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Tsetse EP Protein Protects the Fly Midgut from Trypanosome Establishment


African trypanosomes undergo a complex developmental process in their tsetse fly vector before transmission back to a vertebrate host. Typically, 90% of fly infections fail, most during initial establishment of the parasite in the fly midgut. The specific mechanism(s) underpinning this failure are unknown. We have previously shown that a Glossina-specific, immunoresponsive molecule, tsetse EP protein, is up regulated by the fly in response to gram-negative microbial challenge. Here we show by knockdown using RNA interference that this tsetse EP protein acts as a powerful antagonist of establishment in the fly midgut for both Trypanosoma brucei brucei and T. congolense. We demonstrate that this phenomenon exists in two species of tsetse, Glossina morsitans morsitans and G. palpalis palpalis, suggesting tsetse EP protein may be a major determinant of vector competence in all Glossina species. Tsetse EP protein levels also decline in response to starvation of the fly, providing a possible explanation for increased susceptibility of starved flies to trypanosome infection. As starvation is a common field event, this fact may be of considerable importance in the epidemiology of African trypanosomiasis.


Vyšlo v časopise: Tsetse EP Protein Protects the Fly Midgut from Trypanosome Establishment. PLoS Pathog 6(3): e32767. doi:10.1371/journal.ppat.1000793
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000793

Souhrn

African trypanosomes undergo a complex developmental process in their tsetse fly vector before transmission back to a vertebrate host. Typically, 90% of fly infections fail, most during initial establishment of the parasite in the fly midgut. The specific mechanism(s) underpinning this failure are unknown. We have previously shown that a Glossina-specific, immunoresponsive molecule, tsetse EP protein, is up regulated by the fly in response to gram-negative microbial challenge. Here we show by knockdown using RNA interference that this tsetse EP protein acts as a powerful antagonist of establishment in the fly midgut for both Trypanosoma brucei brucei and T. congolense. We demonstrate that this phenomenon exists in two species of tsetse, Glossina morsitans morsitans and G. palpalis palpalis, suggesting tsetse EP protein may be a major determinant of vector competence in all Glossina species. Tsetse EP protein levels also decline in response to starvation of the fly, providing a possible explanation for increased susceptibility of starved flies to trypanosome infection. As starvation is a common field event, this fact may be of considerable importance in the epidemiology of African trypanosomiasis.


Zdroje

1. PepinJ

MedaHA

2001 The epidemiology and control of human African trypanosomiasis. Advances in Parasitology 49 71 132

2. HurseyBS

2001 The programme against African trypanosomiasis: aims, objectives and achievements. Trends in Parasitology 17 2 3

3. BuddLT

1999 DFID-funded tsetse and trypanosomiasis research and development since 1980 (V. 2. Economic analysis). London Department for International Development

4. KabayoJP

2002 Aiming to eliminate tsetse from Africa. Trends in Parasitology 18 473 475

5. AksoyS

GibsonWC

LehaneMJ

2003 Interactions between tsetse and trypanosomes with implications for the control of trypanosomiasis. Advances in Parasitology 53 1 83

6. Van den AbbeeleJ

ClaesY

van BockstaeleD

Le RayD

CoosemansM

1999 Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118 469 478

7. GibsonW

BaileyM

2003 The development of Trypanosoma brucei within the tsetse fly midgut observed using green fluorescent trypanosomes. Kinetoplastid Biology and Disease 2 1

8. HaoZ

KasumbaI

LehaneMJ

GibsonWC

KwonJ

2001 Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Proceedings of the National Academy of Sciences USA 98 12648 12653

9. WelburnSC

MaudlinI

EllisDS

1989 Rate of trypanosome killing by lectins in midguts of different species and strains of Glossina. Medical and Veterinary Entomology 3 77 82

10. MaudlinI

WelburnSC

1987 Lectin mediated establishment of midgut infections of Trypanosoma congolense and Trypanosoma brucei in Glossina morsitans. Tropical Medicine and Parasitology 38 167 170

11. AbubakarLU

BulimoWD

MulaaFJ

OsirEO

2006 Molecular characterization of a tsetse fly midgut proteolytic lectin that mediates differentiation of African trypanosomes. Insect Biochemistry And Molecular Biology 36 344 352

12. MacleodET

MaudlinI

DarbyAC

WelburnSC

2007 Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology 1 5

13. RoditiI

LehaneMJ

2008 Interactions between trypanosomes and tsetse flies. Current Opinion in Microbiology 11 345 351

14. VassellaE

Acosta-SerranoA

StuderE

LeeSH

EnglundPT

2001 Multiple procyclin isoforms are expressed differentially during the development of insect forms of Trypanosoma brucei. Journal of Molecular Biology 312 597 607

15. HainesLR

JacksonAM

LehaneMJ

ThomasJM

YamaguchiAY

2005 Increased expression of unusual EP repeat-containing proteins in the midgut of the tsetse fly (Glossina) after bacterial challenge. Insect Biochemistry And Molecular Biology 35 413 423

16. HuCY

AksoyS

2006 Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans. Molecular Microbiology 60 1194 1204

17. ChandraM

LinigerM

TetleyL

RoditiI

BarryJD

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 Biochemistry And Molecular Biology 34 1163 1173

18. BendtsenJ

NielsenH

von HeijneG

BrunakS

2004 Improved prediction of signal peptides. SignalP 3.0. Journal of Molecular Biology 340 783 785

19. HaddowJD

HainesLR

GoodingRH

OlafsonRW

PearsonTW

2005 Identification of midgut proteins that are differentially expressed in trypanosome-susceptible and normal tsetse flies (Glossina morsitans morsitans). Insect Biochemistry And Molecular Biology 35 425 433

20. GygiS

RochonY

FranzaB

AebersoldR

1999 Correlation between protein and mRNA abundance in yeast. Molecular & Cellular Biology 19 1720 1730

21. HamiltonJV

MunksRJL

LehaneSM

LehaneMJ

2002 Association of midgut defensin with a novel serine protease in the blood-sucking fly Stomoxys calcitrans. Insect Molecular Biology 11 197 205

22. WalsheDP

LehaneSM

LehaneMJ

HainesLR

2009 Prolonged gene knockdown in the tsetse fly Glossina by feeding double stranded RNA. Insect Molecular Biology 18 11 19

23. MedemaR

2004 Optimizing RNA interference for application in mammalian cells. Biochemical Journal 380 595 603

24. LemaitreB

HoffmannJ

2007 The host defense of Drosophila melanogaster. Annual Review of Immunology 25 697 743

25. MeisterS

KanzokS

ZhengX

LunaC

LiT

2005 Immune signalling pathways regulating bacterial and parasite infection of the mosquito Anopheles gambiae. Proceedings Of The National Academy Of Sciences Of The United States Of America 102 11420 11425

26. ButikoferP

RueppS

BoschungM

RoditiI

1997 ‘GPEET’ procyclin is the major surface protein of procyclic culture forms of Trypanosoma brucei brucei strain 427. Biochemical Journal 326 415 423

27. PearsonTW

BeecroftRP

WelburnSC

RueppS

RoditiI

2000 The major cell surface glycoprotein procyclin is a receptor for induction of a novel form of cell death in African trypanosomes in vitro. Molecular and Biochemical Parasitology 111 333 349

28. UtzS

RoditiI

RenggliCK

AlmeidaIC

Acosta-SerranoA

2006 Trypanosoma congolense procyclins: Unmasking cryptic major surface glycoproteins in procyclic forms. Eukaryotic Cell 5 1430 1440

29. WoolhouseMEJ

HargroveJW

1998 On the interpretation of age-prevalence curves for trypanosome infections of tsetse flies. Parasitology 116 149 156

30. MsangiAR

WhitakerCJ

LehaneMJ

1998 Factors influencing the prevalence of trypanosome infection of Glossina pallidipes on the Ruvu flood plain of Eastern Tanzania. Acta Tropica 70 143 155

31. GingrichJB

WardRA

MackenLM

EsserKM

1982 African sleeping sickness: new evidence that mature tsetse flies (Glossina morsitans) can become potent vectors. Transactions of the Royal Society of Tropical Medicine and Hygiene 76 479 481

32. MakumyaviriAM

DemeyF

ClaesY

VerhulstA

Le RayD

1984 Caracterisation de la capacite vectorielle de Glossina morsitans morsitans (Diptera: Glossinidae) vis a vis de Trypanosoma brucei brucei EATRO 1125 (AnTAR 1). Annals de la Societe Belge de Medicine Tropicale 64 365 372

33. KubiC

van den AbbeeleJ

RDED

MarcottyT

DornyP

2006 The effect of starvation on the susceptibility of teneral and non-teneral tsetse flies to trypanosome infection. Medical and Veterinary Entomology 20 388 392

34. GibsonWC

1989 Analysis of a genetic cross between Trypanosoma brucei rhodesiense and T. b. brucei. Parasitology 99 391 402

35. LehaneMJ

AksoyS

GibsonW

KerhornouA

BerrimanM

2003 Adult midgut expressed sequence tags from the tsetse fly Glossina morsitans morsitans and expression analysis of putative immune response genes. Genome Biology 4 art. no.-R63

36. BeecroftRP

RoditiI

PearsonTW

1993 Identification and characterization of an acidic major surface glycoprotein from procyclic stage Trypanosoma congolense. Molecular And Biochemical Parasitology 61 285 294

37. RichardsonJP

BeecroftRP

TolsonDL

LiuMK

PearsonTW

1988 Procyclin - an unusual immunodominant glycoprotein surface-antigen from the procyclic stage of African trypanosomes. Molecular And Biochemical Parasitology 31 203 216

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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