Anti-Self Phosphatidylserine Antibodies Recognize Uninfected Erythrocytes Promoting Malarial Anemia

Cell Host and Microbe

Volumn 19, Issue 2, 2016, Pages 194-203

  Fernandez Arias, Cristina ^a   Rivera Correa, Juan ^a   Gallego Delgado, Julio ^a   Rudlaff, Rachel ^a   Fernandez, Clemente ^c   Roussel, Camille ^b   Götz, Anton ^a   Gonzalez, Sandra ^a   Mohanty, Akshaya ^d   Mohanty, Sanjib ^e   Wassmer, Samuel ^a   Buffet, Pierre ^b   Ndour, Papa Alioune ^b   Rodriguez, Ana ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b France   (France)

^c UNIVERSIDAD CARLOS III DE MADRID   (Spain)

^d Institute of Life Sciences Laboratory   (India)

^e ISPAT GENERAL HOSPITAL   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CD47 ANTIGEN; HEMOGLOBIN; PHOSPHATIDYLSERINE; PHOSPHATIDYLSERINE ANTIBODY; UNCLASSIFIED DRUG; PROTOZOON ANTIBODY;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; HEMOGLOBIN DETERMINATION; MALARIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RETICULOCYTE; ANIMAL; COMPLICATION; FEMALE; HUMAN; IMMUNOLOGY; MALARIA FALCIPARUM; MALE; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM;

ANEMIA; ANIMALS; ANTIBODIES, PROTOZOAN; ERYTHROCYTES; FEMALE; HUMANS; MALARIA, FALCIPARUM; MALE; MICE; PHAGOCYTOSIS; PHOSPHATIDYLSERINES; PLASMODIUM FALCIPARUM;

EID: 85011977317     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.01.009     Document Type: Article

References (51)

1. Adu, D., Williams, D.G., Quakyi, I.A., Voller, A., Anim-Addo, Y., Bruce-Tagoe, A.A., Johnson, G.D., Holborow, E.J., Anti-ssDNA and antinuclear antibodies in human malaria. Clin. Exp. Immunol. 49 (1982), 310–316.
2. Alzoubi, K., Calabro, S., Bissinger, R., Abed, M., Faggio, C., Lang, F., Stimulation of suicidal erythrocyte death by artesunate. Cell. Physiol. Biochem. 34 (2014), 2232–2244.
3. Arese, P., Turrini, F., Schwarzer, E., Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell. Physiol. Biochem. 16 (2005), 133–146.
4. Banerjee, R., Khandelwal, S., Kozakai, Y., Sahu, B., Kumar, S., CD47 regulates the phagocytic clearance and replication of the Plasmodium yoelii malaria parasite. Proc. Natl. Acad. Sci. USA 112 (2015), 3062–3067.
5. Berzins, K., Wahlgren, M., Perlmann, P., Studies on the specificity of anti-erythrocyte antibodies in the serum of patients with malaria. Clin. Exp. Immunol. 54 (1983), 313–318.
6. Biemba, G., Gordeuk, V.R., Thuma, P.E., Mabeza, G.F., Weiss, G., Prolonged macrophage activation and persistent anaemia in children with complicated malaria. Trop. Med. Int. Health 3 (1998), 60–65.
7. Buttari, B., Profumo, E., Riganò, R., Crosstalk between red blood cells and the immune system and its impact on atherosclerosis. BioMed Res. Int., 2015, 2015, 616834.
8. Collins, W.E., Jeffery, G.M., Roberts, J.M., A retrospective examination of anemia during infection of humans with Plasmodium vivax. Am. J. Trop. Med. Hyg. 68 (2003), 410–412.
9. Consigny, P.H., Cauquelin, B., Agnamey, P., Comby, E., Brasseur, P., Ballet, J.J., Roussilhon, C., High prevalence of co-factor independent anticardiolipin antibodies in malaria exposed individuals. Clin. Exp. Immunol. 127 (2002), 158–164.
10. Daniel Ribeiro, C.T., de Roquefeuil, S., Druilhe, P., Monjour, L., Homberg, J.C., Gentilini, M., Abnormal anti-single stranded (ss) DNA activity in sera from Plasmodium falciparum infected individuals. Trans. R. Soc. Trop. Med. Hyg. 78 (1984), 742–746.
11. Das, B.S., Nanda, N.K., Evidence for erythrocyte lipid peroxidation in acute falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 93 (1999), 58–62.
12. de Jong, K., Emerson, R.K., Butler, J., Bastacky, J., Mohandas, N., Kuypers, F.A., Short survival of phosphatidylserine-exposing red blood cells in murine sickle cell anemia. Blood 98 (2001), 1577–1584.
13. Elkon, K.B., Silverman, G.J., Naturally occurring autoantibodies to apoptotic cells. Adv. Exp. Med. Biol. 750 (2012), 14–26.
14. Evans, K.J., Hansen, D.S., van Rooijen, N., Buckingham, L.A., Schofield, L., Severe malarial anemia of low parasite burden in rodent models results from accelerated clearance of uninfected erythrocytes. Blood 107 (2006), 1192–1199.
15. Facer, C.A., Direct Coombs antiglobulin reactions in Gambian children with Plasmodium falciparum malaria. II. Specificity of erythrocyte-bound IgG. Clin. Exp. Immunol. 39 (1980), 279–288.
16. Facer, C.A., Agiostratidou, G., High levels of anti-phospholipid antibodies in uncomplicated and severe Plasmodium falciparum and in P. vivax malaria. Clin. Exp. Immunol. 95 (1994), 304–309.
17. Ghosh, K., Ghosh, K., Pathogenesis of anemia in malaria: a concise review. Parasitol. Res. 101 (2007), 1463–1469.
18. Giribaldi, G., Ulliers, D., Mannu, F., Arese, P., Turrini, F., Growth of Plasmodium falciparum induces stage-dependent haemichrome formation, oxidative aggregation of band 3, membrane deposition of complement and antibodies, and phagocytosis of parasitized erythrocytes. Br. J. Haematol. 113 (2001), 492–499.
19. Haldar, K., Mohandas, N., Malaria, erythrocytic infection, and anemia. Hematology Am. Soc. Hematol. Educ. Program 2009 (2009), 87–93.
20. Helegbe, G.K., Huy, N.T., Yanagi, T., Shuaibu, M.N., Yamazaki, A., Kikuchi, M., Yasunami, M., Hirayama, K., Rate of red blood cell destruction varies in different strains of mice infected with Plasmodium berghei-ANKA after chronic exposure. Malar. J., 8, 2009, 91.
21. Ho, M., White, N.J., Looareesuwan, S., Wattanagoon, Y., Lee, S.H., Walport, M.J., Bunnag, D., Harinasuta, T., Splenic Fc receptor function in host defense and anemia in acute Plasmodium falciparum malaria. J. Infect. Dis. 161 (1990), 555–561.
22. Jakeman, G.N., Saul, A., Hogarth, W.L., Collins, W.E., Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 119 (1999), 127–133.
23. Jakobsen, P.H., Morris-Jones, S.D., Hviid, L., Theander, T.G., Høier-Madsen, M., Bayoumi, R.A., Greenwood, B.M., Anti-phospholipid antibodies in patients with Plasmodium falciparum malaria. Immunology 79 (1993), 653–657.
24. Jauréguiberry, S., Ndour, P.A., Roussel, C., Ader, F., Safeukui, I., Nguyen, M., Biligui, S., Ciceron, L., Mouri, O., Kendjo, E., et al., French Artesunate Working Group. Postartesunate delayed hemolysis is a predictable event related to the lifesaving effect of artemisinins. Blood 124 (2014), 167–175.
25. Kulkarni, A.G., Suryakar, A.N., Sardeshmukh, A.S., Rathi, D.B., Studies on biochemical changes with special reference to oxidant and antioxidants in malaria patients. Indian J. Clin. Biochem. 18 (2003), 136–149.
26. Lamikanra, A.A., Brown, D., Potocnik, A., Casals-Pascual, C., Langhorne, J., Roberts, D.J., Malarial anemia: of mice and men. Blood 110 (2007), 18–28.
27. Mendis, K.N., David, P.H., Hommel, M., Carter, R., Miller, L.H., Immunity to malarial antigens on the surface of Plasmodium falciparum-infected erythrocytes. Am. J. Trop. Med. Hyg. 32 (1983), 926–930.
28. Oldenborg, P.A., Role of CD47 in erythroid cells and in autoimmunity. Leuk. Lymphoma 45 (2004), 1319–1327.
29. Owens, S., Chamley, L.W., Ordi, J., Brabin, B.J., Johnson, P.M., The association of anti-phospholipid antibodies with parity in placental malaria. Clin. Exp. Immunol. 142 (2005), 512–518.
30. Price, R.N., Simpson, J.A., Nosten, F., Luxemburger, C., Hkirjaroen, L., ter Kuile, F., Chongsuphajaisiddhi, T., White, N.J., Factors contributing to anemia after uncomplicated falciparum malaria. Am. J. Trop. Med. Hyg. 65 (2001), 614–622.
31. Ravichandran, K.S., Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 35 (2011), 445–455.
32. Ravindran, B., Satapathy, A.K., Das, M.K., Naturally-occurring anti-alpha-galactosyl antibodies in human Plasmodium falciparum infections—a possible role for autoantibodies in malaria. Immunol. Lett. 19 (1988), 137–141.
33. Ritter, K., Kuhlencord, A., Thomssen, R., Bommer, W., Prolonged haemolytic anaemia in malaria and autoantibodies against triosephosphate isomerase. Lancet 342 (1993), 1333–1334.
34. Rolling, T., Wichmann, D., Schmiedel, S., Burchard, G.D., Kluge, S., Cramer, J.P., Artesunate versus quinine in the treatment of severe imported malaria: comparative analysis of adverse events focussing on delayed haemolysis. Malar. J., 12, 2013, 241.
35. Rolling, T., Agbenyega, T., Issifou, S., Adegnika, A.A., Sylverken, J., Spahlinger, D., Ansong, D., Löhr, S.J., Burchard, G.D., May, J., et al. Delayed hemolysis after treatment with parenteral artesunate in African children with severe malaria–a double-center prospective study. J. Infect. Dis. 209 (2014), 1921–1928.
36. Satapathy, A.K., Das, M.K., Ravindran, B., Murine malaria: anti-erythrocytic antibodies recognize N-acetyl neuraminic acid residues. Immunology 80 (1993), 546–552.
37. Sène, D., Piette, J.C., Cacoub, P., Antiphospholipid antibodies, antiphospholipid syndrome and infections. Autoimmun. Rev. 7 (2008), 272–277.
38. Skouri, H., Gandouz, R., Kraiem, I., Harrabi, I., Ben Said, M., Antibodies to anionic phospholipids and cofactors in kala-azar. Comparative study with malaria, toxoplasmosis and “autoimmune diseases”. Clin. Exp. Rheumatol. 26 (2008), 894–902.
39. Sosale, N.G., Spinler, K.R., Alvey, C., Discher, D.E., Macrophage engulfment of a cell or nanoparticle is regulated by unavoidable opsonization, a species-specific ‘Marker of Self’ CD47, and target physical properties. Curr. Opin. Immunol. 35 (2015), 107–112.
40. Stoute, J.A., Odindo, A.O., Owuor, B.O., Mibei, E.K., Opollo, M.O., Waitumbi, J.N., Loss of red blood cell-complement regulatory proteins and increased levels of circulating immune complexes are associated with severe malarial anemia. J. Infect. Dis. 187 (2003), 522–525.
41. Ternynck, T., Falanga, P.B., Unterkirscher, C., Gregoire, J., da Silva, L.P., Avrameas, S., Induction of high levels of IgG autoantibodies in mice infected with Plasmodium chabaudi. Int. Immunol. 3 (1991), 29–37.
42. Toplak, N., Avcin, T., Influenza and autoimmunity. Ann. N Y Acad. Sci. 1173 (2009), 619–626.
43. Totino, P.R., Magalhães, A.D., Silva, L.A., Banic, D.M., Daniel-Ribeiro, C.T., Ferreira-da-Cruz, Mde.F., Apoptosis of non-parasitized red blood cells in malaria: a putative mechanism involved in the pathogenesis of anaemia. Malar. J., 9, 2010, 350.
44. Uyoga, S., Skorokhod, O.A., Opiyo, M., Orori, E.N., Williams, T.N., Arese, P., Schwarzer, E., Transfer of 4-hydroxynonenal from parasitized to non-parasitized erythrocytes in rosettes. Proposed role in severe malaria anemia. Br. J. Haematol. 157 (2012), 116–124.
45. van Engeland, M., Nieland, L.J., Ramaekers, F.C., Schutte, B., Reutelingsperger, C.P., Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31 (1998), 1–9.
46. Vergani, D., Mieli-Vergani, G., Autoimmune manifestations in viral hepatitis. Semin. Immunopathol. 35 (2013), 73–85.
47. von Landenberg, P., Lehmann, H.W., Modrow, S., Human parvovirus B19 infection and antiphospholipid antibodies. Autoimmun. Rev. 6 (2007), 278–285.
48. Woodruff, A.W., Ansdell, V.E., Pettitt, L.E., Cause of anaemia in malaria. Lancet 1 (1979), 1055–1057.
49. World Health Organization. Severe falciparum malaria. World Health Organization, Communicable Diseases Cluster. Trans. R. Soc. Trop. Med. Hyg. 94:Suppl 1 (2000), S1–S90.
50. Zouali, M., Druilhe, P., Eyquem, A., IgG-subclass expression of anti-DNA and anti-ribonucleoprotein autoantibodies in human malaria. Clin. Exp. Immunol. 66 (1986), 273–278.
51. Zuckerman, A., Autoimmunization and other types of indirect damage to host cells as factors in certain protozoan diseases. Exp. Parasitol. 15 (1964), 138–183.