Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T05:13:31.115Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  19 June 2020

Reza Mansouri ,
Mohammad Ali-Hassanzadeh ,
Reza Shafiei ,
Amir Savardashtaki ,
Mohammadreza Karimazar ,
Enayat Anvari ,
Paul Nguewa  and
Sajad Rashidi Open the ORCID record for Sajad Rashidi [Opens in a new window]
Reza Mansouri
Affiliation:
Department of Immunology, Faculty of Medicine, Shahid Sadoughi University of Medical Sciences and Health Services, Yazd, Iran
Mohammad Ali-Hassanzadeh
Affiliation:
Department of Immunology, School of Medicine, Jiroft University of Medical Sciences, Jiroft, Iran
Reza Shafiei
Affiliation:
Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran
Amir Savardashtaki
Affiliation:
Department of Medical Biotechnology, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran
Mohammadreza Karimazar
Affiliation:
Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
Enayat Anvari
Affiliation:
Department of Physiology, Faculty of Medicine, Ilam University of Medical Sciences, Ilam, Iran
Paul Nguewa*
Affiliation:
Department of Microbiology and Parasitology, University of Navarra, ISTUN Instituto de Salud Tropical, IdiSNA (Navarra Institute for Health Research), c/ Irunlarrea 1, 31008Pamplona, Spain
Sajad Rashidi*
Affiliation:
Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
*
Author for correspondence: Paul Nguewa, E-mail: [email protected] and Sajad Rashidi, E-mail: [email protected]
Author for correspondence: Paul Nguewa, E-mail: [email protected] and Sajad Rashidi, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Diagnostic markermalariaPlasmodium falciparumproteomicsvaccine target
Type
Review Article
Information
Parasitology , Volume 147 , Issue 12 , October 2020 , pp. 1255 - 1262
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.CrossRefGoogle ScholarPubMed
Alharbi, RA (2020) Proteomics approach and techniques in identification of reliable biomarkers for diseases. Saudi Journal of Biological Sciences 27, 968–974.CrossRefGoogle ScholarPubMed
Antony, HA and Parija, SC (2016) Antimalarial drug resistance: an overview. Tropical Parasitology 6, 30–41.Google ScholarPubMed
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, 1987–1994.CrossRefGoogle ScholarPubMed
Aslam, B, Basit, M, Nisar, MA, Khurshid, M and Rasool, MH (2017) Proteomics: technologies and their applications. Journal of Chromatographic Science 55, 182–196.CrossRefGoogle ScholarPubMed
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 792499.10.1101/792499CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 203–211.CrossRefGoogle ScholarPubMed
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, 43–60.CrossRefGoogle Scholar
Belachew, EB (2018) Immune response and evasion mechanisms of Plasmodium falciparum parasites. Journal of Immunology Research 2018, 1–6.CrossRefGoogle ScholarPubMed
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, 1987–1997.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Blackman, MJ and Bannister, LH (2001) Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Molecular and Biochemical Parasitology 117, 11–25.CrossRefGoogle ScholarPubMed
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, 850–856.CrossRefGoogle ScholarPubMed
Castelli, F, Odolini, S, Autino, B, Foca, E and Russo, R (2010) Malaria prophylaxis: a comprehensive review. Pharmaceuticals 3, 3212–3239.CrossRefGoogle Scholar
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, E7796–E7802.CrossRefGoogle ScholarPubMed
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, 27–37.CrossRefGoogle ScholarPubMed
Chauhan, VS, Yazdani, SS and Gaur, D (2010) Malaria vaccine development based on merozoite surface proteins of Plasmodium falciparum. Human Vaccines 6, 757–762.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Davies, DH, Duffy, P, Bodmer, J-L, Felgner, PL and Doolan, DL (2015) Large screen approaches to identify novel malaria vaccine candidates. Vaccine 33, 7496–7505.CrossRefGoogle ScholarPubMed
Deitsch, KW and Wellems, TE (1996) Membrane modifications in erythrocytes parasitized by Plasmodium falciparum. Molecular and Biochemical Parasitology 76, 1–10.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 9952–9957.CrossRefGoogle ScholarPubMed
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, 520–526.CrossRefGoogle ScholarPubMed
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, 1–11.CrossRefGoogle ScholarPubMed
Fried, M and Duffy, PE (2015) Designing a VAR2CSA-based vaccine to prevent placental malaria. Vaccine 33, 7483–7488.CrossRefGoogle ScholarPubMed
Frimpong, A, Kusi, KA, Ofori, MF and Ndifon, W (2018) Novel strategies for malaria vaccine design. Frontiers in Immunology 9, 2769.CrossRefGoogle ScholarPubMed
Galassie, AC and Link, AJ (2015) Proteomic contributions to our understanding of vaccine and immune responses. PROTEOMICS – Clinical Applications 9, 972–989.CrossRefGoogle ScholarPubMed
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, 498–511.CrossRefGoogle ScholarPubMed
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, 913–923.CrossRefGoogle ScholarPubMed
Gebretsadik, G and Menon, M (2016) Proteomics and its applications in diagnosis of auto immune diseases. Open Journal of Immunology 6, 14–33.10.4236/oji.2016.61003CrossRefGoogle Scholar
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, 4213–4222.CrossRefGoogle ScholarPubMed
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, 1286–1299.CrossRefGoogle ScholarPubMed
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, 1494–1503.CrossRefGoogle ScholarPubMed
Gomase, V, Kapoor, R and Ladak, S (2010) Immuno-proteomics approach for synthetic vaccine development form Haemophilus influenzae. Journal of Infectious Diseases Letters 1, 39–46.Google Scholar
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, 355–361.CrossRefGoogle Scholar
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, 839–847.CrossRefGoogle Scholar
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, 1076–1086.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Hudler, P, Kocevar, N and Komel, R (2014) Proteomic approaches in biomarker discovery: new perspectives in cancer diagnostics. The Scientific World Journal 2014, 260348.CrossRefGoogle ScholarPubMed
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, 2082–2090.CrossRefGoogle ScholarPubMed
Hviid, L (2010) The role of Plasmodium falciparum variant surface antigens in protective immunity and vaccine development. Human Vaccines 6, 84–89.CrossRefGoogle ScholarPubMed
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, 224–231.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 1992–2003.CrossRefGoogle ScholarPubMed
Koncarevic, S, Bogumil, R and Becker, K (2007) SELDI-TOF-MS analysis of chloroquine resistant and sensitive Plasmodium falciparum strains. Proteomics 7, 711–721.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 6087–6101.CrossRefGoogle ScholarPubMed
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, 1–12.10.1186/s13071-019-3725-zCrossRefGoogle ScholarPubMed
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, 1127–1143.CrossRefGoogle ScholarPubMed
Lucchi, N, Oberstaller, J, Kissinger, J and Udhayakumar, V (2013) Malaria diagnostics and surveillance in the post-genomic era. Public Health Genomics 16, 37–43.CrossRefGoogle ScholarPubMed
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, 48–61.CrossRefGoogle ScholarPubMed
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, 253–262.CrossRefGoogle ScholarPubMed
Menard, D and Dondorp, A (2017) Antimalarial drug resistance: a threat to malaria elimination. Cold Spring Harbor Perspectives in Medicine 7, a025619.CrossRefGoogle ScholarPubMed
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, 537–551.CrossRefGoogle ScholarPubMed
Moreno, A and Joyner, C (2015) Malaria vaccine clinical trials: what's on the horizon. Current Opinion in Immunology 35, 98–106.CrossRefGoogle Scholar
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, 19952–19961.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 67–69.CrossRefGoogle ScholarPubMed
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, 111–120.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 5500–5508.CrossRefGoogle ScholarPubMed
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, 21–29.CrossRefGoogle Scholar
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, 663–671.10.1093/infdis/jir812CrossRefGoogle ScholarPubMed
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, 1114–1125.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 103–113.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Richie, TL and Saul, A (2002) Progress and challenges for malaria vaccines. Nature 415, 694–701.CrossRefGoogle ScholarPubMed
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, 468–477.CrossRefGoogle ScholarPubMed
Sam-Yellowe, TY (2015) Immune complex proteomes: tools for vaccine discovery. Journal of Proteomics & Bioinformatics 8, 188.CrossRefGoogle Scholar
Sampaio, NG, Cheng, L and Eriksson, EM (2017) The role of extracellular vesicles in malaria biology and pathogenesis. Malaria Journal 16, 245.CrossRefGoogle ScholarPubMed
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, 3897–3905.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 208–215.CrossRefGoogle ScholarPubMed
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, 27–30.CrossRefGoogle ScholarPubMed
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, 1981–1986.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Souza, WD (2006) Secretory organelles of pathogenic protozoa. Anais da Academia Brasileira de Ciências 78, 271–292.CrossRefGoogle ScholarPubMed
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, 3243–3255.CrossRefGoogle ScholarPubMed
Swearingen, KE and Lindner, SE (2018) Plasmodium parasites viewed through proteomics. Trends in Parasitology 34, 945–960.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 2705–2724.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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, 711–721.Google Scholar
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, 3325–3330.CrossRefGoogle ScholarPubMed
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, 6068–6073.CrossRefGoogle ScholarPubMed