{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T04:33:56Z","timestamp":1791261236455,"version":"4.1.0"},"reference-count":46,"publisher":"National Academy of Sciences","issue":"5","license":[{"start":{"date-parts":[[2020,1,21]],"date-time":"2020-01-21T00:00:00Z","timestamp":1579564800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000865","name":"Bill and Melinda Gates Foundation","doi-asserted-by":"publisher","award":["OPP1139763"],"award-info":[{"award-number":["OPP1139763"]}],"id":[{"id":"10.13039\/100000865","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100001246","name":"Ambrose Monell Foundation","doi-asserted-by":"publisher","award":["Tsetse Transmitted African trypanosomiasis Control"],"award-info":[{"award-number":["Tsetse Transmitted African trypanosomiasis Control"]}],"id":[{"id":"10.13039\/100001246","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"HHS | National Institutes of Health","doi-asserted-by":"publisher","award":["AI051584"],"award-info":[{"award-number":["AI051584"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2020,2,4]]},"abstract":"<jats:p>Tsetse-transmitted African trypanosomes must develop into mammalian-infectious metacyclic cells in the fly\u2019s salivary glands (SGs) before transmission to a new host. The molecular mechanisms that underlie this developmental process, known as metacyclogenesis, are poorly understood. Blocking the few metacyclic parasites deposited in saliva from further development in the mammal could prevent disease. To obtain an in-depth perspective of metacyclogenesis, we performed single-cell RNA sequencing (scRNA-seq) from a pool of 2,045 parasites collected from infected tsetse SGs. Our data revealed three major cell clusters that represent the epimastigote, and pre- and mature metacyclic trypanosome developmental stages. Individual cell level data also confirm that the metacyclic pool is diverse, and that each parasite expresses only one of the unique metacyclic variant surface glycoprotein (mVSG) coat protein transcripts identified. Further clustering of cells revealed a dynamic transcriptomic and metabolic landscape reflective of a developmental program leading to infectious metacyclic forms preadapted to survive in the mammalian host environment. We describe the expression profile of proteins that regulate gene expression and that potentially play a role in metacyclogenesis. We also report on a family of nonvariant surface proteins (Fam10) and demonstrate surface localization of one member (named SGM1.7) on mature metacyclic parasites. Vaccination of mice with recombinant SGM1.7 reduced parasitemia early in the infection. Future studies are warranted to investigate Fam10 family proteins as potential trypanosome transmission blocking vaccine antigens. Our experimental approach is translationally relevant for developing strategies to prevent other insect saliva-transmitted parasites from infecting and causing disease in mammalian hosts.<\/jats:p>","DOI":"10.1073\/pnas.1914423117","type":"journal-article","created":{"date-parts":[[2020,1,21]],"date-time":"2020-01-21T17:55:36Z","timestamp":1579629336000},"page":"2613-2621","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":65,"title":["Single-cell RNA sequencing of\n                    <i>Trypanosoma brucei<\/i>\n                    from tsetse salivary glands unveils metacyclogenesis and identifies potential transmission blocking antigens"],"prefix":"10.1073","volume":"117","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4986-6465","authenticated-orcid":false,"given":"Aur\u00e9lien","family":"Vigneron","sequence":"first","affiliation":[{"name":"Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2079-4122","authenticated-orcid":false,"given":"Michelle B.","family":"O\u2019Neill","sequence":"additional","affiliation":[{"name":"Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian L.","family":"Weiss","sequence":"additional","affiliation":[{"name":"Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amy F.","family":"Savage","sequence":"additional","affiliation":[{"name":"Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivia C.","family":"Campbell","sequence":"additional","affiliation":[{"name":"Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shaden","family":"Kamhawi","sequence":"additional","affiliation":[{"name":"Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20852"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jesus G.","family":"Valenzuela","sequence":"additional","affiliation":[{"name":"Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20852"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9941-143X","authenticated-orcid":false,"given":"Serap","family":"Aksoy","sequence":"additional","affiliation":[{"name":"Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2020,1,21]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"2322","DOI":"10.3201\/eid1712.110921","article-title":"Risk for human African trypanosomiasis, Central Africa, 2000-2009","volume":"17","author":"Simarro P. P.","year":"2011","unstructured":"P. P. Simarro ., Risk for human African trypanosomiasis, Central Africa, 2000-2009. Emerg. Infect. Dis. 17, 2322\u20132324 (2011).","journal-title":"Emerg. Infect. Dis."},{"key":"e_1_3_4_2_2","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1186\/1476-072X-9-57","article-title":"The Atlas of human African trypanosomiasis: A contribution to global mapping of neglected tropical diseases","volume":"9","author":"Simarro P. P.","year":"2010","unstructured":"P. P. Simarro ., The Atlas of human African trypanosomiasis: A contribution to global mapping of neglected tropical diseases. Int. J. Health Geogr. 9, 57 (2010).","journal-title":"Int. J. Health Geogr."},{"key":"e_1_3_4_3_2","doi-asserted-by":"crossref","first-page":"e1007","DOI":"10.1371\/journal.pntd.0001007","article-title":"The human African trypanosomiasis control and surveillance programme of the World Health Organization 2000-2009: The way forward","volume":"5","author":"Simarro P. P.","year":"2011","unstructured":"P. P. Simarro, A. Diarra, J. A. Ruiz Postigo, J. R. Franco, J. G. Jannin, The human African trypanosomiasis control and surveillance programme of the World Health Organization 2000-2009: The way forward. PLoS Negl. Trop. Dis. 5, e1007 (2011).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"e_1_3_4_4_2","doi-asserted-by":"crossref","first-page":"e55","DOI":"10.1371\/journal.pmed.0050055","article-title":"Eliminating human African trypanosomiasis: Where do we stand and what comes next?","volume":"5","author":"Simarro P. P.","year":"2008","unstructured":"P. P. Simarro, J. Jannin, P. Cattand, Eliminating human African trypanosomiasis: Where do we stand and what comes next? PLoS Med. 5, e55 (2008).","journal-title":"PLoS Med."},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"1724","DOI":"10.1111\/j.1462-5822.2009.01383.x","article-title":"Antigenic variation in the African trypanosome: Molecular mechanisms and phenotypic complexity","volume":"11","author":"Morrison L. J.","year":"2009","unstructured":"L. J. Morrison, L. Marcello, R. McCulloch, Antigenic variation in the African trypanosome: Molecular mechanisms and phenotypic complexity. Cell. Microbiol. 11, 1724\u20131734 (2009).","journal-title":"Cell. Microbiol."},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.mib.2008.06.006","article-title":"Interactions between trypanosomes and tsetse flies","volume":"11","author":"Roditi I.","year":"2008","unstructured":"I. Roditi, M. J. Lehane, Interactions between trypanosomes and tsetse flies. Curr. Opin. Microbiol. 11, 345\u2013351 (2008).","journal-title":"Curr. Opin. Microbiol."},{"key":"e_1_3_4_7_2","doi-asserted-by":"crossref","first-page":"6961","DOI":"10.1073\/pnas.1600304113","article-title":"Mammalian African trypanosome VSG coat enhances tsetse\u2019s vector competence","volume":"113","author":"Aksoy E.","year":"2016","unstructured":"E. Aksoy ., Mammalian African trypanosome VSG coat enhances tsetse\u2019s vector competence. Proc. Natl. Acad. Sci. U.S.A. 113, 6961\u20136966 (2016).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_8_2","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1017\/S0031182099004217","article-title":"Trypanosoma brucei spp. development in the tsetse fly: Characterization of the post-mesocyclic stages in the foregut and proboscis","volume":"118","author":"Van Den Abbeele J.","year":"1999","unstructured":"J. Van Den Abbeele, Y. Claes, D. van Bockstaele, D. Le Ray, M. Coosemans, Trypanosoma brucei spp. development in the tsetse fly: Characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118, 469\u2013478 (1999).","journal-title":"Parasitology"},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1111\/j.1365-2958.2006.05492.x","article-title":"A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei","volume":"63","author":"Urwyler S.","year":"2007","unstructured":"S. Urwyler, E. Studer, C. K. Renggli, I. Roditi, A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei. Mol. Microbiol. 63, 218\u2013228 (2007).","journal-title":"Mol. Microbiol."},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"1842","DOI":"10.1242\/dev.072611","article-title":"A new asymmetric division contributes to the continuous production of infective trypanosomes in the tsetse fly","volume":"139","author":"Rotureau B.","year":"2012","unstructured":"B. Rotureau, I. Subota, J. Buisson, P. Bastin, A new asymmetric division contributes to the continuous production of infective trypanosomes in the tsetse fly. Development 139, 1842\u20131850 (2012).","journal-title":"Development"},{"key":"e_1_3_4_11_2","first-page":"269","article-title":"An estimate of the size of the metacyclic variable antigen repertoire of Trypanosoma brucei rhodesiense","volume":"97","author":"Turner C. M.","year":"1988","unstructured":"C. M. Turner, J. D. Barry, I. Maudlin, K. Vickerman, An estimate of the size of the metacyclic variable antigen repertoire of Trypanosoma brucei rhodesiense. Parasitology 97, 269\u2013276 (1988).","journal-title":"Parasitology"},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"e1005784","DOI":"10.1371\/journal.ppat.1005784","article-title":"Masters of disguise: Antigenic variation and the VSG coat in Trypanosoma brucei","volume":"12","author":"Mugnier M. R.","year":"2016","unstructured":"M. R. Mugnier, C. E. Stebbins, F. N. Papavasiliou, Masters of disguise: Antigenic variation and the VSG coat in Trypanosoma brucei. PLoS Pathog. 12, e1005784 (2016).","journal-title":"PLoS Pathog."},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1242\/jcs.87.2.363","article-title":"Onset of expression of the variant surface glycoproteins of Trypanosoma brucei in the tsetse fly studied using immunoelectron microscopy","volume":"87","author":"Tetley L.","year":"1987","unstructured":"L. Tetley, C. M. R. Turner, J. D. Barry, J. S. Crowe, K. Vickerman, Onset of expression of the variant surface glycoproteins of Trypanosoma brucei in the tsetse fly studied using immunoelectron microscopy. J. Cell Sci. 87, 363\u2013372 (1987).","journal-title":"J. Cell Sci."},{"key":"e_1_3_4_14_2","first-page":"313","article-title":"Analysis by flow cytometry of DNA synthesis during the life cycle of African trypanosomes","volume":"41","author":"Shapiro S. Z.","year":"1984","unstructured":"S. Z. Shapiro, J. Naessens, B. Liesegang, S. K. Moloo, J. Magondu, Analysis by flow cytometry of DNA synthesis during the life cycle of African trypanosomes. Acta Trop. 41, 313\u2013323 (1984).","journal-title":"Acta Trop."},{"key":"e_1_3_4_15_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1242\/jcs.74.1.1","article-title":"Differentiation in Trypanosoma brucei: Host-parasite cell junctions and their persistence during acquisition of the variable antigen coat","volume":"74","author":"Tetley L.","year":"1985","unstructured":"L. Tetley, K. Vickerman, Differentiation in Trypanosoma brucei: Host-parasite cell junctions and their persistence during acquisition of the variable antigen coat. J. Cell Sci. 74, 1\u201319 (1985).","journal-title":"J. Cell Sci."},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1093\/oxfordjournals.bmb.a072036","article-title":"Developmental cycles and biology of pathogenic trypanosomes","volume":"41","author":"Vickerman K.","year":"1985","unstructured":"K. Vickerman, Developmental cycles and biology of pathogenic trypanosomes. Br. Med. Bull. 41, 105\u2013114 (1985).","journal-title":"Br. Med. Bull."},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/0248-4900(88)90070-6","article-title":"Biology of African trypanosomes in the tsetse fly","volume":"64","author":"Vickerman K.","year":"1988","unstructured":"K. Vickerman, L. Tetley, K. A. Hendry, C. M. Turner, Biology of African trypanosomes in the tsetse fly. Biol. Cell 64, 109\u2013119 (1988).","journal-title":"Biol. Cell"},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"e0168877","DOI":"10.1371\/journal.pone.0168877","article-title":"Transcriptome profiling of Trypanosoma brucei development in the tsetse fly vector Glossina morsitans","volume":"11","author":"Savage A. F.","year":"2016","unstructured":"A. F. Savage ., Transcriptome profiling of Trypanosoma brucei development in the tsetse fly vector Glossina morsitans. PLoS One 11, e0168877 (2016).","journal-title":"PLoS One"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1016\/j.mib.2007.09.014","article-title":"The cell biology of Trypanosoma brucei differentiation","volume":"10","author":"Fenn K.","year":"2007","unstructured":"K. Fenn, K. R. Matthews, The cell biology of Trypanosoma brucei differentiation. Curr. Opin. Microbiol. 10, 539\u2013546 (2007).","journal-title":"Curr. Opin. Microbiol."},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","first-page":"5945","DOI":"10.1128\/MCB.15.11.5945","article-title":"Transcriptional regulation of metacyclic variant surface glycoprotein gene expression during the life cycle of Trypanosoma brucei","volume":"15","author":"Graham S. V.","year":"1995","unstructured":"S. V. Graham, J. D. Barry, Transcriptional regulation of metacyclic variant surface glycoprotein gene expression during the life cycle of Trypanosoma brucei. Mol. Cell. Biol. 15, 5945\u20135956 (1995).","journal-title":"Mol. Cell. Biol."},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/S0166-6851(99)00128-0","article-title":"A structural and transcription pattern for variant surface glycoprotein gene expression sites used in metacyclic stage Trypanosoma brucei","volume":"103","author":"Graham S. V.","year":"1999","unstructured":"S. V. Graham, S. Terry, J. D. Barry, A structural and transcription pattern for variant surface glycoprotein gene expression sites used in metacyclic stage Trypanosoma brucei. Mol. Biochem. Parasitol. 103, 141\u2013154 (1999).","journal-title":"Mol. Biochem. Parasitol."},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1111\/mmi.13754","article-title":"The proteome and transcriptome of the infectious metacyclic form of Trypanosoma brucei define quiescent cells primed for mammalian invasion","volume":"106","author":"Christiano R.","year":"2017","unstructured":"R. Christiano ., The proteome and transcriptome of the infectious metacyclic form of Trypanosoma brucei define quiescent cells primed for mammalian invasion. Mol. Microbiol. 106, 74\u201392 (2017).","journal-title":"Mol. Microbiol."},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"e21800","DOI":"10.1371\/journal.pone.0021800","article-title":"REVIGO summarizes and visualizes long lists of gene ontology terms","volume":"6","author":"Supek F.","year":"2011","unstructured":"F. Supek, M. Bo\u0161njak, N. \u0160kunca, T. \u0160muc, REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6, e21800 (2011).","journal-title":"PLoS One"},{"key":"e_1_3_4_24_2","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.pt.2005.02.008","article-title":"Energy generation in insect stages of Trypanosoma brucei: Metabolism in flux","volume":"21","author":"Besteiro S.","year":"2005","unstructured":"S. Besteiro, M. P. Barrett, L. Rivi\u00e8re, F. Bringaud, Energy generation in insect stages of Trypanosoma brucei: Metabolism in flux. Trends Parasitol. 21, 185\u2013191 (2005).","journal-title":"Trends Parasitol."},{"key":"e_1_3_4_25_2","doi-asserted-by":"crossref","first-page":"1485","DOI":"10.1126\/science.3883489","article-title":"Trypanothione: A novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids","volume":"227","author":"Fairlamb A. H.","year":"1985","unstructured":"A. H. Fairlamb, P. Blackburn, P. Ulrich, B. T. Chait, A. Cerami, Trypanothione: A novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science 227, 1485\u20131487 (1985).","journal-title":"Science"},{"key":"e_1_3_4_26_2","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1046\/j.1365-2958.2000.01721.x","article-title":"Trypanosomes lacking trypanothione reductase are avirulent and show increased sensitivity to oxidative stress","volume":"35","author":"Krieger S.","year":"2000","unstructured":"S. Krieger ., Trypanosomes lacking trypanothione reductase are avirulent and show increased sensitivity to oxidative stress. Mol. Microbiol. 35, 542\u2013552 (2000).","journal-title":"Mol. Microbiol."},{"key":"e_1_3_4_27_2","doi-asserted-by":"crossref","first-page":"e1004689","DOI":"10.1371\/journal.ppat.1004689","article-title":"Probing the metabolic network in bloodstream-form Trypanosoma brucei using untargeted metabolomics with stable isotope labelled glucose","volume":"11","author":"Creek D. J.","year":"2015","unstructured":"D. J. Creek ., Probing the metabolic network in bloodstream-form Trypanosoma brucei using untargeted metabolomics with stable isotope labelled glucose. PLoS Pathog. 11, e1004689 (2015).","journal-title":"PLoS Pathog."},{"key":"e_1_3_4_28_2","doi-asserted-by":"crossref","first-page":"890","DOI":"10.4269\/ajtmh.15-0566","article-title":"Transcript abundance of putative lipid phosphate phosphatases during development of Trypanosoma brucei in the tsetse fly","volume":"94","author":"Alves e Silva T. L.","year":"2016","unstructured":"T. L. Alves e Silva, A. F. Savage, S. Aksoy, Transcript abundance of putative lipid phosphate phosphatases during development of Trypanosoma brucei in the tsetse fly. Am. J. Trop. Med. Hyg. 94, 890\u2013893 (2016).","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1017\/S0031182009005629","article-title":"Arrested growth of Trypanosoma cruzi by the calpain inhibitor MDL28170 and detection of calpain homologues in epimastigote forms","volume":"136","author":"Sangenito L. S.","year":"2009","unstructured":"L. S. Sangenito ., Arrested growth of Trypanosoma cruzi by the calpain inhibitor MDL28170 and detection of calpain homologues in epimastigote forms. Parasitology 136, 433\u2013441 (2009).","journal-title":"Parasitology"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"e18371","DOI":"10.1371\/journal.pone.0018371","article-title":"MDL28170, a calpain inhibitor, affects Trypanosoma cruzi metacyclogenesis, ultrastructure and attachment to Rhodnius prolixus midgut","volume":"6","author":"Ennes-Vidal V.","year":"2011","unstructured":"V. Ennes-Vidal, R. F. Menna-Barreto, A. L. Santos, M. H. Branquinha, C. M. d\u2019Avila-Levy, MDL28170, a calpain inhibitor, affects Trypanosoma cruzi metacyclogenesis, ultrastructure and attachment to Rhodnius prolixus midgut. PLoS One 6, e18371 (2011).","journal-title":"PLoS One"},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1111\/cmi.12268","article-title":"The emerging role of RNA-binding proteins in the life cycle of Trypanosoma brucei","volume":"16","author":"Kolev N. G.","year":"2014","unstructured":"N. G. Kolev, E. Ullu, C. Tschudi, The emerging role of RNA-binding proteins in the life cycle of Trypanosoma brucei. Cell. Microbiol. 16, 482\u2013489 (2014).","journal-title":"Cell. Microbiol."},{"key":"e_1_3_4_32_2","doi-asserted-by":"crossref","first-page":"146","DOI":"10.4331\/wjbc.v7.i1.146","article-title":"Regulation of RNA binding proteins in trypanosomatid protozoan parasites","volume":"7","author":"Romaniuk M. A.","year":"2016","unstructured":"M. A. Romaniuk, G. Cervini, A. Cassola, Regulation of RNA binding proteins in trypanosomatid protozoan parasites. World J. Biol. Chem. 7, 146\u2013157 (2016).","journal-title":"World J. Biol. Chem."},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.1126\/science.1229641","article-title":"Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein","volume":"338","author":"Kolev N. G.","year":"2012","unstructured":"N. G. Kolev, K. Ramey-Butler, G. A. Cross, E. Ullu, C. Tschudi, Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein. Science 338, 1352\u20131353 (2012).","journal-title":"Science"},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"1048","DOI":"10.1111\/j.1365-2958.2012.07988.x","article-title":"Expression of the RNA recognition motif protein RBP10 promotes a bloodstream-form transcript pattern in Trypanosoma brucei","volume":"83","author":"Wurst M.","year":"2012","unstructured":"M. Wurst ., Expression of the RNA recognition motif protein RBP10 promotes a bloodstream-form transcript pattern in Trypanosoma brucei. Mol. Microbiol. 83, 1048\u20131063 (2012).","journal-title":"Mol. Microbiol."},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"e1006560","DOI":"10.1371\/journal.ppat.1006560","article-title":"Expression of the RNA-binding protein RBP10 promotes the bloodstream-form differentiation state in Trypanosoma brucei","volume":"13","author":"Mugo E.","year":"2017","unstructured":"E. Mugo, C. Clayton, Expression of the RNA-binding protein RBP10 promotes the bloodstream-form differentiation state in Trypanosoma brucei. PLoS Pathog. 13, e1006560 (2017).","journal-title":"PLoS Pathog."},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.molbiopara.2017.06.009","article-title":"Conversion of procyclic-form Trypanosoma brucei to the bloodstream form by transient expression of RBP10","volume":"216","author":"Mugo E.","year":"2017","unstructured":"E. Mugo, F. Egler, C. Clayton, Conversion of procyclic-form Trypanosoma brucei to the bloodstream form by transient expression of RBP10. Mol. Biochem. Parasitol. 216, 49\u201351 (2017).","journal-title":"Mol. Biochem. Parasitol."},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"e2121","DOI":"10.1371\/journal.pntd.0002121","article-title":"A cell-surface phylome for African trypanosomes","volume":"7","author":"Jackson A. P.","year":"2013","unstructured":"A. P. Jackson ., A cell-surface phylome for African trypanosomes. PLoS Negl. Trop. Dis. 7, e2121 (2013).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"e_1_3_4_38_2","doi-asserted-by":"crossref","first-page":"e1708","DOI":"10.1371\/journal.pntd.0001708","article-title":"Transcript expression analysis of putative Trypanosoma brucei GPI-anchored surface proteins during development in the tsetse and mammalian hosts","volume":"6","author":"Savage A. F.","year":"2012","unstructured":"A. F. Savage ., Transcript expression analysis of putative Trypanosoma brucei GPI-anchored surface proteins during development in the tsetse and mammalian hosts. PLoS Negl. Trop. Dis. 6, e1708 (2012).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"e_1_3_4_39_2","doi-asserted-by":"crossref","first-page":"1911","DOI":"10.1074\/mcp.M114.047647","article-title":"Architecture of a host-parasite interface: Complex targeting mechanisms revealed through proteomics","volume":"14","author":"Gadelha C.","year":"2015","unstructured":"C. Gadelha ., Architecture of a host-parasite interface: Complex targeting mechanisms revealed through proteomics. Mol. Cell. Proteomics 14, 1911\u20131926 (2015).","journal-title":"Mol. Cell. Proteomics"},{"key":"e_1_3_4_40_2","doi-asserted-by":"crossref","first-page":"582","DOI":"10.3389\/fimmu.2017.00582","article-title":"African trypanosomes undermine humoral responses and vaccine development: Link with inflammatory responses?","volume":"8","author":"Stijlemans B.","year":"2017","unstructured":"B. Stijlemans, M. Radwanska, C. De Trez, S. Magez, African trypanosomes undermine humoral responses and vaccine development: Link with inflammatory responses? Front. Immunol. 8, 582 (2017).","journal-title":"Front. Immunol."},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1017\/S0031182000000573","article-title":"Studies on Trypanosoma (nannomonas) congolense III. Antigenic variation in three cyclically transmitted stocks","volume":"80","author":"Nantulya V. M.","year":"1980","unstructured":"V. M. Nantulya, J. J. Doyle, L. Jenni, Studies on Trypanosoma (nannomonas) congolense III. Antigenic variation in three cyclically transmitted stocks. Parasitology 80, 123\u2013131 (1980).","journal-title":"Parasitology"},{"key":"e_1_3_4_42_2","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/0169-4758(86)90148-1","article-title":"Immunological approaches to the control of animal trypanosomiasis","volume":"2","author":"Nantulya V. M.","year":"1986","unstructured":"V. M. Nantulya, Immunological approaches to the control of animal trypanosomiasis. Parasitol. Today 2, 168\u2013173 (1986).","journal-title":"Parasitol. Today"},{"key":"e_1_3_4_43_2","doi-asserted-by":"crossref","first-page":"6324","DOI":"10.1128\/IAI.01046-06","article-title":"Tsetse fly saliva accelerates the onset of Trypanosoma brucei infection in a mouse model associated with a reduced host inflammatory response","volume":"74","author":"Caljon G.","year":"2006","unstructured":"G. Caljon ., Tsetse fly saliva accelerates the onset of Trypanosoma brucei infection in a mouse model associated with a reduced host inflammatory response. Infect. Immun. 74, 6324\u20136330 (2006).","journal-title":"Infect. Immun."},{"key":"e_1_3_4_44_2","unstructured":"R Core Team R: A Language and Environment for Statistical Computing (R version 3.5.1 R Foundation for Statistical Computing Vienna Austria 2019)."},{"key":"e_1_3_4_45_2","doi-asserted-by":"crossref","first-page":"D457","DOI":"10.1093\/nar\/gkp851","article-title":"TriTrypDB: A functional genomic resource for the Trypanosomatidae","volume":"38","author":"Aslett M.","year":"2010","unstructured":"M. Aslett ., TriTrypDB: A functional genomic resource for the Trypanosomatidae. Nucleic Acids Res. 38, D457\u2013D462 (2010).","journal-title":"Nucleic Acids Res."},{"key":"e_1_3_4_46_2","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An open-source platform for biological-image analysis","volume":"9","author":"Schindelin J.","year":"2012","unstructured":"J. Schindelin ., Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676\u2013682 (2012).","journal-title":"Nat. Methods"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.pnas.org\/syndication\/doi\/10.1073\/pnas.1914423117","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1914423117","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,6,7]],"date-time":"2022-06-07T17:32:25Z","timestamp":1654623145000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1914423117"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,21]]},"references-count":46,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2020,2,4]]}},"alternative-id":["10.1073\/pnas.1914423117"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1914423117","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.737253572.793570408","asserted-by":"object"}]},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,21]]},"assertion":[{"value":"2020-01-21","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}