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Science 295 (5555): 683-686

Copyright © 2002 by the American Association for the Advancement of Science

SHP-2 Tyrosine Phosphatase as an Intracellular Target of Helicobacter pylori CagA Protein

Hideaki Higashi,1 Ryouhei Tsutsumi,1 Syuichi Muto,1 Toshiro Sugiyama,2 Takeshi Azuma,3 Masahiro Asaka,2 Masanori Hatakeyama1*

Helicobacter pylori CagA protein is associated with severe gastritis and gastric carcinoma. CagA is injected from the attached Helicobacter pylori into host cells and undergoes tyrosine phosphorylation. Wild-type but not phosphorylation-resistant CagA induced a growth factor-like response in gastric epithelial cells. Furthermore, CagA formed a physical complex with the SRC homology 2 domain (SH2)-containing tyrosine phosphatase SHP-2 in a phosphorylation-dependent manner and stimulated the phosphatase activity. Disruption of the CagA-SHP-2 complex abolished the CagA-dependent cellular response. Conversely, the CagA effect on cells was reproduced by constitutively active SHP-2. Thus, upon translocation, CagA perturbs cellular functions by deregulating SHP-2.

1 Division of Molecular Oncology, Institute for Genetic Medicine and Graduate School of Science, Hokkaido University, Sapporo 060-0815, Japan.
2 Department of Gastroenterology & Hematology, Graduate School of Medicine, Hokkaido University, Sapporo 060-0815, Japan.
3 The Second Department of Internal Medicine, Fukui Medical University, Fukui 910-1193, Japan.
*   To whom correspondence should be addressed. E-mail: mhata{at}

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J. Clin. Microbiol. 43, 2635-2641
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Impact of Fasting Plasma Glucose Levels on Gastric Cancer Incidence in a General Japanese Population: The Hisayama Study.
H. Yamagata, Y. Kiyohara, S. Nakamura, M. Kubo, Y. Tanizaki, T. Matsumoto, K. Tanaka, I. Kato, T. Shirota, and M. Iida (2005)
Diabetes Care 28, 789-794
   Abstract »    Full Text »    PDF »
Orchestration of Aberrant Epithelial Signaling by Helicobacter pylori CagA.
R. M. Peek Jr. (2005)
Sci. STKE 2005, pe14
   Abstract »    Full Text »    PDF »
Simple Method for Determination of the Number of Helicobacter pylori CagA Variable-Region EPIYA Tyrosine Phosphorylation Motifs by PCR.
R. H. Argent, Y. Zhang, and J. C. Atherton (2005)
J. Clin. Microbiol. 43, 791-795
   Abstract »    Full Text »    PDF »
Differential Effects of Vasodilatory Prostaglandins on Focal Adhesions, Cytoskeletal Architecture, and Migration in Human Aortic Smooth Muscle Cells.
C. Bulin, U. Albrecht, J.G. Bode, A.-A. Weber, K. Schror, B. Levkau, and J.W. Fischer (2005)
Arterioscler Thromb Vasc Biol 25, 84-89
   Abstract »    Full Text »    PDF »
Induction of peripheral lymph node addressin in human gastric mucosa infected by Helicobacter pylori.
M. Kobayashi, J. Mitoma, N. Nakamura, T. Katsuyama, J. Nakayama, and M. Fukuda (2004)
PNAS 101, 17807-17812
   Abstract »    Full Text »    PDF »
Intact Gram-Negative Helicobacter pylori, Helicobacter felis, and Helicobacter hepaticus Bacteria Activate Innate Immunity via Toll-Like Receptor 2 but Not Toll-Like Receptor 4.
L. Mandell, A. P. Moran, A. Cocchiarella, J. Houghton, N. Taylor, J. G. Fox, T. C. Wang, and E. A. Kurt-Jones (2004)
Infect. Immun. 72, 6446-6454
   Abstract »    Full Text »    PDF »
Phosphorylation-Independent Effects of CagA during Interaction between Helicobacter pylori and T84 Polarized Monolayers.
S. H. El-Etr, A. Mueller, L. S. Tompkins, S. Falkow, and D. S. Merrell (2004)
The Journal of Infectious Disease 190, 1516-1523
   Abstract »    Full Text »    PDF »
Transcription Profile of Helicobacter pylori in the Human Stomach Reflects Its Physiology In Vivo.
J. K. Boonjakuakul, M. Syvanen, A. Suryaprasad, C. L. Bowlus, and J. V. Solnick (2004)
The Journal of Infectious Disease 190, 946-956
   Abstract »    Full Text »    PDF »
Natural Antibiotic Function of a Human Gastric Mucin Against Helicobacter pylori Infection.
M. Kawakubo, Y. Ito, Y. Okimura, M. Kobayashi, K. Sakura, S. Kasama, M. N. Fukuda, M. Fukuda, T. Katsuyama, and J. Nakayama (2004)
Science 305, 1003-1006
   Abstract »    Full Text »    PDF »
Helicobacter pylori Induces Apoptosis of Human Monocytes but Not Monocyte-Derived Dendritic Cells: Role of the cag Pathogenicity Island.
M. Galgani, I. Busiello, S. Censini, S. Zappacosta, L. Racioppi, and R. Zarrilli (2004)
Infect. Immun. 72, 4480-4485
   Abstract »    Full Text »    PDF »
Alanine-Threonine Polymorphism of Helicobacter pylori RpoB Is Correlated with Differential Induction of Interleukin-8 in MKN45 Cells.
K.-H. Lee, M.-J. Cho, Y. Yamaoka, D. Y. Graham, Y.-J. Yun, S.-Y. Woo, C.-Y. Lim, K.-S. Ko, B.-J. Kim, H.-C. Jung, et al. (2004)
J. Clin. Microbiol. 42, 3518-3524
   Abstract »    Full Text »    PDF »
Helicobacter pylori Arginase Inhibits T Cell Proliferation and Reduces the Expression of the TCR {zeta}-Chain (CD3{zeta}).
J. Zabaleta, D. J. McGee, A. H. Zea, C. P. Hernandez, P. C. Rodriguez, R. A. Sierra, P. Correa, and A. C. Ochoa (2004)
J. Immunol. 173, 586-593
   Abstract »    Full Text »    PDF »
Helicobacter pylori Induces AGS Cell Motility and Elongation via Independent Signaling Pathways.
S. Moese, M. Selbach, T. Kwok, V. Brinkmann, W. Konig, T. F. Meyer, and S. Backert (2004)
Infect. Immun. 72, 3646-3649
   Abstract »    Full Text »    PDF »
Distinct Diversity of the cag Pathogenicity Island among Helicobacter pylori Strains in Japan.
T. Azuma, A. Yamakawa, S. Yamazaki, M. Ohtani, Y. Ito, A. Muramatsu, H. Suto, Y. Yamazaki, Y. Keida, H. Higashi, et al. (2004)
J. Clin. Microbiol. 42, 2508-2517
   Abstract »    Full Text »    PDF »
Helicobacter pylori Flagellin Evades Toll-Like Receptor 5-Mediated Innate Immunity.
A. T. Gewirtz, Y. Yu, U. S. Krishna, D. A. Israel, S. L. Lyons, and R. M. Peek (2004)
The Journal of Infectious Disease 189, 1914-1920
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Helicobacter pylori CagA Induces Ras-independent Morphogenetic Response through SHP-2 Recruitment and Activation.
H. Higashi, A. Nakaya, R. Tsutsumi, K. Yokoyama, Y. Fujii, S. Ishikawa, M. Higuchi, A. Takahashi, Y. Kurashima, Y. Teishikata, et al. (2004)
J. Biol. Chem. 279, 17205-17216
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Association between Diversity in the Src Homology 2 Domain-Containing Tyrosine Phosphatase Binding Site of Helicobacter pylori CagA Protein and Gastric Atrophy and Cancer.
T. Azuma, S. Yamazaki, A. Yamakawa, M. Ohtani, A. Muramatsu, H. Suto, Y. Ito, M. Dojo, Y. Yamazaki, M. Kuriyama, et al. (2004)
The Journal of Infectious Disease 189, 820-827
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Functional Analysis of the cag Pathogenicity Island in Helicobacter pylori Isolates from Patients with Gastritis, Peptic Ulcer, and Gastric Cancer.
S. Backert, T. Schwarz, S. Miehlke, C. Kirsch, C. Sommer, T. Kwok, M. Gerhard, U. B. Goebel, N. Lehn, W. Koenig, et al. (2004)
Infect. Immun. 72, 1043-1056
   Abstract »    Full Text »    PDF »

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