Helicobacter pylori-induced alteration of epithelial cell signaling and polarity: A possible mechanism of gastric carcinoma etiology and disparity

Cytoskeleton

Volumn 70, Issue 7, 2013, Pages 349-359

  Osman, Mahasin A ^a   Bloom, George S ^b   Tagoe, Emmanuel A ^c  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF GHANA   (Ghana)

Author keywords

Akt; Cdc42; Erk1 2; Gastric cancer; H. pylori; IQGAP; MTOR

Indexed keywords

BETA1 INTEGRIN; CAGA PROTEIN; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; PROTEIN CDC42; PROTEIN KINASE B; UVOMORULIN;

ACHLORHYDRIA; CARCINOGENESIS; CATALYST; CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL POLARITY; CYTOSKELETON; DEREGULATION; EPITHELIUM CELL; HEALTH DISPARITY; HELICOBACTER PYLORI; HUMAN; INTERNALIZATION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STOMACH ACID SECRETION; STOMACH CARCINOMA;

AKT; CDC42; ERK1/2; GASTRIC CANCER; H. PYLORI; IQGAP; MTOR;

ANIMALS; CELL COMMUNICATION; CELL POLARITY; EPITHELIAL CELLS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; STOMACH NEOPLASMS;

HELICOBACTER PYLORI;

EID: 84880700934     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21114     Document Type: Review

References (81)

1. Awasthi A, Samarakoon A, Chu H, Kamalakannan R, Quilliam LA Chrzanowska-Wodnicka M, Gilbert C. White II GC, Malarkannan S. 2010. Rap1b facilitates NK cell functions via IQGAP1-mediated signalosomes. JEM 207:1923-1938.
2. Backert S, Clyne M, Tegtmeyer N. 2011. Molecular mechanisms of gastric epithelial cell adhesion and injection of CagA by Helicobacter pylori. Cell Commun Signal 9:28. doi:10.1186/1478-811X-9-28. http://www.biosignaling.com/content/9/1/28.
3. Bagnoli F, Buti L, Tompkins A, Covacci A, Aieva MR. 2005. Helicobacter pylori CagA induces a transition from polarized to invasive phenotypes in MDCK cells. Proc Natl Acad Sci U S A 102:16339-16344.
4. Bauer B, Bartfeld S, Meyer TF. 2009. H. pylori selectively blocks EGFR endocytosis via the non-receptor kinase c-Abl and CagA. Cell Microbiol 11:156-169.
5. Bauer B, Meyer TF. 2011. The human gastric pathogen Helicobacter pylori and its association with gastric cancer and ulcer disease. Ulcers, Article ID 340157, 23 pages doi:10.1155/2011/340157
6. Bensenor L, Kan, H-M, Wang N, Wallrabe H, Davidson LA, Cai Y, Schafer DA, Bloom GS. 2007. IQGAP1 regulates cell motility by linking growth factor signaling to actin assembly. J Cell Sci 120:658-669.
7. Brandt DT, Grosse R. 2007. Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep 8:1019-1023.
8. Brandt S, Wessler S, Hartig R, Backert S. 2009. Helicobacter pylori activates protein kinase C delta to control Raf in MAP kinase signalling: role in AGS epithelial cell scattering and elongation. Cell Motil Cytoskeleton 66:874-892.
9. Brandt S, Shafikhani S, Balachandran P, Jin S, Hartig R, König W, Engel J, Backert S. 2007a. Use of a novel coinfection system reveals a role for Rac1, H-Ras, and CrkII phosphorylation in Helicobacter pylori-induced host cell actin cytoskeletal rearrangements. FEMS Immunol Med Microbiol 50:190-205.
10. Brandt DT, Marion S, Griffiths G, Watanabe T, Kaibuchi K, Grosse R. 2007b. Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J Cell Biol 178:193-200.
11. Buffart TE, Louw M, van Grieken NCT, Tijssen M, Carvalho B, Ylstra, B, Grabsch H, Mulder CJJ, van de Velde CJH, van der Merwe SW, Gerrit A, Meijer GA. 2011. Gastric cancers of Western European and African patients show different patterns of genomic instability. BMC Med Genom 4:7
12. Conlin VS, Curtis SB, Zhao Y, Moore EDW, Smith VC, Meloche RM, Finlay BB, Buchan AMJ. 2004. Helicobacter pylori infection targets adherens junction regulatory proteins and results in increased rates of migration in human gastric epithelial cells. Infect Immun 72:5181-5192.
13. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. 2010. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893-2917.
14. Fox GJ, Wang CT, Parsonnet J. 2006. Helicobacter, chronic inflammation, and cancer. In: Hausen ZH, editors. Infections Causing Human Cancer. New York: Wiley-VCH. pp. 386-467.
15. Grohmanova K, Schlaepfer D, Hess D, Gutierrez P, Beck M, Kroschewski R. 2004. Phosphorylation of IQGAP1 modulates its binding to Cdc42, revealing a new type of Rho-GTPase regulator. J Biol Chem 279:48495-48504.
16. Johnson M, Manisha Sharmaa M, Henderson BR. 2009. IQGAP1 regulation and roles in cancer. Cell Signal 10:1471-1478.
17. Horwitz AR. 2012. The origins of the molecular era of adhesion research. Nat Rev Mol Cell Biol 13:805-812.
18. Hoy B, Löwer M, Weydig C, Carra G, Tegtmeyer N, Geppert T, Schröder P, Sewald N, Backert S, Schneider G, Wessler S. 2010. Helicobcter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep 11:798-804.
19. Hoy B, Geppert T, Boehm M, Reisen F, Plattner P, Gadermaier G, Sewald N, Ferreira F, Briza P, Schneider G, Backert S, Wessler S. 2012. Distinct roles of secreted HtrA proteases from gram-negative pathogens in cleaving the junctional protein and tumor suppressor E-cadherin. J Biol Chem 287:10115-10120.
20. Huang Y-W, Yan M, Collins RF, DiCiccio JE, Grinstein S, Trimble WS. 2008. Mammalian septins are required for phagosome formation. Mol Biol Cell 19:1717-1726.
21. Kamangar F, Dores GM, Anderson WF. 2006. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol 24:2137-2150.
22. Katata, T, Irie K, Fukuhara A, Kawakatsu T, Yamada A, Shimizu K, Takai Y. 2003. Involvement of nectin in the localization of IQGAP1 at the cell-cell adhesion sites through the actin cytoskeleton in Madin-Darby canine kidney cells. Oncogene 22:2097-2109.
23. Kaplan-Türköz B, Jiménez-Soto L. F, Dian C, Ertl C, Remaut H, Louche A, Tosi T, Haas R, Terradot L. 2012. Structural insights into Helicobacter pylori oncoprotein CagA interaction with β1 integrin. Proc Natl Acad Sci U S A 109:14640-14645.
24. Kinoshita M. 2003. The septins. Genome Biol 4:236. http:// genomebiology.com/2003/4/11/236.
25. Krishnan S. Fernandez GE. Sacks DB. Prasadarao NV. 2012. IQGAP1 mediates the disruption of adherens junctions to promote Escherichia coli K1 invasion of brain endothelial cells. Cell Microbiol 14:1415-1433.
26. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, König W, Backert S. 2007. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449:862-866.
27. Lal-Nag M, Battis M. Santin AD, Morin PJ. 2012. Claudin-6: a novel receptor for CPE-mediated cytotoxicity in ovarian cancer. Oncogenesis 1, e33; doi:10.1038/oncsis.2012.32. www.nature.com/oncsis
28. Lauren T. 1965. The two histologic main types of gastric carcinoma. Acta Pathol Microbiol Scand 64:31-49.
29. Le Clainche C, Schlaepfer D, Ferrari A, Klingauf M, Grohmanova K, Veligodskiy A, Dirdy D, Le D, Egile C, Carlier MF, Kroschewski R. 2007. IQGAP1 stimulates actin assembly through the N-Wasp-Arp2/3 pathway. J Biol Chem 282:426-435.
30. Lewin D, Lewin K. 1999. Stomach: normal anatomy and histology. In: Graham DY, Genta RM, Dixon F, editors. Gastritis. Philadelphia, PA: Lippincott, Williams &Wilkins.
31. Li S, Wang Q, Chakladar A, Bronson RT, Bernards A. 2000. Gastric hyperplasia in mice lacking the putative Cdc42 effector IQGAP1. Mol. Cell Biol 20:697-701.
32. Malarkannan, S, Awasthi, A, Rajasekaran, K, Kumar P. Schuldt KM, Bartoszek A, Manoharan N, Goldner NK, Umhoefer CM, Thakar MS. 2012. IQGAP1: a regulator of intracellular spacetime relativity. J Immunol 188:2057-2063.
33. Mateer SC, McDaniel AE, Nicolas V, Habermacher GM, Lin MJ, Cromer DA, King ME, Bloom GS. 2002. The mechanism for regulation of the F-actin binding activity of IQGAP1 by calcium/calmodulin. J Biol Chem 277:12324-12333
34. Mateer SC, Wang N, Bloom GS. 2003. IQGAPs: integrators of the cytoskeleton, cell adhesion machinery, and signaling networks. Cell Motil Cytoskeleton 55:147-155.
35. Mateer SC, Morris LE, Cromer DA, Bensenor LB, Bloom GS. 2004. Actin filament binding by a monomeric IQGAP1 fragment with a single calponin homology domain. Cell Motil Cytoskeleton 58:231-241.
36. McNulty DE, Li Z, White CD, Sacks DB, Annan RS. 2011. MAPK scaffold IQGAP1 binds the EGF receptor and modulates its activation. J Biol Chem 286:15010-15021.
37. Mishra A, Verma M. 2010. Cancer biomarkers: Are we ready for the prime time? Cancers 2:190-208.
38. Moese S, Selbach M, Brinkmann V, Karlas A, Haimovich B, Backert S, Meyer TF. 2006. The Helicobacter pylori CagA protein disrupts matrix adhesion of gastric epithelial cells by dephosphorylation of vinculin. Cell Microbiol 9:1148-1161.
39. Morris LE, Bloom GS, Frierson HF, Powell SM. 2005. Nucleotide variants within the IQGAP1 gene in diffuse-type gastric cancers. Genes Chromosomes Cancer 42:280-286.
40. Mostowy S, Nam Tham T, Danckaert A, Guadagnini S, Boisson-Dupuis S, Pizarro-Cerdá J, Cossart P. 2009. Septins regulate bacterial entry into host cells. PLoS ONE 4(1):e4196. doi:10.1371/journal.pone.0004196.
41. Mueller D. Tegtmeyer N, Brandt S, Yamaoka Y, De Poire E, Sgouras D, Wessler S, Torres J, Smolka A, Backert S. 2012. c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains. J Clin Invest 122:1553-1566.
42. Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, Aburatani H, Akiyama T, Peek RM Jr, Azuma T, Hatakeyama M. 2007. Helicobacter pylori CagA interacts with E-cadherin and deregulates the β-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene 26:4617-4626.
43. Murata-Kamiya N, Kikuchi K, Hayashi T, Higashi H, Hatakeyama M. 2010. Helicobacter pylori exploits host membrane phosphatidylserine for delivery, localization, and pathophysiological action of the CagA oncoprotein. Cell Host Microbe 7:399-411.
44. Nelson JW. 2009. Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity. Cold Spring Harb Perspect Biol 1(1):a000513. doi: 10.1101/cshperspect.a 000513.
45. Niessen CM. 2007. Tight junctions/adherens junctions: basic structure and function. J Invest Dermatol 127:2525-2532.
46. Noritake U, Watanabe T, Sato K, Wang S, Kaibuchi K. 2005. IQGAP1: a key regulator of adhesion and migration. J Cell Sci 118:2085-2092.
47. Olofsson A, Vallström A, Petzold K, Tegtmeyer N, Schleucher J, Carlsson S, Haas R, Backert S, Wai SN, Gröbner G, Arnqvist A. 2010. Biochemical and functional characterization of Helicobacter pylori vesicles. Mol Microbiol 77:1539-1555.
48. Ooi CH, Ivanova T, Wu J, Lee M, Tan IB, Tao J, Ward L, Koo JH, Gopalakrishnan V, Zhu Y, Cheng LL, Lee J, Rha SY, Chung HC, Ganesan K, So J, Soo KC, Lim D, Chan WH, Wong WK, Bowtell D, Yeoh KG, Grabsch H, Boussioutas A, Tan P. 2009. Oncogenic pathway combinations predict clinical prognosis in gastric cancer. PLos Genet 5:e1000676.
49. Osman MA. 2010. An emerging role for IQGAP1 in regulating protein traffic. Sci World J 10:944-953.
50. Quadri SK. 2012. Cross talk between focaladhesion kinase and cadherins: role in regulating endothelial barrier function. Microvasc Res 1:3-11.
51. Ratheesh A, Yap AS. 2012. A bigger picture: classical cadherins and the dynamic actin cytoskeleton. Nat Rev Mol Cell Biol 13:673-679.
52. Reymond N, Im JH, Garg R, Vega FM, d'Agua BB, Riou P, Cox S, Valderrama F, Muschel RJ, Ridley AJ. 2012. Cdc42 promotes transendothelial migration of cancer cells through {beta}1 integrin. J Cell Biol 199:653-668.
53. Rittmeyer EN, Daniel S, Hsu SC, Osman MA. 2008. A dual role for IQGAP1 in regulating exocytosis. J Cell Sci 121:391-408.
54. Rottiers V, Näär AM. 2012. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 13:239-251.
55. Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ. 2010. Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H, K-ATPase α subunit. Gastroenterology 139:239-248.
56. Sakisaka T, Ikeda W, Ogita H, Fujita N, Yoshimi Takai Y. 2007. The roles of nectins in cell adhesions: cooperation with other cell adhesion molecules and growth factor receptors. Curr Opin Cell Biol 19:593-602.
57. Schneider S, Weydig C, Wessler S. 2008. Targeting focal adhesions: Helicobacter pylori-host communication in cell migration. Cell Commun Signal 6:2 doi:10.1186/1478-811X-6-2. http://www.biosignaling.com/content/6/1/2
58. Shah MA, Khanin R, Tang L, Janjigian YY, Klimstra DS, Gerdes H, Kelsen DP. 2011. Molecular classification of gastric cancer: a new paradigm. Clin Cancer Res 17:2693-2701.
59. Sirajuddin M, Farkasovsky M, Hauer F, Kuhlmann D, Macara IG, Weyand M, Stark H, Wittinghofer A. 2007. Structural insight into filament formation by mammalian septins. Nature 449:311-315.
60. Spiliotis ET, Hunt SJ, Hu Q, Kinoshita K, Nelson WJ. 2008. Epithelial polarity requires septin coupling of vesicle transport to polyglutamylated microtubules. J Cell Biol 180:295-303.
61. Takahashi A, Kondoh M, Suzuki H, Yagi K. 2011. Claudin as a target for drug development. Curr Med Chem 18:1861-1865.
62. Takemoto H, Yuchiro D, Shiozaki H, Imamura H, Utsunomya T, Miyata H, Yano M, Inoue M, Fujiwara Y, Monden M. 2001. Localization of IQGAP1 is inversely correlated with intercellular adhesion mediated by E-cadherin in gastric cancers. Int J Cancer 91:783-788.
63. Tammer I, Brandt S, Hartig R, König W, Backert, S. 2007. Activation of Abl by Helicobacter pylori: a novel kinase for CagA and crucial mediator of host cell scattering. Gastroenterology 132:1309-1319.
64. Tanaka M, Kitajima Y, Edakuni G, Sato S, Miyazaki K. 2002. Abnormal expression of E-cadherin and beta-catenin may be a molecular marker of submucosal invasion and lymph node metastasis in early gastric cancer. Br J Surg 89:236-244.
65. Tanos B, Rodriguez-Boulan E. 2008. The epithelial polarity program: machineries involved and their hijacking by cancer. Oncogene 27:6939-6957.
66. Tegtmeyer N, Wittelsberger R, Hartig R, Wessler S, Martinez-Quiles N, Backert S. 2011. Serine phosphorylation of cortactin controls focal adhesion kinase activity and cell scattering induced by Helicobacter pylori. Cell Host Microbe 9:520-531.
67. Tekletsadik KY, Sonn R, Osman MA. 2012. A conserved role for IQGAP1 in regulating TOR complex 1. J Cell Sci 125:2041-2052.
68. Tsutsumi R, Takahashi A, Azuma T, Higashi H, Hatakeyama M. 2006. Focal adhesion kinase is a substrate and downstream effector of SHP-2 complexed with Helicobacter pylori CagA. Mol Cell Biol 26:1-276.
69. Valle B, Morin PJ. 2010. Claudins in cancer biology. Curr Top Membr 13:293-333.
70. Walther W, Petkov S, Kuvardina ON, Aumann J, Kobelt D, Fichtner I, Lemm M, Piontek J, Blasig IE, Stein U, Schlag PM. 2012. Novel Clostridium perfringens enterotoxin suicide gene therapy for selective treatment of claudin-3- and -4-overexpressing tumors. Gene Ther 19:494-503.
71. Wang J-B, Sonn R, Tekletsadik YK, Samorodnitsky D, Osman MA. 2009. IQGAP1 regulates cell proliferation through a novel CDC42-mTOR pathway. J Cell Sci 122:2024-2033.
72. Ward E, Jemal A, Cokkinides V, Singh GK, Cardinez C, Ghafoor A, Thun M. 2004. Cancer disparities by race/ethnicity and socioeconomic status. CA Cancer J Clin 54:78-93.
73. Watanabe T, Sato K, Kaibuchi K. 2009. Cadherin-mediated intercellular adhesion and signaling cascades involving small GTPases. Cold Spring Harb Perspect Biol 1:a003020.
74. Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K. 2004. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell 7:871-883.
75. Wessler S, Gimona, M, Rieder G. 2011. Regulation of the actin cytoskeleton in Helicobacter pylori-induced migration and invasive growth of gastric epithelial cells. Cell Comm Signal 9:27. http://www.biosignaling.com/content/9/1/27.
76. Wiredu EK, Armah HB. 2006. Cancer mortality patterns in Ghana: a 10-year review of autopsies and hospital mortality. BMC Public Health 6:159. doi:10.1186/1471-2458-6-159
77. Wu D, Pan W. 2010. GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem Sci 35:161-168.
78. Yao X, Forte JG. 2003. Cell biology of acid secretion by the parietal cell. Annu Reb Physiol 65:103-131.
79. Yeatman TJ, Mule J, Dalton WS, Sullivan D. 2008. On the eve of personalized medicine in oncology. Cancer Res 68:7250-7252.
80. Zhu Y, Zhong X, Zheng S, Du Q, Xu W. 2005. Transformed immortalized gastric epithelial cells by virulence factor CagA of Helicobacter pylori through Erk mitogen-activated protein kinase pathway. Oncogene 24:3886-3995.
81. Ziegler WH, Liddington RC, Critchley DR. 2010. The structure and regulation of vinculin. Trends Cell Biol 16:453-460.