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

Title: 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.

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

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1341864

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

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

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 199 works

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Parasite motility is critical for virulence of African trypanosomes Shimogawa, Michelle M.; Ray, Sunayan S.; Kisalu, Neville Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-27228-0	journal	June 2018
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Masters of Disguise: Antigenic Variation and the VSG Coat in Trypanosoma brucei Mugnier, Monica R.; Stebbins, C. Erec; Papavasiliou, F. Nina PLOS Pathogens, Vol. 12, Issue 9 https://doi.org/10.1371/journal.ppat.1005784	journal	September 2016
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
Biological factors that impinge on Chagas disease drug development Francisco, Amanda F.; Jayawardhana, Shiromani; Lewis, Michael D. Parasitology, Vol. 144, Issue 14 https://doi.org/10.1017/s0031182017001469	journal	August 2017
The single mitochondrion of the kinetoplastid parasite Crithidia fasciculata is a dynamic network DiMaio, John; Ruthel, Gordon; Cannon, Joshua J. PLOS ONE https://doi.org/10.1101/388660	journal	September 2018
Sustainable Elimination (Zero Cases) of Sleeping Sickness: How Far Are We from Achieving This Goal? Akazue, Pearl Ihuoma; Ebiloma, Godwin U.; Ajibola, Olumide Pathogens, Vol. 8, Issue 3 https://doi.org/10.3390/pathogens8030135	journal	August 2019
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
Evolution of Antigenic Variation in African Trypanosomes: Variant Surface Glycoprotein Expression, Structure, and Function Bangs, James D. BioEssays, Vol. 40, Issue 12 https://doi.org/10.1002/bies.201800181	journal	October 2018
Skin deep Casas-Sánchez, Aitor; Acosta-Serrano, Álvaro eLife, Vol. 5 https://doi.org/10.7554/elife.21506	journal	October 2016
Lipids Are the Preferred Substrate of the Protist Naegleria gruberi, Relative of a Human Brain Pathogen Bexkens, Michiel L.; Zimorski, Verena; Sarink, Maarten J. Cell Reports, Vol. 25, Issue 3 https://doi.org/10.1016/j.celrep.2018.09.055	journal	October 2018
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
Identification of Positive Chemotaxis in the Protozoan Pathogen Trypanosoma brucei DeMarco, Stephanie F.; Saada, Edwin A.; Lopez, Miguel A. mSphere, Vol. 5, Issue 4 https://doi.org/10.1128/msphere.00685-20	journal	August 2020
Glycerol supports growth of the Trypanosoma brucei bloodstream forms in the absence of glucose: Analysis of metabolic adaptations on glycerol-rich conditions Pineda, Erika; Thonnus, Magali; Mazet, Muriel PLOS Pathogens, Vol. 14, Issue 11 https://doi.org/10.1371/journal.ppat.1007412	journal	November 2018
A post-transcriptional respiratome regulon in trypanosomes Trenaman, Anna; Glover, Lucy; Hutchinson, Sebastian Nucleic Acids Research, Vol. 47, Issue 13 https://doi.org/10.1093/nar/gkz455	journal	May 2019
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
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
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
Tryp-ing Up Metabolism: Role of Metabolic Adaptations in Kinetoplastid Disease Pathogenesis Parab, Adwaita R.; McCall, Laura-Isobel Infection and Immunity, Vol. 89, Issue 4 https://doi.org/10.1128/iai.00644-20	journal	March 2021
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
TbLpn, a key enzyme in lipid droplet formation and phospholipid metabolism, is essential for mitochondrial integrity and growth of Trypanosoma brucei: Role of lipin in T. brucei growth Dawoody Nejad, Ladan; Serricchio, Mauro; Jelk, Jennifer Molecular Microbiology, Vol. 109, Issue 1 https://doi.org/10.1111/mmi.13976	journal	May 2018

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