Skip to main content Accessibility help
×
Home

The use of proteomics for the identification of promising vaccine and diagnostic biomarkers in Plasmodium falciparum

  • Reza Mansouri (a1), Mohammad Ali-Hassanzadeh (a2), Reza Shafiei (a3), Amir Savardashtaki (a4), Mohammadreza Karimazar (a5), Enayat Anvari (a6), Paul Nguewa (a7) and Sajad Rashidi (a5)...

Abstract

Plasmodium falciparum is the main cause of severe malaria in humans that can lead to death. There is growing evidence of drug-resistance in P. falciparum treatment, and the design of effective vaccines remains an ongoing strategy to control the disease. On the other hand, the recognition of specific diagnostic markers for P. falciparum can accelerate the diagnosis of this parasite in the early stages of infection. Therefore, the identification of novel antigenic proteins especially by proteomic tools is urgent for vaccination and diagnosis of P. falciparum. The proteome diversity of the life cycle stages of P. falciparum, the altered proteome of P. falciparum-infected human sera and altered proteins in P. falciparum-infected erythrocytes could be proposed as appropriate proteins for the aforementioned aims. Accordingly, this review highlights and proposes different proteins identified using proteomic approaches as promising markers in the diagnosis and vaccination of P. falciparum. It seems that most of the candidates identified in this study were able to elicit immune responses in the P. falciparum-infected hosts and they also played major roles in the life cycle, pathogenicity and key pathways of this parasite.

Copyright

Corresponding author

Author for correspondence: Paul Nguewa, E-mail: panguewa@unav.es and Sajad Rashidi, E-mail: sajaderashidi@yahoo.com

References

Hide All
Abdi, A, Yu, L, Goulding, D, Rono, MK, Bejon, P, Choudhary, J and Rayner, J (2017) Proteomic analysis of extracellular vesicles from a Plasmodium falciparum Kenyan clinical isolate defines a core parasite secretome. Wellcome Open Research 2, 50.
Alharbi, RA (2020) Proteomics approach and techniques in identification of reliable biomarkers for diseases. Saudi Journal of Biological Sciences 27, 968974.
Antony, HA and Parija, SC (2016) Antimalarial drug resistance: an overview. Tropical Parasitology 6, 3041.
Arévalo-Pinzón, G, Curtidor, H, Vanegas, M, Vizcaíno, C, Patarroyo, MA and Patarroyo, ME (2010) Conserved high activity binding peptides from the Plasmodium falciparum Pf34 rhoptry protein inhibit merozoites in vitro invasion of red blood cells. Peptides 31, 19871994.
Aslam, B, Basit, M, Nisar, MA, Khurshid, M and Rasool, MH (2017) Proteomics: technologies and their applications. Journal of Chromatographic Science 55, 182196.
Azcárate, IG, Marin-Garcia, P, Abad, P, Perez-Benavente, S, Paz-Artal, E, Reche, PA, Fobil, JN, Rubio, JM, Diez, A, Puyet, A and Bautista, JM (2019) Plasmodium falciparum immunodominant IgG epitopes in subclinical malaria. bioRxiv 792499.10.1101/792499
Bachmann, J, Burté, F, Pramana, S, Conte, I and Brown, B (2014) Affinity proteomics reveals elevated muscle proteins in plasma of children with cerebral malaria. PLoS Pathogens 10, e1004038.
Badaut, C, Bertin, G, Rustico, T, Fievet, N, Massougbodji, A, Gaye, A and Deloron, P (2010) Towards the rational design of a candidate vaccine against pregnancy associated malaria: conserved sequences of the DBL6ɛ domain of VAR2CSA. PLoS ONE 5, e11276.
Bahk, YY, Na, BK, Cho, SH, Kim, JY, Lim, KJ and Kim, TS (2010) Proteomic analysis of haptoglobin and amyloid A protein levels in patients with vivax Malaria. The Korean Journal of Parasitology 48, 203211.
Bark, SKN, Ahmad, R, Dantzler, K, Lukens, AK, De Niz, M, Szucs, MJ, Jin, X, Cotton, J, Hoffmann, D, Bric-Furlong, E, Oomen, R, Parrington, M, Milner, D, Neafsey, DE, Carr, SA, Wirth, DF and Marti, M (2018) Quantitative proteomic profiling reveals novel Plasmodium falciparum surface antigens and possible vaccine candidates. Molecular & Cellular Proteomics 17, 4360.
Belachew, EB (2018) Immune response and evasion mechanisms of Plasmodium falciparum parasites. Journal of Immunology Research 2018, 16.
Bertin, GI, Sabbagh, A, Guillonneau, F, Jafari-Guemouri, S, Ezinmegnon, S, Federici, C, Hounkpatin, B, Fievet, N and Deloron, P (2013) Differential protein expression profiles between Plasmodium falciparum parasites isolated from subjects presenting with pregnancy-associated malaria and uncomplicated malaria in Benin. The Journal of Infectious Diseases 208, 19871997.
Bertin, GI, Sabbagh, A, Argy, N, Salnot, V, Ezinmegnon, S, Agbota, G, Ladipo, Y, Alao, JM, Sagbo, G, Guillonneau, F and Deloron, P (2016) Proteomic analysis of Plasmodium falciparum parasites from patients with cerebral and uncomplicated malaria. Scientific Reports 6, 26773.
Blackman, MJ and Bannister, LH (2001) Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Molecular and Biochemical Parasitology 117, 1125.
Cabral, FJ, Vianna, LG, Medeiros, MM, Carlos, BC, Martha, RD, Silva, NM, Hildebrando, P, da Silva, L, Stabeli, RG and Wunderlich, G (2017) Immunoproteomics of Plasmodium falciparum-infected red blood cell membrane fractions. Memórias do Instituto Oswaldo Cruz 112, 850856.
Castelli, F, Odolini, S, Autino, B, Foca, E and Russo, R (2010) Malaria prophylaxis: a comprehensive review. Pharmaceuticals 3, 32123239.
Cezairliyan, B and Ausubel, FM (2017) Investment in secreted enzymes during nutrient-limited growth is utility dependent. Proceedings of the National Academy of Sciences 114, E7796E7802.
Chan, PP, Wasinger, VC and Leong, RW (2016) Current application of proteomics in biomarker discovery for inflammatory bowel disease. World Journal of Gastrointestinal Pathophysiology 7, 2737.
Chauhan, VS, Yazdani, SS and Gaur, D (2010) Malaria vaccine development based on merozoite surface proteins of Plasmodium falciparum. Human Vaccines 6, 757762.
Costa, RM, Nogueira, F, de Sousa, KP, Vitorino, R and Silva, MS (2013) Immunoproteomic analysis of Plasmodium falciparum antigens using sera from patients with clinical history of imported malaria. Malaria Journal 12, 100.
Davies, DH, Duffy, P, Bodmer, J-L, Felgner, PL and Doolan, DL (2015) Large screen approaches to identify novel malaria vaccine candidates. Vaccine 33, 74967505.
Deitsch, KW and Wellems, TE (1996) Membrane modifications in erythrocytes parasitized by Plasmodium falciparum. Molecular and Biochemical Parasitology 76, 110.
Deress, T and Girma, M (2019) Plasmodium falciparum and Plasmodium vivax prevalence in Ethiopia: a systematic review and meta-analysis. Malaria Research and Treatment 2019, 7065064.
Doolan, DL, Southwood, S, Freilich, DA, Sidney, J, Graber, NL, Shatney, L, Bebris, L, Florens, L, Dobano, C, Witney, AA, Appella, E, Hoffman, SL, Yates, JR, Carucci, DJ and Sette, A (2003) Identification of Plasmodium falciparum antigens by antigenic analysis of genomic and proteomic data. Proceedings of the National Academy of Sciences 100, 99529957.
Florens, L, Washburn, MP, Raine, JD, Anthony, RM, Grainger, M, Haynes, JD, Moch, JK, Muster, N, Sacci, JB, Tabb, DL, Witney, AA, Wolters, D, Wu, Y, Gardner, MJ, Holder, AA, Sinden, RE, Yates, JR and Carucci, DJ (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419, 520526.
Florens, L, Liu, X, Wang, Y, Yang, S, Schwartz, O, Peglar, M, Carucci, D, Yates, JR and Wub, Y (2004) Proteomics approach reveals novel proteins on the surface of malaria-infected erythrocytes. Molecular and Biochemical Parasitology 135, 111.
Fried, M and Duffy, PE (2015) Designing a VAR2CSA-based vaccine to prevent placental malaria. Vaccine 33, 74837488.
Frimpong, A, Kusi, KA, Ofori, MF and Ndifon, W (2018) Novel strategies for malaria vaccine design. Frontiers in Immunology 9, 2769.
Galassie, AC and Link, AJ (2015) Proteomic contributions to our understanding of vaccine and immune responses. PROTEOMICS – Clinical Applications 9, 972989.
Gardner, MJ, Hall, N, Fung, E, White, O, Berriman, M, Hyman, RW, Carlton, JM, Pain, A, Nelson, KE, Bowman, S, Paulsen, IT, James, K, Eisen, J, Rutherford, K, Salzberg, SL, Craig, A, Kyes, S, Chan, MS, Nene, V, Shallom, SJ, Suh, B, Peterson, J, Angiuoli, S, Pertea, M, Allen, J, Selengut, J, Haft, D, Mather, MW, Vaidya, AB, Martin, DMA, Fairlamb, AH, Fraunholz, MJ, Roos, DS, Ralph, SA, McFadden, GI, Cummings, LM, Subramanian, GM, Mungall, C, Venter, JC, Carucci, DJ, Hoffman, SL, Newbold, C, Davis, RW, Fraser, CM and Barrell, B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498511.
Garg, G, Singh, K and Ali, V (2018) Proteomic approaches unravel the intricacy of secreted proteins of Leishmania: an updated review. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics 1866, 913923.
Gebretsadik, G and Menon, M (2016) Proteomics and its applications in diagnosis of auto immune diseases. Open Journal of Immunology 6, 1433.10.4236/oji.2016.61003
Gelhaus, C, Fritsch, J, Krause, E and Leippe, M (2005) Fractionation and identification of proteins by 2-DE and MS: towards a proteomic analysis of Plasmodium falciparum. Proteomics 5, 42134222.
Gilson, PR, Nebl, T, Vukcevic, D, Moritz, RL, Sargeant, T, Speed, TP, Schofield, L and Crabb, BS (2006) Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Molecular & Cellular Proteomics 5, 12861299.
Gitau, EN, Kokwaro, GO, Karanja, H, Newton, CR and Ward, SA (2013) Plasma and cerebrospinal proteomes from children with cerebral malaria differ from those of children with other encephalopathies. The Journal of Infectious Diseases 208, 14941503.
Gomase, V, Kapoor, R and Ladak, S (2010) Immuno-proteomics approach for synthetic vaccine development form Haemophilus influenzae. Journal of Infectious Diseases Letters 1, 3946.
Gour, JK, Kumar, V, Singh, N, Bajpai, S, Pandey, HP and Singh, RK (2012) Identification of Th1-responsive leishmanial excretory–secretory antigens (LESAs). Experimental Parasitology 132, 355361.
Healer, J, Chiu, CY and Hansen, DS (2018) Mechanisms of naturally acquired immunity to P. falciparum and approaches to identify merozoite antigen targets. Parasitology 145, 839847.
Hodgson, SH, Ewer, KJ, Bliss, CM, Edwards, NJ, Rampling, T, Anagnostou, NA, de Barra, E, Havelock, T, Bowyer, G, Poulton, ID, de Cassan, S, Longley, R, Illingworth, JJ, Douglas, AD, Mange, PB, Collins, KA, Roberts, R, Gerry, S, Berrie, E, Moyle, S, Colloca, S, Cortese, R, Sinden, RE, Gilbert, SC, Bejon, PH, Lawrie, AM, Nicosia, A, Faust, SN and Hill, AVS (2018) Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in malaria-naive individuals. The Journal of Infectious Diseases 211, 10761086.
Hu, J, Chen, Z, Gu, J, Wan, M, Shen, Q, Kieny, MP, He, J, Li, Z, Zhang, Q, Reed, ZH, Zhu, Y, Li, W, Cao, Y, Qu, L, Cao, Z, Wang, Q, Liu, H, Pan, X, Huang, X, Zhang, D, Xue, X and Pan, W (2008) Safety and immunogenicity of a malaria vaccine, Plasmodium falciparum AMA-1/MSP-1 chimeric protein formulated in montanide ISA 720 in healthy adults. PLoS ONE 3, e1952.
Hudler, P, Kocevar, N and Komel, R (2014) Proteomic approaches in biomarker discovery: new perspectives in cancer diagnostics. The Scientific World Journal 2014, 260348.
Huynh, MH, Rabenau, KE, Harper, JM, Beatty, WL, Sibley, LD and Carruthers, VB (2003) Rapid invasion of host cells by Toxoplasma requires secretion of the MIC2–M2AP adhesive protein complex. The EMBO Journal 22, 20822090.
Hviid, L (2010) The role of Plasmodium falciparum variant surface antigens in protective immunity and vaccine development. Human Vaccines 6, 8489.
Jahangiri, F, Jalallou, N and Ebrahimi, M (2019) Analysis of apical membrane antigen (AMA)-1 characteristics using bioinformatics tools in order to vaccine design against Plasmodium vivax infection. Genetics and Evolution 71, 224231.
Kamaliddin, C, Salnot, V, Leduc, M, Ezinmegnon, S, Broussard, C, Fievet, N, Deloron, P, Guillonneau, F and Bertin, GI (2017) PFI1785w: a highly conserved protein associated with pregnancy associated malaria. PLoS ONE 12, e0187817.
Kassa, FA, Shio, MT, Bellemare, MJ, Faye, B, Ndao, M and Olivier, M (2012) New inflammation-related biomarkers during malaria infection. PLoS ONE 6, e26495.
Kimani, D, Jagne, YJ, Cox, M, Kimani, E, Bliss, CM, Gitau, E, Ogwang, C, Afolabi, MO, Bowyer, G, Collins, KA, Edwards, N, Hodgson, SH, Duncan, CJA, Spencer, AJ, Knight, MG, Drammeh, A, Anagnostou, NA, Berrie, E, Moyle, S, Gilbert, SC, Soipei, P, Okebe, J, Colloca, S, Cortese, R, Viebig, NK, Roberts, R, Lawrie, AM, Nicosia, A, Imoukhuede, EB, Bejon, PH, Chilengi, R, Bojang, K, Flanagan, KL, Hill, AVS, Urban, BC and Ewer, KJ (2014) Translating the immunogenicity of prime-boost immunization with ChAd63 and MVA ME-TRAP from malaria naive to malaria-endemic populations. Molecular Therapy 22, 19922003.
Koncarevic, S, Bogumil, R and Becker, K (2007) SELDI-TOF-MS analysis of chloroquine resistant and sensitive Plasmodium falciparum strains. Proteomics 7, 711721.
Kumar, M, Varun, CN, Dey, G, Ravikumar, R, Mahadevan, A, Shankar, SK and Prasad, TK (2018) Identification of host-response in cerebral malaria patients using quantitative proteomic analysis. PROTEOMICS – Clinical Applications 12, 1600187.
Lasonder, E, Rijpma, SR, van Schaijk, BC, Hoeijmakers, WA, Kensche, PR, Gresnigt, MS, Italiaander, A, Vos, MW, Woestenenk, R, Bousema, T, Mair, GR, Khan, SM, Janse, CJ, Bártfai, R and Sauerwein, RW (2016) Integrated transcriptomic and proteomic analyses of P. falciparum gametocytes: molecular insight into sex-specific processes and translational repression. Nucleic Acids Research 44, 60876101.
Lin, WC, Tsai, CY, Huang, JM, Wu, SR, Chu, LJ and Huang, KY (2019) Quantitative proteomic analysis and functional characterization of Acanthamoeba castellanii exosome-like vesicles. Parasites & Vectors 12, 112.10.1186/s13071-019-3725-z
Lindner, SE, Swearingen, KE, Harupa, A, Vaughan, AM, Sinnis, P, Moritz, RL and Kappe, SH (2013) Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Molecular & Cellular Proteomics 12, 11271143.
Lucchi, N, Oberstaller, J, Kissinger, J and Udhayakumar, V (2013) Malaria diagnostics and surveillance in the post-genomic era. Public Health Genomics 16, 3743.
Maier, AG, Rug, M, O'Neill, MT, Brown, M, Chakravorty, S, Szestak, T, Chesson, J, Wu, Y, Hughes, K, Coppel, RL, Newbold, C, Beeson, JG, Craig, A, Crabb, BS and Cowman, AF (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134, 4861.
Mathema, VB and Na-Bangchang, K (2015) A brief review on biomarkers and proteomic approach for malaria research. Asian Pacific Journal of Tropical Medicine 8, 253262.
Menard, D and Dondorp, A (2017) Antimalarial drug resistance: a threat to malaria elimination. Cold Spring Harbor Perspectives in Medicine 7, a025619.
Miao, J, Chen, Z, Wang, Z, Shrestha, S, Li, X, Li, R and Cui, L (2017) Sex-specific biology of the human malaria parasite revealed from the proteomes of mature male and female gametocytes. Molecular & Cellular Proteomics 16, 537551.
Moreno, A and Joyner, C (2015) Malaria vaccine clinical trials: what's on the horizon. Current Opinion in Immunology 35, 98106.
Mu, AK-W, Bee, PC, Lau, YL and Chen, Y (2014) Identification of protein markers in patients infected with Plasmodium knowlesi, Plasmodium falciparum and Plasmodium vivax. International Journal of Molecular Sciences 15, 1995219961.
Obiero, JM, Campo, JJ, Scholzen, A, Randall, A, Bijker, EM, Roestenberg, M, Hermsen, CC, Teng, A, Jain, A, Davies, DH, Sauerwein, RW and Felgner, PL (2019) Antibody biomarkers associated with sterile protection induced by controlled human malaria infection under chloroquine prophylaxis. Msphere 4, e00027–e00019.
Ohnishi, K and Kimura, K (2001) Serum levels of vascular cell adhesion molecule 1 in the early post-treatment defervescent phase of falciparum malaria. Parasitology Research 87, 6769.
Ortega, C, Frando, A, Webb-Robertson, B-J, Anderson, LN, Fleck, N, Flannery, EL, Fishbaugher, M, Murphree, TA, Hansen, JR, Smith, RD, Kappe, SHI, Wright, AT and Grundner, C (2018) A global survey of ATPase activity in Plasmodium falciparum asexual blood stages and gametocytes. Molecular & Cellular Proteomics 17, 111120.
Ouédraogo, A, Tiono, AB, Kargougou, D, Yaro, JB, Ouédraogo, E, Kaboré, Y, Kangoye, D, Bougouma, EC, Gansane, A, Henri, N, Diarra, A, Sanon, S, Soulama, I, Konate, AT, Watson, NL, Brown, V, Hendriks, J, Pau, MG, Versteege, I, Wiesken, E, Sadoff, J, Nebie, I and Sirima, SB (2013) A phase 1b randomized, controlled, double-blinded dosage-escalation trial to evaluate the safety, reactogenicity and immunogenicity of an adenovirus type 35 based circumsporozoite malaria vaccine in Burkinabe healthy adults 18 to 45 years of age. PLoS ONE 8, e78679.
Pal-Bhowmick, I, Mehta, M, Coppens, I, Sharma, S and Jarori, GK (2007) Protective properties and surface localization of Plasmodium falciparum enolase. Infection and Immunity 75, 55005508.
Perera, MK, Herath, NP, Pathirana, SL, Phone-Kyaw, M, Alles, HK, Mendis, KN, Premawansa, S and Handunnetti, SM (2013) Association of high plasma TNF-alpha levels and TNF-alpha/IL-10 ratios with TNF2 allele in severe P. falciparum malaria patients in Sri Lanka. Pathogens and Global Health 107, 2129.
Ponsford, MJ, Medana, IM, Prapansilp, P, Hien, TT, Lee, SJ, Dondorp, AM, Esiri, MM, Day, NPJ, White, NJ and Turner, GDH (2012) Sequestration and microvascular congestion are associated with coma in human cerebral malaria. Journal of Infectious Diseases 205, 663671.10.1093/infdis/jir812
Qazi, KR, Wikman, M, Vasconcelos, N-M, Berzins, K, Ståhl, S and Fernández, C (2005) Enhancement of DNA vaccine potency by linkage of Plasmodium falciparum malarial antigen gene fused with a fragment of HSP70 gene. Vaccine 23, 11141125.
Ray, S, Renu, D, Srivastava, R, Gollapalli, K, Taur, S, Jhaveri, T, Dhali, S, Chennareddy, S, Potla, A, Dikshit, JB, Srikanth, R, Gogtay, N, Thatte, U, Patankar, S and Srivastava, S (2012) Proteomic investigation of falciparum and vivax malaria for identification of surrogate protein markers. PLoS ONE 7, e41751.
Ray, S, Kumar, V, Bhave, A, Singh, V, Gogtay, NJ, Thatte, UM, Talukdar, A, Kochar, SK, Patankar, S and Srivastava, S (2015) Proteomic analysis of Plasmodium falciparum induced alterations in humans from different endemic regions of India to decipher malaria pathogenesis and identify surrogate markers of severity. Journal of Proteomics 127, 103113.
Reuterswärd, P, Bergström, S, Orikiiriza, J, Lindquist, E, Bergström, S, Svahn, HA, Ayoglu, B, Uhlén, M, Wahlgren, M, Normark, J, Ribacke, U and Nilsson, P (2018) Levels of human proteins in plasma associated with acute paediatric malaria. Malaria Journal 17, 426.
Richie, TL and Saul, A (2002) Progress and challenges for malaria vaccines. Nature 415, 694701.
Roestenberg, M, McCall, M, Hopman, J, Wiersma, J, Luty, AJ, van Gemert, GJ, van de Vegte-Bolmer, M, van Schaijk, B, Teelen, K, Arens, T, Spaarman, L, de Mast, Q, Roeffen, W, Snounou, G, Rénia, L, van der Ven, A, Hermsen, CC and Sauerwein, R (2009) Protection against a malaria challenge by sporozoite inoculation. New England Journal of Medicine 361, 468477.
Sam-Yellowe, TY (2015) Immune complex proteomes: tools for vaccine discovery. Journal of Proteomics & Bioinformatics 8, 188.
Sampaio, NG, Cheng, L and Eriksson, EM (2017) The role of extracellular vesicles in malaria biology and pathogenesis. Malaria Journal 16, 245.
Sanchez, GI, Sedegah, M, Rogers, WO, Jones, TR, Sacci, J, Witney, A, Carucci, DJ, Kumar, N and Hoffman, SL (2001) Immunogenicity and protective efficacy of a Plasmodium yoelii Hsp60 DNA vaccine in BALB/c mice. Infection and Immunity 69, 38973905.
Sarfo, BO, Hahn, A, Schwarz, NG, Jaeger, A, Sarpong, N, Marks, F, Adu-Sarkodie, Y, Tamminga, T and May, J (2018) The usefulness of C-reactive protein in predicting malaria parasitemia in a sub-Saharan African region. PLoS ONE 13, e0201693.
Seydel, KB, Milner, DA Jr, Kamiza, SB, Molyneux, ME and Taylor, TE (2006) The distribution and intensity of parasite sequestration in comatose Malawian children. The Journal of Infectious Diseases 194, 208215.
Simon, N, Kuehn, A, Williamson, KC and Pradel, G (2016) Adhesion protein complexes of malaria gametocytes assemble following parasite transmission to the mosquito. Parasitology International 65, 2730.
Singh, SK, Roeffen, W, Andersen, G, Bousema, T, Christiansen, M, Sauerwein, R and Theisen, M (2015) A Plasmodium falciparum 48/45 single epitope R0. 6C subunit protein elicits high levels of transmission blocking antibodies. Vaccine 33, 19811986.
Siqueira-Batista, R, Gomes, AP, de Mendonça, EG, Vitorino, RR, de Azevedo, SFM, de Barros Freitas, R, Santana, LA and Goreti de Almeida Oliveira, M (2012) Plasmodium falciparum malaria: proteomic studies. Revista Brasileira de terapia intensiva 24, 394.
Souza, WD (2006) Secretory organelles of pathogenic protozoa. Anais da Academia Brasileira de Ciências 78, 271292.
Suárez-Cortés, P, Sharma, V, Bertuccini, L, Costa, G, Bannerman, N-L, Sannella, AR, Williamson, K, Klemba, M, Levashina, EA, Lasonder, E and Alano, P (2016) Comparative proteomics and functional analysis reveal a role of Plasmodium falciparum osmiophilic bodies in malaria parasite transmission. Molecular & Cellular Proteomics 15, 32433255.
Swearingen, KE and Lindner, SE (2018) Plasmodium parasites viewed through proteomics. Trends in Parasitology 34, 945960.
Swearingen, KE, Lindner, SE, Shi, L, Shears, MJ, Harupa, A, Hopp, CS, Vaughan, AM, Springer, TA, Moritz, RL, Kappe, SHI and Sinnis, P (2016) Interrogating the Plasmodium sporozoite surface: identification of surface-exposed proteins and demonstration of glycosylation on CSP and TRAP by mass spectrometry-based proteomics. PLoS Pathogens 12, e1005606.
Tao, D, Ubaida-Mohien, C, Mathias, DK, King, JG, Pastrana-Mena, R, Tripathi, A, Goldowitz, I, Graham, DR, Moss, E, Marti, M and Dinglasan, RR (2014) Sex-partitioning of the Plasmodium falciparum stage V gametocyte proteome provides insight into falciparum-specific cell biology. Molecular & Cellular Proteomics 13, 27052724.
Thera, MA, Doumbo, OK, Coulibaly, D, Laurens, MB, Kone, AK, Guindo, AB, Traore, K, Sissoko, M, Diallo, DA, Diarra, I, Kouriba, B, Daou, M, Dolo, A, Baby, M, Sissoko, MS, Sagara, I, Niangaly, A, Traore, I, Olotu, A, Godeaux, O, Leach, A, Dubois, MC, Ballou, WR, Cohen, J, Thompson, D, Dube, T, Soisson, L, Diggs, CL, Takala, SL, Lyke, KE, House, B, Lanar, DE, Dutta, S, Heppner, DG and Plowe, CV (2010) Safety and immunogenicity of an AMA1 malaria vaccine in Malian children: results of a phase 1 randomized controlled trial. PLoS ONE 5, e9041.
Thima, K, Reamtong, O, Moonsom, S and Chavalitshewinkoon-Petmitr, P (2017) Proteomic analysis of asexual stages, young and mature gametocytes of Plasmodium falciparum strain NF54 by mass spectrometry. Southeast Asian Journal of Tropical Medicine and Public Health 48, 711721.
Topolska, AE, Richie, TL, Nhan, DH and Coppel, RL (2004) Associations between responses to the rhoptry-associated membrane antigen of Plasmodium falciparum and immunity to malaria infection. Infection and Immunity 72, 33253330.
Zhang, Y, Huang, C, Kim, S, Golkaram, M, Dixon, MW, Tilley, L, Li, J, Zhang, S and Suresh, S (2015) Multiple stiffening effects of nanoscale knobs on human red blood cells infected with Plasmodium falciparum malaria parasite. Proceedings of the National Academy of Sciences 112, 60686073.

Keywords

The use of proteomics for the identification of promising vaccine and diagnostic biomarkers in Plasmodium falciparum

  • Reza Mansouri (a1), Mohammad Ali-Hassanzadeh (a2), Reza Shafiei (a3), Amir Savardashtaki (a4), Mohammadreza Karimazar (a5), Enayat Anvari (a6), Paul Nguewa (a7) and Sajad Rashidi (a5)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.