Examining the tsetse teneral phenomenon and permissiveness to trypanosome infection

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue NOV, 2013, Pages

  Haines, Lee Rafuse ^a  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

African trypanosomiasis; Glossina; Immunity; Peritrophic matrix; Teneral phenomenon; Tsetse symbionts; Vector competence

Indexed keywords

PEPTIDOGLYCAN RECOGNITION PROTEIN;

DISEASE EXACERBATION; DISEASE PREDISPOSITION; DOWN REGULATION; FAT BODY; GLOSSINIDAE; HOST SUSCEPTIBILITY; HUMAN; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; INTESTINE FLORA; NONHUMAN; PHENOTYPE; RNA INTERFERENCE; SEXUAL MATURITY; SHORT SURVEY; TENERAL; TRYPANOSOMA; TRYPANOSOMIASIS; ANIMAL; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; IMMUNOLOGY; PARASITOLOGY; PHYSIOLOGY; UNITED STATES; AFRICAN TRYPANOSOMIASIS; GLOSSINA; IMMUNITY; PERITROPHIC MATRIX; REVIEW; TENERAL PHENOMENON; TSETSE SYMBIONTS; VECTOR COMPETENCE;

ANIMALS; HOST-PARASITE INTERACTIONS; TRYPANOSOMA; TSETSE FLIES; UNITED STATES;

AFRICAN TRYPANOSOMIASIS; GLOSSINA; IMMUNITY; PERITROPHIC MATRIX; TENERAL PHENOMENON; TSETSE SYMBIONTS; VECTOR COMPETENCE;

EID: 84897919455     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00084     Document Type: Short Survey

References (65)

1. Akoda, K., Van den Bossche, P., Marcotty, T., Kubi, C., Coosemans, M., De Deken, R., et al. (2009). Nutritional stress affects the tsetse fly's immune gene expression. Med. Vet. Entomol. 23, 195-201. doi: 10.1111/j.1365-2915.2009.00799.x
2. Aksoy, S. (1995). Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int. J. Syst. Bacteriol. 45, 848-851. doi: 10.1099/00207713-45-4-848
3. Anderson, M., and Finlayson, L. H. (1973). Ulstrastructural changes during growth of flight muscles in adult Glossina austeni. Trans. R. Soc. Trop. Med. Hyg. 67, 296. doi: 10.1016/0035-9203(73)90221-6
4. Attardo, G. M., Lohs, C., Heddi, A., Alam, U. H., Yildirim, S., and Aksoy, S. (2008). Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. J. Insect Physiol. 54, 1236-1242. doi: 10.1016/j.jinsphys.2008.06.008
5. Bogdan, C. (2001). Nitric oxide and the immune response. Nat. Immunol. 2, 907-916. doi: 10.1038/ni1001-907
6. Boulanger, N., Brun, R., Ehret-Sabatier, L., Kunz, C., and Bulet, P. (2002). Immunopeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections. Insect Biochem. Mol. Biol. 32, 369-375. doi: 10.1016/S0965-1748(02)00029-2
7. Chandra, M., Liniger, M., Tetley, L., Roditi, I., and Barry, J. D. (2004). TsetseEP, a gut protein from the tsetse Glossina morsitans, is related to a major surface glycoprotein of trypanosomes transmitted by the fly and to the products of a Drosophila gene family. Insect Biochem. Mol. Biol. 34, 1163-1173. doi: 10.1016/j.ibmb.2004.07.004
8. Dale, C., and Maudlin, I. (1999). Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int. J. Syst. Bacteriol. 49, 267-275. doi: 10.1099/00207713-49-1-267
9. Dale, C., and Welburn, S. C. (2001). The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int. J. Parasitol. 31, 628-631. doi: 10.1016/S0020-7519(01)00151-5
10. Distelmans, W., D'Haeseleer, F., Kaufman, L., and Rousseeuw, P. (1982). The susceptibility of Glossina palpalis palpalis at different ages to infection with Trypanosoma congolense. Ann. Soc. Belg. Med. Trop. 62, 41-47.
11. Ellis, D. S., and Evans, D. A. (1977). Passage of Trypanosoma brucei rhodesiense through the peritrophic membrane of Glossina morsitans morsitans. Nature 267, 834-835. doi: 10.1038/267834a0
12. Farikou, O., Njiokou, F., Mbida Mbida, J. A., Njitchouang, G. R., Djeunga, H. N., Asonganyi, T., et al. (2010). Tripartite interactions between tsetse flies, Sodalis glossinidius and trypanosomes-an epidemiological approach in two historical human African trypanosomiasis foci in Cameroon. Infect. Genet. Evol. 10, 115-121. doi: 10.1016/j.meegid.2009.10.008
13. Foster, W. A. (1976). Male sexual maturation of the tsetse flies Glossina morsitans Westwood and G. austeni Newstead (Dipt., Glossinidae) in relation to blood feeding. Bull. Entomol. Res. 66, 389-399. doi: 10.1017/S0007485300006787
14. Freeman, J. C. (1973). The penetration of the peritrophic membrane of the tsetse flies by trypanosomes. Acta Trop. 30, 347-355.
15. Gibson, W., and Bailey, M. (2003). The development of Trypanosoma brucei within the tsetse fly midgut observed using green fluorescent trypanosomes. Kinetoplastid Biol. Dis. 10, 1. doi: 10.1186/1475-9292-2-1
16. Grébaut, P., Bena, J. M., Manzambi, E. Z., Mansinsa, P., Khande, V., Ollivier, G., et al. (2009). Characterization of sleeping sickness transmission sites in rural and periurban areas of Kinshasa (République Démocratique du Congo). Vector Borne Zoonotic Dis. 9, 631-636. doi: 10.1089/vbz.2008.0118
17. Haines, L. R. (2009). Sleeping with the Enemy: Tsetse-Trypanosome Interactions. PhD Dissertation. Liverpool University Press. Liverpool, UK.
18. Haines, L. R., Jackson, A. M., Lehane, M. J., Thomas, J. M., Yamaguchi, A. Y., Haddow, J. D., et al. (2005). Increased expression of unusual EP repeat-containing proteins in the midgut of the tsetse fly (Glossina) after bacterial challenge. Insect Biochem. Mol. Biol. 35, 413-423. doi: 10.1016/j.ibmb.2005.01.005
19. Haines, L. R., Lehane, S. M., Pearson, T. W., and Lehane, M. J. (2010). Tsetse EP protein protects the fly midgut from trypanosome establishment. PLoS Pathog. 5:e1000793. doi: 10.1371/journal.ppat.1000793
20. Hao, Z., Kasumba, I., and Aksoy, S. (2003). Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae). Insect Biochem. Mol. Biol. 33, 1155-1164. doi: 10.1016/j.ibmb.2003.07.001
21. Hao, Z., Kasumba, I., Lehane, M. J., Gibson, W. C., Kwon, J., and Aksoy, S. (2001). Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Proc. Natl. Acad. Sci. U.S.A. 98, 12648-12653. doi: 10.1073/pnas.221363798
22. Hecker, H., and Moloo, S. K. (1981). Influence of Trypanosoma (trypanozoon) brucei infection on the fine structure of midgut cells in Glossina m. morsitans. Parasitology 82, 106-107.
23. Hegedus, D., Erlandson, M., Gillott, C., and Toprak, U. (2009). New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 54, 285-302. doi: 10.1146/annurev.ento.54.110807.090559
24. Hu, C., and Aksoy, S. (2006) Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans. Mol. Microbiol. 60, 1194-1204. doi: 10.1111/j.1365-2958.2006.05180.x
25. Ibrahim, E. A., Ingram, G. A., and Molyneux, D. H. (1984). Haemagglutinins and parasite agglutinins in haemolymph and gut of Glossina. Tropenmed. Parasitol. 35, 151-156.
26. Jackson, C. H. N. (1946). An artificially isolated generation of tsetse flies (Diptera). Bull. Entomol. Res. 37, 291-299. doi: 10.1017/S0007485300022203
27. Kubi, C., Van den Abbeele, J., De Deken, R., Marcotty, T., Dorny, P., and Van den Bossche, P. (2006). The effect of starvation on the susceptibility of teneral and non-teneral tsetse flies to trypanosome infection. Med. Vet. Entomol. 20, 388-392. doi: 10.1111/j.1365-2915.2006.00644.x
28. Leak, S. G. A. (1998). Tsetse Biology and Ecology: Their Role in the Epidemiology and Control of Trypanosomiasis. Wallingford, UK: CABI Publishing. ISBN 0-85199-300-1.
29. Lehane, M. J. (1997). Peritrophic matrix structure and function. Annu. Rev. Entomol. 42, 525-550. doi: 10.1146/annurev.ento.42.1.525
30. Lehane, M. J., and Msangi, A. R. (1991). Lectin and peritrophic membrane development in the gut of Glossina m. morsitans and a discussion of their role in protecting the fly against trypanosome infection. Med. Vet. Entomol. 5, 495-501. doi: 10.1111/j.1365-2915.1991.tb00578.x
31. Ma, W.-C., and Denlinger, D. L. (1974). Secretory discharge and microflora of milk gland in tsetse flies. Nature 247, 301-303. doi: 10.1038/247301a0
32. MacLeod, E. T, Maudlin, I., Darby, A. C., and Welburn, S. C. (2007). Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology 134, 827-831. doi: 10.1017/S0031182007002247
33. Maudlin, I., and Dukes, P. (1985). Extrachromosomal inheritance of susceptibility to trypanosome infection in tsetse flies. I. Selection of susceptible and refractory lines of Glossina morsitans morsitans. Ann. Trop. Med. Parasitol. 79, 317-324.
34. Maudlin, I., and Ellis, D. S. (1985). Association between intracellular Rickettsia-like infections of midgut cells and susceptibility to trypanosome infection in Glossina spp. Z. Parasitenkd. 71, 683-687. doi: 10.1007/BF00925601
35. Maudlin, I., and Welburn, S. C. (1987). Lectin mediated establishment of midgut infections of Trypanosoma congolense and Trypanosoma brucei in Glossina morsitans. Trop. Med. Parasitol. 38,167-170.
36. Maudlin, I., Welburn, S. C., and Milligan, P. (1990). Salivary-gland infection: a sex-linked recessive character in tsetse. Acta Trop. 48, 9-15. doi: 10.1016/0001-706X(90)90060-D
37. Mellanby, K. (1936). Experimental work on the tsetse fly, Glossina palpalis, in Uganda. Bull. Entomol. Res. 27, 611-633.
38. Mihok, S., Otieno, L. H., Darji, N., and Munyinyi, D. (1992). Influence of D(+)-glucosamine on infection rates and parasite loads in tsetse flies (Glossina spp.) infected with Trypanosoma brucei. Acta Trop. 51, 217-228. doi: 10.1016/0001-706X(92)90040-5
39. Moloo, S. K., and Gray, M. A. (1989). New observations on cyclical development of Trypanosoma vivax in Glossina. Acta Trop. 46, 167-172. doi: 10.1016/0001-706X(89)90033-8
40. Moloo, S. K., Steiger, R. F., and Hecker, H. (1970). Ultrastructure of the peritrophic membrane formation in Glossina Wiedemann. Acta Trop. 274, 378-383.
41. Mor, A. (2009). Multifunctional host defense peptides: antiparasitic activities. FEBS J. 276, 6474-6482. doi: 10.1111/j.1742-4658.2009.07358.x
42. Nayduch, D., and Aksoy, S. (2007). Refractoriness in tsetse flies (Diptera: Glossinidae) may be a matter of timing. J. Med. Entomol. 44, 660-665. doi: 10.1603/0022-2585(2007)44[660:RITFDG]2.0.CO;2
43. Otieno, L. H., Darji, N., Onyango, P., and Mpanga, E. (1983). Some observations on factors associated with the development of Trypanosoma brucei brucei infections in Glossina morsitans morsitans. Acta Trop. 40, 113-120.
44. Pais, R., Lohs, C., Wu, Y., Wang, J., and Aksoy, S. (2008). The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl. Environ. Microbiol. 74, 5965-5974. doi: 10.1128/AEM.00741-08
45. Peacock, L., Ferris, V., Bailey, M., and Gibson, W. (2012). The influence of sex and fly species on the development of trypanosomes in tsetse flies. PLoS Negl. Trop. Dis. 6:e1515. doi: 10.1371/journal.pntd.0001515
46. Reinhardt, C., Steiger, R., and Hecker, H. (1972). Ultrastructural study of the midgut mycetome-bacteroids of the tsetse flies Glossina morsitans, G. fuscipes, and G, brevipalpis (Diptera, Brachycera). Acta Trop. 29, 280-288.
47. Roubaud, É. (1909). La Glossina Palpalis: Sa biologie, Son Role Dans L'étiologie des Trypanosomiases. Laval, France: L. Barneoud & Cie, Imprimeurs.
48. Sharma, R., Gluenz, E., Peacock, L., Gibson, W., Gull, K., and Carrington, M. (2009). The heart of darkness: growth and form of Trypanosoma brucei in the tsetse fly. Trends Parasitol. 25, 517-524. doi: 10.1016/j.pt.2009.08.001
49. Snyder, A. K., Deberry, J. W., Runyen-Janecky, L., and Rio, R. V. (2010). Nutrient provisioning facilitates homeostasis between tsetse fly (Diptera: Glossinidae) symbionts. Proc. Biol. Sci. 277, 2389-2397. doi: 10.1098/rspb.2010.0364
50. Soumana, I. H., Simo, G., Njiokou, F., Tchicaya, B., Abd-Alla, A. M., Cuny, G., et al. (2013). The bacterial flora of tsetse fly midgut and its effect on trypanosome transmission. J. Invertebr. Pathol. 112(Suppl.), S89-S93. doi: 10.1016/j.jip.2012.03.029
51. Tchouomene-Labou, J., Nana-Djeunga, H., Simo, G., Njitchouang, G. R., Cuny, G., Asonganyi, T., et al. (2013). Spatial and temporal variations relevant to tsetse control in the Bipindi focus of southern Cameroon. Parasit. Vectors 6, 193. doi: 10.1186/1756-3305-6-193
52. Tellam, R. L., Wijffels, G., and Willadsen, P. (1999). Peritrophic matrix proteins. Insect Biochem. Mol. Biol. 29, 87-101. doi: 10.1016/S0965-1748(98)00123-4
53. Van Hoof, L., Henrard, C., and Peel, E. (1937). Influences modificatricees de la transmissibilité cylique du Trypanosoma gambiense par Glossina palpalis. Ann. Soc. Belg. Med. Trop. 17, 249-263.
54. Walshe, D. P., Lehane, M. J., and Haines, L. R. (2011). Post eclosion age predicts the prevalence of midgut trypanosome infections in Glossina. PLoS ONE 6:e26984. doi: 10.1371/journal.pone.0026984
55. Wang, J., and Aksoy, S. (2012). PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse's offspring. Proc. Natl. Acad. Sci. U.S.A. 109, 10552-10557. doi: 10.1073/pnas.1116431109
56. Wang, J., Wu, Y., Yang, G., and Aksoy, S. (2009). Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc. Natl. Acad. Sci. U.S.A. 106, 12133-12138. doi: 10.1073/pnas.0901226106
57. Weiss, B., and Aksoy, S. (2011). Microbiome influences on insect host vector competence. Trends Parasitol. 27, 514-522. doi: 10.1016/j.pt.2011.05.001
58. Weiss, B. L., Wang, J., Maltz, M. A., Wu, Y., and Aksoy, S. (2013). Trypanosome infection establishment in the tsetse fly gut is influenced by microbiome-regulated host immune barriers. PLoS Pathog. 9:e1003318. doi: 10.1371/journal.ppat.1003318
59. Welburn, S. C., and Maudlin, I. (1992). The nature of the teneral state in Glossina and its role in the acquisition of trypanosome infection in tsetse. Ann. Trop. Med. Parasitol. 86, 529-536.
60. Welburn, S. C, Maudlin, I., and Ellis, D. S. (1987). In vitro cultivation of rickettsia-like-organisms from Glossina spp. Ann. Trop. Med. Parasitol. 81, 331-335.
61. Welburn, S. C., Maudlin, I., and Ellis, D. S. (1989). Rate of trypanosome killing by lectins in midguts of different species and strains of Glossina. Med. Vet. Entomol. 3, 77-82. doi: 10.1111/j.1365-2915.1989.tb00477.x
62. Welburn, S. C., Maudlin, I., and Molyneux, D. H. (1994). Midgut lectin activity and sugar specificity in teneral and fed tsetse. Med. Vet. Entomol. 8, 81-87. doi: 10.1111/j.1365-2915.1994.tb00391.x
63. Wigglesworth, V. B. (1929). Digestion in the tsetse-fly: a study of structure and function. Parasitology 21, 288. doi: 10.1017/S0031182000022988
64. Wijers, D. J. (1958). Factors that may influence the infection rate of Glossina palpalis with Trypanosoma gambiense. I. The age of the fly at the time of the infected feed. Ann. Trop. Med. Parasitol. 52, 385-390.
65. Wijers, D. J., and Willett, K. C. (1960). Factors that may influence the infection rate of Glossina palpalis with Trypanosoma gambiense. II. The number and morphology of the trypanosomes present in the blood of the host at the time of the infected feed. Ann. Trop. Med. Parasitol. 54, 341-350.