Trypanosoma brucei parasites occupy and functionally adapt to the adipose tissue in mice

Trindade, Sandra; Rijo-Ferreira, Filipa; Carvalho, Tania; Pinto-Neves, Daniel; Guegan, Fabien; Aresta-Branco, Francisco; Bento, Fabio; Young, Simon A.; Pinto, Andreia; Van Den Abbeele, Jan; Ribeiro, Ruy M.; Dias, Sergio; Smith, Terry K.; Figueiredo, Luisa M.

doi:10.1016/j.chom.2016.05.002

Trypanosoma brucei parasites occupy and functionally adapt to the adipose tissue in mice

Journal Article · Thu May 26 00:00:00 EDT 2016 · Cell Host & Microbe

DOI:https://doi.org/10.1016/j.chom.2016.05.002· OSTI ID:1341864

Trindade, Sandra ^[1]; Rijo-Ferreira, Filipa ^[2]; Carvalho, Tania ^[1]; Pinto-Neves, Daniel ^[1]; Guegan, Fabien ^[1]; Aresta-Branco, Francisco ^[1]; Bento, Fabio ^[1]; Young, Simon A. ^[3]; Pinto, Andreia ^[1]; Van Den Abbeele, Jan ^[4]; ^[5]; Dias, Sergio ^[1]; Smith, Terry K. ^[3]; Figueiredo, Luisa M. ^[1]

Univ. de Lisboa, Lisboa (Portugal)
Univ. de Lisboa, Lisboa (Portugal); Univ. of Texas Southwestern Medical Center, Dallas, TX (United States); Univ. do Porto, Porto (Portugal)
Univ. of St. Andrews, Fife (United Kingdom)
Institute of Tropical Medicine Antwerp, Antwerp (Belgium); Univ. of Ghent, Ghent (Belgium)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Univ. de Lisboa, Lisboa (Portugal)

Trypanosoma brucei is an extracellular parasite that causes sleeping sickness. In mammalian hosts, trypanosomes are thought to exist in two major niches: early in infection, they populate the blood; later, they breach the blood-brain barrier. Working with a well-established mouse model, we discovered that adipose tissue constitutes a third major reservoir for T. brucei. Parasites from adipose tissue, here termed adipose tissue forms (ATFs), can replicate and were capable of infecting a naive animal. ATFs were transcriptionally distinct from bloodstream forms, and the genes upregulated included putative fatty acid β-oxidation enzymes. Consistent with this, ATFs were able to utilize exogenous myristate and form β-oxidation intermediates, suggesting that ATF parasites can use fatty acids as an external carbon source. Lastly, these findings identify the adipose tissue as a niche for T. brucei during its mammalian life cycle and could potentially explain the weight loss associated with sleeping sickness.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: National Institutes of Health; USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1341864

Report Number(s):: LA-UR--16-23520

Journal Information:: Cell Host & Microbe, Journal Name: Cell Host & Microbe Journal Issue: 6 Vol. 19; ISSN 1931-3128

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Transcriptomes of Trypanosoma brucei rhodesiense from sleeping sickness patients, rodents and culture: Effects of strain, growth conditions and RNA preparation methods Mulindwa, Julius; Leiss, Kevin; Ibberson, David PLOS Neglected Tropical Diseases, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pntd.0006280	journal	February 2018
Trypanosoma brucei triggers a marked immune response in male reproductive organs Carvalho, Tânia; Trindade, Sandra; Pimenta, Sílvia PLOS Neglected Tropical Diseases, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pntd.0006690	journal	August 2018
The elimination of human African trypanosomiasis is in sight: Report from the third WHO stakeholders meeting on elimination of gambiense human African trypanosomiasis Barrett, Michael P. PLOS Neglected Tropical Diseases, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pntd.0006925	journal	December 2018
Parasite specific 7SL-derived small RNA is an effective target for diagnosis of active trypanosomiasis infection Chiweshe, Stephen M.; Steketee, Pieter C.; Jayaraman, Siddharth PLOS Neglected Tropical Diseases, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pntd.0007189	journal	February 2019
Application of long read sequencing to determine expressed antigen diversity in Trypanosoma brucei infections Jayaraman, Siddharth; Harris, Claire; Paxton, Edith PLOS Neglected Tropical Diseases, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pntd.0007262	journal	April 2019
Gambian human African trypanosomiasis in North West Uganda. Are we on course for the 2020 target? Selby, Richard; Wamboga, Charles; Erphas, Olema PLOS Neglected Tropical Diseases, Vol. 13, Issue 8 https://doi.org/10.1371/journal.pntd.0007550	journal	August 2019
Using detergent-enhanced LAMP for African trypanosome detection in human cerebrospinal fluid and implications for disease staging Grab, Dennis J.; Nikolskaia, Olga V.; Courtioux, Bertrand PLOS Neglected Tropical Diseases, Vol. 13, Issue 8 https://doi.org/10.1371/journal.pntd.0007631	journal	August 2019
Differential virulence of Trypanosoma brucei rhodesiense isolates does not influence the outcome of treatment with anti-trypanosomal drugs in the mouse model Ndung’u, Kariuki; Murilla, Grace Adira; Thuita, John Kibuthu PLOS ONE, Vol. 15, Issue 11 https://doi.org/10.1371/journal.pone.0229060	journal	November 2020
A quorum sensing-independent path to stumpy development in Trypanosoma brucei Zimmermann, Henriette; Subota, Ines; Batram, Christopher PLOS Pathogens, Vol. 13, Issue 4 https://doi.org/10.1371/journal.ppat.1006324	journal	April 2017
Non-linear hierarchy of the quorum sensing signalling pathway in bloodstream form African trypanosomes McDonald, Lindsay; Cayla, Mathieu; Ivens, Alasdair PLOS Pathogens, Vol. 14, Issue 6 https://doi.org/10.1371/journal.ppat.1007145	journal	June 2018
Mitochondrial DNA is critical for longevity and metabolism of transmission stage Trypanosoma brucei Dewar, Caroline E.; MacGregor, Paula; Cooper, Sinclair PLOS Pathogens, Vol. 14, Issue 7 https://doi.org/10.1371/journal.ppat.1007195	journal	July 2018
Gluconeogenesis using glycerol as a substrate in bloodstream-form Trypanosoma brucei Kovářová, Julie; Nagar, Rupa; Faria, Joana PLOS Pathogens, Vol. 14, Issue 12 https://doi.org/10.1371/journal.ppat.1007475	journal	December 2018
The assembly of lipid droplets and their roles in challenged cells Henne, W. Mike; Reese, Michael L.; Goodman, Joel M. The EMBO Journal, Vol. 37, Issue 12 https://doi.org/10.15252/embj.201898947	journal	May 2018
The assembly of lipid droplets and their roles in challenged cells Henne, W. Mike; Reese, Michael L.; Goodman, Joel M. The EMBO Journal, Vol. 38, Issue 9 https://doi.org/10.15252/embj.2019101816	journal	March 2019
DNA lesions and repair in trypanosomatids infection Repolês, Bruno M.; Machado, Carlos Renato; Florentino, Pilar T. V. Genetics and Molecular Biology, Vol. 43, Issue 1 suppl 1 https://doi.org/10.1590/1678-4685-gmb-2019-0163	journal	January 2020
Mitochondrial DNA is critical for longevity and metabolism of transmission stage Trypanosoma brucei. Dewar, Caroline E.; MacGregor, Paula; Cooper, Sinclair Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.32944	text	January 2018
Non-linear hierarchy of the quorum sensing signalling pathway in bloodstream form African trypanosomes. McDonald, Lindsay; Cayla, Mathieu; Ivens, Alasdair Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.37320	text	January 2018
Evaluation of the Anti-Trypanosomal Activity of Vietnamese Essential Oils, with Emphasis on Curcuma longa L. and Its Components Le, Thanh; Beaufay, Claire; Nghiem, Duc Molecules, Vol. 24, Issue 6 https://doi.org/10.3390/molecules24061158	journal	March 2019
The Cytological Events and Molecular Control of Life Cycle Development of Trypanosoma brucei in the Mammalian Bloodstream Silvester, Eleanor; McWilliam, Kirsty; Matthews, Keith Pathogens, Vol. 6, Issue 3 https://doi.org/10.3390/pathogens6030029	journal	June 2017
The skin is a significant but overlooked anatomical reservoir for vector-borne African trypanosomes Capewell, Paul; Cren-Travaillé, Christelle; Marchesi, Francesco eLife, Vol. 5 https://doi.org/10.7554/elife.17716	journal	September 2016
Developmental adaptations of trypanosome motility to the tsetse fly host environments unravel a multifaceted in vivo microswimmer system Schuster, Sarah; Krüger, Timothy; Subota, Ines eLife, Vol. 6 https://doi.org/10.7554/elife.27656	journal	August 2017
Cryo electron tomography with volta phase plate reveals novel structural foundations of the 96-nm axonemal repeat in the pathogen Trypanosoma brucei Imhof, Simon; Zhang, Jiayan; Wang, Hui eLife, Vol. 8 https://doi.org/10.7554/elife.52058	journal	November 2019
TbLpn, a key enzyme in lipid droplet formation and phospholipid metabolism, is essential for mitochondrial integrity and growth of Trypanosoma brucei. Dawoody Nejad, Ladan; Serricchio, Mauro; Jelk, Jennifer Wiley https://doi.org/10.7892/boris.125025	text	January 2018
Flagellar cAMP signaling controls trypanosome progression through host tissues. Shaw, Sebastian; DeMarco, Stephanie F.; Rehmann, Ruth Nature Publishing Group https://doi.org/10.7892/boris.130288	text	January 2019

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