Fine mapping of Plasmodium falciparum ribosomal phosphoprotein PfP0 revealed sequences with highly specific binding activity to human red blood cells

Journal of Molecular Medicine

Volumn 88, Issue 1, 2010, Pages 61-74

  Arevalo Pinzon, Gabriela ^a,b   Curtidor, Hernando ^a,b   Reyes, Claudia ^a,b   Pinto, Martha ^a,b   Vizcaíno, Carolina ^a,b   Patarroyo, Manuel A ^a,b   Patarroyo, Manuel E ^a,c  

^a FUNDACIÓN INSTITUTO DE INMUNOLOGÍA DE COLOMBIA FIDIC   (Colombia)

^b UNIVERSIDAD DEL ROSARIO   (Colombia)

^c UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

High activity binding peptide (HABP); Malaria; Peptides; Plasmodium falciparum; Red blood cells (RBCs); Ribosomal phosphoprotein P0; Vaccine

Indexed keywords

PHOSPHOPROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ERYTHROCYTE; MEROZOITE; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN SYNTHESIS; RIBOSOME;

AMINO ACID SEQUENCE; ERYTHROCYTES; HUMANS; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAN PROTEINS; RIBOSOMAL PROTEINS;

EID: 75749089592     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-009-0533-5     Document Type: Article

References (62)

1. RW Snow CA Guerra AM Noor HY Myint SI Hay 2005 The global distribution of clinical episodes of Plasmodium falciparum malaria Nature 434 214 217 10.1038/nature03342 1:CAS:528:DC%2BD2MXitV2hsr4%3D 15759000 (Pubitemid 40388051)
2. S Cohen GI Mc S Carrington 1961 Gamma-globulin and acquired immunity to human malaria Nature 192 733 737 10.1038/192733a0 1:STN:280: DyaF38%2FitFKitQ%3D%3D 13880318
3. CA Lobo SK Kar B Ravindran L Kabilan S Sharma 1994 Novel proteins of Plasmodium falciparum identified by differential immunoscreening using immune and patient sera Infect Immun 62 651 656 1:CAS:528:DyaK2cXjt1Squrs%3D 7507899
4. DJ Kemp RL Coppel AF Cowman RB Saint GV Brown RF Anders 1983 Expression of Plasmodium falciparum blood-stage antigens in Escherichia coli: detection with antibodies from immune humans Proc Natl Acad Sci U S A 80 3787 3791 10.1073/pnas.80.12.3787 1:CAS:528:DyaL3sXlt1SnsbY%3D 6304737
5. A Goswami S Chatterjee S Sharma 1996 Cloning of a ribosomal phosphoprotein P0 gene homologue from Plasmodium falciparum Mol Biochem Parasitol 82 117 120 10.1016/0166-6851(96)02717-X 1:CAS:528:DyaK28Xms1elsbg%3D 8943156 (Pubitemid 26376810)
6. BE Rich JA Steitz 1987 Human acidic ribosomal phosphoproteins P0, P1, and P2: analysis of cDNA clones, in vitro synthesis, and assembly Mol Cell Biol 7 4065 4074 1:CAS:528:DyaL1cXhtVOhtLw%3D 3323886
7. C Santos JP Ballesta 1994 Ribosomal protein P0, contrary to phosphoproteins P1 and P2, is required for ribosome activity and Saccharomyces cerevisiae viability J Biol Chem 269 15689 15696 1:CAS:528:DyaK2cXktlSlurw%3D 8195220
8. A Goswami S Singh VD Redkar S Sharma 1997 Characterization of P0, a ribosomal phosphoprotein of Plasmodium falciparum antibody against amino-terminal domain inhibits parasite growth J Biol Chem 272 12138 12143 10.1074/jbc.272.18.12138 1:CAS:528:DyaK2sXivF2qsL0%3D 9115284 (Pubitemid 27202795)
9. S Singh A Sehgal S Waghmare T Chakraborty A Goswami S Sharma 2002 Surface expression of the conserved ribosomal protein P0 on parasite and other cells Mol Biochem Parasitol 119 121 124 10.1016/S0166-6851(01)00394-2 1:CAS:528:DC%2BD38XitF2h 11755193 (Pubitemid 34038032)
10. E Koren MW Reichlin M Koscec RD Fugate M Reichlin 1992 Autoantibodies to the ribosomal P proteins react with a plasma membrane-related target on human cells J Clin Invest 89 1236 1241 10.1172/JCI115707 1:CAS:528:DyaK38XitFaktLg%3D 1313450
11. A Sehgal N Kumar VB Carruthers S Sharma 2003 Translocation of ribosomal protein P0 onto the Toxoplasma gondii tachyzoite surface Int J Parasitol 33 1589 1594 10.1016/S0020-7519(03)00267-4 1:CAS:528:DC%2BD3sXptVemt78%3D 14636674 (Pubitemid 37433991)
12. K Aruna T Chakraborty S Nambeesan AB Mannan A Sehgal SR Balachandara S Sharma 2004 Identification of a hypothetical membrane protein interactor of ribosomal phosphoprotein P0 J Biosci 29 33 43 10.1007/BF02702559 1:CAS:528:DC%2BD2cXjsFSktbw%3D 15286401
13. K Elkon S Skelly A Parnassa W Moller W Danho H Weissbach N Brot 1986 Identification and chemical synthesis of a ribosomal protein antigenic determinant in systemic lupus erythematosus Proc Natl Acad Sci U S A 83 7419 7423 10.1073/pnas.83.19.7419 1:CAS:528:DyaL2sXjs1Oj 2429305 (Pubitemid 16000533)
14. M Mahler K Kessenbrock J Raats R Williams MJ Fritzler M Bluthner 2003 Characterization of the human autoimmune response to the major C-terminal epitope of the ribosomal P proteins J Mol Med (Berlin, Germany) 81 194 204 1:CAS:528:DC%2BD3sXislektrY%3D
15. YA Skeiky DR Benson M Elwasila R Badaro JM Burns Jr SG Reed 1994 Antigens shared by Leishmania species and Trypanosoma cruzi: immunological comparison of the acidic ribosomal P0 proteins Infect Immun 62 1643 1651 1:CAS:528: DyaK2MXhtFSquw%3D%3D 7513304
16. MJ Levin M Vazquez D Kaplan AG Schijman 1993 The Trypanosoma cruzi ribosomal P protein family: classification and antigenicity Parasitol Today (Personal ed) 9 381 384 10.1016/0169-4758(93)90088-W 1:CAS:528: DyaK3sXmsVGjsb4%3D (Pubitemid 23278470)
17. D Kaplan I Ferrari PL Bergami E Mahler G Levitus P Chiale J Hoebeke MH Van Regenmortel MJ Levin 1997 Antibodies to ribosomal P proteins of Trypanosoma cruzi in Chagas disease possess functional autoreactivity with heart tissue and differ from anti-P autoantibodies in lupus Proc Natl Acad Sci U S A 94 10301 10306 10.1073/pnas.94.19.10301 1:CAS:528:DyaK2sXmt1GjsLk%3D 9294205 (Pubitemid 27407036)
18. S Singh S Chatterjee R Sohoni S Badakere S Sharma 2001 Sera from lupus patients inhibit growth of P. falciparum in culture Autoimmunity 33 253 263 1:CAS:528:DC%2BD38XitlajsLg%3D 11683400
19. S Chatterjee S Singh R Sohoni V Kattige C Deshpande S Chiplunkar N Kumar S Sharma 2000 Characterization of domains of the phosphoriboprotein P0 of Plasmodium falciparum Mol Biochem Parasitol 107 143 154 10.1016/S0166-6851(99) 00226-1 1:CAS:528:DC%2BD3cXisFGkurw%3D 10779592 (Pubitemid 30211631)
20. S Chatterjee S Singh R Sohoni NJ Singh A Vaidya C Long S Sharma 2000 Antibodies against ribosomal phosphoprotein P0 of Plasmodium falciparum protect mice against challenge with Plasmodium yoelii Infect Immun 68 4312 4318 10.1128/IAI.68.7.4312-4318.2000 1:CAS:528:DC%2BD3cXktlynurw%3D 10858250 (Pubitemid 30434588)
21. K Rajeshwari K Patel S Nambeesan M Mehta A Sehgal T Chakraborty S Sharma 2004 The P domain of the P0 protein of Plasmodium falciparum protects against challenge with malaria parasites Infect Immun 72 5515 5521 10.1128/IAI.72.9. 5515-5521.2004 1:CAS:528:DC%2BD2cXnt1Cht7w%3D 15322057 (Pubitemid 39223446)
22. I Malhotra P Mungai E Muchiri J Ouma S Sharma JW Kazura CL King 2005 Distinct Th1- and Th2-Type prenatal cytokine responses to Plasmodium falciparum erythrocyte invasion ligands Infect Immun 73 3462 3470 10.1128/IAI.73.6.3462- 3470.2005 1:CAS:528:DC%2BD2MXkvFCns74%3D 15908375 (Pubitemid 40745890)
23. S Sharma S Pathak 2008 Malaria vaccine: a current perspective J Vector Borne Dis 45 1 20 1:CAS:528:DC%2BD1cXktVOjtL0%3D 18399312
24. RB Merrifield 1963 Solid phase peptide synthesis. I. The synthesis of a tetrapeptide J Am Chem Soc 85 2149 2154 10.1021/ja00897a025 1:CAS:528: DyaF3sXksVajsLg%3D
25. JP Tam WF Heath RB Merrifield 1983 SN 1 and SN 2 mechanisms for the deprotection of synthetic peptides by hydrogen fluoride. Studies to minimize the tyrosine alkylation side reaction Int J Pept Protein Res 21 57 65 1:CAS:528:DyaL3sXhvFyluro%3D 6826283
26. LE Rodriguez H Curtidor M Urquiza G Cifuentes C Reyes ME Patarroyo 2008 Intimate molecular interactions of P. falciparum merozoite proteins involved in invasion of red blood cells and their implications for vaccine design Chem Rev 108 3656 3705 10.1021/cr068407v 1:CAS:528:DC%2BD1cXhtVWlsr7J 18710292
27. G Deleage C Combet C Blanchet C Geourjon 2001 ANTHEPROT: an integrated protein sequence analysis software with client/server capabilities Comput Biol Med 31 259 267 10.1016/S0010-4825(01)00008-7 1:CAS:528:DC%2BD3MXjtFCmsL4%3D 11334635 (Pubitemid 32378727)
28. I Prieto S Hervas-Stubbs M Garcia-Granero C Berasain JI Riezu-Boj JJ Lasarte P Sarobe J Prieto F Borras-Cuesta 1995 Simple strategy to induce antibodies of distinct specificity: application to the mapping of gp120 and inhibition of HIV-1 infectivity Eur J Immunol 25 877 883 10.1002/eji.1830250403 1:CAS:528:DyaK2MXltFOmsLk%3D 7737288
29. W Trager JB Jenson 1978 Cultivation of malarial parasites Nature 273 621 622 10.1038/273621a0 1:STN:280:DyaE1c7pvFyitw%3D%3D 351412
30. CR Wyatt W Goff WC Davis 1991 A flow cytometric method for assessing viability of intraerythrocytic hemoparasites J Immunol Methods 140 23 30 10.1016/0022-1759(91)90122-V 1:STN:280:DyaK3M3os1Kqsg%3D%3D 2061611
31. N Sreerama SY Venyaminov RW Woody 1999 Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy Protein Sci 8 370 380 1:CAS:528:DyaK1MXhtFGlsr8%3D 10048330
32. D Roccatano G Colombo M Fioroni AE Mark 2002 Mechanism by which 2, 2, 2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study Proc Natl Acad Sci U S A 99 12179 12184 10.1073/pnas.182199699 1:CAS:528:DC%2BD38XntlCksr8%3D 12196631
33. LA Compton WC Johnson Jr 1986 Analysis of protein circular dichroism spectra for secondary structure using a simple matrix multiplication Anal Biochem 155 155 167 10.1016/0003-2697(86)90241-1 1:CAS:528:DyaL28XitVegtLc%3D 3717552
34. PlasmoDB. The Plasmodium Genome Resource. http://www.plasmodb.org/plasmo/ home.jsp
35. H Curtidor G Arevalo M Vanegas C Vizcaino MA Patarroyo M Forero ME Patarroyo 2008 Characterization of Plasmodium falciparum integral membrane protein Pf25-IMP and identification of its red blood cell binding sequences inhibiting merozoite invasion in vitro Protein Sci 17 1494 1504 10.1110/ps.036251.108 1:CAS:528:DC%2BD1cXhtV2rsb7F 18556472
36. C Combet C Blanchet C Geourjon G Deleage 2000 NPS@: network protein sequence analysis Trends Biochem Sci 25 147 150 10.1016/S0968-0004(99)01540-6 1:CAS:528:DC%2BD3cXhsleiu7Y%3D 10694887 (Pubitemid 30122428)
37. M Urquiza LE Rodriguez JE Suarez F Guzman M Ocampo H Curtidor C Segura E Trujillo ME Patarroyo 1996 Identification of Plasmodium falciparum MSP-1 peptides able to bind to human red blood cells Parasite Immunol 18 515 526 10.1046/j.1365-3024.1996.d01-15.x 1:CAS:528:DyaK28XntVCgtLY%3D 9226689
38. Yamamura HI, Enna SJ, Kuhar MJ (1978) Neurotransmitter receptor binding. Raven, New York
39. M Perkins 1981 Inhibitory effects of erythrocyte membrane proteins on the in vitro invasion of the human malarial parasite (Plasmodium falciparum) into its host cell J Cell Biol 90 563 567 10.1083/jcb.90.3.563 1:CAS:528: DyaL3MXlsVyhtL4%3D 7026577
40. Z Bozdech M Llinas BL Pulliam ED Wong J Zhu JL DeRisi 2003 The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum PLoS Biol 1 E5 10.1371/journal.pbio.0000005 12929205 (Pubitemid 39112195)
41. ME Patarroyo MA Patarroyo 2008 Emerging rules for subunit-based, multiantigenic, multistage chemically synthesized vaccines Acc Chem Res 41 377 386 10.1021/ar700120t 1:CAS:528:DC%2BD1cXhvVGgtLw%3D 18266328
42. LM Salazar MP Alba H Curtidor A Bermudez EV Luis ZJ Rivera ME Patarroyo 2004 Changing ABRA protein peptide to fit into the HLA-DRbeta1*0301 molecule renders it protection-inducing Biochem Biophys Res Commun 322 119 125 10.1016/j.bbrc.2004.07.086 1:CAS:528:DC%2BD2cXmslOht7w%3D 15313182 (Pubitemid 39093848)
43. LM Salazar MP Alba MH Torres M Pinto X Cortes L Torres ME Patarroyo 2002 Protection against experimental malaria associated with AMA-1 peptide analogue structures FEBS Lett 527 95 100 10.1016/S0014-5793(02)03174-5 1:CAS:528:DC%2BD38XmvVCltb4%3D 12220641 (Pubitemid 35253846)
44. MH Torres LM Salazar M Vanegas F Guzman R Rodriguez Y Silva J Rosas ME Patarroyo 2003 Modified merozoite surface protein-1 peptides with short alpha helical regions are associated with inducing protection against malaria Eur J Biochem / FEBS 270 3946 3952 10.1046/j.1432-1033.2003.03780.x 1:CAS:528:DC%2BD3sXotFKrurY%3D (Pubitemid 37193871)
45. A Yacoub MR Kelley WA Deutsch 1996 Drosophila ribosomal protein PO contains apurinic/apyrimidinic endonuclease activity Nucleic Acids Res 24 4298 4303 10.1093/nar/24.21.4298 1:CAS:528:DyaK28XntF2hs7k%3D 8932386 (Pubitemid 26377349)
46. E Brockstedt A Rickers S Kostka A Laubersheimer B Dorken B Wittmann-Liebold K Bommert A Otto 1998 Identification of apoptosis-associated proteins in a human Burkitt lymphoma cell line. Cleavage of heterogeneous nuclear ribonucleoprotein A1 by caspase 3 J Biol Chem 273 28057 28064 10.1074/jbc.273.43.28057 1:CAS:528:DyaK1cXntVCmurw%3D 9774422 (Pubitemid 28496099)
47. N Kondoh T Wakatsuki A Ryo A Hada T Aihara S Horiuchi N Goseki O Matsubara K Takenaka M Shichita K Tanaka M Shuda M Yamamoto 1999 Identification and characterization of genes associated with human hepatocellular carcinogenesis Cancer Res 59 4990 4996 1:CAS:528:DyaK1MXmslWktbk%3D 10519413
48. G Pasvol 1984 Receptors on red cells for Plasmodium falciparum and their interaction with merozoites Philos Trans R Soc Lond 307 189 200 10.1098/rstb.1984.0119 1:CAS:528:DyaL2MXmtVChsA%3D%3D
49. J Baum AG Maier RT Good KM Simpson AF Cowman 2005 Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions PLoS Pathog 1 e37 10.1371/journal.ppat.0010037 16362075
50. VK Goel X Li H Chen SC Liu AH Chishti SS Oh 2003 Band 3 is a host receptor binding merozoite surface protein 1 during the Plasmodium falciparum invasion of erythrocytes Proc Natl Acad Sci U S A 100 5164 5169 10.1073/pnas.0834959100 1:CAS:528:DC%2BD3sXjs1yisLg%3D 12692305 (Pubitemid 36542676)
51. ME Perkins 1984 Surface proteins of Plasmodium falciparum merozoites binding to the erythrocyte receptor, glycophorin J Exp Med 160 788 798 10.1084/jem.160.3.788 1:CAS:528:DyaL2cXlsV2nt70%3D 6206188
52. ME Perkins 1984 Binding of glycophorins to Plasmodium falciparum merozoites Mol Biochem Parasitol 10 67 78 10.1016/0166-6851(84)90019-7 1:CAS:528:DyaL2cXmsVKrsg%3D%3D 6363923
53. TL Steck 1974 The organization of proteins in the human red blood cell membrane. A review J Cell Biol 62 1 19 10.1083/jcb.62.1.1 1:CAS:528: DyaE2cXlsVKqsLo%3D 4600883
54. DC Mayer O Kaneko DE Hudson-Taylor ME Reid LH Miller 2001 Characterization of a Plasmodium falciparum erythrocyte-binding protein paralogous to EBA-175 Proc Natl Acad Sci U S A 98 5222 5227 10.1073/pnas. 081075398 1:CAS:528:DC%2BD3MXjt1Onsb4%3D 11309486 (Pubitemid 32397110)
55. JC Rayner E Vargas-Serrato CS Huber MR Galinski JW Barnwell 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 10.1084/jem.194.11.1571 1:CAS:528:DC%2BD3MXovVOkt7o%3D 11733572 (Pubitemid 33126808)
56. BK Sim CE Chitnis K Wasniowska TJ Hadley LH Miller 1994 Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum Science (New York, NY) 264 1941 1944 1:CAS:528:DyaK2cXksFCqtbY%3D
57. T Triglia JK Thompson AF Cowman 2001 An EBA175 homologue which is transcribed but not translated in erythrocytic stages of Plasmodium falciparum Mol Biochem Parasitol 116 55 63 10.1016/S0166-6851(01)00303-6 1:CAS:528:DC%2BD3MXltF2jtrs%3D 11463466 (Pubitemid 32706426)
58. T Triglia MT Duraisingh RT Good AF Cowman 2005 Reticulocyte-binding protein homologue 1 is required for sialic acid-dependent invasion into human erythrocytes by Plasmodium falciparum Mol Microbiol 55 162 174 10.1111/j.1365-2958.2004.04388.x 1:CAS:528:DC%2BD2MXotlSrtQ%3D%3D 15612925 (Pubitemid 40127893)
59. ME Perkins EH Holt 1988 Erythrocyte receptor recognition varies in Plasmodium falciparum isolates Mol Biochem Parasitol 27 23 34 10.1016/0166-6851(88)90021-7 1:CAS:528:DyaL1cXpt1Cmtg%3D%3D 2830508
60. GH Mitchell TJ Hadley MH McGinniss FW Klotz LH Miller 1986 Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors Blood 67 1519 1521 1:STN:280: DyaL287ovVansA%3D%3D 3516259
61. F Espejo A Bermudez E Torres M Urquiza R Rodriguez Y Lopez ME Patarroyo 2004 Shortening and modifying the 1513 MSP-1 peptide's alpha-helical region induces protection against malaria Biochem Biophys Res Commun 315 418 427 10.1016/j.bbrc.2004.01.072 1:CAS:528:DC%2BD2cXps1OnsQ%3D%3D 14766224 (Pubitemid 38185850)
62. JM Lozano ME Patarroyo 2007 A rational strategy for a malarial vaccine development Microbes Infect 9 751 760 10.1016/j.micinf.2007.02.004 1:CAS:528:DC%2BD2sXkvFGqsb8%3D 17434780 (Pubitemid 46660676)