The central role of macrophages in trypanosomiasis-associated anemia: rationale for therapeutical approaches
Abstract
Bovine African trypanosomiasis causes severe economical problems on the African continent and one of the most prominent immunopathological parameters associated with this parasitic infection is anemia. In this report we review the current knowledge of the mechanisms underlying trypanosomiasis-associated anemia. In first instance, the central role of macrophages and particularly their activation state in determining the outcome of the disease (i.e. trypanosusceptibility versus trypanotolerance) will be discussed. In essence, while persistence of classically activated macrophages (M1) contributes to anemia development, switching towards alternatively activated macrophages (M2) alleviates pathology including anemia. Secondly, while parasite-derived glycolipids such as the glycosylphosphatidylinositol (GPI) induce M1, host-derived IL-10 blocks M1-mediated inflammation, promotes M2 development and prevents anemia development. In this context, strategies aimed at inducing the M1 to M2 switch, such as GPI-based treatment, adenoviral delivery of IL-10 and induction of IL-10 producing regulatory T cells will be discussed. Finally, the crucial role of iron-homeostasis in trypanosomiasis-associated anemia development will be documented to stress the analogy with anemia of chronic disease (ACD), hereby providing new insight that might contribute to the treatment of ACD.
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Trypanotolerant animals switch from innate immune response to adaptive immune response with the induction of active macrophages (M2) following trypanosome infection.
“In previous studies, trypanotolerant animals were reported to switch from innate immune response to adaptive immune response with the induction of active macrophages (M2) following trypanosome infection (Stijlemans et al., 2010; Bosschaerts et al., 2011).”
From Identification of Candidate Signature Genes and Key Regulators Associated With Trypanotolerance in the Sheko Breed (2019) · cites this paper as Stijlemans et al., 2010
Cites
The chemokine system in diverse forms of macrophage activation and polarization
MANTOVANI, A., SICA, A., SOZZANI, S., ALLAVENA, P., VECCHI, A., & LOCATI, M. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.09.015 · Cited by 6,534 · see citing works
Weiss, G., & Goodnough, L. T. (2005) · New England Journal of Medicine · doi:10.1056/nejmra041809 · Cited by 3,800 · see citing works
The many faces of macrophage activation
Mosser, D. M. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0602325 · Cited by 1,902 · see citing works
Ferguson, M. A. J. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.17.2799 · Cited by 632 · see citing works
Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria
Schofield, L., Hewitt, M. C., Evans, K. J., Siomos, M., & Seeberger, P. H. (2002) · Nature · doi:10.1038/nature00937 · Cited by 486 · see citing works
The history of African trypanosomiasis
Steverding, D. (2008) · Parasites & Vectors · doi:10.1186/1756-3305-1-3 · Cited by 470 · see citing works
Múñoz, M., Villar, I., & García‐Erce, J. A. (2009) · World Journal of Gastroenterology · doi:10.3748/wjg.15.4617 · Cited by 371 · see citing works
Iron Sequestration and Anemia of Inflammation
Ganz, T., & Nemeth, E. (2009) · Seminars in Hematology · doi:10.1053/j.seminhematol.2009.06.001 · Cited by 361 · see citing works
Iron metabolism in the anemia of chronic disease
Weiss, G. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2008.08.006 · Cited by 322 · see citing works
Pathogenesis and treatment of anaemia of chronic disease
Weiß, G. (2002) · Blood Reviews · doi:10.1054/blre.2002.0193 · Cited by 276 · see citing works
de Almeida, I. C., Camargo, M. M., Procópio, D. O., Silva, L. S., Mehlert, A., Travassos, L. R., Gazzinelli, R. T., & Ferguson, M. A. J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.7.1476 · Cited by 254 · see citing works
Glycosylphosphatidylinositol Anchors ofPlasmodium falciparum
Naik, R. S., Branch, O. H., Woods, A. S., Vijay–Kumar, M., Perkins, D. J., Nahlen, B. L., Lal, A. A., Cotter, R. J., Costello, C. E., Ockenhouse, C. F., et al. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.11.1563 · Cited by 240 · see citing works
Schofield, L., Novakovic, S., Gerold, P., Schwarz, R. Τ., McConville, M. J., & Tachado, S. D. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.5.1886 · Cited by 235 · see citing works
Tachado, S. D., Gerold, P., McConville, M. J., Baldwin, T., Quilici, D. R., Schwarz, R. Τ., & Schofield, L. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.5.1897 · Cited by 233 · see citing works
African bovine trypanosomiasis: the problem of drug resistance
Geerts, S., Holmes, P. H., Eisler, M. C., & Diall, O. (2001) · Trends in Parasitology · doi:10.1016/s1471-4922(00)01827-4 · Cited by 229 · see citing works
Tachado, S. D., Gerold, P., Schwarz, R. Τ., Novakovic, S., McConville, M. J., & Schofield, L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.8.4022 · Cited by 195 · see citing works
The immune response to Plasmodium falciparum malaria
Malaguarnera, L., & Musumeci, S. (2002) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(02)00344-4 · Cited by 193 · see citing works
Magez, S., Radwanska, M., Beschin, A., Sekikawa, K., & BAETSELIER, P. D. (1999) · Infection and Immunity · doi:10.1128/iai.67.6.3128-3132.1999 · Cited by 182 · see citing works
Self-citationBovine 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
Inflammatory cells in asthma: Mechanisms and implications for therapy
Hamid, Q. A., Tulić, M. K., Liu, M. C., & Moqbel, R. (2003) · Journal of Allergy and Clinical Immunology · doi:10.1067/mai.2003.22 · Cited by 180 · see citing works
Liver in sepsis and systemic inflammatory response syndrome
Szabó, G., Romics, L., & Frendl, G. (2002) · Clinics in Liver Disease · doi:10.1016/s1089-3261(02)00058-2 · Cited by 170 · see citing works
Magez, S., Stijlemans, B., Radwanska, M., Pays, É., Ferguson, M. A. J., & BAETSELIER, P. D. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.4.1949 · Cited by 161 · see citing works
Self-citationVincendeau, P., Daulouède, S., Veyret, B., Dardé, M., Bouteille, B., & Lemesre, J. L. (1992) · Experimental Parasitology · doi:10.1016/0014-4894(92)90220-5 · Cited by 145 · see citing works
Fox, J. A., Duszenko, M., Ferguson, M. A. J., Low, M. G., & Cross, G. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)66784-5 · Cited by 142 · see citing works
Shoda, L. K. M., Kegerreis, K. A., Suarez, C. E., Roditi, I. J., Corral, R. S., Bertot, G. M., Norimine, J., & Brown, W. C. (2001) · Infection and Immunity · doi:10.1128/iai.69.4.2162-2171.2001 · Cited by 139 · see citing works
CD8 is critically involved in lymphocyte activation by a T. brucei brucei-released molecule
Olsson, T. P., Bakhiet, M., Höjeberg, B., Ljungdahl, Å., Edlund, C., Andersson, G., Ekre, H. P., Fung‐Leung, W., Mak, T. W., Wigzell, H., et al. (1993) · Cell · doi:10.1016/0092-8674(93)90400-k · Cited by 138 · see citing works
Drug resistance in pathogenic African trypanosomes: what hopes for the future?
Anene, B. M., Onah, D. N., & Nawa, Y. (2001) · Veterinary Parasitology · doi:10.1016/s0304-4017(00)00427-1 · Cited by 136 · see citing works
Drennan, M. B., Stijlemans, B., Abbeele, J. V. D., Quesniaux, V. F. J., Barkhuizen, M., Brombacher, F., BAETSELIER, P. D., Ryffel, B., & Magez, S. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.4.2501 · Cited by 135 · see citing works
Self-citationMultiple mechanisms of immune evasion by African trypanosomes
Donelson, J. E. (1998) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(97)00209-0 · Cited by 134 · see citing works
Specialized Fatty Acid Synthesis in African Trypanosomes: Myristate for GPI Anchors
Morita, Y. S., Paul, K. S., & Englund, P. T. (2000) · Science · doi:10.1126/science.288.5463.140 · Cited by 126 · see citing works
Namangala, B., Noël, W., BAETSELIER, P. D., Brys, L., & Beschin, A. (2001) · The Journal of Infectious Diseases · doi:10.1086/320731 · Cited by 126 · see citing works
Self-citationGuilliams, M., Movahedi, K., Bosschaerts, T., VandenDriessche, T., Chuah, M., Hérin, M., Acosta‐Sanchez, A., Ma, L., Moser, M., Ginderachter, J. A. V., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.2.1107 · Cited by 124 · see citing works
Self-citationRegulation of innate and acquired immunity in African trypanosomiasis
Mansfield, J. M., & Paulnock, D. M. (2005) · Parasite Immunology · doi:10.1111/j.1365-3024.2005.00791.x · Cited by 117 · see citing works
The situation of sleeping sickness in Angola: a calamity
Stanghellini, A., & Josenando, T. (2001) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.2001.00724.x · Cited by 116 · 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
Self-citationMagez, S., Radwanska, M., Drennan, M. B., Fick, L., Baral, T. N., Brombacher, F., & BAETSELIER, P. D. (2006) · The Journal of Infectious Diseases · doi:10.1086/503808 · Cited by 109 · see citing works
Self-citationTachado, S. D., & Schofield, L. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.2763 · Cited by 106 · see citing works
Alternative versus classical macrophage activation during experimental African trypanosomosis
BAETSELIER, P. D., Namangala, B., Noël, W., Brys, L., Pays, É., & Beschin, A. (2001) · International Journal for Parasitology · doi:10.1016/s0020-7519(01)00170-9 · Cited by 103 · see citing works
Self-citationAn update on antigenic variation in African trypanosomes
Vanhamme, L., Pays, É., McCulloch, R., & Barry, J. D. (2001) · Trends in Parasitology · doi:10.1016/s1471-4922(01)01922-5 · Cited by 103 · see citing works
Molecular mechanisms involved in the pathogenesis of septic shock
López-Bojórquez, L. N., Zentella‐Dehesa, A., & Reyes‐Terán, G. (2004) · Archives of Medical Research · doi:10.1016/j.arcmed.2004.07.006 · Cited by 100 · see citing works
The Heme Oxygenase System: Its Role in Liver Inflammation
Wunder, C., & Potter, R. F. (2003) · Cardiovascular & Haematological Disorders - Drug Targets · doi:10.2174/1568006033481410 · Cited by 92 · see citing works
Guilliams, M., Oldenhove, G., Noël, W., Hérin, M., Brys, L., Loi, P., Flamand, V., Moser, M., BAETSELIER, P. D., & Beschin, A. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.5.2748 · Cited by 89 · see citing works
Self-citationExperimental African trypanosomiasis: IFN‐γ mediates early mortality
Shi, M., Pan, W., & Tabel, H. (2002) · European Journal of Immunology · doi:10.1002/immu.200390013 · Cited by 84 · see citing works
Authié, É., Boulangé, A. F., Muteti, D., Lalmanach, G., Gauthier, F., & Musoke, A. J. (2001) · International Journal for Parasitology · doi:10.1016/s0020-7519(01)00266-1 · Cited by 83 · see citing works
A Glycosylphosphatidylinositol-Based Treatment Alleviates Trypanosomiasis-Associated Immunopathology
Stijlemans, B., Baral, T. N., Guilliams, M., Brys, L., Korf, H., Drennan, M. B., Abbeele, J. V. D., BAETSELIER, P. D., & Magez, S. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.6.4003 · Cited by 79 · see citing works
Self-citationGlycosyl-phosphatidylinositol molecules of the parasite and the host
Ferguson, M. A. J., Brimacombe, J. S., Cottaz, S., Field, R. A., Guther, L. S., Homans, S. W., McConville, M. J., Mehlert, A., Milne, K. G., Ralton, J. E., et al. (1994) · Parasitology · doi:10.1017/s0031182000075715 · Cited by 76 · see citing works
Drug transport and drug resistance in African trypanosomes
Mäser, P., Lüscher, A., & Kaminsky, R. (2003) · Drug Resistance Updates · doi:10.1016/j.drup.2003.09.001 · Cited by 75 · see citing works
Magez, S., Truyens, C., Merimi, M., Radwanska, M., Stijlemans, B., Brouckaert, P., Brombacher, F., Pays, É., & BAETSELIER, P. D. (2004) · The Journal of Infectious Diseases · doi:10.1086/381151 · Cited by 75 · see citing works
Self-citationRole 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
Self-citationden Bossche, P. V., & Rowlands, G. J. (2001) · Acta Tropica · doi:10.1016/s0001-706x(00)00182-0 · Cited by 74 · see citing works
Sleeping sickness resurgence in the DRC: the past decade
Nieuwenhove, S. V., Betu‐Ku‐Mesu, V. K., Mansinsa, P., Declercq, J., & Bilenge, C. M. M. (2001) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.2001.00731.x · Cited by 74 · see citing works
Darji, A., Beschin, A., Sileghem, M., Heremans, H., Brys, L., & BAETSELIER, P. D. (1996) · Infection and Immunity · doi:10.1128/iai.64.6.1937-1943.1996 · Cited by 74 · see citing works
Self-citationFatty acid synthesis in African trypanosomes: a solution to the myristate mystery
Paul, K. S., JIANG, D., Morita, Y. S., & Englund, P. T. (2001) · Trends in Parasitology · doi:10.1016/s1471-4922(01)01984-5 · Cited by 73 · see citing works
African trypanosomosis: From immune escape and immunopathology to immune intervention
Stijlemans, B., Guilliams, M., Raes, G., Beschin, A., Magez, S., & BAETSELIER, P. D. (2007) · Veterinary Parasitology · doi:10.1016/j.vetpar.2007.05.005 · Cited by 72 · see citing works
Self-citationMacrophage Reprogramming by Mycolic Acid Promotes a Tolerogenic Response in Experimental Asthma
Korf, H., PYNAERT, G. N., Tournoy, K. G., Boonefaes, T., van Oosterhout, A. J. M., Ginneberge, D., Haegeman, A., Verschoor, J. A., BAETSELIER, P. D., & Grooten, J. (2006) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200507-1175oc · Cited by 69 · see citing works
Self-citationBakhiet, M., Olsson, T. P., Edlund, C., Höjeberg, B., Holmberg, K., LORENTZHN, J., & Kristensson, K. (1993) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.1993.tb01753.x · Cited by 68 · see citing works
Towards the Atlas of human African trypanosomiasis
Cecchi, G., Paone, M., Franco, J. R., Fèvre, E. M., Diarra, A., Ruiz, J. A., Mattioli, R. C., & Simarro, P. P. (2009) · International Journal of Health Geographics · doi:10.1186/1476-072x-8-15 · Cited by 67 · see citing works
Magez, S., Stijlemans, B., Baral, T. N., & BAETSELIER, P. D. (2002) · Microbes and Infection · doi:10.1016/s1286-4579(02)01617-9 · Cited by 67 · see citing works
Self-citationWaking up to sleeping sickness
Stich, A., Barrett, M. P., & Krishna, S. (2003) · Trends in Parasitology · doi:10.1016/s1471-4922(03)00055-2 · Cited by 66 · see citing works
Trypanosoma congolenseinfections: antibody-mediated phagocytosis by Kupffer cells
Shi, M., Wei, G., Pan, W., & Tabel, H. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.1003500 · Cited by 66 · see citing works
Analysis of macrophage activation in African trypanosomiasis
Paulnock, D. M., & Coller, S. P. (2001) · Journal of Leukocyte Biology · doi:10.1189/jlb.69.5.685 · Cited by 65 · see citing works
(2005) · CRC Press eBooks · doi:10.1201/b14192 · Cited by 64 · see citing works
Rolin, S., HANOCQ-QUERTIER, J., Paturiaux-Hanocq, F., Nolan, D. P., Salmon, D., Webb, H., Carrington, M., Voorheis, H. P., & Pays, É. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.18.10844 · Cited by 63 · see citing works
Naessens, J., Kitani, H., Nakamura, Y., Yagi, Y., Sekikawa, K., & Iraqi, F. A. (2005) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2004.02717.x · 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
Sileghem, M., Flynn, J. N., Logan-Henfrey, L. L., & Ellis, J. (1994) · Parasite Immunology · doi:10.1111/j.1365-3024.1994.tb00304.x · Cited by 61 · see citing works
Magez, S., Radwanska, M., Drennan, M. B., Fick, L., Baral, T. N., Allie, N., Jacobs, M., Nedospasov, S. A., Brombacher, F., Ryffel, B., et al. (2007) · The Journal of Infectious Diseases · doi:10.1086/520815 · Cited by 61 · see citing works
Self-citationNok, A. J. (2003) · The Journal of Biochemistry · doi:10.1093/jb/mvg093 · Cited by 58 · see citing works
Shi, M., Wei, G., Pan, W., & Tabel, H. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.3.1724 · Cited by 58 · 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
Coller, S. P., Mansfield, J. M., & Paulnock, D. M. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.3.1466 · Cited by 57 · see citing works
Regulation of host cell function by glycosylphosphatidylinositols of the parasitic protozoa
Schofield, L., & Tachado, S. D. (1996) · Immunology and Cell Biology · doi:10.1038/icb.1996.89 · Cited by 57 · see citing works
Lucas, R., Magez, S., Songa, B., Darji, A., HAMERS, R., & BAETSELIER, P. D. (1993) · Research in Immunology · doi:10.1016/s0923-2494(93)80082-a · Cited by 56 · see citing works
Self-citationImpact of nutrition on the pathophysiology of bovine trypanosomiasis
Holmes, P. H., Katunguka‐Rwakishaya, E., Bennison, J. J., Wassink, G. J., & Parkins, J. J. (2000) · Parasitology · doi:10.1017/s0031182099005806 · Cited by 56 · see citing works
Namangala, B., BAETSELIER, P. D., Brijs, L., Stijlemans, B., Noël, W., Pays, É., Carrington, M., & Beschin, A. (2000) · The Journal of Infectious Diseases · doi:10.1086/315322 · Cited by 56 · see citing works
Self-citationMild acid stress as a differentiation trigger in Trypanosoma brucei
Rolin, S., HANOCQ-QUERTIER, J., Paturiaux-Hanocq, F., Nolan, D. P., & Pays, É. (1998) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(98)00046-2 · Cited by 55 · see citing works
Leppert, B. J., Mansfield, J. M., & Paulnock, D. M. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.1.548 · Cited by 51 · see citing works
Naessens, 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
Mechanisms underlying trypanosome-elicited immunosuppression.
Darji, A., Lucas, R., Magez, S., Torreele, E., Palacios, J., Sileghem, M., Songa, E. B., Hamers, R., & Baetselier, P. D. (1991) · PubMed · Cited by 47 · see citing works
Self-citationStructure of the C-terminal Domain from Trypanosoma brucei Variant Surface Glycoprotein MITat1.2
Chattopadhyay, A., Jones, N. G., Nietlispach, D., Nielsen, P. R., Voorheis, H. P., Mott, H. R., & Carrington, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m410787200 · Cited by 46 · see citing works
Carrington, M. (1998) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(97)00190-4 · Cited by 44 · see citing works
Harris, T. H., Cooney, N. M., Mansfield, J. M., & Paulnock, D. M. (2006) · Infection and Immunity · doi:10.1128/iai.01938-05 · Cited by 44 · see citing works
Guilliams, M., Bosschaerts, T., Hérin, M., Hünig, T., Loi, P., Flamand, V., BAETSELIER, P. D., & Beschin, A. (2008) · The Journal of Infectious Diseases · doi:10.1086/590439 · Cited by 43 · see citing works
Self-citationMerschjohann, K., & Steverding, D. (2006) · Kinetoplastid Biology and Disease · doi:10.1186/1475-9292-5-3 · Cited by 42 · see citing works
Anosa, V. O., & Kaneko, J. J. (1983) · American Journal of Veterinary Research · doi:10.2460/ajvr.1983.44.04.645 · Cited by 42 · see citing works
Serum Xanthine Oxidase: Origin, Regulation, and Contribution to Control of Trypanosome Parasitemia
Wang, J., Praagh, A. D. G. V., Hamilton, E., Wang, Q. L., Zou, B.-X., Muranjan, M., Murphy, N. B., & Black, S. J. (2002) · Antioxidants and Redox Signaling · doi:10.1089/152308602753625933 · Cited by 39 · see citing works
Synthesis of membrane- and matrix-bound colony-stimulating factor-1 by cultured osteoblasts
Felix, R., Halasy-Nagy, J., Wetterwald, A., Cecchini, M. G., Fleisch, H. A., & Hofstetter, W. (1996) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199602)166:2 · Cited by 38 · see citing works
Perraut, R., Diatta, B., Marrama, L., Garraud, O., Jambou, R., Longacre, S., Gowda, K., Dièye, A., & Gowda, D. C. (2005) · Microbes and Infection · doi:10.1016/j.micinf.2005.01.002 · Cited by 37 · see citing works
Roles of free GPIs in amastigotes of Leishmania
Mensa‐Wilmot, K., Garg, N. J., McGwire, B., Lu, H.-G., Li, Z., Armah, D. A., LeBowitz, J., & Chang, K. P. (1999) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(99)00003-1 · Cited by 34 · see citing works
Gómez‐Rodríguez, J., Stijlemans, B., Muylder, G. D., Korf, H., Brys, L., Berberof, M., Darji, A., Pays, É., BAETSELIER, P. D., & Beschin, A. (2009) · The Journal of Infectious Diseases · doi:10.1086/648374 · Cited by 32 · see citing works
Self-citationConnor, R. J. (1994) · PubMed · Cited by 32 · see citing works
Erythrocyte surface sialic acid in Ndama and Zebu cattle
Esievo, K. A. N., Saror, D. I., Kolo, M., & Eduvie, L. O. (1986) · Journal of Comparative Pathology · doi:10.1016/0021-9975(86)90026-5 · Cited by 32 · see citing works
Hanrahan, O., Webb, H., O’Byrne, R., Brabazon, E. D., Treumann, A., Sunter, J. D., Carrington, M., & Voorheis, H. P. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000468 · Cited by 28 · see citing works
Impaired Kupffer Cells in Highly Susceptible Mice Infected withTrypanosoma congolense
Shi, M., Wei, G., Pan, W., & Tabel, H. (2005) · Infection and Immunity · doi:10.1128/iai.73.12.8393-8396.2005 · Cited by 25 · see citing works
Understanding the role of monocytic cells in liver inflammation using parasite infection as a model
Bosschaerts, T., Guilliams, M., Stijlemans, B., BAETSELIER, P. D., & Beschin, A. (2009) · Immunobiology · doi:10.1016/j.imbio.2009.06.010 · Cited by 24 · see citing works
Self-citationBarkhuizen, M., Magez, S., Atkinson, R. A., & Brombacher, F. (2007) · The Journal of Infectious Diseases · doi:10.1086/521681 · Cited by 24 · see citing works
Self-citationMarcello, L., Menon, S., Ward, P. N., Wilkes, J., Jones, N. G., Carrington, M., & Barry, J. D. (2007) · BMC Bioinformatics · doi:10.1186/1471-2105-8-143 · Cited by 23 · see citing works
African bovine trypanosomiasis: the problem of drug resistance
Geerts, S. (2001) · Parasitology Today · doi:10.1016/s0169-4758(00)01827-5 · Cited by 22 · see citing works
NYAKUNDI, J. N., Crawley, B. A., SMITH, R. A., & Pentreath, V. W. (2002) · Parasitology · doi:10.1017/s0031182002001701 · Cited by 21 · see citing works
Katunguka‐Rwakishaya, E., Parkins, J. J., Fishwick, G., Murray, M., & Holmes, P. H. (1995) · Veterinary Parasitology · doi:10.1016/0304-4017(94)00748-2 · Cited by 21 · see citing works
Innate and acquired control of trypanosome parasitaemia in Cape buffalo
Black, S. J., Sicard, E. L., Murphy, N. B., & Nolan, D. P. (2001) · International Journal for Parasitology · doi:10.1016/s0020-7519(01)00160-6 · Cited by 21 · see citing works
Dyserythropoiesis in animal trypanosomosis.
Igbokwe, I. O. (1989) · PubMed · Cited by 21 · see citing works
Faye, D., Fall, A., Leak, S. G. A., Losson, B., & Geerts, S. (2005) · Acta Tropica · doi:10.1016/j.actatropica.2004.10.008 · Cited by 21 · see citing works
NYAKUNDI, J. N., Crawley, B. A., & Pentreath, V. W. (2002) · Parasitology · doi:10.1017/s0031182002001683 · Cited by 19 · see citing works
Katunguka‐Rwakishaya, E., Murray, M., & Holmes, P. H. (1999) · Veterinary Parasitology · doi:10.1016/s0304-4017(99)00088-6 · Cited by 18 · see citing works
Sileghem, M., Saya, R., Grab, D. J., & Naessens, J. (2001) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(01)00241-0 · Cited by 17 · see citing works
Andrianarivo, A. G., Muiya, P., & Logan-Henfrey, L. L. (1996) · Experimental Parasitology · doi:10.1006/expr.1996.0014 · Cited by 16 · see citing works
Ogunsanmi, A. O., Akpavie, S. O., & Anosa, V. O. (1994) · Revue d’élevage et de médecine vétérinaire des pays tropicaux · doi:10.19182/remvt.9132 · Cited by 16 · see citing works
Morita, Y. S. (2001) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(01)00279-1 · Cited by 13 · see citing works
Ojok, L., Kaeufer-Weiss, I., & Weiss, E. (2001) · Journal of Comparative Pathology · doi:10.1053/jcpa.2000.0445 · Cited by 12 · see citing works
Ngure, R. M., Eckersall, P. D., Mungatana, N. W. K., Mburu, J. N., Jennings, F. W., Burke, J., & Murray, M. (2008) · Research in Veterinary Science · doi:10.1016/j.rvsc.2008.09.004 · Cited by 9 · see citing works
Palis, J. (2004) · Nature · doi:10.1038/432964a · Cited by 9 · see citing works
Mb, D., Stijlemans, B., Van den Abbeele, J., Quesniaux, V. F. J., Barkhuizen, M., Brombacher, F., De Baetselier, P., Ryffel, B., & Magez, S. (2005) · HAL · Cited by 5 · see citing works
Self-citationNgure, R. M., Eckersall, P. D., Burke, J., Karori, S. M., Mwangi, W. W., Wachira, F. N., Maathai, R., & Murray, M. (2009) · Parasitology International · doi:10.1016/j.parint.2009.06.008 · Cited by 4 · see citing works
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The Iron age of host–microbe interactions
Soares, M. P., & Weiss, G. (2015) · The EMBO Reports · doi:10.15252/embr.201540558 · Cited by 227 · see citing works
Stijlemans, B., BAETSELIER, P. D., Magez, S., Ginderachter, J. A. V., & Trez, C. D. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00218 · Cited by 101 · see citing works
Self-citationStijlemans, B., Caljon, G., Abbeele, J. V. D., Ginderachter, J. A. V., Magez, S., & Trez, C. D. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00233 · Cited by 92 · see citing works
Self-citationMIF Contributes to Trypanosoma brucei Associated Immunopathogenicity Development
Stijlemans, B., Leng, L., Brys, L., Sparkes, A., Liese, V., Caljon, G., Raes, G., Abbeele, J. V. D., Ginderachter, J. A. V., Beschin, A., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004414 · Cited by 48 · see citing works
Self-citationStijlemans, B., Radwanska, M., Trez, C. D., & Magez, S. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00582 · Cited by 45 · see citing works
Self-citationIlboudo, H., Bras‐Gonçalves, R., Camara, M., Flori, L., Camara, O., Sakandé, H., Léno, M., Petitdidier, E., Jamonneau, V., & Bucheton, B. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004469 · Cited by 42 · see citing works
Alfituri, O. A., Quintana, J. F., MacLeod, A., Garside, P., Benson, R. A., Brewer, J. M., Mabbott, N. A., Morrison, L. J., & Capewell, P. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01250 · Cited by 41 · see citing works
Horses naturally infected by Trypanosoma vivax in southern Brazil
Silva, A. S. D., Garcia, H. A., Costa, M. M., França, R. T., Gasperi, D. D., Zanette, R. A., Amado, J. A., Lopes, S. T. A., Teixeira, M. M. G., & Monteiro, S. G. (2010) · Parasitology Research · doi:10.1007/s00436-010-2036-2 · Cited by 40 · see citing works
Stijlemans, B., Cnops, J., Naniima, P., Vaast, A., Bockstal, V., BAETSELIER, P. D., & Magez, S. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003561 · Cited by 38 · see citing works
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“The disease is characterized by neurological symptoms such as ataxia which is one of the clinical signs of trypanosome infection (Tuntasuvan et al., 1997; Suzuki and Yazawa, 2011; Giordani et al., 2016).”
BackgroundAfrican trypanosome control in the insect vector and mammalian host
Beschin, A., Abbeele, J. V. D., BAETSELIER, P. D., & Pays, É. (2014) · Trends in Parasitology · doi:10.1016/j.pt.2014.08.006 · Cited by 36 · see citing works
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Sirak, B., Bizuneh, G. K., Imming, P., & Asres, K. (2024) · BMC Veterinary Research · doi:10.1186/s12917-023-03856-1 · Cited by 5 · see citing works
Iron Metabolism in Pathogenic Trypanosomes
Manta, B., Fleitas, L., & Comini, M. A. (2012) · BiblioBoard Library Catalog (Open Research Library) · doi:10.5772/34402 · Cited by 5 · see citing works
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. (2025) · doi:10.1101/2025.01.31.635858 · Cited by 4 · see citing works
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Sawitri, D. H., Wardhana, A. H., & Wibowo, H. (2018) · Jurnal Ilmu Ternak dan Veteriner · doi:10.14334/jitv.v22i3.1666 · Cited by 3 · see citing works
Systemic and Multi-Organ Diseases
(2017) · Elsevier eBooks · doi:10.1016/b978-0-7020-5246-0.00021-8 · Cited by 3 · see citing works
Fidélis, O. L., Sampaio, P. H., Gonçalves, L. R., Machado, R. Z., André, M. R., Wijffels, G. L., & Cadioli, F. A. (2021) · Animals · doi:10.3390/ani11113191 · Cited by 2 · see citing works
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Abdeta, D., Kebede, N., Giday, M., Terefe, G., & Abay, S. M. (2019) · Research Square · doi:10.21203/rs.2.13929/v1 · Cited by 2 · see citing works
Živalj, M., Martin, A. S., Baetselier, P. D., Maksymova, L., Berghmans, F., Boon, L., Ginderachter, J. A. V., Magez, S., Trez, C. D., & Stijlemans, B. (2025) · Pathogens · doi:10.3390/pathogens14121276 · Cited by 1 · see citing works
Self-citationAbenga, J. N., & Idowu, T. (2017) · Comparative Clinical Pathology · doi:10.1007/s00580-017-2613-1 · Cited by 1 · see citing works
Stijlemans, B., Beschin, A., BAETSELIER, P. D., & Raes, G. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1311-4_16
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Sirak, B., Bizuneh, G. K., Imming, P., & Asres, K. (2024) · Figshare · doi:10.6084/m9.figshare.25092513
Agina, O. A., Andong, F. A., Omeke, J. N., Eze, U. U., Anyanwu, M. U., Jaja, I. F., & Oguttu, J. W. (2026) · Parasitology Research · doi:10.1007/s00436-026-08652-y
Júnior, F. A. D. S., & Luiz, O. (2014) · Aleph UCLA Undergraduate Research Journal for the Humanities and Social Sciences
- Authors
- Stijlemans, B., Vankrunkelsven, A., Caljon, G., Bockstal, V., Guilliams, M., Bosschaerts, T., Beschin, A., Raes, G., Magez, S., & Baetselier, P.
- Affiliations
- Vrije Universiteit Brussel (BE)
- Corresponding author
- Baetselier, Patrick
- ORCID
- Venue
- Endocrine, Metabolic & Immune Disorders - Drug Targets
- Publisher
- Bentham Science Publishers Ltd.
- Published
- 2010-03-01
- Volume
- 10
- Issue
- 1
- Pages
- 71-82
- ISSN
- 1871-5303 (ISSN-L)
- OpenAlex
- W2159423681
- Cited by
- 35
- References
- 114
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2022: 1 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 3 · 2016: 2 · 2015: 4 · 2014: 5 · 2013: 1 · 2012: 2
- FWCI
- 0.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrine Metabolic & Immune Disorders - Drug Targets (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Trypanosoma species research and implications
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Keywords
- macrophage activation, M1 macrophages, M2 macrophages, glycosylphosphatidylinositol, IL-10, regulatory T cells, iron homeostasis, anemia of chronic disease, trypanotolerance
- MeSH terms
- Anemia, Animals, Homeostasis, Humans, Iron, Macrophage Activation, Macrophages, Trypanosoma, Trypanosomiasis, African, Interleukin-10, Glycosylphosphatidylinositols, T-Lymphocytes, Regulatory
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