دورية أكاديمية

Platelet derived growth factor receptor β (PDGFRβ) is a host receptor for the human malaria parasite adhesin TRAP.

التفاصيل البيبلوغرافية
العنوان: Platelet derived growth factor receptor β (PDGFRβ) is a host receptor for the human malaria parasite adhesin TRAP.
المؤلفون: Steel RWJ; Seattle Children's Research Institute, Seattle, WA, USA.; Infectious Diseases and Immune Defence Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, 3052, Australia., Vigdorovich V; Seattle Children's Research Institute, Seattle, WA, USA., Dambrauskas N; Seattle Children's Research Institute, Seattle, WA, USA., Wilder BK; Seattle Children's Research Institute, Seattle, WA, USA.; Vaccine and Gene Therapy Institute, Oregon Health and Science University, Beaverton, OR, 97006, USA., Arredondo SA; Seattle Children's Research Institute, Seattle, WA, USA., Goswami D; Seattle Children's Research Institute, Seattle, WA, USA., Kumar S; Seattle Children's Research Institute, Seattle, WA, USA., Carbonetti S; Seattle Children's Research Institute, Seattle, WA, USA., Swearingen KE; Institute for Systems Biology, Seattle, WA, USA., Nguyen T; Seattle Children's Research Institute, Seattle, WA, USA., Betz W; Seattle Children's Research Institute, Seattle, WA, USA., Camargo N; Seattle Children's Research Institute, Seattle, WA, USA., Fisher BS; Seattle Children's Research Institute, Seattle, WA, USA., Soden J; Retrogenix Ltd, Chinley, High Peak, SK23 6FJ, UK., Thomas H; Retrogenix Ltd, Chinley, High Peak, SK23 6FJ, UK., Freeth J; Retrogenix Ltd, Chinley, High Peak, SK23 6FJ, UK., Moritz RL; Institute for Systems Biology, Seattle, WA, USA., Noah Sather D; Seattle Children's Research Institute, Seattle, WA, USA. noah.sather@seattlechildrens.org.; Department of Pediatrics, University of Washington, Seattle, WA, USA. noah.sather@seattlechildrens.org.; Department of Global Health, University of Washington, Seattle, WA, USA. noah.sather@seattlechildrens.org., Kappe SHI; Seattle Children's Research Institute, Seattle, WA, USA. stefan.kappe@seattlechildrens.org.; Department of Pediatrics, University of Washington, Seattle, WA, USA. stefan.kappe@seattlechildrens.org.; Department of Global Health, University of Washington, Seattle, WA, USA. stefan.kappe@seattlechildrens.org.
المصدر: Scientific reports [Sci Rep] 2021 May 31; Vol. 11 (1), pp. 11328. Date of Electronic Publication: 2021 May 31.
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE
أسماء مطبوعة: Original Publication: London : Nature Publishing Group, copyright 2011-
مواضيع طبية MeSH: Host-Pathogen Interactions*, Plasmodium falciparum/*metabolism , Protozoan Proteins/*metabolism , Receptor, Platelet-Derived Growth Factor beta/*metabolism, HEK293 Cells ; Humans ; Plasmodium vivax/metabolism ; Plasmodium yoelii/metabolism ; Protozoan Proteins/isolation & purification
مستخلص: Following their inoculation by the bite of an infected Anopheles mosquito, the malaria parasite sporozoite forms travel from the bite site in the skin into the bloodstream, which transports them to the liver. The thrombospondin-related anonymous protein (TRAP) is a type 1 transmembrane protein that is released from secretory organelles and relocalized on the sporozoite plasma membrane. TRAP is required for sporozoite motility and host infection, and its extracellular portion contains adhesive domains that are predicted to engage host receptors. Here, we identified the human platelet-derived growth factor receptor β (hPDGFRβ) as one such protein receptor. Deletion constructs showed that the von Willebrand factor type A and thrombospondin repeat domains of TRAP are both required for optimal binding to hPDGFRβ-expressing cells. We also demonstrate that this interaction is conserved in the human-infective parasite Plasmodium vivax, but not the rodent-infective parasite Plasmodium yoelii. We observed expression of hPDGFRβ mainly in cells associated with the vasculature suggesting that TRAP:hPDGFRβ interaction may play a role in the recognition of blood vessels by invading sporozoites.
References: Geneva: World Health Organization. World malaria report 2020: 20 years of global progress and challenges (2020).
Medica, D. L. & Sinnis, P. Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infect. Immun. 73, 4363–4369 (2005). (PMID: 15972531116860310.1128/IAI.73.7.4363-4369.2005)
Amino, R. et al. Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat. Med. 12, 220–224 (2006). (PMID: 1642914410.1038/nm1350)
Ejigiri, I. & Sinnis, P. Plasmodium sporozoite-host interactions from the dermis to the hepatocyte. Curr. Opin. Microbiol. 12, 401–407 (2009). (PMID: 19608456272522110.1016/j.mib.2009.06.006)
Frevert, U. et al. Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol. 3, e192 (2005). (PMID: 15901208113529510.1371/journal.pbio.0030192)
Mota, M. M. et al. Migration of Plasmodium sporozoites through cells before infection. Science 291, 141–144 (2001). (PMID: 1114156810.1126/science.291.5501.141)
Tavares, J. et al. Role of host cell traversal by the malaria sporozoite during liver infection. J. Exp. Med. 210, 905–915 (2013). (PMID: 23610126364649210.1084/jem.20121130)
Prudêncio, M., Rodriguez, A. & Mota, M. M. The silent path to thousands of merozoites: the Plasmodium liver stage. Nat. Rev. Microbiol. 4, 849–856 (2006). (PMID: 1704163210.1038/nrmicro1529)
Cowman, A. F., Berry, D. & Baum, J. The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J. Cell Biol. 198, 961–971 (2012). (PMID: 22986493344478710.1083/jcb.201206112)
Arredondo, S. A., Schepis, A., Reynolds, L. & Kappe, S. H. I. Secretory organelle function in the plasmodium sporozoite. Trends Parasitol. https://doi.org/10.1016/j.pt.2021.01.008 (2021). (PMID: 10.1016/j.pt.2021.01.00833589364)
Sultan, A. A. et al. TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90, 511–522 (1997). (PMID: 926703110.1016/S0092-8674(00)80511-5)
Buscaglia, C. A., Coppens, I., Hol, W. G. J. & Nussenzweig, V. Sites of interaction between aldolase and thrombospondin-related anonymous protein in Plasmodium. Mol. Biol. Cell 14, 4947–4957 (2003). (PMID: 1459511328479710.1091/mbc.e03-06-0355)
Bergman, L. W. et al. Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J. Cell Sci. 116, 39–49 (2003). (PMID: 1245671410.1242/jcs.00194)
Ejigiri, I. et al. Shedding of TRAP by a Rhomboid Protease from the Malaria Sporozoite Surface Is Essential for Gliding Motility and Sporozoite Infectivity. PLoS Pathog. 8, (2012).
Gantt, S. et al. Antibodies against thrombospondin-related anonymous protein do not inhibit Plasmodium sporozoite infectivity in vivo. Infect. Immun. 68, 3667–3673 (2000). (PMID: 108165269765710.1128/IAI.68.6.3667-3673.2000)
Matuschewski, K., Nunes, A. C., Nussenzweig, V. & Menard, R. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J. 21, 1597–1606 (2002). (PMID: 1192754412593510.1093/emboj/21.7.1597)
Klug, D. et al. Evolutionarily distant I domains can functionally replace the essential ligand-binding domain of Plasmodium TRAP. Elife 9 (2020).
Jethwaney, D. et al. Fetuin-A, a hepatocyte-specific protein that binds Plasmodium berghei thrombospondin-related adhesive protein: a potential role in infectivity. Infect. Immun. 73, 5883–5891 (2005). (PMID: 16113307123112410.1128/IAI.73.9.5883-5891.2005)
Dundas, K. et al. Alpha-v-containing integrins are host receptors for the Plasmodium falciparum sporozoite surface protein, TRAP. Proc. Natl. Acad. Sci. https://doi.org/10.1073/pnas.1719660115 (2018). (PMID: 10.1073/pnas.1719660115296662545939106)
Morahan, B. J., Wang, L. & Coppel, R. L. No TRAP, no invasion. Trends Parasitol. 25, 77–84 (2009). (PMID: 1910120810.1016/j.pt.2008.11.004)
Song, G. J., Koksal, A. C., Lu, C. F. & Springer, T. A. Shape change in the receptor for gliding motility in Plasmodium sporozoites. Proc. Natl. Acad. Sci. U. S. A. 109, 21420–21425 (2012). (PMID: 23236185353562110.1073/pnas.1218581109)
Hodgson, S. H. et al. Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in Malaria-Naive individuals. J. Infect. Dis. 211, 1076–1086 (2015). (PMID: 2533673010.1093/infdis/jiu579)
Ogwang, C. et al. Prime-boost vaccination with chimpanzee adenovirus and modified vaccinia Ankara encoding TRAP provides partial protection against Plasmodium falciparum infection in Kenyan adults. Sci. Transl. Med. 7 (2015).
Cabral-Miranda, G. et al. Virus-Like Particle (VLP) Plus microcrystalline tyrosine (MCT) adjuvants enhance vaccine efficacy improving T and B cell immunogenicity and protection against Plasmodium berghei/vivax. Vaccines 5 (2017).
Kester, K. E. et al. Sequential Phase 1 and Phase 2 randomized, controlled trials of the safety, immunogenicity and efficacy of combined pre-erythrocytic vaccine antigens RTS, S and TRAP formulated with AS02 adjuvant system in healthy, malaria naïve adults. Vaccine 32, 6683–6691 (2014). (PMID: 2495035810.1016/j.vaccine.2014.06.033)
Bauza, K. et al. Efficacy of a Plasmodium vivax malaria vaccine using ChAd63 and modified vaccinia Ankara expressing thrombospondin-related anonymous protein as assessed with transgenic Plasmodium berghei parasites. Infect. Immun. 82, 1277–1286 (2014). (PMID: 24379295395799410.1128/IAI.01187-13)
Shen, J. et al. Development of a fully human anti-PDGFRbeta antibody that suppresses growth of human tumor xenografts and enhances antitumor activity of an anti-VEGFR2 antibody. Neoplasia 11, 594–604 (2009). (PMID: 19484148268544810.1593/neo.09278)
Vaughan, A. M. & Kappe, S. H. I. Malaria Parasite Liver Infection and Exoerythrocytic Biology. Cold Spring Harb. Perspect. Med. 7, (2017).
Silvie, O. et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat. Med. 9, 93–96 (2003). (PMID: 1248320510.1038/nm808)
Rodrigues, C. D. et al. Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4, 271–282 (2008). (PMID: 1877905310.1016/j.chom.2008.07.012)
Kaushansky, A. et al. Malaria parasites target the hepatocyte receptor EphA2 for successful host infection. Science 350, 1089–1092 (2015). (PMID: 26612952478317110.1126/science.aad3318)
Langlois, A.-C., Marinach, C., Manzoni, G. & Silvie, O. Plasmodium sporozoites can invade hepatocytic cells independently of the Ephrin receptor A2. PLoS ONE 13, e0200032 (2018). (PMID: 29975762603342710.1371/journal.pone.0200032)
Miyazaki, H. et al. Expression of platelet-derived growth factor receptor β is maintained by Prox1 in lymphatic endothelial cells and is required for tumor lymphangiogenesis. Cancer Sci. 105, 1116–1123 (2014). (PMID: 24981766446238510.1111/cas.12476)
Andrae, J., Gallini, R. & Betsholtz, C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22, 1276–1312 (2008). (PMID: 18483217273241210.1101/gad.1653708)
Kazlauskas, A. PDGFs and their receptors. Gene 614, 1–7 (2017). (PMID: 28267575672814110.1016/j.gene.2017.03.003)
Werner, S. & Grose, R. Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83, 835–870 (2003). (PMID: 1284341010.1152/physrev.2003.83.3.835)
Manzoni, G. et al. Plasmodium P36 determines host cell receptor usage during sporozoite invasion. Elife 6 (2017).
Harupa, A. et al. SSP3 is a novel plasmodium yoelii sporozoite surface protein with a role in gliding motility. Infect. Immun. 82, 4643–4653 (2014). (PMID: 25156733424934910.1128/IAI.01800-14)
Carbonetti, S. et al. A method for the isolation and characterization of functional murine monoclonal antibodies by single B cell cloning. J. Immunol. Methods 448, 66–73 (2017). (PMID: 28554543554694910.1016/j.jim.2017.05.010)
Wang, J.-Y. et al. Improved expression of secretory and trimeric proteins in mammalian cells via the introduction of a new trimer motif and a mutant of the tPA signal sequence. Appl. Microbiol. Biotechnol. 91, 731–740 (2011). (PMID: 2155692010.1007/s00253-011-3297-0)
Beckett, D., Kovaleva, E. & Schatz, P. J. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci. 8, 921–929 (1999). (PMID: 10211839214431310.1110/ps.8.4.921)
Swearingen, K. E. et al. Proteogenomic analysis of the total and surface-exposed proteomes of Plasmodium vivax salivary gland sporozoites. PLoS Negl. Trop. Dis. 11, e0005791 (2017). (PMID: 28759593555234010.1371/journal.pntd.0005791)
Carlton, J. M. et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455, 757–763 (2008). (PMID: 18843361265115810.1038/nature07327)
Auburn, S. et al. A new Plasmodium vivax reference sequence with improved assembly of the subtelomeres reveals an abundance of pir genes. Wellcome Open Res 1, 4 (2016). (PMID: 28008421517241810.12688/wellcomeopenres.9876.1)
Jex, A. et al. Integrated transcriptomic, proteomic and epigenomic analysis of Plasmodium vivax salivary-gland sporozoites. BioRxiv https://doi.org/10.1101/145250 (2017). (PMID: 10.1101/145250)
von Itzstein, M., Plebanski, M., Cooke, B. M. & Coppel, R. L. Hot, sweet and sticky: the glycobiology of Plasmodium falciparum. Trends Parasitol. 24, 210–218 (2008). (PMID: 10.1016/j.pt.2008.02.007)
Bushkin, G. G. et al. Suggestive evidence for Darwinian Selection against asparagine-linked glycans of Plasmodium falciparum and Toxoplasma gondii. Eukaryot. Cell 9, 228–241 (2010). (PMID: 19783771282300310.1128/EC.00197-09)
Carbonetti, S., Oliver, B. G., Glenn, J., Stamatatos, L. & Sather, D. N. Soluble HIV-1 envelope immunogens derived from an elite neutralizer elicit cross-reactive V1V2 antibodies and low potency neutralizing antibodies. PLoS ONE 9, e86905 (2014). (PMID: 24466285390066310.1371/journal.pone.0086905)
Backliwal, G., Hildinger, M., Hasija, V. & Wurm, F. M. High-density transfection with HEK-293 cells allows doubling of transient titers and removes need for a priori DNA complex formation with PEI. Biotechnol. Bioeng. 99, 721–727 (2008). (PMID: 1768065710.1002/bit.21596)
Miller, J. L. et al. Quantitative bioluminescent imaging of pre-erythrocytic malaria parasite infection using luciferase-expressing Plasmodium yoelii. PLoS ONE 8, e60820 (2013). (PMID: 23593316362396610.1371/journal.pone.0060820)
Foquet, L. et al. Anti-CD81 but not anti-SR-BI blocks Plasmodium falciparum liver infection in a humanized mouse model. J. Antimicrob. Chemother. 70, 1784–1787 (2015). (PMID: 2565641010.1093/jac/dkv019)
Sack, B. K. et al. Model for in vivo assessment of humoral protection against malaria sporozoite challenge by passive transfer of monoclonal antibodies and immune serum. Infect. Immun. 82, 808–817 (2014). (PMID: 24478094391139510.1128/IAI.01249-13)
معلومات مُعتمدة: R01 AI134956 United States AI NIAID NIH HHS; R01 GM087221 United States GM NIGMS NIH HHS; K25AI119229 United States NH NIH HHS; R01GM087221 United States NH NIH HHS
المشرفين على المادة: 0 (Protozoan Proteins)
120300-02-9 (thrombospondin-related adhesive protein, protozoan)
EC 2.7.10.1 (PDGFRB protein, human)
EC 2.7.10.1 (Receptor, Platelet-Derived Growth Factor beta)
تواريخ الأحداث: Date Created: 20210601 Date Completed: 20211119 Latest Revision: 20240505
رمز التحديث: 20240505
مُعرف محوري في PubMed: PMC8166973
DOI: 10.1038/s41598-021-90722-5
PMID: 34059712
قاعدة البيانات: MEDLINE
الوصف
تدمد:2045-2322
DOI:10.1038/s41598-021-90722-5