Uncovering the role of erythrocytederived extracellular vesicles in malaria: From immune regulation to cell communication

Journal of Circulating Biomarkers

Volumn 3, Issue , 2014, Pages

  Ankarklev, Johan ^a,b   Hjelmqvist, Daisy ^a,b   Mantel, Pierre Yves ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cell communication; Extracellular vesicles; Inflammation; Malaria; Plasmodium falciparum

Indexed keywords

EID: 84970035903     PISSN: None     EISSN: 18494544     Source Type: Journal    
DOI: 10.5772/58596     Document Type: Review

References (103)

1. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
2. Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415: 673-679.
3. Baker DA (2010) Malaria gametocytogenesis. Mol Biochem Parasitol 172: 57-65.
4. Alano P (2007) Plasmodium falciparum gametocytes: still many secrets of a hidden life. Mol Microbiol 66: 291-302.
5. Dyer M, Day KP (2003) Regulation of the rate of asexual growth and commitment to sexual development by diffusible factors from in vitro cultures of Plasmodium falciparum. Am J Trop Med Hyg 68: 403-409.
6. Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM (2005) Membrane microparticles: two sides of the coin. Physiology (Bethesda) 20: 22-27.
7. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262: 9412-9420.
8. Bobrie A, Colombo M, Raposo G, Thery C (2011) Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 12: 1659-1668.
9. Théry C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nature Reviews Immunology 9: 581-593.
10. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659.
11. Tetta C, Ghigo E, Silengo L, Deregibus MC, Camussi G (2012) Extracellular vesicles as an emerging mechanism of cell-to-cell communication. Endocrine.
12. Wolfers J, Lozier A, Raposo G, Regnault A, Théry C, et al. (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL crosspriming. Nature Medicine 7: 297-303.
13. van der Heyde HC, Gramaglia I, Combes V, George TC, Grau GE (2011) Flow cytometric analysis of microparticles. Methods Mol Biol 699: 337-354.
14. Pattanapanyasat K, Noulsri E, Fucharoen S, Lerdwana S, Lamchiagdhase P, et al. (2004) Flow cytometric quantitation of red blood cell vesicles in thalassemia. Cytometry B Clin Cytom 57: 23-31.
15. Nilsson J, Skog J, Nordstrand A, Baranov V, Mincheva-Nilsson L, et al. (2009) Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Br J Cancer 100: 1603-1607.
16. Orozco AF, Jorgez CJ, Ramos-Perez WD, Popek EJ, Yu X, et al. (2009) Placental release of distinct DNAassociated micro-particles into maternal circulation: reflective of gestation time and preeclampsia. Placenta 30: 891-897.
17. Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, et al. (2007) Exosomes with immune modulatory features are present in human breast milk. J Immunol 179: 1969-1978.
18. Houali K, Wang X, Shimizu Y, Djennaoui D, Nicholls J, et al. (2007) A new diagnostic marker for secreted Epstein-Barr virus encoded LMP1 and BARF1 oncoproteins in the serum and saliva of patients with nasopharyngeal carcinoma. Clin Cancer Res 13: 4993-5000.
19. Kim HK, Song KS, Park YS, Kang YH, Lee YJ, et al. (2003) Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer 39: 184-191.
20. Distler JH, Pisetsky DS, Huber LC, Kalden JR, Gay S, et al. (2005) Microparticles as regulators of inflammation: novel players of cellular crosstalk in the rheumatic diseases. Arthritis Rheum 52: 3337-3348.
21. VanWijk MJ, VanBavel E, Sturk A, Nieuwland R (2003) Microparticles in cardiovascular diseases. Cardiovasc Res 59: 277-287.
22. Jy W, Horstman LL, Arce M, Ahn YS (1992) Clinical significance of platelet microparticles in autoimmune thrombocytopenias. J Lab Clin Med 119: 334-345.
23. Pattanapanyasat K, Gonwong S, Chaichompoo P, Noulsri E, Lerdwana S, et al. (2007) Activated platelet-derived microparticles in thalassaemia. Br J Haematol 136: 462-471.
24. Aupeix K, Hugel B, Martin T, Bischoff P, Lill H, et al. (1997) The significance of shed membrane particles during programmed cell death in vitro, and in vivo, in HIV-1 infection. J Clin Invest 99: 1546-1554.
25. Geisbert TW, Young HA, Jahrling PB, Davis KJ, Kagan E, et al. (2003) Mechanisms underlying coagulation abnormalities in ebola hemorrhagic fever: overexpression of tissue factor in primate monocytes/macrophages is a key event. J Infect Dis 188: 1618-1629.
26. Inal JM, Fairbrother U, Heugh S (2013) Microvesiculation and disease. Biochem Soc Trans 41: 237-240.
27. Combes V, Taylor TE, Juhan-Vague I, Mege JL, Mwenechanya J, et al. (2004) Circulating endothelial microparticles in malawian children with severe falciparum malaria complicated with coma. JAMA 291: 2542-2544.
28. Moxon CA, Chisala NV, Wassmer SC, Taylor TE, Seydel KB, et al. (2013) Persistent Endothelial Activation and Inflammation After Plasmodium falciparum Infection in Malawian Children. J Infect Dis 209: 610-615.
29. Combes V, Simon AC, Grau GE, Arnoux D, Camoin L, et al. (1999) In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J Clin Invest 104: 93-102.
30. Aringer M, Feierl E, Steiner G, Stummvoll GH, Hofler E, et al. (2002) Increased bioactive TNF in human systemic lupus erythematosus: associations with cell death. Lupus 11: 102-108.
31. Pankoui Mfonkeu JB, Gouado I, Fotso Kuate H, Zambou O, Amvam Zollo PH, et al. (2010) Elevated cell-specific microparticles are a biological marker for cerebral dysfunctions in human severe malaria. PLoS One 5: e13415.
32. Brown GV, Culvenor JG, Crewther PE, Bianco AE, Coppel RL, et al. (1985) Localization of the ringinfected erythrocyte surface antigen (RESA) of Plasmodium falciparum in merozoites and ringinfected erythrocytes. J Exp Med 162: 774-779.
33. Bocci V, Pessina GP, Paulesu L (1980) Studies of factors regulating the ageing of human erythrocytes--III. Metabolism and fate of erythrocytic vesicles. Int J Biochem 11: 139-142.
34. Nantakomol D, Dondorp AM, Krudsood S, Udomsangpetch R, Pattanapanyasat K, et al. (2011) Circulating red cell-derived microparticles in human malaria. J Infect Dis 203: 700-706.
35. Campos FM, Franklin BS, Teixeira-Carvalho A, Filho AL, de Paula SC, et al. (2010) Augmented plasma microparticles during acute Plasmodium vivax infection. Malar J 9: 327.
36. Yokota N, Koizume S, Miyagi E, Hirahara F, Nakamura Y, et al. (2009) Self-production of tissue factor-coagulation factor VII complex by ovarian cancer cells. Br J Cancer 101: 2023-2029.
37. Robert S, Poncelet P, Lacroix R, Arnaud L, Giraudo L, et al. (2009) Standardization of platelet-derived microparticle counting using calibrated beads and a Cytomics FC500 routine flow cytometer: a first step towards multicenter studies? J Thromb Haemost 7: 190-197.
38. Momen-Heravi F, Balaj L, Alian S, Mantel PY, Halleck AE, et al. (2013) Current methods for the isolation of extracellular vesicles. Biol Chem 394: 1253-1262.
39. Silamut K, Phu NH, Whitty C, Turner GD, Louwrier K, et al. (1999) A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am J Pathol 155: 395-410.
40. Schofield L, Grau GE (2005) Immunological processes in malaria pathogenesis. Nat Rev Immunol 5: 722-735.
41. Combes V, El-Assaad F, Faille D, Jambou R, Hunt NH, et al. (2010) Microvesiculation and cell interactions at the brain-endothelial interface in cerebral malaria pathogenesis. Prog Neurobiol 91: 140-151.
42. Newton CR, Krishna S (1998) Severe falciparum malaria in children: current understanding of pathophysiology and supportive treatment. Pharmacol Ther 79: 1-53.
43. Newbold C, Craig A, Kyes S, Rowe A, Fernandez-Reyes D, et al. (1999) Cytoadherence, pathogenesis and the infected red cell surface in Plasmodium falciparum. Int J Parasitol 29: 927-937.
44. Langreth SG, Peterson E (1985) Pathogenicity, stability, and immunogenicity of a knobless clone of Plasmodium falciparum in Colombian owl monkeys. Infect Immun 47: 760-766.
45. Patnaik JK, Das BS, Mishra SK, Mohanty S, Satpathy SK, et al. (1994) Vascular clogging, mononuclear cell margination, and enhanced vascular permeability in the pathogenesis of human cerebral malaria. Am J Trop Med Hyg 51: 642-647.
46. Grau GE, Mackenzie CD, Carr RA, Redard M, Pizzolato G, et al. (2003) Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect Dis 187: 461-466.
47. Satta N, Toti F, Feugeas O, Bohbot A, Dachary-Prigent J, et al. (1994) Monocyte vesiculation is a possible mechanism for dissemination of membraneassociated procoagulant activities and adhesion molecules after stimulation by lipopolysaccharide. J Immunol 153: 3245-3255.
48. Greenwalt TJ (2006) The how and why of exocytic vesicles. Transfusion 46: 143-152.
49. Hrachovinova I, Cambien B, Hafezi-Moghadam A, Kappelmayer J, Camphausen RT, et al. (2003) Interaction of P-selectin and PSGL-1 generates microparticles that correct hemostasis in a mouse model of hemophilia A. Nat Med 9: 1020-1025.
50. Pan Y, Liang H, Liu H, Li D, Chen X, et al. (2013) Platelet-Secreted MicroRNA-223 Promotes Endothelial Cell Apoptosis Induced by Advanced Glycation End Products via Targeting the Insulin-like Growth Factor 1 Receptor. J Immunol.
51. McMorran BJ, Marshall VM, de Graaf C, Drysdale KE, Shabbar M, et al. (2009) Platelets kill intraerythrocytic malarial parasites and mediate survival to infection. Science 323: 797-800.
52. McMorran BJ, Wieczorski L, Drysdale KE, Chan JA, Huang HM, et al. (2012) Platelet factor 4 and Duffy antigen required for platelet killing of Plasmodium falciparum. Science 338: 1348-1351.
53. Boilard E, Nigrovic PA, Larabee K, Watts GFM, Coblyn JS, et al. (2010) Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science (New York, NY) 327: 580-583.
54. Pain A, Ferguson DJ, Kai O, Urban BC, Lowe B, et al. (2001) Platelet-mediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci U S A 98: 1805-1810.
55. Wassmer SC, Lepolard C, Traore B, Pouvelle B, Gysin J, et al. (2004) Platelets reorient Plasmodium falciparum-infected erythrocyte cytoadhesion to activated endothelial cells. J Infect Dis 189: 180-189.
56. Wassmer SC, Combes V, Candal FJ, Juhan-Vague I, Grau GE (2006) Platelets potentiate brain endothelial alterations induced by Plasmodium falciparum. Infect Immun 74: 645-653.
57. Faille D, Combes V, Mitchell AJ, Fontaine A, Juhan-Vague I, et al. (2009) Platelet microparticles: a new player in malaria parasite cytoadherence to human brain endothelium. FASEB J 23: 3449-3458.
58. Wassmer SC, Moxon CA, Taylor T, Grau GE, Molyneux ME, et al. (2011) Vascular endothelial cells cultured from patients with cerebral or uncomplicated malaria exhibit differential reactivity to TNF. Cell Microbiol 13: 198-209.
59. Young SG, Fielding CJ (1999) The ABCs of cholesterol efflux. Nat Genet 22: 316-318.
60. Hamon Y, Broccardo C, Chambenoit O, Luciani MF, Toti F, et al. (2000) ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol 2: 399-406.
61. Combes V, Coltel N, Alibert M, van Eck M, Raymond C, et al. (2005) ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am J Pathol 166: 295-302.
62. Penet MF, Abou-Hamdan M, Coltel N, Cornille E, Grau GE, et al. (2008) Protection against cerebral malaria by the low-molecular-weight thiol pantethine. Proc Natl Acad Sci U S A 105: 1321-1326.
63. Schofield L, Tachado SD (1996) Regulation of host cell function by glycosylphosphatidylinositols of the parasitic protozoa. Immunol Cell Biol 74: 555-563.
64. Tachado SD, Gerold P, McConville MJ, Baldwin T, Quilici D, et al. (1996) Glycosylphosphatidylinositol toxin of Plasmodium induces nitric oxide synthase expression in macrophages and vascular endothelial cells by a protein tyrosine kinase-dependent and protein kinase C-dependent signaling pathway. J Immunol 156: 1897-1907.
65. Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, et al. (2007) Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci U S A 104: 1919-1924.
66. Wu X, Gowda NM, Kumar S, Gowda DC (2010) Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J Immunol 184: 4338-4348.
67. Sharma S, DeOliveira RB, Kalantari P, Parroche P, Goutagny N, et al. (2011) Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity 35: 194-207.
68. Couper KN, Barnes T, Hafalla JC, Combes V, Ryffel B, et al. (2010) Parasite-derived plasma microparticles contribute significantly to malaria infection-induced inflammation through potent macrophage stimulation. PLoS Pathog 6: e1000744.
69. Mantel PY, Hoang AN, Goldowitz I, Potashnikova D, Hamza B, et al. (2013) Malaria-Infected Erythrocyte-Derived Microvesicles Mediate Cellular Communication within the Parasite Population and with the Host Immune System. Cell Host Microbe 13: 521-534.
70. Cyrklaff M, Sanchez CP, Kilian N, Bisseye C, Simpore J, et al. (2011) Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes. Science 334: 1283-1286.
71. Lanzer M, Wickert H, Krohne G, Vincensini L, Braun Breton C (2006) Maurer's clefts: a novel multifunctional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes. Int J Parasitol 36: 23-36.
72. Kwiatkowski D, Hill AV, Sambou I, Twumasi P, Castracane J, et al. (1990) TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336: 1201-1204.
73. Sahu U, Sahoo PK, Kar SK, Mohapatra BN, Ranjit M (2013) Association of TNF level with production of circulating cellular microparticles during clinical manifestation of human cerebral malaria. Hum Immunol 74: 713-721.
74. Regev-Rudzki N, Wilson DW, Carvalho TG, Sisquella X, Coleman BM, et al. (2013) Cell-Cell Communication between Malaria-Infected Red Blood Cells via Exosome-like Vesicles. Cell 153: 1120-1133.
75. Dieckmann-Schuppert A, Franklin RM (1989) Compounds binding to cytoskeletal proteins are active against Plasmodium falciparum in vitro. Cell Biol Int Rep 13: 411-418.
76. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, et al. (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134: 48-61.
77. Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2.
78. Frank SA (1996) Models of parasite virulence. Q Rev Biol 71: 37-78.
79. Matthews KR (2005) The developmental cell biology of Trypanosoma brucei. J Cell Sci 118: 283-290.
80. Vassella E, Reuner B, Yutzy B, Boshart M (1997) Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. J Cell Sci 110 (Pt 21): 2661-2671.
81. Reuner B, Vassella E, Yutzy B, Boshart M (1997) Cell density triggers slender to stumpy differentiation of Trypanosoma brucei bloodstream forms in culture. Mol Biochem Parasitol 90: 269-280.
82. MacGregor P, Savill NJ, Hall D, Matthews KR (2011) Transmission stages dominate trypanosome withinhost dynamics during chronic infections. Cell Host Microbe 9: 310-318.
83. Mantel PY, Marti M (2014) The role of extracellular vesicles in Plasmodium and other protozoan parasites. Cell Microbiol 16: 344-354.
84. Cai J, Han Y, Ren H, Chen C, He D, et al. (2013) Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J Mol Cell Biol 5: 227-238.
85. Waldenstrom A, Genneback N, Hellman U, Ronquist G (2012) Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS One 7: e34653.
86. Guescini M, Guidolin D, Vallorani L, Casadei L, Gioacchini AM, et al. (2010) C2C12 myoblasts release micro-vesicles containing mtDNA and proteins involved in signal transduction. Exp Cell Res 316: 1977-1984.
87. Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, et al. (2011) Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2: 180.
88. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, et al. (2008) Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10: 619-624.
89. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, et al. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476.
90. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, et al. (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18: 883-891.
91. Gross JC, Chaudhary V, Bartscherer K, Boutros M (2012) Active Wnt proteins are secreted on exosomes. Nat Cell Biol 14: 1036-1045.
92. Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, et al. (2012) Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151: 1542-1556.
93. Ghosh J, Bose M, Roy S, Bhattacharyya SN (2013) Leishmania donovani targets Dicer1 to downregulate miR-122, lower serum cholesterol, and facilitate murine liver infection. Cell Host Microbe 13: 277-288.
94. Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, et al. (2000) Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med 6: 769-775.
95. Bellingham SA, Coleman BM, Hill AF (2012) Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res 40: 10937-10949.
96. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, et al. (2011) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nature communications 2: 282.
97. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, et al. (2012) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119: 756-766.
98. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, et al. (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A 107: 6328-6333.
99. Laffont B, Corduan A, Ple H, Duchez AC, Cloutier N, et al. (2013) Activated platelets can deliver mRNA regulatory Ago2*microRNA complexes to endothelial cells via microparticles. Blood 122: 253-261.
100. Forterre A, Jalabert A, Chikh K, Pesenti S, Euthine V, et al. (2014) Myotube-derived exosomal miRNAs downregulate Sirtuin1 in myoblasts during muscle cell differentiation. Cell Cycle 13.
101. LaMonte G, Philip N, Reardon J, Lacsina JR, Majoros W, et al. (2012) Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe 12: 187-199.
102. Baum J, Papenfuss AT, Mair GR, Janse CJ, Vlachou D, et al. (2009) Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res 37: 3788-3798.
103. Campbell TL, De Silva EK, Olszewski KL, Elemento O, Llinas M (2010) Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite. PLoS Pathog 6: e1001165. 9