PRESERVATION; BLOOD TRANSFUSION; DRUG EVALUATION, PRECLINICAL; EQUIPMENT DESIGN; ERYTHROCYTE AGING; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE INDICES; ERYTHROCYTES; ERYTHROCYTES, ABNORMAL; FILTRATION; HUMANS; MALARIA; MICROSPHERES; PARASITEMIA; PLASMODIUM; SPLEEN;

EID: 84938551155     PISSN: 12467820     EISSN: 19538022     Source Type: Journal    
DOI: 10.1016/j.tracli.2015.05.004     Document Type: Short Survey

References (51)

1. Groom A.C., Schmidt E.E., MacDonald I.C. Microcirculatory pathways and blood flow in spleen: new insights from washout kinetics, corrosion casts, and quantitative intravital videomicroscopy. Scanning Microsc 1991, 5:159-173. [discussion 173-4].
2. Picot J., Ndour P.A., Lefevre S.D., El Nemer W., Tawfik H., Galimand J., et al. A biomimetic microfluidic chip to study the circulation and mechanical retention of red blood cells in the spleen. Am J Hematol 2015, 90:339-345.
3. Stuart J., Nash G.B. Red cell deformability and haematological disorders. Blood Rev 1990, 4:141-147.
4. Brousse V., Buffet P., Rees D. The spleen and sickle cell disease: the sick(led) spleen. Br J Haematol 2014, 166:165-176.
5. Mohandas N., Chasis J.A. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol 1993, 30:171-192.
6. Mohandas N., Gallagher P.G. Red cell membrane: past, present, and future. Blood 2008, 112:3939-3948.
7. Perrotta S., Gallagher P.G., Mohandas N. Hereditary spherocytosis. Lancet 2008, 372:1411-1426.
8. Buffet P.A., Milon G., Brousse V., Correas J.-M., Dousset B., Couvelard A., et al. Ex vivo perfusion of human spleens maintains clearing and processing functions. Blood 2006, 107:3745-3752.
9. Safeukui I., Correas J.-M., Brousse V., Hirt D., Deplaine G., Mulé S., et al. Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood 2008, 112:2520-2528.
10. Koyama S., Aoki S., Deguchi D. Electron microscopic observations of the splenic red pulp with special reference to the pitting function. Mie Med J 1964, 14:143-188.
11. Schnitzer B., Sodeman T., Mead M.L., Contacos P.G. Pitting function of the spleen in malaria: ultrastructural observations. Science 1972, 177:175-177.
12. Looareesuwan S., Ho M., Wattanagoon Y., White N.J., Warrell D.A., Bunnag D., et al. Dynamic alteration in splenic function during acute falciparum malaria. N Engl J Med 1987, 317:675-679.
13. Turrini F., Ginsburg H., Bussolino F., Pescarmona G.P., Serra M.V., Arese P. Phagocytosis of Plasmodium falciparum-infected human red blood cells by human monocytes: involvement of immune and nonimmune determinants and dependence on parasite developmental stage. Blood 1992, 80:801-808.
14. Lutz H.U. Innate immune and non-immune mediators of erythrocyte clearance. Cell Mol Biol (Noisy-Le-Grand) 2004, 50:107-116.
15. 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, 119:5512-5521.
16. Dondorp A.M., Chotivanich K.T., Fucharoen S., Silamut K., Vreeken J., Kager P.A., et al. Red cell deformability, splenic function and anaemia in thalassaemia. Br J Haematol 1999, 105:505-508.
17. Keymel S., Heiss C., Kleinbongard P., Kelm M., Lauer T. Impaired red blood cell deformability in patients with coronary artery disease and diabetes mellitus. Horm Metab Res 2011, 43:760-765.
18. Cranston H.A., Boylan C.W., Carroll G.L., Sutera S.P., Williamson J.R., Gluzman I.Y., et al. Plasmodium falciparum maturation abolishes physiologic red cell deformability. Science 1984, 223:400-403.
19. Miller L.H., Usami S., Chien S. Alteration in the rheologic properties of Plasmodium knowlesi--infected red cells. A possible mechanism for capillary obstruction. J Clin Invest 1971, 50:1451-1455.
20. Dondorp A.M., Angus B.J., Hardeman M.R., Chotivanich K.T., Silamut K., Ruangveerayuth R., et al. Prognostic significance of reduced red blood cell deformability in severe falciparum malaria. Am J Trop Med Hyg 1997, 57:507-511.
21. Buffet P.A., Safeukui I., Deplaine G., Brousse V., Prendki V., Thellier M., et al. The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology. Blood 2011, 117:381-392.
22. Ndour P.A., Lopera-Mesa T.M., Diakité S.A.S., Chiang S., Mouri O., Roussel C., et al. Plasmodium falciparum clearance is rapid and pitting independent in immune Malian children treated with artesunate for malaria. J Infect Dis 2015, 211:290-297.
23. Berezina T.L., Zaets S.B., Morgan C., Spillert C.R., Kamiyama M., Spolarics Z., et al. Influence of storage on red blood cell rheological properties. J Surg Res 2002, 102:6-12.
24. Frank S.M., Abazyan B., Ono M., Hogue C.W., Cohen D.B., Berkowitz D.E., et al. Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration. Anesth Analg 2013, 116:975-981.
25. Grigoleit H.G., Leonhardt H., Schröer R., Lehrach F. Red blood cell aging as a model to influence pharmacologically the red cell filterability. Res Exp Med (Berl) 1981, 179:249-254.
26. Bessis M., Mohandas N., Feo C. Automated ektacytometry: a new method of measuring red cell deformability and red cell indices. Blood Cells 1980, 6:315-327.
27. Li J., Dao M., Lim C.T., Suresh S. Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte. Biophys J 2005, 88:3707-3719.
28. Shelby J.P., White J., Ganesan K., Rathod P.K., Chiu D.T. A microfluidic model for single-cell capillary obstruction by Plasmodium falciparum-infected erythrocytes. PNAS 2003, 100:14618-14622.
29. Antia M., Herricks T., Rathod P.K. Microfluidic approaches to malaria pathogenesis. Cell Microbiol 2008, 10:1968-1974.
30. Deplaine G., Safeukui I., Jeddi F., Lacoste F., Brousse V., Perrot S., et al. The sensing of poorly deformable red blood cells by the human spleen can be mimicked in vitro. Blood 2011, 117:e88-e95.
31. Duez J., Holleran J.P., Ndour P.A., Loganathan S., Pascal Amireault, Olivier Français, et al. Splenic retention of Plasmodium falciparum gametocytes to block the transmission of malaria. AAC 2015, [in press].
32. Rigat-Brugarolas L.G., Elizalde-Torrent A., Bernabeu M., Niz M.D., Martin-Jaular L., Fernandez-Becerra C., et al. A functional microengineered model of the human splenon-on-a-chip. Lab Chip 2014, 14:1715-1724.
33. Maier A.G., Cooke B.M., Cowman A.F., Tilley L. Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol 2009, 7:341-354.
34. Duffy S., Avery V.M. Development and optimization of a novel 384-well anti-malarial imaging assay validated for high-throughput screening. Am J Trop Med Hyg 2012, 86:84-92.
35. Duffy S., Avery V.M. Identification of inhibitors of Plasmodium falciparum gametocyte development. Malar J 2013, 12:408.
36. Lucantoni L., Duffy S., Adjalley S.H., Fidock D.A., Avery V.M. Identification of MMV malaria box inhibitors of plasmodium falciparum early-stage gametocytes using a luciferase-based high-throughput assay. Antimicrob Agents Chemother 2013, 57:6050-6062.
37. Peatey C.L., Spicer T.P., Hodder P.S., Trenholme K.R., Gardiner D.L. A high-throughput assay for the identification of drugs against late-stage Plasmodium falciparum gametocytes. Mol Biochem Parasitol 2011, 180:127-131.
38. Tanaka T.Q., Dehdashti S.J., Nguyen D.-T., McKew J.C., Zheng W., Williamson K.C. A quantitative high throughput assay for identifying gametocytocidal compounds. Mol Biochem Parasitol 2013, 188:20-25.
39. Lelièvre J., Almela M.J., Lozano S., Miguel C., Franco V., Leroy D., et al. Activity of clinically relevant antimalarial drugs on Plasmodium falciparum mature gametocytes in an ATP bioluminescence "transmission blocking" assay. PLoS ONE 2012, 7:e35019.
40. D'Alessandro S., Silvestrini F., Dechering K., Corbett Y., Parapini S., Timmerman M., et al. A Plasmodium falciparum screening assay for anti-gametocyte drugs based on parasite lactate dehydrogenase detection. J Antimicrob Chemother 2013, 68:2048-2058.
41. Tibúrcio M., Niang M., Deplaine G., Perrot S., Bischoff E., Ndour P.A., et al. A switch in infected erythrocyte deformability at the maturation and blood circulation of Plasmodium falciparum transmission stages. Blood 2012, 119:e172-e180.
42. Aingaran M., Zhang R., Law S.K., Peng Z., Undisz A., Meyer E., et al. Host cell deformability is linked to transmission in the human malaria parasite Plasmodium falciparum. Cell Microbiol 2012, 14:983-993.
43. Farfour E., Charlotte F., Settegrana C., Miyara M., Buffet P. The extravascular compartment of the bone marrow: a niche for Plasmodium falciparum gametocyte maturation?. Malar J 2012, 11:285.
44. Aguilar R., Magallon-Tejada A., Achtman A.H., Moraleda C., Joice R., Cisteró P., et al. Molecular evidence for the localization of Plasmodium falciparum immature gametocytes in bone marrow. Blood 2014, 123:959-966.
45. Luten M., Roerdinkholder-Stoelwinder B., Schaap N.P.M., de Grip W.J., Bos H.J., Bosman GJCG.M. Survival of red blood cells after transfusion: a comparison between red cells concentrates of different storage periods. Transfusion 2008, 48:1478-1485.
46. D'Alessandro A., Kriebardis A.G., Rinalducci S., Antonelou M.H., Hansen K.C., Papassideri I.S., et al. An update on red blood cell storage lesions, as gleaned through biochemistry and omics technologies. Transfusion 2015, 55:205-219.
47. D'Alessandro A., Nemkov T., Kelher M., West F.B., Schwindt R.K., Banerjee A., et al. Routine storage of red blood cell (RBC) units in additive solution-3: a comprehensive investigation of the RBC metabolome. Transfusion 2014.
48. Koch C., Li L., Figueroa P., Mihaljevic T., Svensson L., Blackstone E.H. Transfusion and pulmonary morbidity after cardiac surgery. Ann Thorac Surg 2009, 88:1410-1418.
49. Lacroix J., Hébert P.C., Fergusson D.A., Tinmouth A., Cook D.J., Marshall J.C., et al. Age of transfused blood in critically ill adults. N Engl J Med 2015, 372:1410-1418.
50. Steiner M.E., Ness P.M., Assmann S.F., Triulzi D.J., Sloan S.R., Delaney M., et al. Effects of red-cell storage duration on patients undergoing cardiac surgery. N Engl J Med 2015, 372:1419-1429.
51. Ramdani G., Naissant B., Thompson E., Breil F., Lorthiois A., Dupuy F., et al. cAMP-Signalling regulates gametocyte-infected erythrocyte deformability required for malaria parasite transmission. PLoS Pathog 2015, 11:e1004815.