{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,6]],"date-time":"2026-11-06T07:07:23Z","timestamp":1793948843984,"version":"4.8.0"},"reference-count":75,"publisher":"Springer Science and Business Media LLC","issue":"8042","license":[{"start":{"date-parts":[[2024,10,30]],"date-time":"2024-10-30T00:00:00Z","timestamp":1730246400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,10,30]],"date-time":"2024-10-30T00:00:00Z","timestamp":1730246400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nature"],"published-print":{"date-parts":[[2024,12,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    The protozoan parasite\n                    <jats:italic>Trypanosoma brucei<\/jats:italic>\n                    evades clearance by the host immune system through antigenic variation of its dense variant surface glycoprotein (VSG) coat, periodically \u2018switching\u2019 expression of the VSG using a large genomic repertoire of VSG-encoding genes\n                    <jats:sup>1\u20136<\/jats:sup>\n                    . Recent studies of antigenic variation in vivo have focused near exclusively on parasites in the bloodstream\n                    <jats:sup>6\u20138<\/jats:sup>\n                    , but research has shown that many, if not most, parasites reside in the interstitial spaces of tissues\n                    <jats:sup>9\u201313<\/jats:sup>\n                    . We sought to explore the dynamics of antigenic variation in extravascular parasite populations using VSG-seq\n                    <jats:sup>7<\/jats:sup>\n                    , a high-throughput sequencing approach for profiling VSGs expressed in populations of\n                    <jats:italic>T. brucei<\/jats:italic>\n                    . Here we show that tissues, not the blood, are the primary reservoir of antigenic diversity during both needle- and tsetse bite-initiated\n                    <jats:italic>T. brucei<\/jats:italic>\n                    infections, with more than 75% of VSGs found exclusively within extravascular spaces. We found that this increased diversity is correlated with slower parasite clearance in tissue spaces. Together, these data support a model in which the slower immune response in extravascular spaces provides more time to generate the antigenic diversity needed to maintain a chronic infection. Our findings reveal the important role that extravascular spaces can have in pathogen diversification.\n                  <\/jats:p>","DOI":"10.1038\/s41586-024-08151-z","type":"journal-article","created":{"date-parts":[[2024,10,30]],"date-time":"2024-10-30T13:01:59Z","timestamp":1730293319000},"page":"430-437","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Tissue spaces are reservoirs of antigenic diversity for Trypanosoma brucei"],"prefix":"10.1038","volume":"636","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-6314-5934","authenticated-orcid":false,"given":"Alexander K.","family":"Beaver","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhibek","family":"Keneskhanova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2124-8198","authenticated-orcid":false,"given":"Ra\u00fal O.","family":"Cosentino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian L.","family":"Weiss","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erick O.","family":"Awuoche","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gretchen M.","family":"Smallenberger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gracyn Y.","family":"Buenconsejo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nathan P.","family":"Crilly","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2392-0585","authenticated-orcid":false,"given":"Jaclyn E.","family":"Smith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jill M. C.","family":"Hakim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7606-4014","authenticated-orcid":false,"given":"Bailin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bryce","family":"Bobb","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4003-020X","authenticated-orcid":false,"given":"Filipa","family":"Rijo-Ferreira","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5752-6586","authenticated-orcid":false,"given":"Luisa M.","family":"Figueiredo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9941-143X","authenticated-orcid":false,"given":"Serap","family":"Aksoy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1715-7907","authenticated-orcid":false,"given":"T. Nicolai","family":"Siegel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1535-2530","authenticated-orcid":false,"given":"Monica R.","family":"Mugnier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,10,30]]},"reference":[{"key":"8151_CR1","doi-asserted-by":"crossref","first-page":"e1000122","DOI":"10.1371\/journal.ppat.1000122","volume":"4","author":"S Magez","year":"2008","unstructured":"Magez, S. et al. The role of B-cells and IgM antibodies in parasitemia, anemia, and VSG switching in Trypanosoma brucei-infected mice. PLoS Pathog. 4, e1000122 (2008).","journal-title":"PLoS Pathog."},{"key":"8151_CR2","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.molbiopara.2014.06.004","volume":"195","author":"GAM Cross","year":"2014","unstructured":"Cross, G. A. M., Kim, H. S. & Wickstead, B. Capturing the variant surface glycoprotein repertoire (the VSGnome) of Trypanosoma brucei Lister 427. Mol. Biochem. Parasitol. 195, 59\u201373 (2014).","journal-title":"Mol. Biochem. Parasitol."},{"key":"8151_CR3","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1038\/s41586-018-0619-8","volume":"563","author":"LSM M\u00fcller","year":"2018","unstructured":"M\u00fcller, L. S. M. et al. Genome organization and DNA accessibility control antigenic variation in trypanosomes. Nature 563, 121\u2013125 (2018).","journal-title":"Nature"},{"key":"8151_CR4","doi-asserted-by":"crossref","first-page":"e3527","DOI":"10.1371\/journal.pone.0003527","volume":"3","author":"C Hertz-Fowler","year":"2008","unstructured":"Hertz-Fowler, C. et al. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS ONE 3, e3527 (2008).","journal-title":"PLoS ONE"},{"key":"8151_CR5","doi-asserted-by":"crossref","first-page":"lqab082","DOI":"10.1093\/nargab\/lqab082","volume":"3","author":"RO Cosentino","year":"2021","unstructured":"Cosentino, R. O., Brink, B. G. & Nicolai Siegel, T. Allele-specific assembly of a eukaryotic genome corrects apparent frameshifts and reveals a lack of nonsense-mediated mRNA decay. NAR Genom. Bioinform. 3, lqab082 (2021).","journal-title":"NAR Genom. Bioinform."},{"key":"8151_CR6","doi-asserted-by":"crossref","first-page":"e1003502","DOI":"10.1371\/journal.ppat.1003502","volume":"9","author":"JPJ Hall","year":"2013","unstructured":"Hall, J. P. J., Wang, H. & David Barry, J. Mosaic VSGs and the scale of Trypanosoma brucei antigenic variation. PLoS Pathog. 9, e1003502 (2013).","journal-title":"PLoS Pathog."},{"key":"8151_CR7","doi-asserted-by":"crossref","first-page":"1470","DOI":"10.1126\/science.aaa4502","volume":"347","author":"MR Mugnier","year":"2015","unstructured":"Mugnier, M. R., Cross, G. A. M. & Papavasiliou, F. N. The in vivo dynamics of antigenic variation in Trypanosoma brucei. Science 347, 1470\u20131473 (2015).","journal-title":"Science"},{"key":"8151_CR8","doi-asserted-by":"crossref","first-page":"e0007262","DOI":"10.1371\/journal.pntd.0007262","volume":"13","author":"S Jayaraman","year":"2019","unstructured":"Jayaraman, S. et al. Application of long read sequencing to determine expressed antigen diversity in Trypanosoma brucei infections. PLoS Negl. Trop. Dis. 13, e0007262 (2019).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"8151_CR9","doi-asserted-by":"crossref","first-page":"e17716","DOI":"10.7554\/eLife.17716","volume":"5","author":"P Capewell","year":"2016","unstructured":"Capewell, P. et al. The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes. eLife 5, e17716 (2016).","journal-title":"eLife"},{"key":"8151_CR10","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1093\/cid\/ciaa897","volume":"73","author":"M Camara","year":"2021","unstructured":"Camara, M. et al. Extravascular dermal trypanosomes in suspected and confirmed cases of gambiense human African trypanosomiasis. Clin. Infect. Dis. 73, 12\u201320 (2021).","journal-title":"Clin. Infect. Dis."},{"key":"8151_CR11","doi-asserted-by":"publisher","unstructured":"Trindade, S. et al. Trypanosoma brucei parasites occupy and functionally adapt to the adipose tissue in mice. Cell Host Microbe https:\/\/doi.org\/10.1016\/j.chom.2016.05.002 (2016).","DOI":"10.1016\/j.chom.2016.05.002"},{"key":"8151_CR12","doi-asserted-by":"publisher","unstructured":"Carvalho, T. et al. Trypanosoma brucei triggers a marked immune response in male reproductive organs. PLoS Negl. Trop. Dis. https:\/\/doi.org\/10.1371\/journal.pntd.0006690 (2018).","DOI":"10.1371\/journal.pntd.0006690"},{"key":"8151_CR13","doi-asserted-by":"crossref","first-page":"109741","DOI":"10.1016\/j.celrep.2021.109741","volume":"36","author":"M De Niz","year":"2021","unstructured":"De Niz, M. et al. Organotypic endothelial adhesion molecules are key for Trypanosoma brucei tropism and virulence. Cell Rep 36, 109741 (2021).","journal-title":"Cell Rep"},{"key":"8151_CR14","unstructured":"Control and Surveillance of Human African Trypanosomiasis: Report of a WHO Expert Committee. WHO Technical Report Series (WHO, 2013)."},{"key":"8151_CR15","doi-asserted-by":"crossref","first-page":"e1009866","DOI":"10.1371\/journal.ppat.1009866","volume":"17","author":"NP Crilly","year":"2021","unstructured":"Crilly, N. P. & Mugnier, M. R. Thinking outside the blood: perspectives on tissue-resident Trypanosoma brucei. PLoS Pathog. 17, e1009866 (2021).","journal-title":"PLoS Pathog."},{"key":"8151_CR16","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/0166-6851(92)90004-4","volume":"53","author":"SM Kamper","year":"1992","unstructured":"Kamper, S. M. & Barbet, A. F. Surface epitope variation via mosaic gene formation is potential key to long-term survival of Trypanosoma brucei. Mol. Biochem. Parasitol. 53, 33\u201344 (1992).","journal-title":"Mol. Biochem. Parasitol."},{"key":"8151_CR17","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1017\/S0031182000045200","volume":"66","author":"JR Seed","year":"1973","unstructured":"Seed, J. R. & Effron, H. G. Simultaneous presence of different antigenic populations of Trypanosoma brucei gambiense in Microtus montanus. Parasitology 66, 269\u2013278 (1973).","journal-title":"Parasitology"},{"key":"8151_CR18","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1111\/j.1550-7408.1984.tb04288.x","volume":"31","author":"JR Seed","year":"1984","unstructured":"Seed, J. R., Edwards, R. & Sechelski, J. The ecology of antigenic variation. J. Protozool. 31, 48\u201353 (1984).","journal-title":"J. Protozool."},{"key":"8151_CR19","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1017\/S0031182000054354","volume":"88","author":"JD Barry","year":"1984","unstructured":"Barry, J. D. & Emery, D. L. Parasite development and host responses during the establishment of Trypanosoma brucei infection transmitted by tsetse fly. Parasitology 88, 67\u201384 (1984).","journal-title":"Parasitology"},{"key":"8151_CR20","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1017\/S0031182000000834","volume":"80","author":"M Tanner","year":"1980","unstructured":"Tanner, M., Jenni, L., Hecker, H. & Brun, R. Characterization of Trypanosoma brucei isolated from lymph nodes of rats. Parasitology 80, 383\u2013391 (1980).","journal-title":"Parasitology"},{"key":"8151_CR21","doi-asserted-by":"crossref","first-page":"S37","DOI":"10.1017\/S0031182000083402","volume":"99","author":"K Vickerman","year":"1989","unstructured":"Vickerman, K. Trypanosome sociology and antigenic variation. Parasitology 99, S37\u2013S47 (1989).","journal-title":"Parasitology"},{"key":"8151_CR22","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/0169-4758(91)90143-C","volume":"7","author":"JD Barry","year":"1991","unstructured":"Barry, J. D. & Turner, C. M. R. The dynamics of antigenic variation and growth of African trypanosomes. Parasitol. Today 7, 207\u2013211 (1991).","journal-title":"Parasitol. Today"},{"key":"8151_CR23","doi-asserted-by":"crossref","first-page":"2798","DOI":"10.1101\/gad.323404","volume":"18","author":"M Engstler","year":"2004","unstructured":"Engstler, M. & Boshart, M. Cold shock and regulation of surface protein trafficking convey sensitization to inducers of stage differentiation in Trypanosoma brucei. Genes Dev. 18, 2798\u20132811 (2004).","journal-title":"Genes Dev."},{"key":"8151_CR24","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1016\/0035-9203(86)90395-0","volume":"80","author":"CM Turner","year":"1986","unstructured":"Turner, C. M., Hunter, C. A., Barry, J. D. & Vickerman, K. Similarity in variable antigen type composition of Trypanosoma brucei Rhodesiense populations in different sites within the mouse host. Trans. R. Soc. Trop. Med. Hyg. 80, 824\u2013830 (1986).","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"8151_CR25","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1017\/S0031182000061035","volume":"99","author":"CMR Turner","year":"1989","unstructured":"Turner, C. M. R. & Barry, J. D. High frequency of antigenic variation in Trypanosoma brucei rhodesiense infections. Parasitology 99, 67\u201375 (1989).","journal-title":"Parasitology"},{"key":"8151_CR26","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1084\/jem.20041579","volume":"200","author":"A Salanti","year":"2004","unstructured":"Salanti, A. et al. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 200, 1197\u20131203 (2004).","journal-title":"J. Exp. Med."},{"key":"8151_CR27","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/S1369-5274(03)00090-0","volume":"6","author":"PE Duffy","year":"2003","unstructured":"Duffy, P. E. & Fried, M. Plasmodium falciparum adhesion in the placenta. Curr. Opin. Microbiol. 6, 371\u2013376 (2003).","journal-title":"Curr. Opin. Microbiol."},{"key":"8151_CR28","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1111\/j.1365-2958.1994.tb00435.x","volume":"13","author":"A\u2010B Jonsson","year":"1994","unstructured":"Jonsson, A. \u2010B., Ilver, D., Falk, P., Pepose, J. & Normark, S. Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol. Microbiol. 13, 403\u2013416 (1994).","journal-title":"Mol. Microbiol."},{"key":"8151_CR29","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1111\/j.1365-2958.1993.tb01615.x","volume":"8","author":"X Nassif","year":"1993","unstructured":"Nassif, X. et al. Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 8, 719\u2013725 (1993).","journal-title":"Mol. Microbiol."},{"key":"8151_CR30","doi-asserted-by":"crossref","first-page":"3439","DOI":"10.1111\/j.1365-2958.1992.tb02211.x","volume":"6","author":"T Rudel","year":"1992","unstructured":"Rudel, T., van Putten, J. P. M., Gibbs, C. P., Haas, R. & Meyer, T. F. Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol. Microbiol. 6, 3439\u20133450 (1992).","journal-title":"Mol. Microbiol."},{"key":"8151_CR31","first-page":"1089","volume":"130","author":"M Virji","year":"1984","unstructured":"Virji, M. & Heckels, J. E. The role of common and type-specific pilus antigenic domains in adhesion and virulence of gonococci for human epithelial cells. J. Gen. Microbiol. 130, 1089\u20131095 (1984).","journal-title":"J. Gen. Microbiol."},{"key":"8151_CR32","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1038\/nature07997","volume":"459","author":"S Dean","year":"2009","unstructured":"Dean, S., Marchetti, R., Kirk, K. & Matthews, K. R. A surface transporter family conveys the trypanosome differentiation signal. Nature 459, 213\u2013217 (2009).","journal-title":"Nature"},{"key":"8151_CR33","doi-asserted-by":"publisher","unstructured":"McWilliam, K. R. et al. High-resolution scRNA-seq reveals genomic determinants of antigen expression hierarchy in African Trypanosomes. Preprint at bioRxiv https:\/\/doi.org\/10.1101\/2024.03.22.586247 (2024).","DOI":"10.1101\/2024.03.22.586247"},{"key":"8151_CR34","doi-asserted-by":"publisher","unstructured":"Smith, J. E. et al. DNA damage drives antigen diversification through mosaic VSG formation in Trypanosoma brucei. Preprint at bioRxiv https:\/\/doi.org\/10.1101\/2024.03.22.582209 (2024).","DOI":"10.1101\/2024.03.22.582209"},{"key":"8151_CR35","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/j.meegid.2018.01.011","volume":"63","author":"E Calvo-Alvarez","year":"2018","unstructured":"Calvo-Alvarez, E., Cren-Travaill\u00e9, C., Crouzols, A. & Rotureau, B. A new chimeric triple reporter fusion protein as a tool for in vitro and in vivo multimodal imaging to monitor the development of African trypanosomes and Leishmania parasites. Infect. Genet. Evol. 63, 391\u2013403 (2018).","journal-title":"Infect. Genet. Evol."},{"key":"8151_CR36","doi-asserted-by":"crossref","first-page":"e1009904","DOI":"10.1371\/journal.ppat.1009904","volume":"17","author":"S Hutchinson","year":"2021","unstructured":"Hutchinson, S. et al. The establishment of variant surface glycoprotein monoallelic expression revealed by single-cell RNA-seq of Trypanosoma brucei in the tsetse fly salivary glands. PLoS Pathog. 17, e1009904 (2021).","journal-title":"PLoS Pathog."},{"key":"8151_CR37","doi-asserted-by":"crossref","first-page":"1708","DOI":"10.1371\/journal.pntd.0001708","volume":"6","author":"AF Savage","year":"2012","unstructured":"Savage, A. F. et al. Transcript expression analysis of putative Trypanosoma brucei GPI-anchored surface proteins during development in the tsetse and mammalian hosts. PLoS Negl. Trop. Dis. 6, 1708 (2012).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"8151_CR38","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1128\/IAI.66.2.451-461.1998","volume":"66","author":"LR Schopf","year":"1998","unstructured":"Schopf, L. R., Filutowicz, H., Bi, X. J. & Mansfield, J. M. Interleukin-4-dependent immunoglobulin G1 isotype switch in the presence of a polarized antigen-specific Th1-cell response to the trypanosome variant surface glycoprotein. Infect. Immun. 66, 451 (1998).","journal-title":"Infect. Immun."},{"key":"8151_CR39","doi-asserted-by":"crossref","first-page":"2785","DOI":"10.1128\/IAI.00357-15","volume":"83","author":"G Liu","year":"2015","unstructured":"Liu, G. et al. Distinct contributions of CD4+ and CD8+ T cells to pathogenesis of trypanosoma brucei infection in the context of gamma interferon and interleukin-10. Infect. Immun. 83, 2785\u20132795 (2015).","journal-title":"Infect. Immun."},{"key":"8151_CR40","doi-asserted-by":"crossref","first-page":"2337","DOI":"10.1128\/iai.58.7.2337-2342.1990","volume":"58","author":"DM Reinitz","year":"1990","unstructured":"Reinitz, D. M. & Mansfield, J. M. T-cell-independent and T-cell-dependent B-cell responses to exposed variant surface glycoprotein epitopes in trypanosome-infected mice. Infect. Immun. 58, 2337\u20132342 (1990).","journal-title":"Infect. Immun."},{"key":"8151_CR41","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1128\/IAI.68.2.848-860.2000","volume":"68","author":"M Radwanska","year":"2000","unstructured":"Radwanska, M. et al. Comparative analysis of antibody responses against HSP60, invariant surface glycoprotein 70, and variant surface glycoprotein reveals a complex antigen-specific pattern of immunoglobulin isotype switching during infection by Trypanosoma brucei. Infect. Immun. 68, 848\u2013860 (2000).","journal-title":"Infect. Immun."},{"key":"8151_CR42","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.1016\/j.cell.2008.09.062","volume":"135","author":"DF Robbiani","year":"2008","unstructured":"Robbiani, D. F. et al. AID is required for the chromosomal breaks in c-myc that lead to c-myc\/IgH translocations. Cell 135, 1028\u20131038 (2008).","journal-title":"Cell"},{"key":"8151_CR43","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1093\/infdis\/160.3.483","volume":"160","author":"RF Hector","year":"1989","unstructured":"Hector, R. F., Collins, M. S. & Pennington, J. E. Treatment of experimental Pseudomonas aeruginosa pneumonia with a human IgM monoclonal antibody. J. Infect. Dis. 160, 483\u2013489 (1989).","journal-title":"J. Infect. Dis."},{"key":"8151_CR44","doi-asserted-by":"crossref","first-page":"1036","DOI":"10.1172\/JCI104987","volume":"43","author":"WF Barth","year":"1964","unstructured":"Barth, W. F., Wochner, R. D., Waldmann, T. A. & Fahey, J. L. Metabolism of human gamma macroglobulins. J. Clin. Invest. 43, 1036 (1964).","journal-title":"J. Clin. Invest."},{"key":"8151_CR45","doi-asserted-by":"crossref","first-page":"e00113","DOI":"10.1016\/j.parepi.2019.e00113","volume":"6","author":"D Mehlitz","year":"2019","unstructured":"Mehlitz, D. & Molyneux, D. H. The elimination of Trypanosoma brucei gambiense? Challenges of reservoir hosts and transmission cycles: expect the unexpected. Parasite Epidemiol. Control 6, e00113 (2019).","journal-title":"Parasite Epidemiol. Control"},{"key":"8151_CR46","doi-asserted-by":"crossref","first-page":"e2306848120","DOI":"10.1073\/pnas.2306848120","volume":"120","author":"SD Larcombe","year":"2023","unstructured":"Larcombe, S. D., Briggs, E. M., Savill, N., Szoor, B. & Matthews, K. The developmental hierarchy and scarcity of replicative slender trypanosomes in blood challenges their role in infection maintenance. Proc. Natl Acad. Sci. USA 120, e2306848120 (2023).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"8151_CR47","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1016\/j.ijpara.2005.05.004","volume":"35","author":"LJ Morrison","year":"2005","unstructured":"Morrison, L. J., Majiwa, P., Read, A. F. & Barry, J. D. Probabilistic order in antigenic variation of Trypanosoma brucei. Int. J. Parasitol. 35, 961\u2013972 (2005).","journal-title":"Int. J. Parasitol."},{"key":"8151_CR48","doi-asserted-by":"crossref","unstructured":"Pinger, J., Chowdhury, S. & Papavasiliou, F. N. Variant surface glycoprotein density defines an immune evasion threshold for African trypanosomes undergoing antigenic variation. Nat. Commun. 8, 828 (2017).","DOI":"10.1038\/s41467-017-00959-w"},{"key":"8151_CR49","doi-asserted-by":"crossref","first-page":"7548","DOI":"10.1038\/s41467-022-34622-w","volume":"13","author":"S Trindade","year":"2022","unstructured":"Trindade, S. et al. Slow growing behavior in African trypanosomes during adipose tissue colonization. Nat. Commun. 13, 7548 (2022).","journal-title":"Nat. Commun."},{"key":"8151_CR50","doi-asserted-by":"crossref","unstructured":"Shimogawa, M. M. et al. Parasite motility is critical for virulence of African trypanosomes. Sci. Rep. 8, 9122 (2018).","DOI":"10.1038\/s41598-018-27228-0"},{"key":"8151_CR51","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1038\/nprot.2013.084","volume":"8","author":"BJ Haas","year":"2013","unstructured":"Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494\u20131512 (2013).","journal-title":"Nat. Protoc."},{"key":"8151_CR52","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1038\/nbt.1883","volume":"29","author":"MG Grabherr","year":"2011","unstructured":"Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat. Biotechnol. 29, 644\u2013652 (2011).","journal-title":"Nat. Biotechnol."},{"key":"8151_CR53","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2009-10-3-r25","volume":"10","author":"B Langmead","year":"2009","unstructured":"Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).","journal-title":"Genome Biol."},{"key":"8151_CR54","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.1093\/bioinformatics\/btp163","volume":"25","author":"PJA Cock","year":"2009","unstructured":"Cock, P. J. A. et al. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25, 1422\u20131423 (2009).","journal-title":"Bioinformatics"},{"key":"8151_CR55","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1186\/1471-2105-10-421","volume":"10","author":"C Camacho","year":"2009","unstructured":"Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinf. 10, 421 (2009).","journal-title":"BMC Bioinf."},{"key":"8151_CR56","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","volume":"215","author":"SF Altschul","year":"1990","unstructured":"Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403\u2013410 (1990).","journal-title":"J. Mol. Biol."},{"key":"8151_CR57","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","volume":"26","author":"AR Quinlan","year":"2010","unstructured":"Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841\u2013842 (2010).","journal-title":"Bioinformatics"},{"key":"8151_CR58","doi-asserted-by":"crossref","first-page":"3150","DOI":"10.1093\/bioinformatics\/bts565","volume":"28","author":"L Fu","year":"2012","unstructured":"Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150\u20133152 (2012).","journal-title":"Bioinformatics"},{"key":"8151_CR59","doi-asserted-by":"crossref","first-page":"1658","DOI":"10.1093\/bioinformatics\/btl158","volume":"22","author":"W Li","year":"2006","unstructured":"Li, W. & Godzik, A. CD-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658\u20131659 (2006).","journal-title":"Bioinformatics"},{"key":"8151_CR60","doi-asserted-by":"publisher","unstructured":"Krueger, F. et al. FelixKrueger\/TrimGalore: v.0.6.4 - add default decompression path. Zenodo https:\/\/doi.org\/10.5281\/zenodo.5127898 (2023).","DOI":"10.5281\/zenodo.5127898"},{"key":"8151_CR61","doi-asserted-by":"crossref","first-page":"giab008","DOI":"10.1093\/gigascience\/giab008","volume":"10","author":"P Danecek","year":"2021","unstructured":"Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).","journal-title":"Gigascience"},{"key":"8151_CR62","doi-asserted-by":"crossref","first-page":"e1002195","DOI":"10.1371\/journal.pcbi.1002195","volume":"7","author":"SR Eddy","year":"2011","unstructured":"Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).","journal-title":"PLoS Comput. Biol."},{"key":"8151_CR63","doi-asserted-by":"crossref","unstructured":"So, J. et al. VSGs expressed during natural T. b. gambiense infection exhibit extensive sequence divergence and a subspecies-specific bias towards type B N-terminal domains. mBio 13, e02553-22 (2022).","DOI":"10.1128\/mbio.02553-22"},{"key":"8151_CR64","doi-asserted-by":"crossref","first-page":"24665","DOI":"10.1074\/jbc.M301497200","volume":"278","author":"AE Gruszynski","year":"2003","unstructured":"Gruszynski, A. E., DeMaster, A., Hooper, N. M. & Bangs, J. D. Surface coat remodeling during differentiation of Trypanosoma brucei. J. Biol. Chem. 278, 24665\u201324672 (2003).","journal-title":"J. Biol. Chem."},{"key":"8151_CR65","doi-asserted-by":"publisher","unstructured":"Lee, J.-Y. & Kitaoka, M. A beginner\u2019s guide to rigor and reproducibility in fluorescence imaging experiments. Mol. Biol. Cell https:\/\/doi.org\/10.1091\/mbc.E17-05-0276 (2018).","DOI":"10.1091\/mbc.E17-05-0276"},{"key":"8151_CR66","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/S0166-6851(99)00002-X","volume":"99","author":"E Wirtz","year":"1999","unstructured":"Wirtz, E., Leal, S., Ochatt, C. & Cross, G. A. M. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99, 89\u2013101 (1999).","journal-title":"Mol. Biochem. Parasitol."},{"key":"8151_CR67","doi-asserted-by":"crossref","first-page":"10","DOI":"10.14806\/ej.17.1.200","volume":"17","author":"M Martin","year":"2011","unstructured":"Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10\u201312 (2011).","journal-title":"EMBnet J."},{"key":"8151_CR68","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","volume":"29","author":"A Dobin","year":"2013","unstructured":"Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15\u201321 (2013).","journal-title":"Bioinformatics"},{"key":"8151_CR69","doi-asserted-by":"crossref","first-page":"e0011058","DOI":"10.1371\/journal.pntd.0011058","volume":"17","author":"A Shanmugasundram","year":"2023","unstructured":"Shanmugasundram, A. et al. TriTrypDB: an integrated functional genomics resource for kinetoplastida. PLoS Negl. Trop. Dis. 17, e0011058 (2023).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"8151_CR70","doi-asserted-by":"crossref","first-page":"W160","DOI":"10.1093\/nar\/gkw257","volume":"44","author":"F Ram\u00edrez","year":"2016","unstructured":"Ram\u00edrez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160\u2013W165 (2016).","journal-title":"Nucleic Acids Res."},{"key":"8151_CR71","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1186\/s12859-023-05438-2","volume":"24","author":"Y Song","year":"2023","unstructured":"Song, Y. & Wang, J. ggcoverage: an R package to visualize and annotate genome coverage for various NGS data. BMC Bioinf. 24, 309 (2023).","journal-title":"BMC Bioinf."},{"key":"8151_CR72","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1017\/S0031182000080021","volume":"63","author":"SK Moloo","year":"1971","unstructured":"Moloo, S. K. An artificial feeding technique for Glossina. Parasitology 63, 507\u2013512 (1971).","journal-title":"Parasitology"},{"key":"8151_CR73","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1017\/S0031182007002247","volume":"134","author":"ET MacLeod","year":"2007","unstructured":"MacLeod, E. T., Maudlin, I., Darby, A. C. & Welburn, S. C. Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology 134, 827\u2013831 (2007).","journal-title":"Parasitology"},{"key":"8151_CR74","doi-asserted-by":"publisher","unstructured":"Beaver, A. mugnierlab\/Beaver2022: Release for publication. Zenodo https:\/\/doi.org\/10.5281\/zenodo.13684001 (2024).","DOI":"10.5281\/zenodo.13684001"},{"key":"8151_CR75","first-page":"35","volume":"44","author":"SA Barnett","year":"1959","unstructured":"Barnett, S. A. The skin and hair of mice living at a low environmental temperature. Q. J. Exp. Physiol. Cogn. Med. Sci. 44, 35\u201342 (1959).","journal-title":"Q. J. Exp. Physiol. Cogn. Med. Sci."}],"updated-by":[{"DOI":"10.1038\/s41586-024-08389-7","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2024,11,16]],"date-time":"2024-11-16T00:00:00Z","timestamp":1731715200000}}],"container-title":["Nature"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-08151-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-08151-z","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-08151-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,11]],"date-time":"2024-12-11T18:55:40Z","timestamp":1733943340000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-08151-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,30]]},"references-count":75,"journal-issue":{"issue":"8042","published-print":{"date-parts":[[2024,12,12]]}},"alternative-id":["8151"],"URL":"https:\/\/doi.org\/10.1038\/s41586-024-08151-z","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.06.27.497797","asserted-by":"object"}]},"ISSN":["0028-0836","1476-4687"],"issn-type":[{"value":"0028-0836","type":"print"},{"value":"1476-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,30]]},"assertion":[{"value":"10 January 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 October 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 October 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 November 2024","order":4,"name":"change_date","label":"Change Date","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Correction","order":5,"name":"change_type","label":"Change Type","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"A Correction to this paper has been published:","order":6,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"https:\/\/doi.org\/10.1038\/s41586-024-08389-7","URL":"https:\/\/doi.org\/10.1038\/s41586-024-08389-7","order":7,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}