دورية أكاديمية

In vitro production of infectious Plasmodium falciparum sporozoites.

التفاصيل البيبلوغرافية
العنوان: In vitro production of infectious Plasmodium falciparum sporozoites.
المؤلفون: Eappen AG; Sanaria, Rockville, MD, USA., Li T; Sanaria, Rockville, MD, USA., Marquette M; Sanaria, Rockville, MD, USA., Chakravarty S; Sanaria, Rockville, MD, USA., Kc N; Sanaria, Rockville, MD, USA.; Protein Potential, Rockville, MD, USA., Zanghi G; Center for Global Infectious Disease Research, Seattle Children's Research Institute, Seattle, WA, USA., Hoffman BU; Columbia University Irving Medical Center, New York, NY, USA.; Department of Medicine, UCSF, San Francisco, CA, USA., Hettiarachchi H; Sanaria, Rockville, MD, USA.; Heritage College of Osteopathic Medicine, Ohio University, Dublin, OH, USA., Patil A; Sanaria, Rockville, MD, USA., Abebe Y; Sanaria, Rockville, MD, USA., Tran C; Sanaria, Rockville, MD, USA., Yossef AA; Sanaria, Rockville, MD, USA., McWilliams I; Sanaria, Rockville, MD, USA., Morrison RD; Center for Global Infectious Disease Research, Seattle Children's Research Institute, Seattle, WA, USA., Rathakrishnan A; Sanaria, Rockville, MD, USA., Inbar E; Sanaria, Rockville, MD, USA., Aly ASI; Sanaria, Rockville, MD, USA., De La Vega P; Sanaria, Rockville, MD, USA., Belmonte M; Malaria Department, Naval Medical Research Center, Silver Spring, MD, USA.; Henry M. Jackson Foundation, Bethesda, MD, USA., Sedegah M; Malaria Department, Naval Medical Research Center, Silver Spring, MD, USA., Wai T; Sanaria, Rockville, MD, USA.; Protein Potential, Rockville, MD, USA., Campo JJ; Antigen Discovery Incorporated (ADI), Irvine, CA, USA., King H; Institute for Bioscience and Biotechnology Research, Rockville, MD, USA., Kappe SHI; Center for Global Infectious Disease Research, Seattle Children's Research Institute, Seattle, WA, USA.; Department of Pediatrics, University of Washington, Seattle, WA, USA.; Department of Global Health, University of Washington, Seattle, WA, USA., Li M; Sanaria, Rockville, MD, USA.; Protein Potential, Rockville, MD, USA., Billingsley PF; Sanaria, Rockville, MD, USA., Sim BKL; Sanaria, Rockville, MD, USA.; Protein Potential, Rockville, MD, USA., Hoffman SL; Sanaria, Rockville, MD, USA. slhoffman@sanaria.com.
المصدر: Nature [Nature] 2022 Dec; Vol. 612 (7940), pp. 534-539. Date of Electronic Publication: 2022 Dec 07.
نوع المنشور: Journal Article; Research Support, U.S. Gov't, P.H.S.; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE
أسماء مطبوعة: Publication: Basingstoke : Nature Publishing Group
Original Publication: London, Macmillan Journals ltd.
مواضيع طبية MeSH: Plasmodium falciparum*/growth & development , Sporozoites*/growth & development , Sporozoites*/pathogenicity, Animals ; Humans ; Mice ; Culicidae/parasitology ; Malaria/parasitology ; Malaria/prevention & control ; Malaria Vaccines/biosynthesis ; Malaria Vaccines/chemistry ; Malaria, Falciparum/parasitology ; Hepatocytes/parasitology ; Liver/parasitology ; Merozoite Surface Protein 1 ; Erythrocytes/parasitology ; In Vitro Techniques
مستخلص: An effective vaccine is needed for the prevention and elimination of malaria. The only immunogens that have been shown to have a protective efficacy of more than 90% against human malaria are Plasmodium falciparum (Pf) sporozoites (PfSPZ) manufactured in mosquitoes (mPfSPZ) 1-7 . The ability to produce PfSPZ in vitro (iPfSPZ) without mosquitoes would substantially enhance the production of PfSPZ vaccines and mosquito-stage malaria research, but this ability is lacking. Here we report the production of hundreds of millions of iPfSPZ. iPfSPZ invaded human hepatocytes in culture and developed to mature liver-stage schizonts expressing P. falciparum merozoite surface protein 1 (PfMSP1) in numbers comparable to mPfSPZ. When injected into FRGhuHep mice containing humanized livers, iPfSPZ invaded the human hepatocytes and developed to PfMSP1-expressing late liver stage parasites at 45% the quantity of cryopreserved mPfSPZ. Human blood from FRGhuHep mice infected with iPfSPZ produced asexual and sexual erythrocytic-stage parasites in culture, and gametocytes developed to PfSPZ when fed to mosquitoes, completing the P. falciparum life cycle from infectious gametocyte to infectious gametocyte without mosquitoes or primates.
(© 2022. The Author(s), under exclusive licence to Springer Nature Limited.)
References: Hoffman, S. L. et al. Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum. Vaccin. 6, 97–106 (2010). (PMID: 10.4161/hv.6.1.10396)
Seder, R. A. et al. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341, 1359–1365 (2013). (PMID: 10.1126/science.1241800)
Epstein, J. E. et al. Protection against Plasmodium falciparum malaria by PfSPZ vaccine. JCI Insight 2, e89154 (2017). (PMID: 10.1172/jci.insight.89154)
Mordmuller, B. et al. Sterile protection against human malaria by chemoattenuated PfSPZ vaccine. Nature 542, 445–449 (2017). (PMID: 10.1038/nature21060)
Jongo, S. A. et al. Increase of dose associated with decrease in protection against controlled human malaria infection by PfSPZ vaccine in Tanzanian adults. Clin. Infect. Dis. 71, 2849–2857 (2020). (PMID: 10.1093/cid/ciz1152)
Mwakingwe-Omari, A. et al. Two chemoattenuated PfSPZ malaria vaccines induce sterile hepatic immunity. Nature 595, 289–294 (2021). (PMID: 10.1038/s41586-021-03684-z)
Sissoko, M. S. et al. Safety and efficacy of a three-dose regimen of Plasmodium falciparum sporozoite vaccine in adults during an intense malaria transmission season in Mali: a randomised, controlled phase 1 trial. Lancet Infect. Dis. 22, 377–389 (2022). (PMID: 10.1016/S1473-3099(21)00332-7)
Trager, W. & Jensen, J. B. Human malaria parasites in continuous culture. Science 193, 673–675 (1976). (PMID: 10.1126/science.781840)
Haynes, J. D., Diggs, C. L., Hines, F. A. & Desjardins, R. E. Culture of human malaria parasites Plasmodium falciparum. Nature 263, 767–769 (1976). (PMID: 10.1038/263767a0)
Ifediba, T. & Vanderberg, J. P. Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature 294, 364–366 (1981). (PMID: 10.1038/294364a0)
Campbell, C. C., Collins, W. E., Nguyen Dinh, P., Barber, A. & Broderson, J. R. Plasmodium falciparum gametocytes from culture in vitro develop to sporozoites that are infectious to primates. Science 217, 1048–1050 (1982). (PMID: 10.1126/science.7051285)
Warburg, A. & Schneider, I. In vitro culture of the mosquito stages of Plasmodium falciparum. Exp. Parasitol. 76, 121–126 (1993). (PMID: 10.1006/expr.1993.1014)
World Malaria Report 2021 (WHO, 2021).
Epstein, J. E. et al. Live attenuated malaria vaccine designed to protect through hepatic CD8 + T cell immunity. Science 334, 475–480 (2011). (PMID: 10.1126/science.1211548)
Ishizuka, A. S. et al. Protection against malaria at 1 year and immune correlates following PfSPZ vaccination. Nat. Med. 22, 614–623 (2016). (PMID: 10.1038/nm.4110)
Sissoko, M. S. et al. Safety and efficacy of PfSPZ Vaccine against Plasmodium falciparum via direct venous inoculation in healthy malaria-exposed adults in Mali: a randomised, double-blind phase 1 trial. Lancet Infect. Dis. 17, 498–509 (2017). (PMID: 10.1016/S1473-3099(17)30104-4)
Lyke, K. E. et al. Attenuated PfSPZ Vaccine induces strain-transcending T cells and durable protection against heterologous controlled human malaria infection. Proc. Natl Acad. Sci. USA 114, 2711–2716 (2017). (PMID: 10.1073/pnas.1615324114)
Goswami, D. et al. A replication-competent late liver stage–attenuated human malaria parasite. JCI Insight 5, e135589 (2020). (PMID: 10.1172/jci.insight.135589)
Warburg, A. & Miller, L. H. Sporogonic development of a malaria parasite in vitro. Science 255, 448–450 (1992). (PMID: 10.1126/science.1734521)
Al-Olayan, E. M., Beetsma, A. L., Butcher, G. A., Sinden, R. E. & Hurd, H. Complete development of mosquito phases of the malaria parasite in vitro. Science 295, 677–679 (2002). (PMID: 10.1126/science.1067159)
Porter-Kelley, J. M. et al. Plasmodium yoelii: axenic development of the parasite mosquito stages. Exp. Parasitol. 112, 99–108 (2006). (PMID: 10.1016/j.exppara.2005.09.011)
Barr, P. J. et al. Recombinant Pfs25 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in experimental animals. J. Exp. Med. 174, 1203–1208 (1991). (PMID: 10.1084/jem.174.5.1203)
Posthuma, G. et al. Immunogold localization of circumsporozoite protein of the malaria parasite Plasmodium falciparum during sporogony in Anopheles stephensi midguts. J. Cell Biol. 46, 18–24 (1988).
Benton, G., Arnaoutova, I., George, J., Kleinman, H. K. & Koblinski, J. Matrigel: from discovery and ECM mimicry to assays and models for cancer research. Adv. Drug Deliv. Rev. 79-80, 3–18 (2014). (PMID: 10.1016/j.addr.2014.06.005)
Hoffman, S. L. et al. Sporozoite vaccine induces genetically restricted T cell elimination of malaria from hepatocytes. Science 244, 1078–1081 (1989). (PMID: 10.1126/science.2524877)
Doolan, D. L. & Hoffman, S. L. The complexity of protective immunity against liver-stage malaria. J. Immunol. 165, 1453–1462 (2000). (PMID: 10.4049/jimmunol.165.3.1453)
Hoffman, S. L. & Doolan, D. L. Malaria vaccines-targeting infected hepatocytes. Nat. Med. 6, 1218–1219 (2000). (PMID: 10.1038/81315)
Weiss, W. R. & Jiang, C. G. Protective CD8+ T lymphocytes in primates immunized with malaria sporozoites. PLoS ONE 7, e31247 (2012). (PMID: 10.1371/journal.pone.0031247)
Camponovo, F. et al. Proteome-wide analysis of a malaria vaccine study reveals personalized humoral immune profiles in Tanzanian adults. eLife 9, e53080 (2020). (PMID: 10.7554/eLife.53080)
Aly, A. S., Vaughan, A. M. & Kappe, S. H. Malaria parasite development in the mosquito and infection of the mammalian host. Annu. Rev. Microbiol. 63, 195–221 (2009). (PMID: 10.1146/annurev.micro.091208.073403)
Longley, R. J. et al. Comparative assessment of vaccine vectors encoding ten malaria antigens identifies two protective liver-stage candidates. Sci. Rep. 5, 11820 (2015). (PMID: 10.1038/srep11820)
Atella, G. C., Silva-Neto, M. A., Golodne, D. M., Arefin, S. & Shahabuddin, M. Anopheles gambiae lipophorin: characterization and role in lipid transport to developing oocyte. Insect Biochem. Mol. Biol. 36, 375–386 (2006). (PMID: 10.1016/j.ibmb.2006.01.019)
Costa, G. et al. Non-competitive resource exploitation within mosquito shapes within-host malaria infectivity and virulence. Nat. Commun. 9, 3474 (2018). (PMID: 10.1038/s41467-018-05893-z)
Gare, D. C., Piertney, S. B. & Billingsley, P. F. Anopheles gambiae collagen IV genes: cloning, phylogeny and midgut expression associated with blood feeding and Plasmodium infection. Int. J. Parasitol. 33, 681–690 (2003). (PMID: 10.1016/S0020-7519(03)00055-9)
Nacer, A., Walker, K. & Hurd, H. Localisation of laminin within Plasmodium berghei oocysts and the midgut epithelial cells of Anopheles stephensi. Parasit. Vectors 1, 33 (2008). (PMID: 10.1186/1756-3305-1-33)
Ponnudurai, T., Meuwissen, J. H., Leeuwenberg, A. D., Verhave, J. P. & Lensen, A. H. The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans. R. Soc. Trop. Med. Hyg. 76, 242–250 (1982). (PMID: 10.1016/0035-9203(82)90289-9)
Li, T. et al. Robust, reproducible, industrialized, standard membrane feeding assay for assessing the transmission blocking activity of vaccines and drugs against Plasmodium falciparum. Malar. J. 14, 150 (2015). (PMID: 10.1186/s12936-015-0665-8)
Feldmann, A. M. & Ponnudurai, T. Selection of Anopheles stephensi for refractoriness and susceptibility to Plasmodium falciparum. Med. Vet. Entomol. 3, 41–52 (1989). (PMID: 10.1111/j.1365-2915.1989.tb00473.x)
Bounkeua, V., Li, F. & Vinetz, J. M. In vitro generation of Plasmodium falciparum ookinetes. Am. J. Trop. Med. Hyg. 83, 1187–1194 (2010). (PMID: 10.4269/ajtmh.2010.10-0433)
FiberCell Systems Hollow Fiber Cell Culture: An Overview (FibreCellSystems); https://www.fibercellsystems.com/instructional-video-fibercell-systems-hollow-fiber-cell-culture-an-overview/ (2012).
Operation of a FiberCell Systems Duet Pump (FibreCellSystems); https://www.fibercellsystems.com/instructional-video-operation-of-a-fibercell-systems-duet-pump/ (2013).
Zavala, F., Gwadz, R. W., Collins, F. H., Nussenzweig, R. S. & Nussenzweig, V. Monoclonal antibodies to circumsporozoite proteins identify the species of malaria parasites in infected mosquitoes. Nature 299, 737–738 (1982). (PMID: 10.1038/299737a0)
Roestenberg, M. et al. Controlled human malaria infections by intradermal injection of cryopreserved Plasmodium falciparum sporozoites. Am. J. Trop. Med. Hyg. 88, 5–13 (2013). (PMID: 10.4269/ajtmh.2012.12-0613)
Sattabongkot, J. et al. Establishment of a human hepatocyte line that supports in vitro development of the exo-erythrocytic stages of the malaria parasites Plasmodium falciparum and P. vivax. Am. J. Trop. Med. Hyg. 74, 708–715 (2006). (PMID: 10.4269/ajtmh.2006.74.708)
Holder, A. A. The carboxy-terminus of merozoite surface protein 1: structure, specific antibodies and immunity to malaria. Parasitology 136, 1445–1456 (2009). (PMID: 10.1017/S0031182009990515)
Tsuji, M., Mattei, D., Nussenzweig, R. S., Eichinger, D. & Zavala, F. Demonstration of heat-shock protein 70 in the sporozoite stage of malaria parasites. Parasitol. Res. 80, 16–21 (1994). (PMID: 10.1007/BF00932618)
Sanchez, G. I., Rogers, W. O., Mellouk, S. & Hoffman, S. L. Plasmodium falciparum: exported protein-1, a blood stage antigen, is expressed in liver stage parasites. Exp. Parasitol. 79, 59–62 (1994). (PMID: 10.1006/expr.1994.1060)
Guerin-Marchand, C. et al. A liver-stage-specific antigen of Plasmodium falciparum characterized by gene cloning. Nature 329, 164–167 (1987). (PMID: 10.1038/329164a0)
Vaughan, A. M. et al. Complete Plasmodium falciparum liver-stage development in liver-chimeric mice. J. Clin. Invest. 122, 3618–3628 (2012). (PMID: 10.1172/JCI62684)
Kefi, M. et al. New rapid one-step PCR diagnostic assay for Plasmodium falciparum infective mosquitoes. Sci. Rep. 8, 1462 (2018). (PMID: 10.1038/s41598-018-19780-6)
Mensah, V. A. et al. Safety, immunogenicity and efficacy of prime-boost vaccination with ChAd63 and MVA encoding ME-TRAP against Plasmodium falciparum infection in adults in Senegal. PLoS ONE 11, e0167951 (2016). (PMID: 10.1371/journal.pone.0167951)
Zanghì, G. et al. A specific PfEMP1 is expressed in P. falciparum sporozoites and plays a role in hepatocyte infection. Cell Rep. 22, 2951–2963 (2018). (PMID: 10.1016/j.celrep.2018.02.075)
Gardner, M. J. et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498–511 (2002). (PMID: 10.1038/nature01097)
Celniker, S. E. et al. Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence. Genome Biol. 3, research0079.1 (2002). (PMID: 10.1186/gb-2002-3-12-research0079)
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012). (PMID: 10.1038/nmeth.1923)
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat. Methods 5, 621–628 (2008). (PMID: 10.1038/nmeth.1226)
Wagner, G. P., Kin, K. & Lynch, V. J. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci. 131, 281–285 (2012). (PMID: 10.1007/s12064-012-0162-3)
Breitling, R., Armengaud, P., Amtmann, A. & Herzyk, P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573, 83–92 (2004). (PMID: 10.1016/j.febslet.2004.07.055)
Tusher, V. G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl Acad. Sci. USA 98, 5116–5121 (2001). (PMID: 10.1073/pnas.091062498)
Robinson, M. D. & Smyth, G. K. Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 9, 321–332 (2008). (PMID: 10.1093/biostatistics/kxm030)
Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010). (PMID: 10.1186/gb-2010-11-10-r106)
Diehl, K. H. et al. A good practice guide to the administration of substances and removal of blood, including routes and volumes. J. Appl. Toxicol. 21, 15–23 (2001). (PMID: 10.1002/jat.727)
معلومات مُعتمدة: R43 AI085740 United States AI NIAID NIH HHS; 2R44AI085740-03A1 United States AI NIAID NIH HHS; 2R44AI085740-06A1 United States AI NIAID NIH HHS; W81XWH-16-2-0025 US Department of Defense
المشرفين على المادة: 0 (Malaria Vaccines)
0 (Merozoite Surface Protein 1)
تواريخ الأحداث: Date Created: 20221208 Date Completed: 20230111 Latest Revision: 20230201
رمز التحديث: 20231215
DOI: 10.1038/s41586-022-05466-7
PMID: 36477528
قاعدة البيانات: MEDLINE
الوصف
تدمد:1476-4687
DOI:10.1038/s41586-022-05466-7