收稿日期: 2021-12-27
修回日期: 2022-03-13
网络出版日期: 2022-07-06
基金资助
上海市公共卫生体系建设三年行动计划(2020-2022)重点学科(GWV-10.1-XK13);上海市国际科技合作基金(18490741100)
Research progress on reticulocyte binding proteins associated with Plasmodium vivax invasion of reticulocytes
Received date: 2021-12-27
Revised date: 2022-03-13
Online published: 2022-07-06
Supported by
Fifth Round of Three-Year Public Health Action Plan of Shanghai(GWV-10.1-XK13);Project of Shanghai Science and Technology Commission(18490741100)
间日疟原虫是世界上分布最广泛的疟原虫,也是造成非洲以外地区人群感染疟疾的主要原因。间日疟原虫优先入侵网织红细胞,呈现高度的种特异性。间日疟原虫网织红细胞结合蛋白(PvRBP)家族作为入侵配体,介导了间日疟原虫入侵网织红细胞的新途径,是重要的免疫靶点。其中PvRBP2b与转铁蛋白受体1(TfR1),PvRBP2a与CD98的相互作用对间日疟原虫入侵网织红细胞至关重要。Pvrbp家族具有高度多态性并且可产生免疫逃避,能够增加间日疟入侵的效率和致病的严重程度。随着对间日疟原虫入侵分子机制研究的日益加深,研究产生高滴度抗体的疟疾疫苗将成为有效预防和控制疟疾的关键方法。本文就网织红细胞在间日疟原虫感染中的作用,以及PvRBP家族在人群产生免疫应答的研究进展作一综述。
石天琪 , 陈军虎 . 间日疟原虫入侵网织红细胞相关蛋白的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2022 , 40(3) : 396 -401 . DOI: 10.12140/j.issn.1000-7423.2022.03.018
Plasmodium vivax is the most geographically widespread malaria parasite that causes most malaria infection cases outside the most malarious continent, sub-Saharan Africa. P. vivax preferentially invades reticulocytes, with a high species specificity. P. vivax reticulocyte binding protein (PvRBP) family has been implicated in roles in reticulocyte invasion and severity of P. vivax infections. The members of PvRBP family act as invasion ligands that mediate new pathways for the parasites to invade reticulocytes, and therefore, are considered important immune targets. Importantly, PvRBP2a-CD98 and PvRBP2b-TfR1 have been identified as two major ligand-receptor pairs implicated in the invasion of reticulocytes by P. vivax. The Pvrbp family is highly polymorphic and can generate immune evasion, which can increase the efficiency of vivax malaria invasion and the severity of the disease. With the advances in research on the molecular mechanisms of P. vivax invasion, insights have been provided on members of this protein family as promising antimalarial vaccine candidates, able to generate high titer antibodies for effective prevention and control of vivax malaria. This review summarizes the role of reticulocytes in P. vivax infection and the function of the PvRBP proteins family as immune targets in the human population.
| [1] | WHO. World malaria report 2021[M]. Geneva: WHO, 2021: 17. |
| [2] | Fola AA,, Harrison GLA,, Hazairin MH, et al. Higher complexity of infection and genetic diversity of Plasmodium vivax than Plasmodium falciparum across all malaria transmission zones of Papua New Guinea[J]. Am J Trop Med Hyg, 2017, 96(3): 630-641. |
| [3] | Guerra CA,, Howes RE,, Patil AP, et al. The international limits and population at risk of Plasmodium vivax transmission in 2009[J]. PLoS Negl Trop Dis, 2010, 4(8): e774. |
| [4] | Zhang XX,, Chu RL,, Xuan YH, et al. Research progress on proteins associated with Plasmodium vivax invasion of erythrocytes[J]. Chin J Parasitol Parasit Dis, 2018, 36(2): 161-165. (in Chinese) |
| [4] | ( 张馨心,, 楚瑞林,, 玄英花, 等. 间日疟原虫入侵红细胞的相关蛋白研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2018, 36(2): 161-165.) |
| [5] | Zhang L,, YI BY,, Xia ZG, et al. Epidemiological characteristics of malaria in China, 2021[J]. Chin J Parasitol Parasit Dis, 2022, 40(2): 135-139. (in Chinese) |
| [5] | ( 张丽,, 易博禹,, 夏志贵, 等. 2021年全国疟疾疫情特征分析[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(2): 135-139.) |
| [6] | Feng J,, Zhang L,, Tu H, et al. From elimination to post-elimination: characteristics, challenges and re-transmission preventing strategy of imported malaria in China[J]. Chin Trop Med, 2021, 21(1): 5-10. (in Chinese) |
| [6] | ( 丰俊,, 张丽,, 涂宏, 等. 从消除到消除后: 中国输入性疟疾的疫情特征、挑战及防止再传播策略[J]. 中国热带医学, 2021, 21(1): 5-10.) |
| [7] | Cao J,, Liu YB,, Cao YY, et al. Sustained challenge to malaria elimination in China: imported malaria[J]. Chin J Parasitol Parasit Dis, 2018, 36(2): 93-96. (in Chinese) |
| [7] | ( 曹俊,, 刘耀宝,, 曹园园, 等. 中国消除疟疾的持续挑战:输入性疟疾[J]. 中国寄生虫学与寄生虫病杂志, 2018, 36(2): 93-96.) |
| [8] | Cowman AF,, Tonkin CJ,, Tham WH, et al. The molecular basis of erythrocyte invasion by malaria parasites[J]. Cell Host Microbe, 2017, 22(2): 232-245. |
| [9] | Pasvol G,, Weatherall DJ,, Wilson RJ. The increased susceptibility of young red cells to invasion by the malarial parasite Plasmodium falciparum[J]. Br J Haematol, 1980, 45(2): 285-295. |
| [10] | Mitchell GH,, Hadley TJ,, McGinniss MH, et al. Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors[J]. Blood, 1986, 67(5): 1519-1521. |
| [11] | Griffiths RE,, Kupzig S,, Cogan N, et al. The ins and outs of human reticulocyte maturation: autophagy and the endosome/exosome pathway[J]. Autophagy, 2012, 8(7): 1150-1151. |
| [12] | Lim C,, Pereira L,, Saliba KS, et al. Reticulocyte preference and stage development of Plasmodium vivax isolates[J]. J Infect Dis, 2016, 214(7): 1081-1084. |
| [13] | Chitnis CE,, Sharma A. Targeting the Plasmodium vivax Duffy-binding protein[J]. Trends Parasitol, 2008, 24(1): 29-34. |
| [14] | Ovchynnikova E,, Aglialoro F,, Bentlage AEH, et al. DARC extracellular domain remodeling in maturating reticulocytes explains Plasmodium vivax tropism[J]. Blood, 2017, 130(12): 1441-1444. |
| [15] | Kaur H,, Sehgal R,, Rani S. Duffy antigen receptor for chemokines (DARC) and susceptibility to Plasmodium vivax malaria[J]. Parasitol Int, 2019, 71: 73-75. |
| [16] | Gruszczyk J,, Kanjee U,, Chan LJ, et al. Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax[J]. Science, 2018, 359(6371): 48-55. |
| [17] | Kanjee U,, Rangel GW,, Clark MA, et al. Molecular and cellular interactions defining the tropism of Plasmodium vivax for reticulocytes[J]. Curr Opin Microbiol, 2018, 46: 109-115. |
| [18] | Galinski MR,, Medina CC,, Ingravallo P, et al. A reticulocyte-binding protein complex of Plasmodium vivax merozoites[J]. Cell, 1992, 69(7): 1213-1226. |
| [19] | Galinski MR,, Xu M,, Barnwell JW. Plasmodium vivax reticulocyte binding protein-2 (PvRBP-2) shares structural features with PvRBP-1 and the Plasmodium yoelii 235 kDa rhoptry protein family[J]. Mol Biochem Parasitol, 2000, 108(2): 257-262. |
| [20] | Urquiza M,, Patarroyo MA,, Marí V, et al. Identification and polymorphism of Plasmodium vivax RBP-1 peptides which bind specifically to reticulocytes[J]. Peptides, 2002, 23(12): 2265-2277. |
| [21] | Gaur D,, Singh S,, Singh S,, et al. Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion[J]. Proc Natl Acad Sci USA, 2007, 104(45): 17789-17794. |
| [22] | Carlton JM,, Adams JH,, Silva JC, et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax[J]. Nature, 2008, 455(7214): 757-763. |
| [23] | Li J,, Han ET. Dissection of the Plasmodium vivax reticulocyte binding-like proteins (PvRBPs)[J]. Biochem Biophys Res Commun, 2012, 426(1): 1-6. |
| [24] | Hester J,, Chan ER,, Menard D, et al. De novo assembly of a field isolate genome reveals novel Plasmodium vivax erythrocyte invasion genes[J]. PLoS Negl Trop Dis, 2013, 7(12): e2569. |
| [25] | Gupta ED,, Anand G,, Singh H, et al. Naturally acquired human antibodies against reticulocyte-binding domains of Plasmodium vivax proteins, PvRBP2c and PvRBP1a, exhibit binding-inhibitory activity[J]. J Infect Dis, 2017, 215(10): 1558-1568. |
| [26] | França CT,, He WQ,, Gruszczyk J, et al. Plasmodium vivax reticulocyte binding proteins are key targets of naturally acquired immunity in young Papua new Guinean children[J]. PLoS Negl Trop Dis, 2016, 10(9): e0005014. |
| [27] | Chim-Ong A,, Surit T,, Chainarin S, et al. The blood stage antigen RBP2-P1 of Plasmodium vivax binds reticulocytes and is a target of naturally acquired immunity[J]. Infect Immun, 2020, 88(4): e00616-e00619. |
| [28] | Han JH,, Lee SK,, Wang B, et al. Identification of a reticulocyte-specific binding domain of Plasmodium vivax reticulocyte-binding protein 1 that is homologous to the PfRh4 erythrocyte-binding domain[J]. Sci Rep, 2016, 6: 26993. |
| [29] | Han JH,, Lee SK,, Wang B, et al. Identification of a reticulocyte-specific binding domain of Plasmodium vivax reticulocyte-binding protein 1 that is homologous to the PfRh4 erythrocyte-binding domain[J]. Sci Rep, 2016, 6: 26993. |
| [30] | Ntumngia FB,, Thomson-Luque R,, Galusic S, et al. Identification and immunological characterization of the ligand domain of Plasmodium vivax reticulocyte binding protein 1a[J]. J Infect Dis, 2018, 218(7): 1110-1118. |
| [31] | Gupta S,, Singh S,, Popovici J, et al. Targeting a reticulocyte binding protein and Duffy binding protein to inhibit reticulocyte invasion by Plasmodium vivax[J]. Sci Rep, 2018, 8: 10511. |
| [32] | Rayner JC,, Galinski MR,, Ingravallo P, et al. 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[J]. Proc Natl Acad Sci USA, 2000, 97(17): 9648-9653. |
| [33] | Chan LJ,, Dietrich MH,, Nguitragool W, et al. Plasmodium vivax reticulocyte binding proteins for invasion into reticulocytes[J]. Cell Microbiol, 2020, 22(1): e13110. |
| [34] | Malleret B,, Sahili AE,, Tay MZ, et al. Plasmodium vivax binds host CD98hc (SLC3A2) to enter immature red blood cells[J]. Nat Microbiol, 2021, 6(8): 991-999. |
| [35] | Wright KE,, Hjerrild KA,, Bartlett J, et al. Structure of malaria invasion protein RH5 with erythrocyte basigin and blocking antibodies[J]. Nature, 2014, 515(7527): 427-430. |
| [36] | Gruszczyk J,, Lim NTY,, Arnott A, et al. Structurally conserved erythrocyte-binding domain in Plasmodium provides a versatile scaffold for alternate receptor engagement[J]. Proc Natl Acad Sci USA, 2016, 113(2): E191-E200. |
| [37] | Gruszczyk J,, Huang RK,, Chan LJ, et al. Cryo-EM structure of an essential Plasmodium vivax invasion complex[J]. Nature, 2018, 559(7712): 135-139. |
| [38] | Galinski MR,, Barnwell JW. Plasmodium vivax: merozoites, invasion of reticulocytes and considerations for malaria vaccine development[J]. Parasitol Today, 1996, 12(1): 20-29. |
| [39] | Ford A,, Kepple D,, Abagero BR, et al. Whole genome sequencing of Plasmodium vivax isolates reveals frequent sequence and structural polymorphisms in erythrocyte binding genes[J]. PLoS Negl Trop Dis, 2020, 14(10): e0008234. |
| [40] | Kosaisavee V,, Lek-Uthai U,, Suwanarusk R, et al. Genetic diversity in new members of the reticulocyte binding protein family in Thai Plasmodium vivax isolates[J]. PLoS One, 2012, 7(3): e32105. |
| [41] | Han JH,, Li J,, Wang B, et al. Identification of immunodominant B-cell epitope regions of reticulocyte binding proteins in Plasmodium vivax by protein microarray based immunoscreening[J]. Korean J Parasitol, 2015, 53(4): 403-411. |
| [42] | Ovchynnikova E,, Aglialoro F,, Bentlage AEH, et al. DARC extracellular domain remodeling in maturating reticulocytes explains Plasmodium vivax tropism[J]. Blood, 2017, 130(12): 1441-1444. |
| [43] | Kanjee U,, Rangel GW,, Clark MA, et al. Molecular and cellular interactions defining the tropism of Plasmodium vivax for reticulocytes[J]. Curr Opin Microbiol, 2018, 46: 109-115. |
| [44] | Moras M,, Lefevre SD,, Ostuni MA. From erythroblasts to mature red blood cells: organelle clearance in mammals[J]. Front Physiol, 2017, 8: 1076. |
| [45] | Thomson-Luque R,, Wang CQ,, Ntumngia FB, et al. In-depth phenotypic characterization of reticulocyte maturation using mass cytometry[J]. Blood Cells Mol Dis, 2018, 72: 22-33. |
| [46] | Lawrence CM,, Ray S,, Babyonyshev M, et al. Crystal structure of the ectodomain of human transferrin receptor[J]. Science, 1999, 286(5440): 779-782. |
| [47] | Kawabata H. Transferrin and transferrin receptors update[J]. Free Radic Biol Med, 2019, 133: 46-54. |
| [48] | Cheng YF,, Zak O,, Aisen P, et al. Structure of the human transferrin receptor-transferrin complex[J]. Cell, 2004, 116(4): 565-576. |
| [49] | Chan LJ,, Gandhirajan A,, Carias LL, et al. Naturally acquired blocking human monoclonal antibodies to Plasmodium vivax reticulocyte binding protein 2b[J]. Nat Commun, 2021, 12(1): 1538. |
| [50] | Malleret B,, Rénia L,, Russell B. The unhealthy attraction of Plasmodium vivax to reticulocytes expressing transferrin receptor 1 (CD71)[J]. Int J Parasitol, 2017, 47(7): 379-383. |
| [51] | Segawa H,, Fukasawa Y,, Miyamoto K, et al. Identification and functional characterization of a Na+-independent neutral amino acid transporter with broad substrate selectivity[J]. J Biol Chem, 1999, 274(28): 19745-19751. |
| [52] | Malleret B,, Li A,, Zhang R, et al. Plasmodium vivax: restricted tropism and rapid remodeling of CD71-positive reticulocytes[J]. Blood, 2015, 125(8): 1314-1324. |
| [53] | Mueller I,, Galinski MR,, Tsuboi T, et al. Natural acquisition of immunity to Plasmodium vivax: epidemiological observations and potential targets[J]. Adv Parasitol, 2013, 81: 77-131. |
| [54] | Céspedes N,, Li Wai Suen CSN,, Koepfli C, et al. Natural immune response to Plasmodium vivax alpha-helical coiled coil protein motifs and its association with the risk of P. vivax malaria[J]. PLoS One, 2017, 12(6): e0179863. |
| [55] | Tran TM,, Oliveira-Ferreira J,, Moreno A, et al. Comparison of IgG reactivities to Plasmodium vivax merozoite invasion antigens in a Brazilian Amazon population[J]. Am J Trop Med Hyg, 2005, 73(2): 244-255. |
| [56] | França CT,, White MT,, He WQ, et al. Identification of highly-protective combinations of Plasmodium vivax recombinant proteins for vaccine development[J]. eLife, 2017, 6: e28673. |
| [57] | Longley RJ,, França CT,, White MT, et al. Asymptomatic Plasmodium vivax infections induce robust IgG responses to multiple blood-stage proteins in a low-transmission region of western Thailand[J]. Malar J, 2017, 16(1): 178. |
| [58] | Chuquiyauri R,, Molina DM,, Moss EL, et al. Genome-scale protein microarray comparison of human antibody responses in Plasmodium vivax relapse and reinfection[J]. Am J Trop Med Hyg, 2015, 93(4): 801-809. |
| [59] | Longley RJ,, White MT,, Takashima E, et al. Development and validation of serological markers for detecting recent Plasmodium vivax infection[J]. Nat Med, 2020, 26(5): 741-749. |
| [60] | Hietanen J,, Chim-Ong A,, Chiramanewong T, et al. Gene models, expression repertoire, and immune response of Plasmodium vivax reticulocyte binding proteins[J]. Infect Immun, 2015, 84(3): 677-685. |
| [61] | Chen SL,, Liu TP,, Xu WY. Development of malaria vaccines and the challenges[J]. Chin J Parasitol Parasit Dis, 2021, 39(3): 283-295. (in Chinese) |
| [61] | ( 陈穗林,, 刘太平,, 徐文岳. 疟疾疫苗研制及其存在的问题[J]. 中国寄生虫学与寄生虫病杂志, 2021, 39(3): 283-295.) |
/
| 〈 |
|
〉 |