Heat Shock Protein 90 Regulates Encystation in Entamoeba

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2015 Nov 4

PMID 26528271

Citations 13

Authors

Meetali Singh

Shalini Sharma

Alok Bhattacharya

Utpal Tatu

Affiliations

Soon will be listed here.

Abstract

Enteric protozoan Entamoeba histolytica is a major cause of debilitating diarrheal infection worldwide with high morbidity and mortality. Even though the clinical burden of this parasite is very high, this infection is categorized as a neglected disease. Parasite is transmitted through feco-oral route and exhibit two distinct stages namely - trophozoites and cysts. Mechanism and regulation of encystation is not clearly understood. Previous studies have established the role of Heat shock protein 90 (Hsp90) in regulating stage transition in various protozoan parasites like Giardia, Plasmodium, Leishmania, and Toxoplasma. Our study for the first time reports that Hsp90 plays a crucial role in life cycle of Entamoeba as well. We identify Hsp90 to be a negative regulator of encystation in Entamoeba. We also show that Hsp90 inhibition interferes with the process of phagocytosis in Entamoeba. Overall, we show that Hsp90 plays an important role in virulence and transmission of Entamoeba.

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References

Keestra A, Winter M, Auburger J, Frassle S, Xavier M, Winter S . Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature. 2013; 496(7444):233-7. PMC: 3625479. DOI: 10.1038/nature12025. View

Graefe S, Wiesgigl M, Gaworski I, MacDonald A, Clos J . Inhibition of HSP90 in Trypanosoma cruzi induces a stress response but no stage differentiation. Eukaryot Cell. 2002; 1(6):936-43. PMC: 138760. DOI: 10.1128/EC.1.6.936-943.2002. View

De Cadiz A, Jeelani G, Nakada-Tsukui K, Caler E, Nozaki T . Transcriptome analysis of encystation in Entamoeba invadens. PLoS One. 2013; 8(9):e74840. PMC: 3770568. DOI: 10.1371/journal.pone.0074840. View

Aguilar-Diaz H, Carrero J, Arguello-Garcia R, Laclette J, Morales-Montor J . Cyst and encystment in protozoan parasites: optimal targets for new life-cycle interrupting strategies?. Trends Parasitol. 2011; 27(10):450-8. DOI: 10.1016/j.pt.2011.06.003. View

Ehrenkaufer G, Weedall G, Williams D, Lorenzi H, Caler E, Hall N . The genome and transcriptome of the enteric parasite Entamoeba invadens, a model for encystation. Genome Biol. 2013; 14(7):R77. PMC: 4053983. DOI: 10.1186/gb-2013-14-7-r77. View

Taiyab A, Rao C . HSP90 modulates actin dynamics: inhibition of HSP90 leads to decreased cell motility and impairs invasion. Biochim Biophys Acta. 2010; 1813(1):213-21. DOI: 10.1016/j.bbamcr.2010.09.012. View

Rochani A, Mithra C, Singh M, Tatu U . Heat shock protein 90 as a potential drug target against surra. Parasitology. 2014; 141(9):1148-55. DOI: 10.1017/S0031182014000845. View

Pearl L, Prodromou C . Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem. 2006; 75:271-94. DOI: 10.1146/annurev.biochem.75.103004.142738. View

Cowen L, Singh S, Kohler J, Collins C, Zaas A, Schell W . Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci U S A. 2009; 106(8):2818-23. PMC: 2650349. DOI: 10.1073/pnas.0813394106. View

10.

Bracha R, Mirelman D . Virulence of Entamoeba histolytica trophozoites. Effects of bacteria, microaerobic conditions, and metronidazole. J Exp Med. 1984; 160(2):353-68. PMC: 2187461. DOI: 10.1084/jem.160.2.353. View

11.

Singh M, Shah V, Tatu U . A novel C-terminal homologue of Aha1 co-chaperone binds to heat shock protein 90 and stimulates its ATPase activity in Entamoeba histolytica. J Mol Biol. 2014; 426(8):1786-98. DOI: 10.1016/j.jmb.2014.01.008. View

12.

Mi-Ichi F, Miyamoto T, Takao S, Jeelani G, Hashimoto T, Hara H . Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis. Proc Natl Acad Sci U S A. 2015; 112(22):E2884-90. PMC: 4460517. DOI: 10.1073/pnas.1423718112. View

13.

Bailey G, Rengypian S . Osmotic stress as a factor controlling encystation of Entamoeba invadens. Arch Invest Med (Mex). 1980; 11(1 Suppl):11-6. View

14.

. Induction of encystation of Entamoeba invadens by removal of glucose from the culture medium. J Parasitol. 1984; 70(5):629-33. View

15.

Bozza G, Capitani M, Montanari P, Benucci B, Biancucci M, Nardi-Dei V . Role of ARF6, Rab11 and external Hsp90 in the trafficking and recycling of recombinant-soluble Neisseria meningitidis adhesin A (rNadA) in human epithelial cells. PLoS One. 2014; 9(10):e110047. PMC: 4210143. DOI: 10.1371/journal.pone.0110047. View

16.

Yan L, Cerny R, Cirillo J . Evidence that hsp90 is involved in the altered interactions of Acanthamoeba castellanii variants with bacteria. Eukaryot Cell. 2004; 3(3):567-78. PMC: 420136. DOI: 10.1128/EC.3.3.567-578.2004. View

17.

Somlata , Kamanna S, Agrahari M, Babuta M, Bhattacharya S, Bhattacharya A . Autophosphorylation of Ser428 of EhC2PK plays a critical role in regulating erythrophagocytosis in the parasite Entamoeba histolytica. J Biol Chem. 2012; 287(14):10844-52. PMC: 3322815. DOI: 10.1074/jbc.M111.308874. View

18.

Johnson J, Brown C . Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress Chaperones. 2008; 14(1):83-94. PMC: 2673905. DOI: 10.1007/s12192-008-0058-9. View

19.

Wiesgigl M, Clos J . Heat shock protein 90 homeostasis controls stage differentiation in Leishmania donovani. Mol Biol Cell. 2001; 12(11):3307-16. PMC: 60256. DOI: 10.1091/mbc.12.11.3307. View

20.

DIAMOND L, Harlow D, Cunnick C . A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans R Soc Trop Med Hyg. 1978; 72(4):431-2. DOI: 10.1016/0035-9203(78)90144-x. View