Targeted disruption of a ring-infected erythrocyte surface antigen (RESA)-like export protein gene in Plasmodium falciparum confers stable chondroitin 4-sulfate cytoadherence capacity

Journal of Biological Chemistry

Volumn 289, Issue 49, 2014, Pages 34408-34421

  Goel, Suchi ^a,e   Muthusamy, Arivalagan ^a,f   Miao, Jun ^b   Cui, Liwang ^b   Salanti, Ali ^c   Winzeler, Elizabeth A ^d   Gowda, D Channe ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c Mental Health Center Glostrup   (Denmark)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; CELL ADHESION; CELL MEMBRANES; TRANSCRIPTION;

BINDING CAPACITIES; ERYTHROCYTE MEMBRANE; INFECTED ERYTHROCYTES; MICROVASCULAR ENDOTHELIUM; PLASMODIUM FALCIPARUM; SURFACE EXPRESSION; SWITCHING PROCESS; TRANSCRIPTOME ANALYSIS;

PROTEINS;

CHONDROITIN 4 SULFATE; ERYTHROCYTE MEMBRANE PROTEIN 1; CD36 ANTIGEN; CHONDROITIN SULFATE; EMP3 PROTEIN, PLASMODIUM FALCIPARUM; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; HEAT SHOCK PROTEIN 40; KNOB PROTEIN, PLASMODIUM FALCIPARUM; MEMBRANE PROTEIN; PARASITE ANTIGEN; PEPTIDE; PROTEIN BINDING; PROTOZOAL PROTEIN; VAR2CSA PROTEIN, PLASMODIUM FALCIPARUM;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; ERYTHROCYTE MEMBRANE; GENE; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE SILENCING; GENE SWITCHING; GENETIC TRANSCRIPTION; KAHRP GENE; MICROARRAY ANALYSIS; NONHUMAN; PF3D7 0201600 GENE; PFB0080C GENE; PFEMP1 GENE; PFEMP3 GENE; PLASMODIUM FALCIPARUM; CHEMISTRY; CHROMOSOME; DEFICIENCY; ERYTHROCYTE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; HUMAN; METABOLISM; MULTIGENE FAMILY; PARASITOLOGY;

PLASMODIUM FALCIPARUM;

ANTIGENS, CD36; ANTIGENS, PROTOZOAN; CELL ADHESION; CHONDROITIN SULFATES; CHROMOSOMES; ERYTHROCYTES; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HSP40 HEAT-SHOCK PROTEINS; HUMANS; MEMBRANE PROTEINS; MULTIGENE FAMILY; PEPTIDES; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAN PROTEINS;

EID: 84917710533     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.615393     Document Type: Article

References (58)

1. Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y., and Hay, S. I. (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214-217
2. Hay, S. I., Guerra, C. A., Gething, P. W., Patil, A. P., Tatem, A. J., Noor, A. M., Kabaria, C. W., Manh, B. H., Elyazar, I. R., Brooker, S., Smith, D. L., Moyeed, R.A., and Snow, R.W. (2009) A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 6, e1000048
3. World Heath Organization (2012) World malaria report 2013. World Heath Organization, Geneva, Switzerland
4. Ockenhouse, C. F., Ho, M., Tandon, N. N., Van Seventer, G. A., Shaw, S., White, N. J., Jamieson, G. A., Chulay, J. D., and Webster, H. K. (1991) Molecular basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria: differential adhesion of infected erythrocytes to CD36 and ICAM-1. J. Infect. Dis. 164, 163-169
5. Baruch, D. I., Gormely, J. A., Ma, C., Howard, R. J., and Pasloske, B. L. (1996) Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proc. Natl. Acad. Sci. U.S.A. 93, 3497-3502
6. Fried, M., and Duffy, P. E. (1996) Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272, 1502-1504
7. Weatherall, D. J., Miller, L. H., Baruch, D. I., Marsh, K., Doumbo, O. K., Casals-Pascual, C., and Roberts, D. J. (2002) Malaria and the red cell. Hematol. Am. Soc. Hematol. Edu. Program 35-57
8. Brabin, B. J., Romagosa, C., Abdelgalil, S., Menéndez, C., Verhoeff, F. H., McGready, R., Fletcher, K. A., Owens, S., D'Alessandro, U., Nosten, F., Fischer, P. R., and Ordi, J. (2004) The sick placenta: the role of malaria. Placenta 25, 359-378
9. Miller, L. H., Baruch, D. I., Marsh, K., and Doumbo, O. K. (2002) The pathogenic basis of malaria. Nature 415, 673-679
10. Desai, M., ter Kuile, F. O., Nosten, F., McGready, R., Asamoa, K., Brabin, B., and Newman, R. D. (2007) Epidemiology and burden of malaria in pregnancy. Lancet Infect. Dis. 7, 93-104
11. Su, X. Z., Heatwole, V. M., Wertheimer, S. P., Guinet, F., Herrfeldt, J. A., Peterson, D. S., Ravetch, J. A., and Wellems, T. E. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82, 89-100
12. Smith, J. D., Chitnis, C. E., Craig, A. G., Roberts, D. J., Hudson-Taylor, D. E., Peterson, D. S., Pinches, R., Newbold, C. I., and Miller, L. H. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82, 101-110
13. Flick, K., Chen, Q. (2004) var genes, PfEMP1 and the human host. Mol. Biochem. Parasitol. 134, 3-9
14. Kraemer, S. M., and Smith, J. D. (2006) A family affair: var genes, PfEMP1 binding, and malaria disease. Curr. Opin. Microbiol. 9, 374-380
15. Salanti, A., Dahlbäck, M., Turner, L., Nielsen, M. A., Barfod, L., Magistrado, P., Jensen, A. T., Lavstsen, T., Ofori, M. F., Marsh, K., Hviid, L., and Theander, T. G. (2004) Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 200, 1197-1203
16. Waller, K. L., Nunomura, W., An, X., Cooke, B. M., Mohandas, N., and Coppel, R. L. (2003) Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malaria-infected red blood cells. Blood 102, 1911-1914
17. Horrocks, P., Pinches, R. A., Chakravorty, S. J., Papakrivos, J., Christodoulou, Z., Kyes, S. A., Urban, B.C., Ferguson, D. J., and Newbold, C. I. (2005) PfEMP1 expression is reduced on the surface of knobless Plasmodium falciparum infected erythrocytes. J. Cell Sci. 118, 2507-2518
18. Rug, M., Prescott, S. W., Fernandez, K. M., Cooke, B. M., and Cowman, A. F. (2006) The role of KAHRP domains in knob formation and cytoadherence of P. falciparum-infected human erythrocytes. Blood 108, 370-378
19. Pei, X., Guo, X., Coppel, R., Bhattacharjee, S., Haldar, K., Gratzer, W., Mohandas, N., and An, X. (2007) The ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110, 1036-1042
20. Waller, K. L., Cooke, B. M., Nunomura, W., Mohandas, N., and Coppel, R. L. (1999) Mapping the binding domains involved in the interaction between the Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and the cytoadherence ligand P. falciparum erythrocyte membrane protein 1 (PfEMP1). J. Biol. Chem. 274, 23808-23813
21. Mayer, C., Slater, L., Erat, M. C., Konrat, R., and Vakonakis, I. (2012) Structural analysis of the Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) intracellular domain reveals a conserved interaction epitope. J. Biol. Chem. 287, 7182-7189
22. Maier, A. G., Cooke, B. M., Cowman, A. F., and Tilley, L. (2009) Malaria parasite proteins that remodel the host erythrocyte. Nat. Rev. Microbiol. 7, 341-354
23. Kilili, G. K., and LaCount, D. J. (2011) An erythrocyte cytoskeleton-binding motif in exported Plasmodium falciparum proteins. Eukaryot. Cell 10, 1439-1447
24. Parish, L. A., Mai, D. W., Jones, M. L., Kitson, E. L., and Rayner, J. C. (2013) A member of the Plasmodium falciparum PHIST family binds to the erythrocyte cytoskeleton component band 4.1. Malar. J. 12, 160
25. Cooke, B. M., Glenister, F. K., Mohandas, N., and Coppel, R. L. (2002) Assignment of functional roles to parasite proteins in malaria-infected red blood cells by competitive flow-based adhesion assay. Br. J. Haematol. 117, 203-211
26. Lanzer, M., de Bruin, D., Wertheimer, S. P., and Ravetch, J. V. (1994) Transcriptional and nucleosomal characterization of a subtelomeric gene cluster flanking a site of chromosomal rearrangements in Plasmodium falciparum. Nucleic Acids Res. 22, 4176-4182
27. Biggs, B. A., Kemp, D. J., and Brown, G. V. (1989) Subtelomeric chromosome deletions in field isolates of Plasmodium falciparum and their relationship to loss of cytoadherence in vitro. Proc. Natl. Acad. Sci. U.S.A. 86, 2428-2432
28. Trenholme, K. R., Gardiner, D. L., Holt, D. C., Thomas, E. A., Cowman, A. F., and Kemp, D. J. (2000) clag9: A cytoadherence gene in Plasmodium falciparum is essential for binding of parasitized erythrocytes to CD36. Proc. Natl. Acad. Sci. U.S.A. 97, 4029-4033
29. Goel, S., Valiyaveettil, M., Achur, R. N., Goyal, A., Mattei, D., Salanti, A., Trenholme, K. R., Gardiner, D. L., and Gowda, D. C. (2010) Dual stage synthesis and crucial role of cytoadherence-linked asexual gene 9 in the surface expression of malaria parasite var proteins. Proc. Natl. Acad. Sci. U.S.A. 107, 16643-16648
30. Srivastava, A., Gangnard, S., Round, A., Dechavanne, S., Juillerat, A., Raynal, B., Faure, G., Baron, B., Ramboarina, S., Singh, S. K., Belrhali, H., England, P., Lewit-Bentley, A., Scherf, A., Bentley, G.A., and Gamain, B. (2010) Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc. Natl. Acad. Sci. U.S.A. 107, 4884-4889
31. Khunrae, P., Dahlbäck, M., Nielsen, M. A., Andersen, G., Ditlev, S. B., Resende, M., Pinto, V. V., Theander, T. G., Higgins, M. K., and Salanti, A. (2010) Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J. Mol. Biol. 397, 826-834
32. Acharya, P., Chaubey, S., Grover, M., and Tatu, U. (2012) An exported heat shock protein 40 associates with pathogenesis-related knobs in Plas-modium falciparum infected erythrocytes. PLoS One 7, e44605
33. Grover, M., Chaubey, S., Ranade, S., and Tatu, U. (2013) Identification of an exported heat shock protein 70 in Plasmodium falciparum. Parasite 20, 2
34. Maier, A. G., Rug, M., O'Neill, M.T., Brown, M., Chakravorty, S., Szestak, T., Chesson, J., Wu, Y., Hughes, K., Coppel, R. L., Newbold, C., Beeson, J. G., Craig, A., Crabb, B. S., and Cowman, A. F. (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134, 48-61
35. Madhunapantula, S. V., Achur, R. N., and Gowda, D. C. (2007) Developmental stage- and cell cycle number-dependent changes in characteristics of Plasmodium falciparum-infected erythrocyte adherence to placental chondroitin-4-sulfate proteoglycan. Infect. Immun. 75, 4409-4415
36. Alkhalil, A., Achur, R. N., Valiyaveettil, M., Ockenhouse, C. F., and Gowda, D. C. (2000) Structural requirements for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate proteoglycans of human placenta. J. Biol. Chem. 275, 40357-40364
37. Achur, R. N., Valiyaveettil, M., Alkhalil, A., Ockenhouse, C. F., and Gowda, D. C. (2000) Characterization of proteoglycans of human placenta and identification of unique chondroitin sulfate proteoglycans of the intervillous spaces that mediate the adherence of Plasmodium falciparum-infected erythrocytes to the placenta. J. Biol. Chem. 275, 40344-40356
38. Greenwalt, D. E., Lipsky, R. H., Ockenhouse, C. F., Ikeda, H., Tandon, N. N., and Jamieson, G. A. (1992) Membrane glycoprotein CD36: a review of its roles in adherence, signal transduction, and transfusion medicine. Blood 80, 1105-1115
39. Achur, R. N., Valiyaveettil, M., and Gowda, D. C. (2003) The low sulfated chondroitin sulfate proteoglycans of human placenta have sulfate groupclustered domains that can efficiently bind Plasmodium falciparum-infected erythrocytes. J. Biol. Chem. 278, 11705-11713
40. Le Roch, K. G., Zhou, Y., Blair, P. L., Grainger, M., Moch, J. K., Haynes, J. D., De La Vega, P., Holder, A. A., Batalov, S., Carucci, D. J., and Winzeler, E. A. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 1503-1508
41. Young, J. A., Fivelman, Q. L., Blair, P. L., de la Vega, P., Le Roch, K. G., Zhou, Y., Carucci, D. J., Baker, D. A., and Winzeler, E. A. (2005) The Plasmodium falciparum sexual development transcriptome: A microarray analysis using ontology-based pattern identification. Mol. Biochem. Parasitol. 143, 67-79
42. Zhou, Y., and Abagyan, R. (2002) Match-only integral distribution (MOID) algorithm for high-density oligonucleotide array analysis. BMC Bioinformatics 3, 3
43. Maier, A. G., Braks, J. A., Waters, A. P., and Cowman, A. F. (2006) Negative selection using yeast cytosine deaminase/uracil phosphoribosyl transferase in Plasmodium falciparum for targeted gene deletion by double crossover recombination. Mol. Biochem. Parasitol. 150, 118-121
44. Deitsch, K. W., Calderwood, M. S., and Wellems, T. E. (2001) Malaria: cooperative silencing elements in var genes. Nature 412, 875-876
45. Barfod, L., Nielsen, M. A., Turner, L., Dahlbäck, M., Jensen, A. T., Hviid, L., Theander, T. G., and Salanti, A. (2006) Baculovirus-expressed constructs induce immunoglobulin G that recognizes VAR2CSA on Plasmodium falciparum-infected erythrocytes. Infect. Immun. 74, 4357-4360
46. Bopp, S. E., Manary, M. J., Bright, A. T., Johnston, G. L., Dharia, N. V., Luna, F. L., McCormack, S., Plouffe, D., McNamara, C. W., Walker, J. R., Fidock, D. A., Denchi, E. L., and Winzeler, E. A. (2013) Mitotic evolution of Plasmodium falciparum shows a stable core genome but recombination in antigen families. PLoS Genet. 9, e1003293
47. Le Roch, K. G., Zhou, Y., Batalov, S., and Winzeler, E. A. (2002) Monitoring the chromosome 2 intraerythrocytic transcriptome of Plasmodium falciparum using oligonucleotide arrays. Am. J. Trop. Med. Hyg. 67, 233-243
48. Kidgell, C., Volkman, S. K., Daily, J., Borevitz, J. O., Plouffe, D., Zhou, Y., Johnson, J. R., Le Roch, K., Sarr, O., Ndir, O., Mboup, S., Batalov, S., Wirth, D. F., and Winzeler, E. A. (2006) A systematic map of genetic variation in Plasmodium falciparum. PLoS Pathog. 2, e57
49. Gowda, A. S. P., Madhunapantula, S. V., Achur, R. N., Valiyaveettil, M., Bhavanandan, V. P., and Gowda, D. C. (2007) Structural basis for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin 4-sulfate and design of novel photoactivable reagents for the identification of parasite adhesive proteins. J. Biol. Chem. 282, 916-928
50. Achur, R. N., Kakizaki, I., Goel, S., Kojima, K., Madhunapantula, S. V., Goyal, A., Ohta, M., Kumar, S., Takagaki, K., and Gowda, D. C. (2008) Structural interactions in chondroitin 4-sulfate mediated adherence of Plasmodium falciparum infected erythrocytes in human placenta during pregnancy-associated malaria. Biochemistry 47, 12635-12643
51. Dzikowski, R., Li, F., Amulic, B., Eisberg, A., Frank, M., Patel, S., Wellems, T. E., and Deitsch, K. W. (2007) Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep. 8, 959-965
52. Zhang, Q., Huang, Y., Zhang, Y., Fang, X., Claes, A., Duchateau, M., Namane, A., Lopez-Rubio, J. J., Pan, W., and Scherf, A. (2011) Critical role of perinuclear filamentous actin in spatial repositioning and mutually exclusive expression of virulence genes in malaria parasites. Cell Host Microbe. 10, 451-463
53. Brolin, K. J., Ribacke, U., Nilsson, S., Ankarklev, J., Moll, K., Wahlgren, M., and Chen, Q. (2009) Simultaneous transcription of duplicated var2csa gene copies in individual Plasmodium falciparum parasites. Genome Biol. 10, R117
54. Jiang, L., Mu, J., Zhang, Q., Ni, T., Srinivasan, P., Rayavara, K., Yang, W., Turner, L., Lavstsen, T., Theander, T. G., Peng, W., Wei, G., Jing, Q., Wakabayashi, Y., Bansal, A., Luo, Y., Ribeiro, J. M. C., Scherf, A., Aravind, L., Zhu, J., Zhao, K., and Miller, L. H. (2013) PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499, 223-227
55. Marti, M., Baum, J., Rug, M., Tilley, L., and Cowman, A. F. (2005) Signal mediated export of the proteins from the malaria parasite to the host erythrocyte. J. Cell Biol. 171, 587-592
56. Sargeant, T. J., Marti, M., Caler, E., Carlton, J. M., Simpson, K., Speed, T. P., and Cowman, A. F. (2006) Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol. 7, R12
57. Cowman, A. F., Coppel, R. L., Saint, R. E., Favaloro, J., Crewther, P. E., Stahl, H.-D., Bianco A. E., Brown, G. V., Anders, R. F., and Kemp, D. J. (1984) The ring-infected erythrocyte surface antigen (RESA) polypeptide of Plasmodium falciparum contains two separate blocks of tandem repeats encoding antigenic epitopes that are naturally immunogenic in man. Mol. Biol. Med. 2, 207-221
58. Silva, M. D., Cooke, B. M., Guillotte, M., Buckingham, D. W., Sauzet, J.-P., Le Scanf, C., Contamin, H., David, P., Mercereau-Puijalon, O., and Bonnefoy, S. (2005) A role for the Plasmodium falciparum RESA protein in resistance against heat shock demonstrated using gene disruption. Mol. Microbiol. 56, 990-1003