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Chapter 18 : Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis

Authors: Charles L. Larson1, Jeffrey E. Christensen2, Sophia A. Pacheco3, Scott A. Minnich4, Michael E. Konkel5
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Affiliations: 1: School of Molecular Biosciences, Washington State University, Pullman, WA 99164-4234; 2: School of Molecular Biosciences, Washington State University, Pullman, WA 99164-4234; 3: School of Molecular Biosciences, Washington State University, Pullman, WA 99164-4234; 4: Department of Microbiology, Molecular Biology and Biochemistry, Life Science South 146, P.O. Box 443052, University of Idaho, Moscow, ID 83844–3052; 5: School of Molecular Biosciences, Washington State University, Pullman, WA 99164-4234
Content Type: Monograph
Publication Year: 2008

Category: Bacterial Pathogenesis

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Abstract:

This chapter is divided into three major sections. In the first section, a model of -mediated enteritis is presented. The second section presents a general overview of the organism's pathogenic mechanisms and virulence determinants. Finally, in the third section, various aspects of -host cell invasion and protein secretion are discussed. Specifically, in the third section protein export via the flagellar type III secretion system (T3SS), the development of an assay to identify secreted proteins, the evolutionary relatedness of the flagellum and virulence T3SS, and the putative roles of secreted proteins in disease, are discussed. Although much remains unknown regarding the identity and functional characteristics of the proteins exported via the flagellar apparatus, the chapter highlights evidence supporting the proposal that these proteins contribute to -mediated enteritis. Motility, adherence, invasion, protein secretion, intracellular survival, and toxin production may contribute to the pathogenicity of a given strain. nonmotile strain can be either secretion positive (i.e., the mutant) or secretion negative (i.e., the mutant), and the ability of the bacterium to secrete proteins can result in an increase in its invasive potential. Although these data helped clarify the relationship between motility, secretion, and host cell invasion, the significance of protein secretion and host cell invasion in -mediated gastroenteritis was not known.

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18

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Campylobacter jejuni Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis
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Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
/content/10.1128/9781555815554.ch18.ch18fig01
Figure 1.
Model of pathogenesis. The clinical manifestation of infection is a result of bacterial activities (white box) and the host immune response (gray box). Dotted lines indicate processes that can potentiate infection.
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10.1128/9781555815554/f0316-01.gif
Image of Figure 1.
Figure 1.

Model of pathogenesis. The clinical manifestation of infection is a result of bacterial activities (white box) and the host immune response (gray box). Dotted lines indicate processes that can potentiate infection.

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
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/content/10.1128/9781555815554.ch18.ch18fig02
Figure 2.
Adherence, protein secretion, and invasion are a few of the virulence attributes that contribute to acute infection. As depicted, bacterial colonization of the intestinal tract can occur by different routes. Several virulence attributes may stimulate the host inflammatory response and in turn promote additional bacteria–host cell interactions. Other factors (not listed) are also capable of triggering the host inflammatory response. The dotted line represents the possibility that secreted proteins may enhance the cytokine response.
10.1128/9781555815554/f0317-01_thmb.gif
10.1128/9781555815554/f0317-01.gif
Image of Figure 2.
Figure 2.

Adherence, protein secretion, and invasion are a few of the virulence attributes that contribute to acute infection. As depicted, bacterial colonization of the intestinal tract can occur by different routes. Several virulence attributes may stimulate the host inflammatory response and in turn promote additional bacteria–host cell interactions. Other factors (not listed) are also capable of triggering the host inflammatory response. The dotted line represents the possibility that secreted proteins may enhance the cytokine response.

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
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Figure 3.
Secretion of the Cia proteins is dependent on an intact flagellar T3SS. Culture medium supplemented with fetal bovine serum (FBS) triggers secretion of the Cia proteins. were suspended in minimal essential medium, either with or without FBS, and radiolabeled with [S]-methionine for 3 h. Supernatant fluids were harvested, concentrated fourfold, and solubilized in double-strength sample buffer. Equal volumes of samples were separated in a sodium dodecyl sulfate 12.5% polyacrylamide gel. The gel was dried and analyzed by phosphorimaging (Molecular Dynamics, Inc., ImageQuant, Sunnyvale, CA). Lanes: 1, 81-176 (+) FBS; 2, 81-176 (−) FBS.
10.1128/9781555815554/f0322-01_thmb.gif
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Image of Figure 3.
Figure 3.

Secretion of the Cia proteins is dependent on an intact flagellar T3SS. Culture medium supplemented with fetal bovine serum (FBS) triggers secretion of the Cia proteins. were suspended in minimal essential medium, either with or without FBS, and radiolabeled with [S]-methionine for 3 h. Supernatant fluids were harvested, concentrated fourfold, and solubilized in double-strength sample buffer. Equal volumes of samples were separated in a sodium dodecyl sulfate 12.5% polyacrylamide gel. The gel was dried and analyzed by phosphorimaging (Molecular Dynamics, Inc., ImageQuant, Sunnyvale, CA). Lanes: 1, 81-176 (+) FBS; 2, 81-176 (−) FBS.

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
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Figure 4.
type III secretion system (T3SS) is the flagellum that secretes the secreted proteins (Csp). A subset of the Csps, termed the invasion antigens (Cia), are required for maximal invasion. Both the Csp and Cia proteins harbor nonconsensus secretion signals, which are required for export.
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10.1128/9781555815554/f0324-01.gif
Image of Figure 4.
Figure 4.

type III secretion system (T3SS) is the flagellum that secretes the secreted proteins (Csp). A subset of the Csps, termed the invasion antigens (Cia), are required for maximal invasion. Both the Csp and Cia proteins harbor nonconsensus secretion signals, which are required for export.

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
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/content/10.1128/9781555815554.ch18.ch18fig05
Figure 5.
Depiction of the pCSP50 shuttle vector and phospholipase indicator plate results for controls. The pCSP50 vector includes a cassette, a constitutive promoter , a 5′ truncated (lacking 150 nt encoding the native T3SS signal), and the gene (cognate chaperone). The NdeI and BglII sites facilitate directional cloning of sequences as fusions with the truncated . (A to E) Scans of phospholipase indicator plates under flagellar T3SS induction. (A) JB580v (wild type); (B) mutant; (C) mutant with pCSP50; (D) mutant with pCSP50: (E) mutant with pCSP50: . All strains show strong growth; (A) and (D) show strong secretion of YplA and CiaB:YplA fusion protein, respectively, resulting in a zone of precipitate due to hydrolysis of fatty acids by the phospholipase.
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Image of Figure 5.
Figure 5.

Depiction of the pCSP50 shuttle vector and phospholipase indicator plate results for controls. The pCSP50 vector includes a cassette, a constitutive promoter , a 5′ truncated (lacking 150 nt encoding the native T3SS signal), and the gene (cognate chaperone). The NdeI and BglII sites facilitate directional cloning of sequences as fusions with the truncated . (A to E) Scans of phospholipase indicator plates under flagellar T3SS induction. (A) JB580v (wild type); (B) mutant; (C) mutant with pCSP50; (D) mutant with pCSP50: (E) mutant with pCSP50: . All strains show strong growth; (A) and (D) show strong secretion of YplA and CiaB:YplA fusion protein, respectively, resulting in a zone of precipitate due to hydrolysis of fatty acids by the phospholipase.

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
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Figure 6.
Functional categories of secreted proteins. Shown are the numbers of proteins, categorized according to function, encoding signal sequences that elicited strong secretion from both the flagellar and Ysa T3SS.
10.1128/9781555815554/f0327-01_thmb.gif
10.1128/9781555815554/f0327-01.gif
Image of Figure 6.
Figure 6.

Functional categories of secreted proteins. Shown are the numbers of proteins, categorized according to function, encoding signal sequences that elicited strong secretion from both the flagellar and Ysa T3SS.

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
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Tables

Campylobacter jejuni Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis
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Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18
/content/10.1128/9781555815554.ch18.ch18tab01
Table 1.
Relative molecular mass of secreted proteins
Generic image for table
Table 1.

Relative molecular mass of secreted proteins

Citation: Larson C, Christensen J, Pacheco S, Minnich S, Konkel M. 2008. Secretes Proteins via the Flagellar Type III Secretion System That Contribute to Host Cell Invasion and Gastroenteritis, p 315-332. In Nachamkin I, Szymanski C, Blaser M (ed), , Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch18

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