Functional genomics of trypanotolerant and trypanosusceptible cattle infected with Trypanosoma congolense across multiple time points and tissues
Open accessAbstract
Human African trypanosomiasis (HAT), or sleeping sickness, is a neglected tropical disease caused by infection with trypanosome parasites ( Trypanosoma spp.). These are transmitted by infected tsetse flies ( Glossina spp.) and cause a similar disease in animals, known as African animal trypanosomiasis (AAT). AAT is one of the largest constraints to livestock production in sub-Saharan Africa and causes a financial burden of approximately $4.5 billion annually. Some African Bos taurus cattle populations have an important evolutionary adaptation known as trypanotolerance, a genetically determined tolerance of infection by trypanosome parasites ( Trypanosoma spp.). Trypanotolerant African B. taurus N’Dama and trypanosusceptible Bos indicus Boran cattle responded in largely similar ways during trypanosome infection when gene expression was examined using blood, liver, lymph node, and spleen samples with peaks and troughs of gene expression differences following the cyclic pattern of parasitaemia exhibited during trypanosome infection. However, differences in response to infection between the two breeds were reflected in differential expression of genes related to the immune system such as those encoding antimicrobial peptides and cytokines, including, for example, the antimicrobial peptide encoding genes LEAP2 , CATHL3 , DEFB4A , and S100A7 and the cytokine genes CCL20 , CXCL11 , CXCL13 , CXCL16 , CXCL17 , IL33 , and TNFSF13B . In addition, transcriptional profiling of peripheral blood identified expression differences in genes relating to coagulation and iron homeostasis, which supports the hypothesis that the dual control of parasitaemia and the anaemia resulting from the innate immune response to trypanosome parasites is key to trypanotolerance and provide new insights into the molecular mechanisms underlying this phenomenon. Author Summary: Trypanosome parasites are transmitted by infected tsetse flies and cause the neglected tropical disease human African trypanosomiasis (HAT) and the similar African animal trypanosomiasis (AAT), which is one of the largest impediments to livestock production in sub-Saharan Africa. Taurine ( Bos taurus ) and indicine ( Bos indicus ) cattle shared a common ancestor more than 150,000 years ago, and in the intervening period significant genomic differences have evolved between the two groups. Importantly, several African B. taurus populations have evolved an adaptation known as trypanotolerance, a genetically determined tolerance of infection by trypanosome parasites. Trypanotolerant African taurine and trypanosusceptible indicine cattle responded in largely similar ways during trypanosome infection when gene expression was examined using blood, liver, lymph node, and spleen samples with peaks and troughs of gene expression differences following the cyclic pattern of the number of trypanosome parasites in the blood. Transcriptional profiling of these tissues highlighted genes related to the multiple facets of the immune system; notably, for peripheral blood, differences observed for genes relating to coagulation and iron homeostasis support the existing hypothesis that control of both parasite number and anaemia is an important feature of the trypanotolerance trait and provide new insights into the molecular mechanisms underlying this phenomenon.
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The dual capacity to control both parasitaemia and the anemia resulting from the innate immune response is key to trypanotolerance.
“These findings support the hypothesis that the dual capacity to control both parasitaemia and the anemia resulting from the innate immune response is key to trypanotolerance [123].”
From The Genomic Landscape of Cattle: Domestication, Dispersal, and Adaptive Evolution (2026) · cites this paper as [123]
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R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888 · see citing works
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458 · see citing works
ggplot2: Elegant Graphics for Data Analysis
Wickham, H. (2009) · doi:10.1007/978-0-387-98141-3 · Cited by 14,447 · see citing works
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829 · see citing works
affy—analysis of Affymetrix GeneChip data at the probe level
Gautier, L., Cope, L., Bolstad, B. M., & Irizarry, R. A. (2004) · Bioinformatics · doi:10.1093/bioinformatics/btg405 · Cited by 5,221 · see citing works
Orchestrating high-throughput genomic analysis with Bioconductor
Huber, W. K., Carey, V. J., Gentleman, R. C., Anders, S., Carlson, M. R. J., Carvalho, B. S., Bravo, H. C., Davis, S. R., Gatto, L., Girke, T., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3252 · Cited by 3,499 · see citing works
dplyr: A Grammar of Data Manipulation
Wickham, H., François, R., Henry, L., Müller, K., & Vaughan, D. (2014) · doi:10.32614/cran.package.dplyr · Cited by 3,457 · see citing works
Reshaping Data with the reshape Package
Wickham, H. (2007) · Journal of Statistical Software · doi:10.18637/jss.v021.i12 · Cited by 3,167 · see citing works
Enrichment Map: A Network-Based Method for Gene-Set Enrichment Visualization and Interpretation
Merico, D., Isserlin, R., Stueker, O., Emili, A., & Bader, G. D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013984 · Cited by 2,235 · see citing works
Livestock production: recent trends, future prospects
Thornton, P. K. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0134 · Cited by 2,217 · see citing works
Association of Trypanolytic ApoL1 Variants with Kidney Disease in African Americans
Genovese, G., Friedman, D. J., Ross, M. D., Lecordier, L., Uzureau, P., Freedman, B. I., Bowden, D. W., Langefeld, C. D., Oleksyk, T. K., Uscinski Knob, A. L., et al. (2010) · Science · doi:10.1126/science.1193032 · Cited by 2,028 · see citing works
Reimand, J., Isserlin, R., Voisin, V., Kucera, M., Tannus-Lopes, C., Rostamianfar, A., Wadi, L., Meyer, M., Wong, J., Xu, C., et al. (2019) · Nature Protocols · doi:10.1038/s41596-018-0103-9 · Cited by 1,970 · see citing works
Kolberg, L., Raudvere, U., Kuzmin, I., Adler, P., Vilo, J., & Peterson, H. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad347 · Cited by 1,673 · see citing works
The Genetic Structure and History of Africans and African Americans
Tishkoff, S. A., Reed, F. A., Friedlaender, F. R., Ehret, C., Ranciaro, A., Froment, A., Hirbo, J. B., Awomoyi, A. A., Bodo, J.-M., Doumbo, O., et al. (2009) · Science · doi:10.1126/science.1172257 · Cited by 1,573 · cited 1× · see citing works
“The spread of agriculture and livestock herding has also shaped African human genetics and linguistic variation, illustrating the importance of domesticated species in influencing recent human evolution [25,26].”
Use of within-array replicate spots for assessing differential expression in microarray experiments
Smyth, G. K., Michaud, J., & Scott, H. S. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti270 · Cited by 1,406 · see citing works
Structure and function of the immune system in the spleen
Lewis, S. M., Williams, A., & Eisenbarth, S. C. (2019) · Science Immunology · doi:10.1126/sciimmunol.aau6085 · Cited by 1,301 · see citing works
The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis
Donovan, A., Lima, C. A., Pinkus, J. L., Pinkus, G. S., Zon, L. I., Robine, S., & Andrews, N. C. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.01.003 · Cited by 1,275 · see citing works
arrayQualityMetrics—a bioconductor package for quality assessment of microarray data
Kauffmann, A., Gentleman, R., & Huber, W. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btn647 · Cited by 946 · cited 1× · see citing works
“Quality control with log transformation was performed using affy (v. 1.80.0) [57], Biobase (v. 2.62.0) [58], and arrayQuality-Metrics (v. 3.58.0) [59] with R (v. 4.3.2) [60].”
InfluentialBrun, R., Blum, J., Chappuis, F., & Burri, C. (2010) · The Lancet · doi:10.1016/s0140-6736(09)60829-1 · Cited by 926 · see citing works
patchwork: The Composer of Plots
Pedersen, T. L. (2019) · doi:10.32614/cran.package.patchwork · Cited by 904 · see citing works
Interpreting principal component analyses of spatial population genetic variation
Novembre, J., & Stephens, M. (2008) · Nature Genetics · doi:10.1038/ng.139 · Cited by 663 · see citing works
MYH9 is associated with nondiabetic end-stage renal disease in African Americans
Kao, W. H. L., Klag, M. J., Meoni, L. A., Reich, D., Berthier‐Schaad, Y., Li, M., Coresh, J., Patterson, N. J., Tandon, A., Powe, N. R., et al. (2008) · Nature Genetics · doi:10.1038/ng.232 · Cited by 649 · see citing works
stringr: Simple, Consistent Wrappers for Common String Operations
Wickham, H. (2009) · doi:10.32614/cran.package.stringr · Cited by 620 · see citing works
clusterMaker: a multi-algorithm clustering plugin for Cytoscape
Morris, J. H., Apeltsin, L., Newman, A. M., Baumbach, J., Wittkop, T., Su, G., Bader, G. D., & Ferrin, T. E. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-436 · Cited by 609 · see citing works
African Pastoralism: Genetic Imprints of Origins and Migrations
Hanotte, O., Bradley, D. G., Ochieng, J. W., Verjee, Y., Hill, E. W., & Rege, J. E. O. (2002) · Science · doi:10.1126/science.1069878 · Cited by 567 · see citing works
Self-citationA Genealogical Interpretation of Principal Components Analysis
McVean, G. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000686 · Cited by 566 · see citing works
MacHugh, D. E., Shriver, M. D., Loftus, R. T., Cunningham, P., & Bradley, D. G. (1997) · Genetics · doi:10.1093/genetics/146.3.1071 · Cited by 547 · see citing works
Self-citationThe history of African trypanosomiasis
Steverding, D. (2008) · Parasites & Vectors · doi:10.1186/1756-3305-1-3 · Cited by 470 · see citing works
Selsted, M. E., Tang, Y., Morris, W. L., McGuire, P. A., Novotny, M., Smith, W. W., Henschen, A., & Cullor, J. S. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53298-1 · Cited by 443 · see citing works
Livestock and global change: Emerging issues for sustainable food systems
Herrero, M., & Thornton, P. K. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1321844111 · Cited by 413 · see citing works
scales: Scale Functions for Visualization
Wickham, H., Pedersen, T. L., & Seidel, D. P. (2011) · doi:10.32614/cran.package.scales · Cited by 373 · see citing works
AutoAnnotate: A Cytoscape app for summarizing networks with semantic annotations
Kucera, M., Isserlin, R., Arkhangorodsky, A., & Bader, G. D. (2016) · F1000Research · doi:10.12688/f1000research.9090.1 · Cited by 351 · see citing works
ggrepel: Automatically Position Non-Overlapping Text Labels with 'ggplot2'
Slowikowski, K. (2016) · doi:10.32614/cran.package.ggrepel · Cited by 349 · see citing works
purrr: Functional Programming Tools
Wickham, H., & Henry, L. (2015) · doi:10.32614/cran.package.purrr · Cited by 341 · see citing works
magrittr: A Forward-Pipe Operator for R
Bache, S. M., & Wickham, H. (2014) · doi:10.32614/cran.package.magrittr · Cited by 318 · see citing works
- Invited Review - African Indigenous Cattle: Unique Genetic Resources in a Rapidly Changing World
Mwai, O., Hanotte, O., Kwon, Y.-J., & Cho, S. (2015) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.15.0002r · Cited by 300 · see citing works
Holden, C. J. (2002) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.1955 · Cited by 295 · see citing works
The Genome Landscape of Indigenous African Cattle
Kim, J., Hanotte, O., Mwai, O. A., Dessie, T., Bashir, S., Diallo, B., Agaba, M., Kim, K., Kwak, W., Sung, S., et al. (2017) · Genome biology · doi:10.1186/s13059-017-1153-y · Cited by 271 · see citing works
readr: Read Rectangular Text Data
Wickham, H., Hester, J., & Bryan, J. (2015) · doi:10.32614/cran.package.readr · Cited by 262 · see citing works
A new summarization method for affymetrix probe level data
Hochreiter, S., Clevert, D.-A., & Obermayer, K. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl033 · Cited by 249 · see citing works
Protein tyrosine phosphatase receptor type C (PTPRC or CD45)
Barashdi, M. A. A., Ali, A., McMullin, M. F., & Mills, K. (2021) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2020-206927 · Cited by 244 · see citing works
The Mitogen-Activated Protein Kinase (MAPK) Pathway: Role in Immune Evasion by Trypanosomatids
Soares-Silva, M., Diniz, F. F., Gomes, G. N., & Bahia, D. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00183 · Cited by 233 · see citing works
Isolation and biochemical characterization of LEAP‐2, a novel blood peptide expressed in the liver
Krause, A., Sillard, R., Kleemeier, B., Klüver, E., Maronde, E., Conejo-Garcia, J. R., Forssmann, W. G., Schulz‐Knappe, P., Nehls, M. C., Wattler, F., et al. (2003) · Protein Science · doi:10.1110/ps.0213603 · Cited by 232 · see citing works
[1] The Affymetrix GeneChip® Platform: An Overview
Dalma‐Weiszhausz, D. D., Warrington, J. A., Tanimoto, E. Y., & Miyada, C. G. (2006) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(06)10001-4 · Cited by 215 · see citing works
Atypical Human Infections by Animal Trypanosomes
Truc, P., Büscher, P., Cuny, G., Gonzatti, M. I., Jannin, J. G., Joshi, P., Juyal, P. D., Lun, Z., Mattioli, R. C., Pays, É., et al. (2013) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002256 · Cited by 201 · see citing works
Toll-like receptor and antimicrobial peptide expression in the bovine endometrium
Davies, D., Meade, K. G., Herath, S., Eckersall, P. D., González, D., WHITE, J. O., Conlan, R. S., O’Farrelly, C., & Sheldon, I. M. (2008) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-6-53 · Cited by 201 · see citing works
Self-citationThe trypanolytic factor of human serum
Pays, É., Vanhollebeke, B., Vanhamme, L., Paturiaux-Hanocq, F., Nolan, D. P., & Pérez-Morga, D. L. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1428 · Cited by 196 · see citing works
A whole genome Bayesian scan for adaptive genetic divergence in West African cattle
Gautier, M., Flori, L., Riebler, A., Jaffrézic, F., Laloë, D., Gut, I. G., Moazami‐Goudarzi, K., & Foulley, J. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-550 · Cited by 196 · see citing works
Bovine trypanotolerance: A natural ability to prevent severe anaemia and haemophagocytic syndrome?
Naessens, J. (2006) · International Journal for Parasitology · doi:10.1016/j.ijpara.2006.02.012 · Cited by 180 · see citing works
WordCloud: a Cytoscape plugin to create a visual semantic summary of networks
Oesper, L., Merico, D., Isserlin, R., & Bader, G. D. (2011) · Source Code for Biology and Medicine · doi:10.1186/1751-0473-6-7 · Cited by 175 · see citing works
NANTULYA, V. M., Musoke, A. J., Rurangirwa, F. R., & Moloo, S. K. (1984) · Infection and Immunity · doi:10.1128/iai.43.2.735-738.1984 · Cited by 148 · see citing works
Geigy, R., & Kauffmann, M. (1973) · PubMed · Cited by 137 · see citing works
A graph layout algorithm for drawing metabolic pathways
Becker, M. Y., & Rojas, I. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.5.461 · Cited by 134 · see citing works
Immune responses of cattle to African trypanosomes: protective or pathogenic?
Taylor, K. (1998) · International Journal for Parasitology · doi:10.1016/s0020-7519(97)00154-9 · Cited by 121 · see citing works
Olfactomedin 4 expression and functions in innate immunity, inflammation, and cancer
Liu, W., & Rodgers, G. P. (2016) · Cancer and Metastasis Reviews · doi:10.1007/s10555-016-9624-2 · Cited by 115 · see citing works
Killing of African Trypanosomes by Antimicrobial Peptides
McGwire, B. S., Olson, C. L., Tack, B. F., & Engman, D. M. (2003) · The Journal of Infectious Diseases · doi:10.1086/375747 · Cited by 114 · see citing works
Combatting African Animal Trypanosomiasis (AAT) in livestock: The potential role of trypanotolerance
Yaro, M., Munyard, K. A., Stear, M. J., & Groth, D. M. (2016) · Veterinary Parasitology · doi:10.1016/j.vetpar.2016.05.003 · Cited by 114 · see citing works
D'Ieteren, G. D. M., Authié, É., Wissocq, N. M., & Murray, M. (1998) · Scientific and Technical Review (World Organisation for Animal Health) · doi:10.20506/rst.17.1.1088 · Cited by 112 · see citing works
Magez, S., Schwegmann, A., Atkinson, R., Claes, F., Drennan, M., Baetselier, P. D., & Brombacher, F. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000122 · Cited by 110 · see citing works
ggtext: Improved Text Rendering Support for 'ggplot2'
Wilke, C. O., & Wiernik, B. M. (2020) · doi:10.32614/cran.package.ggtext · Cited by 109 · see citing works
Admixture and diversity in West African cattle populations
Freeman, A., Meghen, C., MacHugh, D., Loftus, R., Achukwi, M. D., Bado, A., Sauveroche, B., & Bradley, D. (2004) · Molecular Ecology · doi:10.1111/j.1365-294x.2004.02311.x · Cited by 108 · see citing works
Self-citationA General Framework for Increasing the Robustness of PCA-Based Correlation Clustering Algorithms
Kriegel, H., Kröger, P., Schubert, E., & Zimek, A. (2008) · Lecture notes in computer science · doi:10.1007/978-3-540-69497-7_27 · Cited by 103 · see citing works
Iron metabolism in trypanosomatids, and its crucial role in infection
Taylor, M. C., & Kelly, J. M. (2010) · Parasitology · doi:10.1017/s0031182009991880 · Cited by 95 · see citing works
Lymph node dissection – understanding the immunological function of lymph nodes
Büettner, M., & Bode, U. (2012) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2012.04602.x · Cited by 90 · see citing works
Noyes, H., Brass, A., Obara, I., Anderson, S., Archibald, A. L., Bradley, D. G., Fisher, P., Freeman, A., Gibson, J., Gicheru, M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013486108 · Cited by 88 · see citing works
Trypanotolerance in cattle and prospects for the control of trypanosomiasis by selective breeding
Murray, M., Trail, J. C. M., & D'Ieteren, G. D. (1990) · Scientific and Technical Review (World Organisation for Animal Health) · doi:10.20506/rst.9.2.506 · Cited by 86 · see citing works
Uzonna, J. E., KAUSHIK, R. S., GORDON, J. R., & TABEL, H. (1999) · Parasite Immunology · doi:10.1046/j.1365-3024.1999.00202.x · Cited by 81 · see citing works
N’Djetchi, M. K., Ilboudo, H., Koffi, M., Kaboré, J., Kaboré, J. W., Kaba, D., Courtin, F., Coulibaly, B., Fauret, P., Kouakou, L., et al. (2017) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0005993 · Cited by 79 · see citing works
Role of iron homeostasis in trypanosomiasis-associated anemia
Stijlemans, B., Vankrunkelsven, A., Brys, L., Magez, S., & BAETSELIER, P. D. (2008) · Immunobiology · doi:10.1016/j.imbio.2008.07.023 · Cited by 74 · see citing works
Toxicogenomics of subchronic hexachlorobenzene exposure in Brown Norway rats.
Ezendam, J., Staedtler, F., Pennings, J. L. A., Vandebriel, R. J., Pieters, R. H. H., Boffetta, P., Harleman, J. H., & Vos, J. G. (2004) · Environmental Health Perspectives · doi:10.1289/ehp.112-1241993 · Cited by 74 · see citing works
MacHugh, D. E., Taraktsoglou, M., Killick, K. E., Nalpas, N., Browne, J. A., Park, S. D., Hokamp, K., Gormley, E. P., & Magee, D. A. (2012) · Veterinary Research · doi:10.1186/1297-9716-43-25 · Cited by 74 · see citing works
Self-citationIdentification of mechanisms of natural resistance to African trypanosomiasis in cattle
Naessens, J., Teale, A. J., & Sileghem, M. (2002) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(02)00070-3 · Cited by 69 · see citing works
Constrained chromatin accessibility in PU.1-mutated agammaglobulinemia patients
Le Coz, C., Nguyen, D. N., Su, C., Nolan, B. E., Albrecht, A. V., Xhani, S., Sun, D., Demaree, B., Pillarisetti, P., Khanna, C., et al. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20201750 · Cited by 69 · see citing works
McLoughlin, K. E., Nalpas, N., Rue-Albrecht, K., Browne, J. A., Magee, D. A., Killick, K. E., Park, S. D. E., Hokamp, K., Meade, K. G., O’Farrelly, C., et al. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00396 · Cited by 67 · see citing works
Self-citationTolerance to trypanosomatids: a threat, or a key for disease elimination?
Berthier, D., Brenière, S. F., Bras-Gonçalves, R., Lemesre, J.-L., Jamonneau, V., Solano, P., Lejon, V., Thévenon, S., & Bucheton, B. (2016) · Trends in Parasitology · doi:10.1016/j.pt.2015.11.001 · Cited by 65 · see citing works
Understanding bovine trypanosomiasis and trypanotolerance: the promise of functional genomics
Hill, E. W., O’Gorman, G. M., Agaba, M. K., Gibson, J. P., Hanotte, O., Kemp, S. J., Naessens, J., Coussens, P. M., & MacHugh, D. E. (2005) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2005.02.004 · Cited by 64 · see citing works
Self-citationAkol, G. W. O., & Murray, M. (1982) · Veterinary Record · doi:10.1136/vr.110.13.295 · Cited by 63 · see citing works
Magick 1.0: 🎩 ✨🐇 Advanced Graphics and Image Processing in R
Ooms, J. C. L. (2017) · doi:10.59350/th49p-22b65 · Cited by 62 · see citing works
Mechanisms Controlling Anaemia in Trypanosoma congolense Infected Mice
Noyes, H. A., Alimohammadian, M. H., Agaba, M. K., Brass, A., Fuchs, H., Gailus‐Durner, V., Hulme, H., Iraqi, F. A., Kemp, S. J., Rathkolb, B., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005170 · Cited by 61 · see citing works
Kumar, R., Ali, S. A., Singh, S. K., Bhushan, V., Mathur, M., Jamwal, S., Mohanty, A. K., Kaushik, J. K., & Kumar, S. (2020) · Veterinary Sciences · doi:10.3390/vetsci7040206 · Cited by 61 · see citing works
Bloodstream forms of Trypanosoma brucei require only small amounts of iron for growth
Steverding, D. (1997) · Parasitology Research · doi:10.1007/s004360050357 · Cited by 57 · see citing works
Contributions of experimental mouse models to the understanding of African trypanosomiasis
Antoine‐Moussiaux, N., Magez, S., & Desmecht, D. J.-M. (2008) · Trends in Parasitology · doi:10.1016/j.pt.2008.05.010 · Cited by 57 · see citing works
O’Gorman, G. M., Park, S. D. E., Hill, E. W., Meade, K. G., Mitchell, L. C., Agaba, M. K., Gibson, J. P., Hanotte, O., Naessens, J., Kemp, S. J., et al. (2006) · Physiological Genomics · doi:10.1152/physiolgenomics.00100.2006 · Cited by 56 · see citing works
Self-citationO’Gorman, G. M., Park, S. D. E., Hill, E. W., Meade, K. G., Coussens, P. M., Agaba, M. K., Naessens, J., Kemp, S. J., & MacHugh, D. E. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-207 · Cited by 55 · see citing works
Self-citationArcher, N., Nassif, N. T., & O’Brien, B. A. (2015) · Genes and Immunity · doi:10.1038/gene.2015.8 · Cited by 52 · see citing works
Characterisation and expression profile of the bovine cathelicidin gene repertoire in mammary tissue
Whelehan, C. J., Barry-Reidy, A., Meade, K. G., Eckersall, P. D., Chapwanya, A., Narciandi, F., Lloyd, A. T., & O’Farrelly, C. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-128 · Cited by 52 · see citing works
Self-citationNalpas, N., Park, S. D. E., Magee, D. A., Taraktsoglou, M., Browne, J. A., Conlon, K. M., Rue-Albrecht, K., Killick, K. E., Hokamp, K., Lohan, A. J., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-230 · Cited by 51 · see citing works
Self-citationMagee, D. A., Taraktsoglou, M., Killick, K. E., Nalpas, N., Browne, J. A., Park, S. D. E., Conlon, K. M., Lynn, D. J., Hokamp, K., Gordon, S. V., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032034 · Cited by 50 · see citing works
Self-citationBerthier, D., Peylhard, M., Dayo, G., Flori, L., Sylla, S., Bolly, S., Sakandé, H., Chantal, I., & Thévenon, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126498 · Cited by 49 · see citing works
Cattle genome-wide analysis reveals genetic signatures in trypanotolerant N’Dama
Kim, S., Ka, S., Ha, J.-W., Kim, J., Yoo, D., Kim, K., Lee, H., Lim, D., Cho, S., Hanotte, O., et al. (2017) · BMC Genomics · doi:10.1186/s12864-017-3742-2 · Cited by 49 · see citing works
Casey, M. E., Meade, K. G., Nalpas, N., Taraktsoglou, M., Browne, J. A., Killick, K. E., Park, S. D. E., Gormley, E. P., Hokamp, K., Magee, D. A., et al. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00023 · Cited by 48 · see citing works
Self-citationNaessens, J., Leak, S. G. A., Kennedy, D. J., Kemp, S. J., & Teale, A. J. (2003) · Veterinary Parasitology · doi:10.1016/s0304-4017(02)00360-6 · Cited by 48 · see citing works
Killick, K. E., Browne, J. A., Park, S. D. E., Magee, D. A., Martin, I., Meade, K. G., Gordon, S. V., Gormley, E. P., O’Farrelly, C., Hokamp, K., et al. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-611 · Cited by 46 · see citing works
Self-citationThe spatial expression pattern of antimicrobial peptides across the healthy bovine udder
Tetens, J., Friedrich, J. J., Hartmann, A., Schwerin, M., Kalm, E., & Thaller, G. E. (2010) · Journal of Dairy Science · doi:10.3168/jds.2009-2729 · Cited by 45 · see citing works
Genetic aspects of control of anaemia development in trypanotolerant N'Dama cattle
Trail, J. C. M., D'Ieteren, G. D. M., Maille, J. C., & Yangari, G. (1991) · Acta Tropica · doi:10.1016/0001-706x(91)90016-d · Cited by 45 · see citing works
Okello, I., Mafie, E. M., Eastwood, G., Nzalawahe, J. S., & Mboera, L. E. G. (2022) · Journal of Medical Entomology · doi:10.1093/jme/tjac018 · Cited by 45 · see citing works
Trypanosomosis: potential driver of selection in African cattle
Smetko, A., Soudré, A., Silbermayr, K., Müller, S., Brem, G., Hanotte, O., Boettcher, P. J., Stella, A., Mészáros, G., Wurzinger, M., et al. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00137 · Cited by 44 · see citing works
Magez, S., & Caljon, G. (2011) · Parasite Immunology · doi:10.1111/j.1365-3024.2011.01293.x · Cited by 39 · see citing works
Antimicrobial activity of bovine psoriasin
Regenhard, P., Leippe, M., Schubert, S., Podschun, R., Kalm, E., Grötzinger, J., & Looft, C. (2008) · Veterinary Microbiology · doi:10.1016/j.vetmic.2008.12.001 · Cited by 38 · see citing works
Kuriakose, S. M., Onyilagha, C., Singh, R. V., Olayinka‐Adefemi, F., Jia, P., & Uzonna, J. E. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02673 · Cited by 38 · see citing works
Bahbahani, H. M., Afana, A., & Wragg, D. (2018) · PLoS ONE · doi:10.1371/journal.pone.0202479 · Cited by 37 · see citing works
rlang: Functions for Base Types and Core R and 'Tidyverse' Features
Henry, L., & Wickham, H. (2017) · doi:10.32614/cran.package.rlang · Cited by 36 · see citing works
Stijlemans, B., Vankrunkelsven, A., Caljon, G., Bockstal, V., Guilliams, M., Bosschaerts, T., Beschin, A., Raes, G., Magez, S., & Baetselier, P. (2010) · Endocrine, Metabolic & Immune Disorders - Drug Targets · doi:10.2174/187153010790827966 · Cited by 35 · see citing works
African trypanosomiasis in cattle: Working with nature's solution
Murray, M., & Black, S. J. (1985) · Veterinary Parasitology · doi:10.1016/0304-4017(85)90065-2 · Cited by 34 · see citing works
Guerrero, N. A., Camacho, M., Vila, L., Iñiguez, M. A., Chillón-Marinas, C., Cuervo, H., Poveda, C., Fresno, M., & Gironès, N. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0004025 · Cited by 33 · see citing works
Uzonna, J. E., Kaushik, R. S., Gordon, J., & Tabel, H. (1999) · Parasite Immunology · doi:10.1111/cge.1999.21.2.57 · Cited by 33 · see citing works
Immune Response of Cattle Infected with African Trypanosomes
Taylor, K. A., & Mertens, B. (1999) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02761999000200022 · Cited by 32 · see citing works
Rue-Albrecht, K., Magee, D. A., Killick, K. E., Nalpas, N., Gordon, S. V., & MacHugh, D. E. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00536 · Cited by 31 · see citing works
Self-citationStijlemans, B., Beschin, A., Magez, S., Ginderachter, J. A. V., & BAETSELIER, P. D. (2015) · BioMed Research International · doi:10.1155/2015/819389 · Cited by 30 · see citing works
Dwinger, R. H., Murray, M., & Moloo, S. K. (1987) · Parasite Immunology · doi:10.1111/j.1365-3024.1987.tb00513.x · Cited by 30 · see citing works
Atypical human trypanosomosis: Potentially emerging disease with lack of understanding
Kumar, R., Gupta, S., Bhutia, W. D., Vaid, R. K., & Kumar, S. (2022) · Zoonoses and Public Health · doi:10.1111/zph.12945 · Cited by 29 · see citing works
Goyache, F., Pérez-Pardal, L., Fernández, I., Traoré, A., Menéndez‐Arias, N. A., & Álvarez, I. (2021) · Gene · doi:10.1016/j.gene.2021.145899 · Cited by 28 · see citing works
Holder, A. L., Garty, R., Elder, C., Mesnard, P., Laquerbe, C., Bartens, M.-C., Salavati, M., Shabbir, M. Z., Tzelos, T., Connelly, T., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01420 · Cited by 26 · see citing works
Trypanotolerance and the value of conserving livestock genetic resources
Trail, J. C. M., D'Ieteren, G. D. M., & Teale, A. J. (1989) · Genome · doi:10.1139/g89-142 · Cited by 25 · see citing works
Ibrahim, M. A. M., Weber, J. S., Ngomtcho, S. C. H., Signaboubo, D., Berger, P., Hassane, H. M., & Kelm, S. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009323 · Cited by 25 · see citing works
Röder, A., Hüsken, S., Hutter, M. C., Rettie, A. E., Hanenberg, H., Wiek, C., & Girhard, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032038 · Cited by 25 · see citing works
Neutrophil metalloproteinase driven spleen damage hampers infection control of trypanosomiasis
Phạm, H. T. T., Magez, S., Choi, B., Baatar, B., Jung, J., & Radwanska, M. (2023) · Nature Communications · doi:10.1038/s41467-023-41089-w · Cited by 25 · see citing works
Genetic Basis of Trypanotolerance in Cattle and Mice
Kemp, S. J., & Teale, A. J. (1998) · Parasitology Today · doi:10.1016/s0169-4758(98)01334-9 · Cited by 24 · see citing works
Novel aspects of iron homeostasis in pathogenic bloodstream form Trypanosoma brucei
Carbajo, C. G., Cornell, L., Madbouly, Y., Lai, Z., Yates, P. A., Tinti, M., & Tiengwe, C. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009696 · Cited by 24 · see citing works
Dayo, G., Gautier, M., Berthier, D., Poivey, J. P., Sidibé, I., Bengaly, Z., Eggen, A., Boichard, D., & Thévenon, S. (2011) · Animal Genetics · doi:10.1111/j.1365-2052.2011.02227.x · Cited by 22 · see citing works
Tmem45b is essential for inflammation- and tissue injury–induced mechanical pain hypersensitivity
Tanioku, T., Nishibata, M., Tokinaga, Y., Konno, K., Watanabe, M., Hemmi, H., Fukuda‐Ohta, Y., Kaisho, T., Furue, H., & Kawamata, T. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2121989119 · Cited by 22 · see citing works
khroma: Colour Schemes for Scientific Data Visualization
Frèrebeau, N. (2018) · HAL · doi:10.5281/zenodo.1472077 · Cited by 22 · see citing works
Iron-associated biology of Trypanosoma brucei
Basu, S., Horáková, E., & Lukeš, J. (2015) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2015.10.027 · Cited by 21 · see citing works
Coagulation Studies in Gambian Trypanosomiasis
Greenwood, B. M., & Whittle, H. (1976) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1976.25.390 · Cited by 20 · see citing works
Expression of antimicrobial peptides by bovine endothelial cells
Alva-Murillo, N., Téllez-Pérez, A. D., Sagrero-Cisneros, E., López-Meza, J. E., & Ochoa‐Zarzosa, A. (2012) · Cellular Immunology · doi:10.1016/j.cellimm.2012.11.016 · Cited by 17 · see citing works
Autoimmunity to phosphatidylserine and anemia in African Trypanosome infections
Rivera‐Correa, J., Verdi, J., Sherman, J., Sternberg, J. M., Raper, J., & Rodrı́guez, A. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009814 · Cited by 17 · see citing works
Quintana, J. F., Sinton, M. C., Chandrasegaran, P. R. G., Dubey, L. K., Ogunsola, J. O., Samman, M. A., Haley, M., McConnell, G., Swar, N.-R. K., Ngoyi, D. M., et al. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002389 · Cited by 17 · see citing works
Meade, K. G., O’Gorman, G. M., Hill, E. W., Narciandi, F., Agaba, M. K., Kemp, S. J., O’Farrelly, C., & MacHugh, D. E. (2009) · Molecular Immunology · doi:10.1016/j.molimm.2009.09.042 · Cited by 15 · see citing works
Self-citationLack of haplotype structuring for two candidate genes for trypanotolerance in cattle
Álvarez, I., Pérez-Pardal, L., Traoré, A., Fernández, I., & Goyache, F. (2015) · Journal of Animal Breeding and Genetics · doi:10.1111/jbg.12181 · Cited by 15 · see citing works
Goodhead, I., Archibald, A. L., Amwayi, P. W., Brass, A., Gibson, J. P., Hall, N., HUGHES, M. A., Limo, M., Iraqi, F. A., Kemp, S. J., et al. (2010) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000880 · Cited by 14 · see citing works
Advocacy for identifying certain animal diseases as “neglected”
Roger, F. L., Solano, P., Bouyer, J., Porphyre, V., Berthier, D., Peyre, M., & Bonnet, P. (2017) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0005843 · Cited by 14 · see citing works
Platelets, Macrophages, and Thromboinflammation in Chagas Disease
Choudhuri, S., & Garg, N. J. (2022) · Journal of Inflammation Research · doi:10.2147/jir.s380896 · Cited by 14 · see citing works
A Non-Cytosolic Protein of Trypanosoma evansi Induces CD45-Dependent Lymphocyte Death
Antoine‐Moussiaux, N., Cornet, A. M., Cornet, F., Glineur, S., Dermine, M., & Desmecht, D. J.-M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005728 · Cited by 11 · see citing works
Rajavel, A., Heinrich, F., Schmitt, A. O., & Gültaş, M. (2020) · Vaccines · doi:10.3390/vaccines8020246 · Cited by 11 · see citing works
Molecular epidemiology of Animal African Trypanosomosis in southwest Burkina Faso
Hounyèmè, R. E., Kaboré, J., Gimonneau, G., Somda, M. B., Salou, E. W., Missihoun, A. A., Bengaly, Z., Jamonneau, V., & Boulangé, A. F. (2022) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0010106 · Cited by 11 · see citing works
Choi, B., Vu, H. T., Vu, H. T., Radwanska, M., & Magez, S. (2024) · Pathogens · doi:10.3390/pathogens13030188 · Cited by 11 · see citing works
Comparison and definition of spleen and lymph node: A phylogenetic analysis
Jønsson, V. (1985) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(85)80247-2 · Cited by 10 · see citing works
Iron Uptake Controls Trypanosoma cruzi Metabolic Shift and Cell Proliferation
Dick, C. F., Alcantara, C. D. L., Carvalho‐Kelly, L. F., Lacerda‐Abreu, M. A., Cunha‐e‐Silva, N. L., Meyer‐Fernandes, J. R., & Vieyra, A. R. (2023) · Antioxidants · doi:10.3390/antiox12050984 · Cited by 10 · see citing works
Animal model of human disease: trypanosomiasis, sleeping sickness.
Moulton, J. E., & Stevens, D. R. (1978) · PubMed · Cited by 9 · see citing works
Pathogenic role of mitogen activated protein kinases in protozoan parasites
Kaur, P., & Goyal, N. (2021) · Biochimie · doi:10.1016/j.biochi.2021.10.012 · Cited by 8 · see citing works
Peylhard, M., Berthier, D., Dayo, G., Chantal, I., Sylla, S., Nidelet, S., Dubois, E., Martin, G., Sempéré, G., Flori, L., et al. (2023) · Peer Community Journal · doi:10.24072/pcjournal.239 · Cited by 8 · see citing works
Jentzsch, J., Wunderlich, H., Thein, M., Bechthold, J., Brehm, L., Krauss, S. W. D., Weiß, M., & Ersfeld, K. (2024) · Journal of Cell Science · doi:10.1242/jcs.261740 · Cited by 8 · see citing works
Trypanosoma vivax: disseminated intravascular coagulation in cattle
Wellde, B. T., Chumo, D. A., Onyango, F. K., Reardon, M. J., Roberts, L. M., Njogu, A. R., & Opiyo, E. A. (1989) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1989.11812422 · Cited by 5 · see citing works
Rajavel, A., Klees, S., Hui, Y., Schmitt, A. O., & Gültaş, M. (2022) · Biology · doi:10.3390/biology11050742 · Cited by 5 · see citing works
Banworth, M. J., Liang, Z., & Li, G. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102281 · Cited by 5 · see citing works
Gitau, J., Macharia, R. W., Mwangi, K. W., Ongeso, N., & Murungi, E. K. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e18175 · Cited by 3 · see citing works
Kuiper, J. W., Krause, J., Potgeter, L., Adrian, J., & Hauck, C. R. (2023) · Journal of Cell Science · doi:10.1242/jcs.260771 · Cited by 2 · see citing works
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2 of the 151 references couldn’t be matched to a known paper.
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The Genomic Landscape of Cattle: Domestication, Dispersal, and Adaptive Evolution
Liu, Y., Dao, W., Gao, R., Fan, X., Yang, R., & Miao, Y. (2026) · Animals · doi:10.3390/ani16050776 · Cited by 1 · see citing works
Somé, G. F., Séré, M., Chantal, I., Somda, M. B., Dayo, G., Ouaré, M., Sakandé, H., Sempéré, G., Thévenon, S., & Berthier, D. (2025) · BMC Veterinary Research · doi:10.1186/s12917-025-05235-4 · Cited by 1 · see citing works
Integrative Genomics Identifies Candidate Genes Underlying Trypanotolerance in Hybrid African Cattle
McHugo, G. P., Ward, J. A., Ng’ang’a, S. I., Frantz, L., Browne, J. A., Salter‐Townshend, M., O’Gorman, G. M., Meade, K. G., Hill, E. W., Hall, T. J., et al. (2026) · Evolutionary Applications · doi:10.1111/eva.70274
Self-citationGenome editing in Africa: A review of technological advances, applications, and the path forward
Johnson, A. M., Isiaka, I. D., Merenini, I. F., Iyanuoluwa, O. V., Violet, M. S., & Abubakari, A. W. (2026) · Scientific African · doi:10.1016/j.sciaf.2026.e03445
- Authors
- McHugo, G. P., Ward, J. A., Browne, J. A., O’Gorman, G. M., Meade, K. G., Hill, E. W., Hall, T. J., & MacHugh, D. E.
- Affiliations
- University College Dublin (IE)
- UK Agri-Tech Centre, Innovation Centre, York Science Park, York, UK
- Corresponding author
- MacHugh, David E.
- ORCID
- Venue
- PLoS neglected tropical diseases
- Publisher
- openRxiv
- Published
- 2025-01-31
- Volume
- 19
- Issue
- 8
- Pages
- e0012882-e0012882
- ISSN
- 1935-2727 (ISSN-L)
- PMC
- PMC12342285
- OpenAlex
- W4412932781
- Cited by
- 4
- References
- 151
- Citations by year
- 2026: 3 · 2025: 1
- FWCI
- 2.75
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS neglected tropical diseases (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Science Foundation Ireland (SFI/15/IA/3154, SFI/18/CRT/6214, SFI/01/F.1/B028)
- Topics
- Health Sciences › Medicine › Epidemiology › Trypanosoma species research and implications
- Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
- Health Sciences › Veterinary › Small Animals › Animal health and immunology
- Keywords
- trypanotolerance, Trypanosoma congolense, African animal trypanosomosis, cattle, N'Dama cattle, Boran cattle, gene expression profiling, immune response, antimicrobial peptides, cytokines, parasitemia, anemia, iron homeostasis, coagulation, innate immunity
- MeSH terms
- Animals, Cattle, Cattle Diseases, Trypanosoma congolense, Trypanosomiasis, African, Gene Expression Profiling, Genomics
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