An EGF-like Protein Forms a Complex with PfRh5 and Is Required for Invasion of Human Erythrocytes by

English version České info

Invasion of erythrocytes by Plasmodium falciparum involves a complex cascade of protein-protein interactions between parasite ligands and host receptors. The reticulocyte binding-like homologue (PfRh) protein family is involved in binding to and initiating entry of the invasive merozoite into erythrocytes. An important member of this family is PfRh5. Using ion-exchange chromatography, immunoprecipitation and mass spectroscopy, we have identified a novel cysteine-rich protein we have called P. falciparum Rh5 interacting protein (PfRipr) (PFC1045c), which forms a complex with PfRh5 in merozoites. Mature PfRipr has a molecular weight of 123 kDa with 10 epidermal growth factor-like domains and 87 cysteine residues distributed along the protein. In mature schizont stages this protein is processed into two polypeptides that associate and form a complex with PfRh5. The PfRipr protein localises to the apical end of the merozoites in micronemes whilst PfRh5 is contained within rhoptries and both are released during invasion when they form a complex that is shed into the culture supernatant. Antibodies to PfRipr1 potently inhibit merozoite attachment and invasion into human red blood cells consistent with this complex playing an essential role in this process.

Vyšlo v časopise: An EGF-like Protein Forms a Complex with PfRh5 and Is Required for Invasion of Human Erythrocytes by. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002199
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002199

Souhrn

Zdroje

1. MillerLHGreenwoodB 2002 Malaria–a shadow over Africa. Science 298 121 122

2. CowmanAFCrabbBS 2006 Invasion of red blood cells by malaria parasites. Cell 124 755 766

3. SimBKLOrlandiPAHaynesJDKlotzFWCarterJM 1990 Primary structure of the 175K Plasmodium falciparum erythrocyte binding antigen and identification of a peptide which elicits antibodies that inhibit malaria merozoite invasion. J Cell Biol 111 1877 1884

4. RaynerJCVargas-SerratoEHuberCSGalinskiMRBarnwellJW 2001 A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. J Exp Med 194 1571 1581

5. TrigliaTThompsonJCaruanaSRDelorenziMSpeedT 2001 Identification of proteins from Plasmodium falciparum that are homologous to reticulocyte binding proteins in Plasmodium vivax. Infect Immun 69 1084 1092

6. MaierAGDuraisinghMTReederJCPatelSSKazuraJW 2003 Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9 87 92

7. DuraisinghMTTrigliaTRalphSARaynerJCBarnwellJW 2003 Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J 22 1047 1057

8. StubbsJSimpsonKMTrigliaTPlouffeDTonkinCJ 2005 Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 309 1384 1387

9. TrigliaTDuraisinghMTGoodRTCowmanAF 2005 Reticulocyte-binding protein homologue 1 is required for sialic acid-dependent invasion into human erythrocytes by Plasmodium falciparum. Mol Microbiol 55 162 174

10. GaurDFuruyaTMuJJiangLBSuXZ 2006 Upregulation of expression of the reticulocyte homology gene 4 in the Plasmodium falciparum clone Dd2 is associated with a switch in the erythrocyte invasion pathway. Mol Biochem Parasitol 145 205 215

11. GaoXYeoKPAwSSKussCIyerJK 2008 Antibodies targeting the PfRH1 binding domain inhibit invasion of Plasmodium falciparum merozoites. PLoS Pathog 4 e1000104

12. TrigliaTThamWHHodderACowmanAF 2009 Reticulocyte binding protein homologues are key adhesins during erythrocyte invasion by Plasmodium falciparum. Cell Microbiol 11 1671 1687

13. ThamWHWilsonDWReilingLChenLBeesonJG 2009 Antibodies to reticulocyte binding protein-like homologue 4 inhibit invasion of Plasmodium falciparum into human erythrocytes. Infect Immun 77 2427 2435

14. DeSimoneTMBeiAKJenningsCVDuraisinghMT 2009 Genetic analysis of the cytoplasmic domain of the PfRh2b merozoite invasion protein of Plasmodium falciparum. Int J Parasitol 39 399 405

15. DesimoneTMJenningsCVBeiAKComeauxCColemanBI 2009 Cooperativity between Plasmodium falciparum adhesive proteins for invasion into erythrocytes. Mol Microbiol 72 578 589

16. RaynerJCGalinskiMRIngravalloPBarnwellJW 2000 Two Plasmodium falciparum genes express merozoite proteins that are related to Plasmodium vivax and Plasmodium yoelii adhesive proteins involved in host cell selection and invasion. Proc Natl Acad Sci USA 97 9648 9653

17. KanekoOMuJTsuboiTSuXToriiM 2002 Gene structure and expression of a Plasmodium falciparum 220-kDa protein homologous to the Plasmodium vivax reticulocyte binding proteins. Mol Biochem Parasitol 121 275 278

18. RodriguezMLustigmanSMonteroEOksovYLoboCA 2008 PfRH5: a novel reticulocyte-binding family homolog of Plasmodium falciparum that binds to the erythrocyte, and an investigation of its receptor. PLoS ONE 3 e3300

19. HaytonKGaurDLiuATakahashiJHenschenB 2008 Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4 40 51

20. BaumJChenLHealerJLopatickiSBoyleM 2009 Reticulocyte-binding protein homologue 5-an essential adhesin involved in invasion of human erythrocytes by Plasmodium falciparum. Int J Parasitol 39 371 380

21. TaylorHMTrigliaTThompsonJSajidMFowlerR 2001 Plasmodium falciparum homologue of the genes for Plasmodium vivax and Plasmodium yoelii adhesive proteins, which is transcribed but not translated. Infect Immun 69 3635 3645

22. GaurDSinghSSinghSJiangLDioufA 2007 Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion. Proc Natl Acad Sci U S A 104 17789 17794

23. SaharTReddyKSBharadwajMPandeyAKSinghS 2011 Plasmodium falciparum Reticulocyte Binding-Like Homologue Protein 2 (PfRH2) Is a Key Adhesive Molecule Involved in Erythrocyte Invasion. PLoS ONE 6 e17102

24. TrigliaTChenLLopatickiSDekiwadiaCRiglarDT 2011 Plasmodium falciparum merozoite invasion is inhibited by antibodies that target the PfRh2a and b binding domains. Plos Pathogen In Press

25. SpadaforaCAwandareGAKopydlowskiKMCzegeJMochJK 2010 Complement receptor 1 is a sialic acid-independent erythrocyte receptor of Plasmodium falciparum. PLoS Pathog 6 e1000968

26. OrlandiPASimKLChulayJDHaynesJD 1990 Characterization of the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum. Mol Biochem Parasitol 40 285 294

27. GilbergerTWThompsonJKTrigliaTGoodRTDuraisinghMT 2003 A novel erythrocyte binding antigen-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. J Biol Chem 278 14480 14486

28. MayerDCMuJBKanekoODuanJSuXZ 2004 Polymorphism in the Plasmodium falciparum erythrocyte-binding ligand JESEBL/EBA-181 alters its receptor specificity. Proc Natl Acad Sci U S A 101 2518 2523

29. ThompsonJKTrigliaTReedMBCowmanAF 2001 A novel ligand from Plasmodium falciparum that binds to a sialic acid-containing receptor on the surface of human erythrocytes. Mol Micro 41 47 58

30. MayerDCKanekoOHudson-TaylorDEReidMEMillerLH 2001 Characterization of a Plasmodium falciparum erythrocyte-binding protein paralogous to EBA-175. Proc Natl Acad Sci U S A 98 5222 5227

31. NarumDLFuhrmannSRLuuTSimBK 2002 A novel Plasmodium falciparum erythrocyte binding protein-2 (EBP2/BAEBL) involved in erythrocyte receptor binding. Mol Biochem Parasitol 119 159 168

32. MayerDCCofieJJiangLHartlDLTracyE 2009 Glycophorin B is the erythrocyte receptor of Plasmodium falciparum erythrocyte-binding ligand, EBL-1. Proc Natl Acad Sci USA 106 5348 5352

33. OrlandiPAKlotzFWHaynesJD 1992 A malaria invasion receptor, the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha2-3)Gal- sequences of glycophorin A. J Cell Biol 116 901 909

34. AdamsJHSimBKLDolanSAFangXKaslowDC 1992 A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci USA 89 7085 7089

35. SimBKLChitnisCEWasniowskaKHadleyTJMillerLH 1994 Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 264 1941 1944

36. LoboCARodriguezMReidMLustigmanS 2003 Glycophorin C is the receptor for the Plasmodium falciparum erythrocyte binding ligand PfEBP-2 (baebl). Blood 6 6

37. SinghSAlamMMPal-BhowmickIBrzostowskiJAChitnisCE 2010 Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog 6 e1000746

38. MayerDCMuJBFengXSuXZMillerLH 2002 Polymorphism in a Plasmodium falciparum erythrocyte-binding ligand changes its receptor specificity. J Exp Med 196 1523 1528

39. PerssonKEMcCallumFJReilingLListerNAStubbsJ 2008 Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest 118 342 351

40. ReilingLRichardsJSFowkesFJBarryAETrigliaT 2010 Evidence that the erythrocyte invasion ligand PfRh2 is a target of protective immunity against Plasmodium falciparum malaria. J Immunol 185 6157 6167

41. RichardsJSStanisicDIFowkesFJTavulLDabodE 2011 Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clin Infect Dis 51 e50 60

42. BoddeyJAMoritzRLSimpsonRJCowmanAF 2009 Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10 285 299

43. AlexanderDLArastu-KapurSDubremetzJFBoothroydJC 2006 Plasmodium falciparum AMA1 binds a rhoptry neck protein homologous to TgRON4, a component of the moving junction in Toxoplasma gondii. Eukaryot Cell 5 1169 1173

44. RichardDMacRaildCARiglarDTChanJAFoleyM 2010 Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites. J Biol Chem 285 14815 14822

45. RiglarDTRichardDWilsonDWBoyleMJDekiwadiaC 2011 Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 9 9 20

46. SavageCRJrInagamiTCohenS 1972 The primary structure of epidermal growth factor. J Biol Chem 247 7612 7621

47. SavageCRJrHashJHCohenS 1973 Epidermal growth factor. Location of disulfide bonds. J Biol Chem 248 7669 7672

48. HaradaYLiHWallJSLennarzWJ 2011 Structural studies and the assembly of the heptameric post-translational translocon complex. J Biol Chem 286 2956 2965

49. ThamWHWilsonDWLopatickiSSchmidtCQTetteh-QuarcooPB 2010 Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc Natl Acad Sci U S A 107 17327 17332

50. BoyleMJWilsonDWRichardsJSRiglarDTTettehKK 2010 Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci U S A 107 14378 14383

51. BaumJMaierAGGoodRTSimpsonKMCowmanAF 2005 Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog 1 e37

52. AlexanderDLMitalJWardGEBradleyPBoothroydJC 2005 Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog 1 e17

53. BesteiroSMichelinAPoncetJDubremetzJFLebrunM 2009 Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathog 5 e1000309

54. LopatickiSMaierAGThompsonJWilsonDWThamWH 2011 Reticulocyte and erythrocyte binding-like proteins function cooperatively in invasion of human erythrocytes by malaria parasites. Infect Immun 79 1107 1117

55. MaierAGBaumJSmithBConwayDJCowmanAF 2009 Polymorphisms in erythrocyte binding antigens 140 and 181 affect function and binding but not receptor specificity in Plasmodium falciparum. Infect Immun 77 1689 1699

56. HolderAA 1988 The precursor to major merozoite surface antigens: structure and role in immunity. Prog Allergy 41 72 97

57. ChitarraVHolmIBentleyGPetresSLongacreS 1999 The crystal structure of the C-terminal merozoite protein 1 at 1.8A resolution, a highly protective malaria vaccine candidate. Mol Cell 3 457 464

58. TomasAMMargosGDimopoulosGvan LinLHde Koning-WardTF 2001 P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J 20 3975 3983

59. AnsariFAKumarNBala SubramanyamMGnanamaniMRamachandranS 2008 MAAP: malarial adhesins and adhesin-like proteins predictor. Proteins 70 659 666

60. TragerWJensenJB 1976 Human malaria parasites in continuous culture. Science 193 673 675

61. LambrosCVanderbergJP 1979 Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65 418 420

62. CrabbBSCookeBMReederJCWallerRFCaruanaSR 1997 Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89 287 296

63. VossTSHealerJMartyAJDuffyMFThompsonJK 2006 A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439 1004 1008

64. BiancoAEFavaloroJMBurkotTRCulvenorJGCrewtherPE 1986 A repetitive antigen of Plasmodium falciparum that is homologous to heat shock protein 70 of Drosophila melanogaster. Proc Natl Acad Sci USA 83 8713 8717

65. SchofieldLBushellGRCooperJASaulAJUpcroftJA 1986 A rhoptry antigen of Plasmodium falciparum contains conserved and variable epitopes recognized by inhibitory monoclonal antibodies. Mol Biochem Parasitol 18 183 195

66. ReedMBCaruanaSRBatchelorAHThompsonJKCrabbBS 2000 Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid independent pathway of invasion. Proc Natl Acad Sci USA 97 7509 7514

67. PerssonKELeeCTMarshKBeesonJG 2006 Development and optimization of high-throughput methods to measure Plasmodium falciparum-specific growth inhibitory antibodies. J Clin Microbiol 44 1665 1673

68. SalmonBLOksmanAGoldbergDE 2001 Malaria parasite exit from the host erythrocyte: A two- step process requiring extraerythrocytic proteolysis. Proc Natl Acad Sci U S A 98 271 276

69. WickhamMECulvenorJGCowmanAF 2003 Selective inhibition of a two-step egress of malaria parasites from the host erythrocyte. J Biol Chem 278 37658 37663

70. TonkinCJvan DoorenGGSpurckTPStruckNSGoodRT 2004 Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137 13 21

71. HealerJCrawfordSRalphSMcFaddenGCowmanAF 2002 Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infect Immun 70 5751 5758