#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

ABO Blood Groups Influence Macrophage-mediated Phagocytosis of -infected Erythrocytes


Erythrocyte polymorphisms associated with a survival advantage to Plasmodium falciparum infection have undergone positive selection. There is a predominance of blood group O in malaria-endemic regions, and several lines of evidence suggest that ABO blood groups may influence the outcome of P. falciparum infection. Based on the hypothesis that enhanced innate clearance of infected polymorphic erythrocytes is associated with protection from severe malaria, we investigated whether P. falciparum-infected O erythrocytes are more efficiently cleared by macrophages than infected A and B erythrocytes. We show that human macrophages in vitro and mouse monocytes in vivo phagocytose P. falciparum-infected O erythrocytes more avidly than infected A and B erythrocytes and that uptake is associated with increased hemichrome deposition and high molecular weight band 3 aggregates in infected O erythrocytes. Using infected A1, A2, and O erythrocytes, we demonstrate an inverse association of phagocytic capacity with the amount of A antigen on the surface of infected erythrocytes. Finally, we report that enzymatic conversion of B erythrocytes to type as O before infection significantly enhances their uptake by macrophages to observed level comparable to that with infected O wild-type erythrocytes. These data provide the first evidence that ABO blood group antigens influence macrophage clearance of P. falciparum-infected erythrocytes and suggest an additional mechanism by which blood group O may confer resistance to severe malaria.


Vyšlo v časopise: ABO Blood Groups Influence Macrophage-mediated Phagocytosis of -infected Erythrocytes. PLoS Pathog 8(10): e32767. doi:10.1371/journal.ppat.1002942
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002942

Souhrn

Erythrocyte polymorphisms associated with a survival advantage to Plasmodium falciparum infection have undergone positive selection. There is a predominance of blood group O in malaria-endemic regions, and several lines of evidence suggest that ABO blood groups may influence the outcome of P. falciparum infection. Based on the hypothesis that enhanced innate clearance of infected polymorphic erythrocytes is associated with protection from severe malaria, we investigated whether P. falciparum-infected O erythrocytes are more efficiently cleared by macrophages than infected A and B erythrocytes. We show that human macrophages in vitro and mouse monocytes in vivo phagocytose P. falciparum-infected O erythrocytes more avidly than infected A and B erythrocytes and that uptake is associated with increased hemichrome deposition and high molecular weight band 3 aggregates in infected O erythrocytes. Using infected A1, A2, and O erythrocytes, we demonstrate an inverse association of phagocytic capacity with the amount of A antigen on the surface of infected erythrocytes. Finally, we report that enzymatic conversion of B erythrocytes to type as O before infection significantly enhances their uptake by macrophages to observed level comparable to that with infected O wild-type erythrocytes. These data provide the first evidence that ABO blood group antigens influence macrophage clearance of P. falciparum-infected erythrocytes and suggest an additional mechanism by which blood group O may confer resistance to severe malaria.


Zdroje

1. MurrayCJ, RosenfeldLC, LimSS, AndrewsKG, ForemanKJ, et al. (2012) Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413–431.

2. CsertiCM, DzikWH (2007) The ABO blood group system and Plasmodium falciparum malaria. Blood 110: 2250–2258.

3. KwiatkowskiDP (2005) How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet 77: 171–192.

4. RuwendeC, KhooSC, SnowRW, et al. (1995) Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 376: 246–249.

5. AllisonAC (1954) The distribution of the sickle-cell trait in East Africa and elsewhere, and its apparent relationship to the incidence of subtertian malaria. Trans R Soc Trop Med Hyg 48: 312–318.

6. AllenSJ, O'DonnellA, AlexanderND, AlpersMP, PetoTE, et al. (1997) alpha+-Thalassemia protects children against disease caused by other infections as well as malaria. Proc Natl Acad Sci U S A 94: 14736–14741.

7. RoubinetF, DespiauS, CalafellF, JinF, BertranpetitJ, et al. (2004) Evolution of the O alleles of the human ABO blood group gene. Transfusion 44: 707–715.

8. YamamotoF, ClausenH, WhiteT, MarkenJ, HakomoriS (1990) Molecular genetic basis of the histo-blood group ABO system. Nature 345: 229–233.

9. StorryJR, OlssonML (2009) The ABO blood group system revisited: a review and update. Immunohematology 25: 48–59.

10. BergerSA, YoungNA, EdbergSC (1989) Relationship between infectious diseases and human blood type. Eur J Clin Microbiol Infect Dis 8: 681–689.

11. FischerPR, BooneP (1998) Short report: severe malaria associated with blood group. Am J Trop Med Hyg 58: 122–123.

12. RoweJA, HandelIG, TheraMA, DeansAM, LykeKE, et al. (2007) Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci U S A 104: 17471–17476.

13. PathiranaSL, AllesHK, BandaraS, Phone-KyawM, PereraMK, et al. (2005) ABO-blood-group types and protection against severe, Plasmodium falciparum malaria. Ann Trop Med Parasitol 99: 119–124.

14. FryAE, GriffithsMJ, AuburnS, DiakiteM, FortonJT, et al. (2008) Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet 17: 567–576.

15. LellB, MayJ, Schmidt-OttRJ, LehmanLG, LucknerD, et al. (1999) The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis 28: 794–799.

16. SaitouN, YamamotoF (1997) Evolution of primate ABO blood group genes and their homologous genes. Mol Biol Evol 14: 399–411.

17. MartinSK, MillerLH, HicksCU, David-WestA, UgbodeC, DeaneM (1979) Frequency of blood group antigens in Nigerian children with falciparum malaria. Trans R Soc Trop Med Hyg 73: 216–218.

18. ChungWY, GardinerDL, HylandC, GattonM, KempDJ, TrenholmeKR (2005) Enhanced invasion of blood group A1 erythrocytes by Plasmodium falciparum. Mol Biochem Parasitol 144: 128–130.

19. Mercereau-PuijalonO, GuillotteM, Vigan-WomasI (2008) Rosetting in Plasmodium falciparum: a cytoadherence phenotype with multiple actors. Transfus Clin Biol 15: 62–71.

20. LoscertalesMP, OwensS, O'DonnellJ, BunnJ, Bosch-CapblanchX, BrabinBJ (2007) ABO blood group phenotypes and Plasmodium falciparum malaria: unlocking a pivotal mechanism. Adv Parasitol 65: 1–50.

21. PipitapornB, SueblinvongT, Dharmkrong-atA, UdomsangpetchR (2000) Rosetting of Plasmodium falciparum required multiple components of the uninfected erythrocytes. Asian Pac J Allergy Immunol 18: 29–35.

22. BarraganA, KremsnerPG, WahlgrenM, CarlsonJ (2000) Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun 68: 2971–2975.

23. CarlsonJ, WahlgrenM (1992) Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 176: 1311–1317.

24. CarlsonJ (1993) Erythrocyte rosetting in Plasmodium falciparum malaria–with special reference to the pathogenesis of cerebral malaria. Scand J Infect Dis Suppl 86: 1–79.

25. Lutz HU (1990) Erythrocyte clearance. In: Blood cells Subcellular Biochemistry. Vol 17. Harris JR editors. New York: Plenum. pp. 81–120.

26. CappadoroM, GiribaldiG, O'BrienE, TurriniF, MannuF, et al. (1998) Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 92: 2527–2534.

27. AyiK, TurriniF, PigaA, AreseP (2004) Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 104: 3364–3371.

28. AyiK, Min-OoG, SerghidesL, CrockettM, Kirby-AllenM, et al. (2008) Pyruvate kinase deficiency and malaria. N Engl J Med 358: 1805–1810.

29. ErdmanLK, CosioG, HelmersAJ, GowdaDC, GrinsteinS, KainKC (2009) CD36 and TLR interactions in inflammation and phagocytosis: implication for malaria. J Immunology 183: 6452–6459.

30. PatelSN, SerghidesL, SmithTG, FebbraioM, SilversteinRL, et al. (2004) CD36 mediates the phagocytosis of Plasmodium falciparum-infected erythrocytes by rodent macrophages. J Infect Dis 189: 204–213.

31. SerghidesL, PatelSN, AyiK, KainKC (2006) Placental chondroitin sulfate A-binding malarial isolates evade innate phagocytic clearance. J Infect Dis 194: 133–139.

32. ClausenH, HakomoriS (1989) ABH and related histo-blood group antigens; immunochemical differences in carrier isotypes and their distribution. Vox Sang 56: 1–20.

33. YamamotoF, McNeillPD, HakomoriS (1992) Human histo-blood group A2 transferase coded by A2 allele, one of the A subtypes, is characterized by a single base deletion in the coding sequence, which results in an additional domain at the carboxyl terminal. Biochem Biophys Res Commun 187: 366–374.

34. LiuQP, SulzenbacherG, YuanH, BennettEP, PietzG, et al. (2007) Bacterial glycosidases for the production of universal red blood cells. Nat Biotechnol 25: 454–464.

35. YamamotoM, LinXH, KominatoY, HataY, NodaR, et al. (2001) Murine equivalent of the human histo-blood group ABO gene is a cis-AB gene and encodes a glycosyltransferase with both A and B transferase activity. J Biol Chem 276: 13701–13708.

36. TurriniF, GinsburgH, BussolinoF, PescarmonaGP, SerraMV, AreseP (1992) 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 80: 801–808.

37. Winterbourne CC (1985) CRC Handbook of Methods of Oxygen Radical Research. Greenward, RA editor. Boca Raton, FL: CRC Press. pp. 137–141.

38. TurriniF, MannuF, AreseP, JieYuan, LowPhilip S (1993) Characterization of the autologous that opsonized erythrocytes with clustered integral membrane proteins. Blood 81: 3146–3152.

39. Cooling L (2008) ABO, H, and Lewis blood groups and structurally related antigens. In: Roback J, Combs MR, Grossmann B, Hillyer C, editions. Technical Manual, American Association of Blood Banks. Bethesda, MD, pp 363–387.

40. CohenM, Hurtado-ZiolaN, VarkiA (2009) ABO blood group glycans modulate sialic acid recognition on erythrocytes. Blood 114: 3668–3676.

41. FlickK, ChenQ (2004) var genes, PfEMP1 and the human host. Mol Biochem Parasitol 134: 3–9.

42. FairhurstRM, BaruchDI, BrittainNJ, OsteraGR, WallachJS, et al. (2005) Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature 435: 1117–1121.

43. AnsteeDJ (1990) The nature and abundance of human red cell surface glycoproteins. J Immunogenet 17: 219–225.

44. FadokVA, de CathelineauA, DalekeDL, HensonPM, BrattonDL (2001) Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J Biol Chem 276: 1071–1077.

45. LangPA, KasinathanRS, BrandVB, DurantonC, LangC, et al. (2009) Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell Physiol Biochem 24: 415–428.

46. PantaleoA, FerruE, GiribaldiG, MannuF, CartaF, et al. (2009) Oxidized and poorly glycosylated band 3 is selectively phosphorylated by Syk kinase to from large membrane clusters in normal and G6PD-deficient red blood cells. Biochem J 418: 359–367.

47. FukudaMN, DellA, ScartezziniP (1987) Primary defect of congenital dyserythropoietic anemia type II. Failure in glycosylation of erythrocyte lactosaminoglycan proteins caused by lowered N-acetylglucosaminyltransferase II. J Biol Chem 262: 7195–7206.

48. De FranceschiL, TurriniF, del GiudiceEM, PerrottaS, OlivieriO, et al. (1998) Decreased band 3 anion transport activity and 3 clusterization in congenital dysthropoietic anemia type II. Exp Hematol 26: 869–873.

49. McGilvrayID, SerghidesL, KapusA, RotsteinOD, KainKC (2000) Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 96: 3231–3240.

50. LambrosC, VanderbergJP (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418–420.

51. LiuQP, YuanH, BennettEP, LeverySB, NudelmanE, et al. (2008) Identification of a GH110 subfamily of alpha 1,3-galactosidases: novel enzymes for removal of the alpha 3Gal xenotransplantation antigen. J Biol Chem 283: 8545–8554.

52. CobbCE, BethAH (1990) Identification of the eosinyl-5-maleimide reaction site on the human erythrocyte anion-exchange protein: Overlap with the reaction sites of other chemical probes. Biochemistry 29: 8283–8290.

53. GiribaldiG, UlliersD, MannuF, AreseP, TurriniF (2001) 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: 492–499.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2012 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#