The Dermis as a Delivery Site of Trypanosoma brucei for Tsetse Flies

PLoS Pathogens

Volumn 12, Issue 7, 2016, Pages

  Caljon, Guy ^a,b,c   Van Reet, Nick ^a   De Trez, Carl ^c,d   Vermeersch, Marjorie ^e   Pérez Morga, David ^e   Van Den Abbeele, Jan ^a  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^e UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN;

AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONFOCAL MICROSCOPY; DERMIS; FLUORESCENCE MICROSCOPY; GENE AMPLIFICATION; GENETIC TRANSFECTION; GLOSSINA MORSITANS; MICROBIAL KINETICS; MIXED INFECTION; MOUSE; NONHUMAN; PARASITE TRANSMISSION; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SKIN TEMPERATURE; THERMOGRAPHIC IMAGING SYSTEM; TRYPANOSOMA BRUCEI; ANIMAL; BITES AND STINGS; C57BL MOUSE; DISEASE MODEL; FLOW CYTOMETRY; GLOSSINIDAE; HOST PARASITE INTERACTION; INSECT VECTOR; PARASITOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRYPANOSOMA BRUCEI BRUCEI;

ANIMALS; BITES AND STINGS; DERMIS; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; HOST-PARASITE INTERACTIONS; INSECT VECTORS; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; POLYMERASE CHAIN REACTION; TRYPANOSOMA BRUCEI BRUCEI; TSETSE FLIES;

EID: 84982924029     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005744     Document Type: Article

References (48)

1. Simarro PP, Cecchi G, Franco JR, Paone M, Diarra A, et al. (2015) Monitoring the Progress towards the Elimination of Gambiense Human African Trypanosomiasis. PLoS Negl Trop Dis9: e0003785. doi: 10.1371/journal.pntd.000378526056823
2. Aksoy S, (2011) Sleeping sickness elimination in sight: time to celebrate and reflect, but not relax. PLoS Negl Trop Dis5: e1008. doi: 10.1371/journal.pntd.000100821364971
3. Chitanga S, Marcotty T, Namangala B, Van den Bossche P, Van Den Abbeele J, et al. (2011) High prevalence of drug resistance in animal trypanosomes without a history of drug exposure. PLoS Negl Trop Dis5: e1454. doi: 10.1371/journal.pntd.000145422206039
4. Van den Bossche P, Chitanga S, Masumu J, Marcotty T, Delespaux V, (2011) Virulence in Trypanosoma congolense Savannah subgroup. A comparison between strains and transmission cycles. Parasite Immunol33: 456–460. doi: 10.1111/j.1365-3024.2010.01277.x21204855
5. von Wissmann B, Machila N, Picozzi K, Fevre EM, de CBBM, et al. (2011) Factors associated with acquisition of human infective and animal infective trypanosome infections in domestic livestock in Western Kenya. PLoS Negl Trop Dis5: e941. doi: 10.1371/journal.pntd.000094121311575
6. Rotureau B, Van Den Abbeele J, (2013) Through the dark continent: African trypanosome development in the tsetse fly. Front Cell Infect Microbiol3: 53. doi: 10.3389/fcimb.2013.0005324066283
7. Vickerman K, (1985) Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull41: 105–114. 3928017
8. Van Den Abbeele J, Caljon G, De Ridder K, De Baetselier P, Coosemans M, (2010) Trypanosoma brucei modifies the tsetse salivary composition, altering the fly feeding behavior that favors parasite transmission. PLoS Pathog6: e1000926. doi: 10.1371/journal.ppat.100092620532213
9. Urwyler S, Studer E, Renggli CK, Roditi I, (2007) A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei. Molecular Microbiology63: 218–228. 17229212
10. Barry JD, Emery DL, (1984) Parasite development and host responses during the establishment of Trypanosoma brucei infection transmitted by tsetse fly. Parasitology88 (Pt 1): 67–84. 6709396
11. Barry JD, Graham SV, Fotheringham M, Graham VS, Kobryn K, et al. (1998) VSG gene control and infectivity strategy of metacyclic stage Trypanosoma brucei. Mol Biochem Parasitol91: 93–105. 9574928
12. Wei G, Bull H, Zhou X, Tabel H, (2011) Intradermal infections of mice by low numbers of african trypanosomes are controlled by innate resistance but enhance susceptibility to reinfection. J Infect Dis203: 418–429. doi: 10.1093/infdis/jiq05121208931
13. Caljon G, Van Den Abbeele J, Stijlemans B, Coosemans M, De Baetselier P, et al. (2006) Tsetse fly saliva accelerates the onset of Trypanosoma brucei infection in a mouse model associated with a reduced host inflammatory response. Infect Immun74: 6324–6330. 16954393
14. Bai X, Yao H, Du C, Chen Y, Lai R, et al. (2015) An immunoregulatory peptide from tsetse fly salivary glands of Glossina morsitans morsitans. Biochimie118: 123–128. doi: 10.1016/j.biochi.2015.09.00126342879
15. Magez S, Caljon G, (2011) Mouse models for pathogenic African trypanosomes: unravelling the immunology of host-parasite-vector interactions. Parasite Immunol33: 423–429. doi: 10.1111/j.1365-3024.2011.01293.x21480934
16. Cochran R, Rosen T, (1983) African trypanosomiasis in the United States. Arch Dermatol119: 670–674. 6870320
17. Thuita JK, Kagira JM, Mwangangi D, Matovu E, Turner CM, et al. (2008) Trypanosoma brucei rhodesiense transmitted by a single tsetse fly bite in vervet monkeys as a model of human African trypanosomiasis. PLoS Negl Trop Dis2: e238. doi: 10.1371/journal.pntd.000023818846231
18. Akol GW, Murray M, (1982) Early events following challenge of cattle with tsetse infected with Trypanosoma congolense: development of the local skin reaction. Vet Rec110: 295–302. 7072104
19. Dwinger RH, Lamb G, Murray M, Hirumi H, (1987) Dose and stage dependency for the development of local skin reactions caused by Trypanosoma congolense in goats. Acta Trop44: 303–314. 2892366
20. Dwinger RH, Rudin W, Moloo SK, Murray M, (1988) Development of Trypanosoma congolense, T vivax and T brucei in the skin reaction induced in goats by infected Glossina morsitans centralis: a light and electron microscopical study. Res Vet Sci44: 154–163. 3387665
21. Mwangi DM, Hopkins J, Luckins AG, (1990) Cellular phenotypes in Trypanosoma congolense infected sheep: the local skin reaction. Parasite Immunol12: 647–658. 2084609
22. Luckins AG, Gray AR, (1978) An extravascular site of development of Trypanosoma congolense. Nature272: 613–614. 643055
23. Wolbach SB, Binger CA, (1912) A Contribution to the Parasitology of Trypanosomiasis. J Med Res27: 83–108 113. 19972075
24. Mwangi DM, Hopkins J, Luckins AG, (1995) Trypanosoma congolense infection in sheep: ultrastructural changes in the skin prior to development of local skin reactions. Vet Parasitol60: 45–52. 8644458
25. Van Reet N, Van de Vyver H, Pyana PP, Van der Linden AM, Buscher P, (2014) A panel of Trypanosoma brucei strains tagged with blue and red-shifted luciferases for bioluminescent imaging in murine infection models. PLoS Negl Trop Dis8: e3054. doi: 10.1371/journal.pntd.000305425144573
26. Claes F, Vodnala SK, van Reet N, Boucher N, Lunden-Miguel H, et al. (2009) Bioluminescent imaging of Trypanosoma brucei shows preferential testis dissemination which may hamper drug efficacy in sleeping sickness. PLoS Negl Trop Dis3: e486. doi: 10.1371/journal.pntd.000048619621071
27. McLatchie AP, Burrell-Saward H, Myburgh E, Lewis MD, Ward TH, et al. (2013) Highly sensitive in vivo imaging of Trypanosoma brucei expressing "red-shifted" luciferase. PLoS Negl Trop Dis7: e2571. doi: 10.1371/journal.pntd.000257124278497
28. Gibson W, Peacock L, Ferris V, Williams K, Bailey M, (2008) The use of yellow fluorescent hybrids to indicate mating in Trypanosoma brucei. Parasit Vectors1: 4. doi: 10.1186/1756-3305-1-418298832
29. Sbarbati A, Accorsi D, Benati D, Marchetti L, Orsini G, et al. (2010) Subcutaneous adipose tissue classification. Eur J Histochem54: e48. 21263747
30. Le Ray D, Barry JD, Easton C, Vickerman K, (1977) First tsetse fly transmission of the "AnTat" serodeme of Trypanosoma brucei. Ann Soc Belg Med Trop57: 369–381. 610616
31. MacLeod ET, Maudlin I, Darby AC, Welburn SC, (2007) Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology134: 827–831. 17306056
32. Belkaid Y, Jouin H, Milon G, (1996) A method to recover, enumerate and identify lymphomyeloid cells present in an inflammatory dermal site: a study in laboratory mice. J Immunol Methods199: 5–25. 8960094
33. Gonzalez-Andrade P, Camara M, Ilboudo H, Bucheton B, Jamonneau V, et al. (2014) Diagnosis of trypanosomatid infections: targeting the spliced leader RNA. J Mol Diagn16: 400–404. doi: 10.1016/j.jmoldx.2014.02.00624814957
34. Panettiere P, Accorsi D, Marchetti L, Minicozzi AM, Orsini G, et al. (2011) The trochanteric fat pad. Eur J Histochem55: e16. doi: 10.4081/ejh.2011.e1622193296
35. Fairbairn H, Burtt E, (1946) The infectivity to man of a strain of Trypanosoma rhodesiense transmitted cyclically by Glossina morsitans through sheep and antelope; evidence that man requires a minimum infective dose of metacyclic trypanosomes. Ann Trop Med Parasitol40: 270–313. 20289229
36. Telleria EL, Benoit JB, Zhao X, Savage AF, Regmi S, et al. (2014) Insights into the trypanosome-host interactions revealed through transcriptomic analysis of parasitized tsetse fly salivary glands. PLoS Negl Trop Dis8: e2649. doi: 10.1371/journal.pntd.000264924763140
37. Combs TP, Nagajyothi Mukherjee S, de Almeida CJ, Jelicks LA, et al. (2005) The adipocyte as an important target cell for Trypanosoma cruzi infection. J Biol Chem280: 24085–24094. 15843370
38. Zhang LJ, Guerrero-Juarez CF, Hata T, Bapat SP, Ramos R, et al. (2015) Innate immunity. Dermal adipocytes protect against invasive Staphylococcus aureus skin infection. Science347: 67–71. doi: 10.1126/science.126097225554785
39. Trindade S, Rijo-Ferreira F, Carvalho T, Pinto-Neves D, Guegan F, et al. (2016) Trypanosoma brucei Parasites Occupy and Functionally Adapt to the Adipose Tissue in Mice. Cell Host Microbedoi: 10.1016/j.chom.2016.05.002
40. Singh B, Fleury C, Jalalvand F, Riesbeck K, (2012) Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev36: 1122–1180. doi: 10.1111/j.1574-6976.2012.00340.x22537156
41. Bastos IM, Motta FN, Charneau S, Santana JM, Dubost L, et al. (2010) Prolyl oligopeptidase of Trypanosoma brucei hydrolyzes native collagen, peptide hormones and is active in the plasma of infected mice. Microbes Infect12: 457–466. doi: 10.1016/j.micinf.2010.02.00720188209
42. Hirumi H, Doyle JJ, Hirumi K, (1977) African trypanosomes: cultivation of animal-infective Trypanosoma brucei in vitro. Science196: 992–994. 558652
43. Balber AE, (1983) Primary murine bone marrow cultures support continuous growth of infectious human trypanosomes. Science220: 421–423. 6836284
44. Reinouts van Haga HA, Mitchell BK, (1975) Temperature receptors on tarsi of the tsetse fly Glossina morsitans west. Nature255: 225–226. 1143318
45. Lahondere C, Lazzari CR, (2015) Thermal effect of blood feeding in the telmophagous fly Glossina morsitans morsitans. J Therm Biol48: 45–50. doi: 10.1016/j.jtherbio.2014.12.00925660629
46. Dethier VG, (1954) Notes on the biting response of tsetse flies. Am J Trop Med Hyg3: 160–171. 13114601
47. Torr SJ, Maudlin I, Vale GA, (2007) Less is more: resitricted application of insecticide to cattle to improve the cost and efficacy of tsetse control. Med. Vet Entomol21: 53–64. 17373947
48. Aslan H, Oliveira F, Meneses C, Castrovinci P, Gomes R, et al. (2016) New Insights Into the Transmissibility of Leishmania infantum From Dogs to Sand Flies: Experimental Vector-Transmission Reveals Persistent Parasite Depots at Bite Sites. J Infect Dis213: 1752–61. doi: 10.1093/infdis/jiw02226768257