An update on recent studies of extracellular vesicles and their role in hypercoagulability in thalassemia (Review)
- Authors:
- Phatchanat Klaihmon
- Kovit Pattanapanyasat
- Phatchariya Phannasil
-
Affiliations: Siriraj Center of Excellence for Stem Cell Research, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand, Center of Excellence for Microparticle and Exosome in Diseases, Research Department, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand, Thalassemia Research Center, Institute of Molecular Biosciences, Mahidol University, Nakhon Pathom 73170, Thailand - Published online on: December 28, 2023 https://doi.org/10.3892/br.2023.1719
- Article Number: 31
-
Copyright: © Klaihmon et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Rund D and Rachmilewitz E: Beta-thalassemia. N Engl J Med. 353:1135–1146. 2005.PubMed/NCBI View Article : Google Scholar | |
Piel FB and Weatherall DJ: The α-thalassemias. N Engl J Med. 371:1908–1916. 2014.PubMed/NCBI View Article : Google Scholar | |
Borgna-Pignatti C, Rugolotto S, De Stefano P, Zhao H, Cappellini MD, Del Vecchio GC, Romeo MA, Forni GL, Gamberini MR, Ghilardi R, et al: Survival and complications in patients with thalassemia major treated with transfusion and deferoxamine. Haematologica. 89:1187–1193. 2004.PubMed/NCBI | |
Zurlo MG, De Stefano P, Borgna-Pignatti C, Di Palma A, Piga A, Melevendi C, Di Gregorio F, Burattini MG and Terzoli S: Survival and causes of death in thalassaemia major. Lancet. 2:27–30. 1989.PubMed/NCBI View Article : Google Scholar | |
Sleiman J, Tarhini A, Bou-Fakhredin R, Saliba AN, Cappellini MD and Taher AT: Non-Transfusion-Dependent Thalassemia: An update on complications and management. Int J Mol Sci. 19(182)2018.PubMed/NCBI View Article : Google Scholar | |
Cappellini MD, Robbiolo L, Bottasso BM, Coppola R, Fiorelli G and Mannucci AP: Venous thromboembolism and hypercoagulability in splenectomized patients with thalassaemia intermedia. Br J Haematol. 111:467–473. 2000.PubMed/NCBI View Article : Google Scholar | |
Eldor A and Rachmilewitz EA: The hypercoagulable state in thalassemia. Blood. 99:36–43. 2002.PubMed/NCBI View Article : Google Scholar | |
Atichartakarn V, Angchaisuksiri P, Aryurachai K, Chuncharunee S and Thakkinstian A: In vivo platelet activation and hyperaggregation in hemoglobin E/beta-thalassemia: A consequence of splenectomy. Int J Hematol. 77:299–303. 2003.PubMed/NCBI View Article : Google Scholar | |
Atichartakarn V, Chuncharunee S, Chandanamattha P, Likittanasombat K and Aryurachai K: Correction of hypercoagulability and amelioration of pulmonary arterial hypertension by chronic blood transfusion in an asplenic hemoglobin E/beta-thalassemia patient. Blood. 103:2844–2846. 2004.PubMed/NCBI View Article : Google Scholar | |
Atichartakarn V, Angchaisuksiri P, Aryurachai K, Onpun S, Chuncharunee S, Thakkinstian A and Atamasirikul K: Relationship between hypercoagulable state and erythrocyte phosphatidylserine exposure in splenectomized haemoglobin E/beta-thalassaemic patients. Br J Haematol. 118:893–898. 2002.PubMed/NCBI View Article : Google Scholar | |
Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, et al: Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 4(27066)2015.PubMed/NCBI View Article : Google Scholar | |
Loyer X, Vion AC, Tedgui A and Boulanger CM: Microvesicles as cell-cell messengers in cardiovascular diseases. Circ Res. 114:345–353. 2014.PubMed/NCBI View Article : Google Scholar | |
Westerman M, Pizzey A, Hirschman J, Cerino M, Weil-Weiner Y, Ramotar P, Eze A, Lawrie A, Purdy G, Mackie I and Porter J: Microvesicles in haemoglobinopathies offer insights into mechanisms of hypercoagulability, haemolysis and the effects of therapy. Br J Haematol. 142:126–135. 2008.PubMed/NCBI View Article : Google Scholar | |
Aharon A, Rebibo-Sabbah A, Tzoran I and Levin C: Extracellular vesicles in hematological disorders. Rambam Maimonides Med J. 5(e0032)2014.PubMed/NCBI View Article : Google Scholar | |
Klaihmon P, Vimonpatranon S, Noulsri E, Lertthammakiat S, Anurathapan U, Sirachainan N, Hongeng S and Pattanapanyasat K: Normalized levels of red blood cells expressing phosphatidylserine, their microparticles, and activated platelets in young patients with β-thalassemia following bone marrow transplantation. Ann Hematol. 96:1741–1747. 2017.PubMed/NCBI View Article : Google Scholar | |
Klaihmon P, Lertthammakiat S, Anurathapan U, Pakakasama S, Sirachainan N, Hongeng S and Pattanapanyasat K: Activated platelets and leukocyte activations in young patients with β-thalassemia/HbE following bone marrow transplantation. Thromb Res. 169:8–14. 2018.PubMed/NCBI View Article : Google Scholar | |
Origa R: β-Thalassemia. Genet Med. 19:609–619. 2017.PubMed/NCBI View Article : Google Scholar | |
Cazzola M: Ineffective erythropoiesis and its treatment. Blood. 139:2460–2470. 2022.PubMed/NCBI View Article : Google Scholar | |
Galanello R and Origa R: Beta-thalassemia. Orphanet J Rare Dis. 5(11)2010.PubMed/NCBI View Article : Google Scholar | |
Taher AT, Otrock ZK, Uthman I and Cappellini MD: Thalassemia and hypercoagulability. Blood Rev. 22:283–292. 2008.PubMed/NCBI View Article : Google Scholar | |
Vichinsky EP: Clinical manifestations of alpha-thalassemia. Cold Spring Harb Perspect Med. 3(a011742)2013.PubMed/NCBI View Article : Google Scholar | |
Sirachainan N, Chuansumrit A, Kadegasem P, Sasanakul W, Wongwerawattanakoon P and Mahaklan L: Normal hemostatic parameters in children and young adults with α-thalassemia diseases. Thromb Res. 146:35–42. 2016.PubMed/NCBI View Article : Google Scholar | |
Pattanapanyasat K, Gonwong S, Chaichompoo P, Noulsri E, Lerdwana S, Sukapirom K, Siritanaratkul N and Fucharoen S: Activated platelet-derived microparticles in thalassaemia. Br J Haematol. 136:462–471. 2007.PubMed/NCBI View Article : Google Scholar | |
Klaihmon P, Phongpao K, Kheansaard W, Noulsri E, Khuhapinant A, Fucharoen S, Morales NP, Svasti S, Pattanapanyasat K and Chaichompoo P: Microparticles from splenectomized β-thalassemia/HbE patients play roles on procoagulant activities with thrombotic potential. Ann Hematol. 96:189–198. 2017.PubMed/NCBI View Article : Google Scholar | |
Tantawy AA, Adly AA, Ismail EA, Habeeb NM and Farouk A: Circulating platelet and erythrocyte microparticles in young children and adolescents with sickle cell disease: Relation to cardiovascular complications. Platelets. 24:605–614. 2013.PubMed/NCBI View Article : Google Scholar | |
Manodori AB, Barabino GA, Lubin BH and Kuypers FA: Adherence of phosphatidylserine-exposing erythrocytes to endothelial matrix thrombospondin. Blood. 95:1293–1300. 2000.PubMed/NCBI | |
Zahedpanah M, Azarkeivan A, Aghaieepour M, Nikogoftar M, Ahmadinegad M, Hajibeigi B, Tabatabaiee MR and Maghsudlu M: Erythrocytic phosphatidylserine exposure and hemostatic alterations in beta-thalassemia intermediate patients. Hematology. 19:472–476. 2014.PubMed/NCBI View Article : Google Scholar | |
Mahdi ZN, Al-Mudallal SS and Hameed BM: Role of red blood cells ‘annexin V’ and platelets ‘P-selectin’ in patients with thalassemia. Hematol Oncol Stem Cell Ther. 12:15–18. 2019.PubMed/NCBI View Article : Google Scholar | |
Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS and Chung JH: Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol. 27:414–421. 2007.PubMed/NCBI View Article : Google Scholar | |
Willekens FL, Were JM, Groenen-Döpp YA, Roerdinkholder-Stoelwinder B, de Pauw B and Bosman GJ: Erythrocyte vesiculation: A self-protective mechanism? Br J Haematol. 141:549–556. 2008.PubMed/NCBI View Article : Google Scholar | |
Camus SM, Gausserès B, Bonnin P, Loufrani L, Grimaud L, Charue D, De Moraes JA, Renard JM, Tedgui A, Boulanger CM, et al: Erythrocyte microparticles can induce kidney vaso-occlusions in a murine model of sickle cell disease. Blood. 120:5050–5058. 2012.PubMed/NCBI View Article : Google Scholar | |
Pattanapanyasat K, Noulsri E, Fucharoen S, Lerdwana S, Lamchiagdhase P, Siritanaratkul N and Webster HK: Flow cytometric quantitation of red blood cell vesicles in thalassemia. Cytometry B Clin Cytom. 57:23–31. 2004.PubMed/NCBI View Article : Google Scholar | |
Lamchiagdhase P, Nitipongwanich R, Rattanapong C, Noulsri E, Lerdwana S and Pattanapanyasat K: Red blood cell vesicles in thalassemia. J Med Assoc Thai. 87:233–238. 2004.PubMed/NCBI | |
Agouti I, Cointe S, Robert S, Judicone C, Loundou A, Driss F, Brisson A, Steschenko D, Rose C, Pondarré C, et al: Platelet and not erythrocyte microparticles are procoagulant in transfused thalassaemia major patients. Br J Haematol. 171:615–624. 2015.PubMed/NCBI View Article : Google Scholar | |
Youssry I, Soliman N, Ghamrawy M, Samy RM, Nasr A, Abdel Mohsen M, ElShahaat M, Bou Fakhredin R and Taher A: Circulating microparticles and the risk of thromboembolic events in Egyptian beta thalassemia patients. Ann Hematol. 96:597–603. 2017.PubMed/NCBI View Article : Google Scholar | |
Habib A, Kunzelmann C, Shamseddeen W, Zobairi F, Freyssinet JM and Taher A: Elevated levels of circulating procoagulant microparticles in patients with beta-thalassemia intermedia. Haematologica. 93:941–942. 2008.PubMed/NCBI View Article : Google Scholar | |
Nielsen MH, Beck-Nielsen H, Andersen MN and Handberg A: A flow cytometric method for characterization of circulating cell-derived microparticles in plasma. J Extracell Vesicles. 3:2014.PubMed/NCBI View Article : Google Scholar | |
Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, Dingli F, Loew D, Tkach M and Théry C: Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA. 113:E968–E977. 2016.PubMed/NCBI View Article : Google Scholar | |
Kowal EJK, Ter-Ovanesyan D, Regev A and Church GM: Extracellular Vesicle Isolation and Analysis by Western Blotting. Methods Mol Biol. 1660:143–152. 2017.PubMed/NCBI View Article : Google Scholar | |
Tijssen MR, Cvejic A, Joshi A, Hannah RL, Ferreira R, Forrai A, Bellissimo DC, Oram SH, Smethurst PA, Wilson NK, et al: Genome-wide analysis of simultaneous GATA1/2, RUNX1, FLI1, and SCL binding in megakaryocytes identifies hematopoietic regulators. Dev Cell. 20:597–609. 2011.PubMed/NCBI View Article : Google Scholar | |
Rikkert LG, Nieuwland R, Terstappen Lwmm and Coumans FAW: Quality of extracellular vesicle images by transmission electron microscopy is operator and protocol dependent. J Extracell Vesicles. 8(1555419)2019.PubMed/NCBI View Article : Google Scholar | |
El Andaloussi S, Mäger I, Breakefield XO and Wood MJA: Extracellular vesicles: Biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 12:347–357. 2013.PubMed/NCBI View Article : Google Scholar | |
Lee H, He X, Le T, Carnino JM and Jin Y: Single-step RT-qPCR for detection of extracellular vesicle microRNAs in vivo: A time- and cost-effective method. Am J Physiol Lung Cell Mol Physiol. 318:L742–l749. 2020.PubMed/NCBI View Article : Google Scholar | |
Comfort N, Cai K, Bloomquist TR, Strait MD, Ferrante AW Jr and Baccarelli AA: Nanoparticle tracking analysis for the quantification and size determination of extracellular vesicles. J Vis Exp: Mar 28, 2021 (Epub ahead of print). doi: 10.3791/62447. | |
Chaichompoo P, Kumya P, Khowawisetsut L, Chiangjong W, Chaiyarit S, Pongsakul N, Sirithanaratanakul N, Fucharoen S, Thongboonkerd V and Pattanapanyasat K: Characterizations and proteome analysis of platelet-free plasma-derived microparticles in β-thalassemia/hemoglobin E patients. J Proteomics 76 Spec No.: 239-250, 2012. | |
Kittivorapart J, Crew VK, Wilson MC, Heesom KJ, Siritanaratkul N and Toye AM: Quantitative proteomics of plasma vesicles identify novel biomarkers for hemoglobin E/β-thalassemic patients. Blood Adv. 2:95–104. 2018.PubMed/NCBI View Article : Google Scholar | |
Ferru E, Pantaleo A, Carta F, Mannu F, Khadjavi A, Gallo V, Ronzoni L, Graziadei G, Cappellini MD and Turrini F: Thalassemic erythrocytes release microparticles loaded with hemichromes by redox activation of p72Syk kinase. Haematologica. 99:570–578. 2014.PubMed/NCBI View Article : Google Scholar | |
Levin C, Koren A, Rebibo-Sabbah A, Koifman N, Brenner B and Aharon A: Extracellular Vesicle Characteristics in β-thalassemia as Potential Biomarkers for Spleen Functional Status and Ineffective Erythropoiesis. Front Physiol. 9(1214)2018.PubMed/NCBI View Article : Google Scholar | |
Tzounakas VL, Anastasiadi AT, Dzieciatkowska M, Karadimas DG, Stamoulis K, Papassideri IS, Hansen KC, D'Alessandro A, Kriebardis AG and Antonelou MH: Proteome of Stored RBC membrane and vesicles from heterozygous beta thalassemia donors. Int J Mol Sci. 22(3369)2021.PubMed/NCBI View Article : Google Scholar | |
Elsayh KI, Zahran AM, El-Abaseri TB, Mohamed AO and El-Metwally TH: Hypoxia biomarkers, oxidative stress, and circulating microparticles in pediatric patients with thalassemia in Upper Egypt. Clin Appl Thromb Hemost. 20:536–545. 2014.PubMed/NCBI View Article : Google Scholar | |
Adly AA, El-Sherif NH, Ismail EA, El-Zaher YA, Farouk A, El-Refaey AM and Wahba MS: Vascular dysfunction in patients with young β-thalassemia: Relation to cardiovascular complications and subclinical atherosclerosis. Clin Appl Thromb Hemost. 21:733–744. 2015.PubMed/NCBI View Article : Google Scholar | |
Manakeng K, Prasertphol P, Phongpao K, Chuncharunee S, Tanyong D, Worawichawong S, Svasti S and Chaichompoo P: Elevated levels of platelet- and red cell-derived extracellular vesicles in transfusion-dependent β-thalassemia/HbE patients with pulmonary arterial hypertension. Ann Hematol. 98:281–288. 2019.PubMed/NCBI View Article : Google Scholar | |
Li N, Wu B, Wang J, Yan Y, An P, Li Y, Liu Y, Hou Y, Qing X, Niu L, et al: Differential proteomic patterns of plasma extracellular vesicles show potential to discriminate β-thalassemia subtypes. iScience. 26(106048)2023.PubMed/NCBI View Article : Google Scholar | |
Chaemsaithong P, Luewan S, Taweevisit M, Chiangjong W, Pongchaikul P, Thorner PS, Tongsong T and Chutipongtanate S: Placenta-Derived extracellular vesicles in pregnancy complications and prospects on a liquid biopsy for hemoglobin Bart's Disease. Int J Mol Sci. 24(5658)2023.PubMed/NCBI View Article : Google Scholar | |
Kheansaard W, Phongpao K, Paiboonsukwong K, Pattanapanyasat K, Chaichompoo P and Svasti S: Microparticles from β-thalassaemia/HbE patients induce endothelial cell dysfunction. Sci Rep. 8(13033)2018.PubMed/NCBI View Article : Google Scholar | |
Klaihmon P, Khuhapinant A, Kheansaard W and Pattanapanyasat K: Internalization of cell-derived microparticles triggers endothelial pro-inflammatory responses. Asian Pac J Allergy Immunol: Apr 18, 2021 (Epub ahead of print). | |
Atipimonpat A, Siwaponanan P, Khuhapinant A, Svasti S, Sukapirom K, Khowawisetsut L and Pattanapanyasat K: Extracellular vesicles from thalassemia patients carry iron-containing ferritin and hemichrome that promote cardiac cell proliferation. Ann Hematol. 100:1929–1946. 2021.PubMed/NCBI View Article : Google Scholar | |
Sun KT, Huang YN, Palanisamy K, Chang SS, Wang IK, Wu KH, Chen P, Peng CT and Li CY: Reciprocal regulation of ү-globin expression by exo-miRNAs: Relevance to ү-globin silencing in β-thalassemia major. Sci Rep. 7(202)2017.PubMed/NCBI View Article : Google Scholar | |
Levin C, Koren A, Rebibo-Sabbah A, Levin M, Koifman N, Brenner B and Aharon A: Extracellular Vesicle MicroRNA That Are Involved in β-Thalassemia complications. Int J Mol Sci. 22(9760)2021.PubMed/NCBI View Article : Google Scholar | |
Anurathapan U, Hongeng S, Pakakasama S, Sirachainan N, Songdej D, Chuansumrit A, Charoenkwan P, Jetsrisuparb A, Sanpakit K, Rujkijyanont P, et al: Hematopoietic stem cell transplantation for homozygous β-thalassemia and β-thalassemia/hemoglobin E patients from haploidentical donors. Bone Marrow Transplant. 51:813–818. 2016.PubMed/NCBI View Article : Google Scholar | |
Anurathapan U, Hongeng S, Pakakasama S, Songdej D, Sirachainan N, Pongphitcha P, Chuansumrit A, Charoenkwan P, Jetsrisuparb A, Sanpakit K, et al: Hematopoietic stem cell transplantation for severe thalassemia patients from haploidentical donors using a novel conditioning regimen. Biol Blood Marrow Transplant. 26:1106–1112. 2020.PubMed/NCBI View Article : Google Scholar | |
Lertthammakiat S, Sitthirat P, Anurathapan U, Songdej D, Pakakasama S, Chuansumrit A, Putawornsub N, Sirasittikarn S, Wantanawijarn S, Kadegasem P, et al: No differences in hemostatic and endothelial activations between haploidentical and matched-donor hematopoietic stem cell transplantation in thalassemia disease. Thromb J. 18(21)2020.PubMed/NCBI View Article : Google Scholar | |
Sirachainan N, Thongsad J, Pakakasama S, Hongeng S, Chuansumrit A, Kadegasem P, Tirakanjana A, Archararit N and Sirireung S: Normalized coagulation markers and anticoagulation proteins in children with severe β-thalassemia disease after stem cell transplantation. Thromb Res. 129:765–770. 2012.PubMed/NCBI View Article : Google Scholar | |
Trummer A, De Rop C, Stadler M, Ganser A and Buchholz S: P-selectin glycoprotein ligand-1 positive microparticles in allogeneic stem cell transplantation of hematologic malignancies. Exp Hematol. 9:1047–1055. 2011.PubMed/NCBI View Article : Google Scholar | |
Ataga KI, Cappellini MD and Rachmilewitz EA: Beta-thalassaemia and sickle cell anaemia as paradigms of hypercoagulability. Br J Haematol. 139:3–13. 2007.PubMed/NCBI View Article : Google Scholar | |
Garnier Y, Ferdinand S, Garnier M, Cita KC, Hierso R, Claes A, Connes P, Hardy-Dessources MD, Lapouméroulie C, Lemonne N, et al: Plasma microparticles of sickle patients during crisis or taking hydroxyurea modify endothelium inflammatory properties. Blood. 136:247–256. 2020.PubMed/NCBI View Article : Google Scholar | |
Camus SM, De Moraes JA, Bonnin P, Abbyad P, Le Jeune S, Lionnet F, Loufrani L, Grimaud L, Lambry JC, Charue D, et al: Circulating cell membrane microparticles transfer heme to endothelial cells and trigger vasoocclusions in sickle cell disease. Blood. 125:3805–3814. 2015.PubMed/NCBI View Article : Google Scholar | |
An R, Man Y, Cheng K, Zhang T, Chen C, Wang F, Abdulla F, Kucukal E, Wulftange WJ, Goreke U, et al: Sickle red blood cell-derived extracellular vesicles activate endothelial cells and enhance sickle red cell adhesion mediated by von Willebrand factor. Br J Haematol. 201:552–563. 2023.PubMed/NCBI View Article : Google Scholar | |
van Beers EJ, Schaap MC, Berckmans RJ, Nieuwland R, Sturk A, van Doormaal FF, Meijers JC and Biemond BJ: CURAMA study group. Circulating erythrocyte-derived microparticles are associated with coagulation activation in sickle cell disease. Haematologica. 94:1513–1519. 2009.PubMed/NCBI View Article : Google Scholar | |
Nebor D, Bowers A, Connes P, Hardy-Dessources MD, Knight-Madden J, Cumming V, Reid M and Romana M: Plasma concentration of platelet-derived microparticles is related to painful vaso-occlusive phenotype severity in sickle cell anemia. PLoS One. 9(e87243)2014.PubMed/NCBI View Article : Google Scholar | |
Gerotziafas GT, Van Dreden P, Chaari M, Galea V, Khaterchi A, Lionnet F, Stankovic-Stojanovic K, Blanc-Brude O, Woodhams B, Maier-Redelsperger M, et al: The acceleration of the propagation phase of thrombin generation in patients with steady-state sickle cell disease is associated with circulating erythrocyte-derived microparticles. Thromb Haemost. 107:1044–1052. 2012.PubMed/NCBI View Article : Google Scholar | |
Smith RA, Mankelow TJ, Drizou D, Bullock T, Latham T, Trompeter S, Blair A and Anstee DJ: Large red cell-derived membrane particles are major contributors to hypercoagulability in sickle cell disease. Sci Rep. 11(11035)2021.PubMed/NCBI View Article : Google Scholar | |
Nouraie M, Lee JS, Zhang Y, Kanias T, Zhao X, Xiong Z, Oriss TB, Zeng Q, Kato GJ, Gibbs JS, et al: The relationship between the severity of hemolysis, clinical manifestations and risk of death in 415 patients with sickle cell anemia in the US and Europe. Haematologica. 98:464–472. 2013.PubMed/NCBI View Article : Google Scholar | |
Garnier Y, Ferdinand S, Connes P, Garnier M, Etienne-Julan M, Lemonne N and Romana M: Decrease of externalized phosphatidylserine density on red blood cell-derived microparticles in SCA patients treated with hydroxycarbamide. Br J Haematol. 182:448–451. 2018.PubMed/NCBI View Article : Google Scholar | |
Hierso R, Lemonne N, Villaescusa R, Lalanne-Mistrih ML, Charlot K, Etienne-Julan M, Tressières B, Lamarre Y, Tarer V, Garnier Y, et al: Exacerbation of oxidative stress during sickle vaso-occlusive crisis is associated with decreased anti-band 3 autoantibodies rate and increased red blood cell-derived microparticle level: A prospective study. Br J Haematol. 176:805–813. 2017.PubMed/NCBI View Article : Google Scholar | |
Marsh A, Schiffelers R, Kuypers F, Larkin S, Gildengorin G, van Solinge W and Hoppe C: Microparticles as biomarkers of osteonecrosis of the hip in sickle cell disease. Br J Haematol. 168:135–138. 2015.PubMed/NCBI View Article : Google Scholar | |
Olatunya OS, Lanaro C, Longhini AL, Penteado CFF, Fertrin KY, Adekile A, Saad STO and Costa FF: Red blood cells microparticles are associated with hemolysis markers and may contribute to clinical events among sickle cell disease patients. Ann Hematol. 98:2507–2521. 2019.PubMed/NCBI View Article : Google Scholar | |
Khalyfa A, Khalyfa AA, Akbarpour M, Connes P, Romana M, Lapping-Carr G, Zhang C, Andrade J and Gozal D: Extracellular microvesicle microRNAs in children with sickle cell anaemia with divergent clinical phenotypes. Br J Haematol. 174:786–798. 2016.PubMed/NCBI View Article : Google Scholar |