The β1 Integrin Activates JNK Independent of CagA, and JNK Activation Is Required for Helicobacter pylori CagA+-induced Motility of Gastric Cancer Cells

The Helicobacter pylori CagA protein is translocated into gastric epithelial cells through a type IVsecretion system (TFSS), and published studies suggest CagA is critical for H. pylori-associated carcinogenesis. CagA is thought to be necessary and sufficient to induce the motogenic response observe...

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Published inThe Journal of biological chemistry Vol. 283; no. 20; pp. 13952 - 13963
Main Authors Snider, Jared L., Allison, Cody, Bellaire, Bryan H., Ferrero, Richard L., Cardelli, James A.
Format Journal Article
LanguageEnglish
Published Elsevier Inc 16.05.2008
American Society for Biochemistry and Molecular Biology
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Abstract The Helicobacter pylori CagA protein is translocated into gastric epithelial cells through a type IVsecretion system (TFSS), and published studies suggest CagA is critical for H. pylori-associated carcinogenesis. CagA is thought to be necessary and sufficient to induce the motogenic response observed in response to CagA+ strains, as CagA interacts with proteins involved in adhesion and motility. We report that H. pylori strain 60190 stimulated AGS cell motility through a CagA- and TFSS-dependent mechanism, because strains 60190ΔcagA or 60190ΔcagE (TFSS-defective) did not increase motility. The JNK pathway is critical for H. pylori-dependent cell motility, as inhibition using SP600125 (JNK1/2/3 inhibitor) or a JNK2/3-specific inhibitor blocked motility. JNK mediates H. pylori-induced cell motility by activating paxillin, because JNK inhibition blocked paxillinTyr-118 phosphorylation, and paxillin expression knockdown completely abrogated bacteria-induced motility. Furthermore, JNK and paxillinTyr-118 were activated by 60190ΔcagA but not 60190ΔcagE, demonstrating CagA-independent signaling critical for cell motility. A β1 integrin-blocking antibody significantly inhibited JNK and paxillinTyr-118 phosphorylation and cell scattering, demonstrating that CagA-independent signaling required for cell motility occurs through β1. The requirement of both Src and focal adhesion kinase for signaling and motility further suggests the importance of integrin signaling in H. pylori-induced cell motility. Finally, we show that JNK activation occurs independent of known upstream kinases and signaling molecules, including Nod1, Cdc42, Rac1, MKK4, and MKK7, which demonstrates novel signaling leading to JNK activation. We report for the first time that H. pylori mediates CagA-independent signaling that promotes cell motility through the β1 integrin pathway.
AbstractList The Helicobacter pylori CagA protein is translocated into gastric epithelial cells through a type IV secretion system (TFSS), and published studies suggest CagA is critical for H. pylori-associated carcinogenesis. CagA is thought to be necessary and sufficient to induce the motogenic response observed in response to CagA⁺ strains, as CagA interacts with proteins involved in adhesion and motility. We report that H. pylori strain 60190 stimulated AGS cell motility through a CagA- and TFSS-dependent mechanism, because strains 60190ΔcagA or 60190ΔcagE (TFSS-defective) did not increase motility. The JNK pathway is critical for H. pylori-dependent cell motility, as inhibition using SP600125 (JNK1/2/3 inhibitor) or a JNK2/3-specific inhibitor blocked motility. JNK mediates H. pylori-induced cell motility by activating paxillin, because JNK inhibition blocked paxillinTyr⁻¹¹⁸ phosphorylation, and paxillin expression knockdown completely abrogated bacteria-induced motility. Furthermore, JNK and paxillinTyr⁻¹¹⁸ were activated by 60190ΔcagA but not 60190ΔcagE, demonstrating CagA-independent signaling critical for cell motility. A β₁ integrin-blocking antibody significantly inhibited JNK and paxillinTyr⁻¹¹⁸ phosphorylation and cell scattering, demonstrating that CagA-independent signaling required for cell motility occurs through β₁. The requirement of both Src and focal adhesion kinase for signaling and motility further suggests the importance of integrin signaling in H. pylori-induced cell motility. Finally, we show that JNK activation occurs independent of known upstream kinases and signaling molecules, including Nod1, Cdc42, Rac1, MKK4, and MKK7, which demonstrates novel signaling leading to JNK activation. We report for the first time that H. pylori mediates CagA-independent signaling that promotes cell motility through the β₁ integrin pathway.
The Helicobacter pylori CagA protein is translocated into gastric epithelial cells through a type IVsecretion system (TFSS), and published studies suggest CagA is critical for H. pylori-associated carcinogenesis. CagA is thought to be necessary and sufficient to induce the motogenic response observed in response to CagA+ strains, as CagA interacts with proteins involved in adhesion and motility. We report that H. pylori strain 60190 stimulated AGS cell motility through a CagA- and TFSS-dependent mechanism, because strains 60190ΔcagA or 60190ΔcagE (TFSS-defective) did not increase motility. The JNK pathway is critical for H. pylori-dependent cell motility, as inhibition using SP600125 (JNK1/2/3 inhibitor) or a JNK2/3-specific inhibitor blocked motility. JNK mediates H. pylori-induced cell motility by activating paxillin, because JNK inhibition blocked paxillinTyr-118 phosphorylation, and paxillin expression knockdown completely abrogated bacteria-induced motility. Furthermore, JNK and paxillinTyr-118 were activated by 60190ΔcagA but not 60190ΔcagE, demonstrating CagA-independent signaling critical for cell motility. A β1 integrin-blocking antibody significantly inhibited JNK and paxillinTyr-118 phosphorylation and cell scattering, demonstrating that CagA-independent signaling required for cell motility occurs through β1. The requirement of both Src and focal adhesion kinase for signaling and motility further suggests the importance of integrin signaling in H. pylori-induced cell motility. Finally, we show that JNK activation occurs independent of known upstream kinases and signaling molecules, including Nod1, Cdc42, Rac1, MKK4, and MKK7, which demonstrates novel signaling leading to JNK activation. We report for the first time that H. pylori mediates CagA-independent signaling that promotes cell motility through the β1 integrin pathway.
Author Cardelli, James A.
Allison, Cody
Snider, Jared L.
Ferrero, Richard L.
Bellaire, Bryan H.
Author_xml – sequence: 1
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  surname: Snider
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  organization: Department of Microbiology and Immunology and the Feist-Weiller Cancer Center, Louisiana State University Health Sciences Center, Shreveport, Louisiana 71130
– sequence: 2
  givenname: Cody
  surname: Allison
  fullname: Allison, Cody
  organization: Department of Microbiology, Monash University, Clayton 3800, Victoria, Australia
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  givenname: Bryan H.
  surname: Bellaire
  fullname: Bellaire, Bryan H.
  organization: Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University of Science and Technology, Ames, Iowa 50011-1240
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  givenname: Richard L.
  surname: Ferrero
  fullname: Ferrero, Richard L.
  organization: Department of Microbiology, Monash University, Clayton 3800, Victoria, Australia
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  givenname: James A.
  surname: Cardelli
  fullname: Cardelli, James A.
  email: jcarde@lsuhsc.edu
  organization: Department of Microbiology and Immunology and the Feist-Weiller Cancer Center, Louisiana State University Health Sciences Center, Shreveport, Louisiana 71130
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Snippet The Helicobacter pylori CagA protein is translocated into gastric epithelial cells through a type IVsecretion system (TFSS), and published studies suggest CagA...
The Helicobacter pylori CagA protein is translocated into gastric epithelial cells through a type IV secretion system (TFSS), and published studies suggest...
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Title The β1 Integrin Activates JNK Independent of CagA, and JNK Activation Is Required for Helicobacter pylori CagA+-induced Motility of Gastric Cancer Cells
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