#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Social Motility of African Trypanosomes Is a Property of a Distinct Life-Cycle Stage That Occurs Early in Tsetse Fly Transmission


African trypanosomes, single-celled parasites that cause human sleeping sickness and Nagana in animals, are transmitted by tsetse flies. Bloodstream form trypanosomes ingested by tsetse differentiate into procyclic forms in the midgut lumen of the insect. Successful transmission to a new mammalian host requires at least two migrations within the fly: one from the midgut lumen to the ectoperitrophic space, and a subsequent migration from the ectoperitrophic space to the salivary glands. Procyclic forms can exhibit social motility, a form of coordinated movement, on semi-solid surfaces. While social motility in bacteria is linked to virulence, the biological significance for trypanosomes is unknown. We demonstrate that social motility is a property of early procyclic forms, which are equivalent to the forms present during the first week of fly infection. In contrast, late procyclic forms characteristic for established infections are deficient for social motility. Our findings link social motility to a biological process, confirm that early and late procyclic forms are distinct life-cycle stages and imply that genes essential for social motility will be of key importance in fly transmission. We suggest that using the social motility assay as a surrogate for fly experiments should enable many more laboratories to examine this aspect of parasite transmission.


Vyšlo v časopise: Social Motility of African Trypanosomes Is a Property of a Distinct Life-Cycle Stage That Occurs Early in Tsetse Fly Transmission. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004493
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004493

Souhrn

African trypanosomes, single-celled parasites that cause human sleeping sickness and Nagana in animals, are transmitted by tsetse flies. Bloodstream form trypanosomes ingested by tsetse differentiate into procyclic forms in the midgut lumen of the insect. Successful transmission to a new mammalian host requires at least two migrations within the fly: one from the midgut lumen to the ectoperitrophic space, and a subsequent migration from the ectoperitrophic space to the salivary glands. Procyclic forms can exhibit social motility, a form of coordinated movement, on semi-solid surfaces. While social motility in bacteria is linked to virulence, the biological significance for trypanosomes is unknown. We demonstrate that social motility is a property of early procyclic forms, which are equivalent to the forms present during the first week of fly infection. In contrast, late procyclic forms characteristic for established infections are deficient for social motility. Our findings link social motility to a biological process, confirm that early and late procyclic forms are distinct life-cycle stages and imply that genes essential for social motility will be of key importance in fly transmission. We suggest that using the social motility assay as a surrogate for fly experiments should enable many more laboratories to examine this aspect of parasite transmission.


Zdroje

1. SchwedeA, CarringtonM (2010) Bloodstream form Trypanosome plasma membrane proteins: antigenic variation and invariant antigens. Parasitology 137: 2029–2039.

2. ReunerB, VassellaE, YutzyB, BoshartM (1997) Cell density triggers slender to stumpy differentiation of Trypanosoma brucei bloodstream forms in culture. Molecular and biochemical parasitology 90: 269–280.

3. VassellaE, ReunerB, YutzyB, BoshartM (1997) Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. Journal of cell science 110 (Pt 21): 2661–2671.

4. VassellaE, Den AbbeeleJV, ButikoferP, RenggliCK, FurgerA, et al. (2000) A major surface glycoprotein of Trypanosoma brucei is expressed transiently during development and can be regulated post-transcriptionally by glycerol or hypoxia. Genes Dev 14: 615–626.

5. GibsonW, BaileyM (2003) The development of Trypanosoma brucei within the tsetse fly midgut observed using green fluorescent trypanosomes. Kinetoplastid Biol Dis 2: 1.

6. VassellaE, OberleM, UrwylerS, RenggliCK, StuderE, et al. (2009) Major surface glycoproteins of insect forms of Trypanosoma brucei are not essential for cyclical transmission by tsetse. PLoS One 4: e4493.

7. KnüselS, RoditiI (2013) Insights into the regulation of GPEET procyclin during differentiation from early to late procyclic forms of Trypanosoma brucei. Molecular and biochemical parasitology 191: 66–74.

8. RoditiI, FurgerA, RueppS, SchurchN, ButikoferP (1998) Unravelling the procyclin coat of Trypanosoma brucei. Molecular and biochemical parasitology 91: 117–130.

9. MorrisJC, WangZ, DrewME, EnglundPT (2002) Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. The EMBO journal 21: 4429–4438.

10. VassellaE, ProbstM, SchneiderA, StuderE, RenggliCK, et al. (2004) Expression of a major surface protein of Trypanosoma brucei insect forms is controlled by the activity of mitochondrial enzymes. Molecular biology of the cell 15: 3986–3993.

11. OberleM, BalmerO, BrunR, RoditiI (2010) Bottlenecks and the maintenance of minor genotypes during the life cycle of Trypanosoma brucei. PLoS pathogens 6: e1001023.

12. ShapiroJA (1998) Thinking about bacterial populations as multicellular organisms. Annual review of microbiology 52: 81–104.

13. FraserGM, HughesC (1999) Swarming motility. Current opinion in microbiology 2: 630–635.

14. HarsheyRM (2003) Bacterial motility on a surface: many ways to a common goal. Annual review of microbiology 57: 249–273.

15. BasslerBL, LosickR (2006) Bacterially speaking. Cell 125: 237–246.

16. BlankenshipJR, MitchellAP (2006) How to build a biofilm: a fungal perspective. Current opinion in microbiology 9: 588–594.

17. FirtelRA, MeiliR (2000) Dictyostelium: a model for regulated cell movement during morphogenesis. Current opinion in genetics & development 10: 421–427.

18. ShaulskyG, KessinRH (2007) The cold war of the social amoebae. Current biology: CB 17: R684–692.

19. LopezMA, NguyenHT, OberholzerM, HillKL (2011) Social parasites. Current opinion in microbiology 14: 642–648.

20. OberholzerM, LopezMA, McLellandBT, HillKL (2010) Social motility in African trypanosomes. PLoS Pathog 6: e1000739.

21. FreireER, VashishtAA, MalvezziAM, ZuberekJ, LangousisG, et al. (2014) eIF4F-like complexes formed by cap-binding homolog TbEIF4E5 with TbEIF4G1 or TbEIF4G2 are implicated in post-transcriptional regulation in Trypanosoma brucei. RNA

22. VassellaE, ProbstM, SchneiderA, StuderE, RenggliCK, et al. (2004) Expression of a major surface protein of Trypanosoma brucei insect forms is controlled by the activity of mitochondrial enzymes. Mol Biol Cell 15: 3986–3993.

23. Schumann BurkardG, KaserS, de AraujoPR, SchimanskiB, NaguleswaranA, et al. (2013) Nucleolar proteins regulate stage-specific gene expression and ribosomal RNA maturation in Trypanosoma brucei. Molecular microbiology 88: 827–840.

24. UrwylerS, VassellaE, Van Den AbbeeleJ, RenggliCK, BlundellP, et al. (2005) Expression of procyclin mRNAs during cyclical transmission of Trypanosoma brucei. PLoS Pathog 1: e22.

25. MorandS, RenggliCK, RoditiI, VassellaE (2012) MAP kinase kinase 1 (MKK1) is essential for transmission of Trypanosoma brucei by Glossina morsitans. Mol Biochem Parasitol 186: 73–76.

26. FragosoCM, Schumann BurkardG, OberleM, RenggliCK, HilzingerK, et al. (2009) PSSA-2, a membrane-spanning phosphoprotein of Trypanosoma brucei, is required for efficient maturation of infection. PLoS One 4: e7074.

27. NudlemanE, WallD, KaiserD (2005) Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309: 125–127.

28. VassellaE, ButikoferP, EngstlerM, JelkJ, RoditiI (2003) Procyclin null mutants of Trypanosoma brucei express free glycosylphosphatidylinositols on their surface. Molecular biology of the cell 14: 1308–1318.

29. EmmerBT, DanielsMD, TaylorJM, EptingCL, EngmanDM (2010) Calflagin inhibition prolongs host survival and suppresses parasitemia in Trypanosoma brucei infection. Eukaryot Cell 9: 934–942.

30. KolevNG, Ramey-ButlerK, CrossGA, UlluE, TschudiC (2012) Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein. Science 338: 1352–1353.

31. RotureauB, SubotaI, BuissonJ, BastinP (2012) A new asymmetric division contributes to the continuous production of infective trypanosomes in the tsetse fly. Development 139: 1842–1850.

32. Acosta-SerranoA, VassellaE, LinigerM, Kunz RenggliC, BrunR, et al. (2001) The surface coat of procyclic Trypanosoma brucei: programmed expression and proteolytic cleavage of procyclin in the tsetse fly. Proc Natl Acad Sci U S A 98: 1513–1518.

33. SchlaeppiAC, MalherbeT, BütikoferP (2003) Coordinate expression of GPEET procyclin and its membrane-associated kinase in Trypanosoma brucei procyclic forms. The Journal of biological chemistry 278: 49980–49987.

34. BütikoferP, VassellaE, BoschungM, RenggliCK, BrunR, et al. (2002) Glycosylphosphatidylinositol-anchored surface molecules of Trypanosoma congolense insect forms are developmentally regulated in the tsetse fly. Molecular and biochemical parasitology 119: 7–16.

35. UtzS, RoditiI, Kunz RenggliC, AlmeidaIC, Acosta-SerranoA, et al. (2006) Trypanosoma congolense procyclins: unmasking cryptic major surface glycoproteins in procyclic forms. Eukaryotic cell 5: 1430–1440.

36. 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 (Pt 5): 469–478.

37. StevensJR, Mathieu-DaudeF, McNamaraJJ, MizenVH, NzilaA (1994) Mixed populations of Trypanosoma brucei in wild Glossina palpalis palpalis. Tropical medicine and parasitology: official organ of Deutsche Tropenmedizinische Gesellschaft and of Deutsche Gesellschaft fur Technische Zusammenarbeit 45: 313–318.

38. MacLeodA, TurnerCM, TaitA (1999) A high level of mixed Trypanosoma brucei infections in tsetse flies detected by three hypervariable minisatellites. Molecular and biochemical parasitology 102: 237–248.

39. DelauwMF, PaysE, SteinertM, AertsD, Van MeirvenneN, et al. (1985) Inactivation and reactivation of a variant-specific antigen gene in cyclically transmitted Trypanosoma brucei. EMBO J 4: 989–993.

40. Le RayD, BarryJD, EastonC, VickermanK (1977) First tsetse fly transmission of the “AnTat” serodeme of Trypanosoma brucei. Ann Soc Belg Med Trop 57: 369–381.

41. BrunR, Schonenberger (1979) Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop 36: 289–292.

42. RueppS, FurgerA, KurathU, RenggliCK, HemphillA, et al. (1997) Survival of Trypanosoma brucei in the tsetse fly is enhanced by the expression of specific forms of procyclin. J Cell Biol 137: 1369–1379.

43. ChomczynskiP, SacchiN (1987) Single-step RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anan Biochem 162: 156–159.

44. BrunR, SchonenbergerM (1981) Stimulating effect of citrate and cis-Aconitate on the transformation of Trypanosoma brucei bloodstream forms to procyclic forms in vitro. Z Parasitenkd 66: 17–24.

45. RichardsonJP, BeecroftRP, TolsonDL, LiuMK, PearsonTW (1988) Procyclin: an unusual immunodominant glycoprotein surface antigen from the procyclic stage of African trypanosomes. Mol Biochem Parasitol 31: 203–216.

46. GunasekeraK, WüthrichD, Braga-LagacheS, HellerM, OchsenreiterT (2012) Proteome remodelling during development from blood to insect-form Trypanosoma brucei quantified by SILAC and mass spectrometry. BMC Genomics 13: 556.

47. FlückC, SalomoneJY, KurathU, RoditiI (2003) Cycloheximide-mediated accumulation of transcripts from a procyclin expression site depends on the intergenic region. Mol Biochem Parasitol 127: 93–97.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#