Host-Toxin Interactions Involving EspC and Pet, Two Serine Protease Autotransporters of the Enterobacteriaceae

Overview

Journal Toxins (Basel)

Publisher MDPI

Specialty Toxicology

Date 2011 Jan 19

PMID 21243083

Citations 15

Authors

Fernando Navarro-Garcia

Michael Sonnested

Ken Teter

Affiliations

Soon will be listed here.

Abstract

EspC and Pet are toxins secreted by the diarrheagenic enteropathogenic and enteroaggregative Escherichia coli pathotypes, respectively. Both toxins have a molecular mass around 110 kDa and belong to the same protein family called Serine Protease Autotransporters of the Enterobacteriaceae (SPATE). Furthermore, both toxins act within the cytosol of intoxicated epithelial cells to disrupt the architecture of the actin cytoskeleton. This cytopathic and enterotoxic effect results from toxin cleavage of the actin-binding protein fodrin, although the two toxins recognize different cleavage sites on fodrin. EspC and Pet also have dramatically different mechanisms of entering the target cell which appear dependent upon the E. coli pathotype. In this review, we compare/contrast EspC and Pet in regards to their mode of delivery into the target cell, their effects on fodrin and the actin cytoskeleton, and their possible effects on the physiology of the intestinal epithelial cell.

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References

Betancourt-Sanchez M, Navarro-Garcia F . Pet secretion, internalization and induction of cell death during infection of epithelial cells by enteroaggregative Escherichia coli. Microbiology (Reading). 2009; 155(Pt 9):2895-2906. DOI: 10.1099/mic.0.029116-0. View

Dutta P, Cappello R, Navarro-Garcia F, Nataro J . Functional comparison of serine protease autotransporters of enterobacteriaceae. Infect Immun. 2002; 70(12):7105-13. PMC: 133081. DOI: 10.1128/IAI.70.12.7105-7113.2002. View

Yen Y, Kostakioti M, Henderson I, Stathopoulos C . Common themes and variations in serine protease autotransporters. Trends Microbiol. 2008; 16(8):370-9. DOI: 10.1016/j.tim.2008.05.003. View

Navarro-Garcia F, Canizalez-Roman A, Vidal J, Salazar M . Intoxication of epithelial cells by plasmid-encoded toxin requires clathrin-mediated endocytosis. Microbiology (Reading). 2007; 153(Pt 9):2828-2838. DOI: 10.1099/mic.0.2007/007088-0. View

Harris A, Morrow J . Calmodulin and calcium-dependent protease I coordinately regulate the interaction of fodrin with actin. Proc Natl Acad Sci U S A. 1990; 87(8):3009-13. PMC: 53823. DOI: 10.1073/pnas.87.8.3009. View

Vial P, Robins-Browne R, Lior H, Prado V, Kaper J, Nataro J . Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988; 158(1):70-9. DOI: 10.1093/infdis/158.1.70. View

Henderson I, Navarro-Garcia F, Desvaux M, Fernandez R, AlaAldeen D . Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev. 2004; 68(4):692-744. PMC: 539010. DOI: 10.1128/MMBR.68.4.692-744.2004. View

Ruiz-Perez F, Henderson I, Leyton D, Rossiter A, Zhang Y, Nataro J . Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol. 2009; 191(21):6571-83. PMC: 2795308. DOI: 10.1128/JB.00754-09. View

Navarro-Garcia F, Sears C, Eslava C, Cravioto A, Nataro J . Cytoskeletal effects induced by pet, the serine protease enterotoxin of enteroaggregative Escherichia coli. Infect Immun. 1999; 67(5):2184-92. PMC: 115956. DOI: 10.1128/IAI.67.5.2184-2192.1999. View

10.

Chakrabarti A, Kelkar D, Chattopadhyay A . Spectrin organization and dynamics: new insights. Biosci Rep. 2006; 26(6):369-86. DOI: 10.1007/s10540-006-9024-x. View

11.

Pande A, Moe D, Jamnadas M, Tatulian S, Teter K . The pertussis toxin S1 subunit is a thermally unstable protein susceptible to degradation by the 20S proteasome. Biochemistry. 2006; 45(46):13734-40. PMC: 2518456. DOI: 10.1021/bi061175+. View

12.

Eslava C, Navarro-Garcia F, Czeczulin J, Henderson I, Cravioto A, Nataro J . Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun. 1998; 66(7):3155-63. PMC: 108327. DOI: 10.1128/IAI.66.7.3155-3163.1998. View

13.

Henderson I, Czeczulin J, Eslava C, Noriega F, Nataro J . Characterization of pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun. 1999; 67(11):5587-96. PMC: 96930. DOI: 10.1128/IAI.67.11.5587-5596.1999. View

14.

Nath R, Raser K, Stafford D, Hajimohammadreza I, Posner A, Allen H . Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem J. 1996; 319 ( Pt 3):683-90. PMC: 1217843. DOI: 10.1042/bj3190683. View

15.

Elliott S, Sperandio V, Giron J, Shin S, Mellies J, Wainwright L . The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun. 2000; 68(11):6115-26. PMC: 97688. DOI: 10.1128/IAI.68.11.6115-6126.2000. View

16.

Moreira C, Carneiro S, Nataro J, Trabulsi L, Elias W . Role of type I fimbriae in the aggregative adhesion pattern of enteroaggregative Escherichia coli. FEMS Microbiol Lett. 2003; 226(1):79-85. DOI: 10.1016/S0378-1097(03)00561-5. View

17.

Pande A, Scaglione P, Taylor M, Nemec K, Tuthill S, Moe D . Conformational instability of the cholera toxin A1 polypeptide. J Mol Biol. 2007; 374(4):1114-28. PMC: 2175082. DOI: 10.1016/j.jmb.2007.10.025. View

18.

Dautin N, Bernstein H . Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol. 2007; 61:89-112. DOI: 10.1146/annurev.micro.61.080706.093233. View

19.

Lord J, Roberts L, Lencer W . Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: co-opting basic mechanisms of endoplasmic reticulum-associated degradation. Curr Top Microbiol Immunol. 2006; 300:149-68. DOI: 10.1007/3-540-28007-3_7. View

20.

Kizhatil K, Yoon W, Mohler P, Davis L, Hoffman J, Bennett V . Ankyrin-G and beta2-spectrin collaborate in biogenesis of lateral membrane of human bronchial epithelial cells. J Biol Chem. 2006; 282(3):2029-37. DOI: 10.1074/jbc.M608921200. View