Helicobacter pylori infection of gastrointestinal epithelial cells in vitro induces mesenchymal stem cell migration through an NF-κB-dependent pathway

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Ferrand, Jonathan ^a,b   Lehours, Philippe ^a,b   Schmid Alliana, Annie ^c,d   Mégraud, Francis ^a,b   Varon, Christine ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b Institut National de la Santé et de la Recherche Médicale ^*  (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; GASTROINTESTINAL EPITHELIAL CELL; HELICOBACTER PYLORI; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; CELL MOTION; GASTROINTESTINAL TRACT; HELICOBACTER INFECTION; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PATHOLOGY;

HELICOBACTER PYLORI;

ANIMALS; CELL MOVEMENT; EPITHELIAL CELLS; GASTROINTESTINAL TRACT; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; MESENCHYMAL STEM CELLS; MICE; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84555218888     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029007     Document Type: Article

References (57)

1. Park DH, Borlongan CV, Eve DJ, Sanberg PR, (2008) The emerging field of cell and tissue engineering. Med Sci Monit 14: RA206-220.
2. Korbling M, Katz RL, Khanna A, Ruifrok AC, Rondon G, et al. (2002) Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells. N Engl J Med 346: 738-746.
3. Matsumoto T, Okamoto R, Yajima T, Mori T, Okamoto S, et al. (2005) Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine. Gastroenterology 128: 1851-1867.
4. Okamoto R, Watanabe M, (2004) Molecular and clinical basis for the regeneration of human gastrointestinal epithelia. J Gastroenterol 39: 1-6.
5. Francois S, Bensidhoum M, Mouiseddine M, Mazurier C, Allenet B, et al. (2006) Local irradiation not only induces homing of human mesenchymal stem cells at exposed sites but promotes their widespread engraftment to multiple organs: a study of their quantitative distribution after irradiation damage. Stem Cells 24: 1020-1029.
6. Houghton J, Stoicov C, Nomura S, Rogers AB, Carlson J, et al. (2004) Gastric cancer originating from bone marrow-derived cells. Science 306: 1568-1571.
7. Varon C, Dubus P, Mazurier F, Asencio C, Chambonnier L, et al. (2011) Helicobacter pylori infection recruits bone marrow-derived cells that participate in gastric preneoplasia in mice. Gastroenterology In press.
8. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, et al. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41-49.
9. Rizvi AZ, Swain JR, Davies PS, Bailey AS, Decker AD, et al. (2006) Bone marrow-derived cells fuse with normal and transformed intestinal stem cells. Proc Natl Acad Sci U S A 103: 6321-6325.
10. Charbord P, (2010) Bone Marrow Mesenchymal Stem Cells: Historical Overview and Concepts. Hum Gene Ther 21: 1045-1056.
11. Phinney DG, Prockop DJ, (2007) Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 25: 2896-2902.
12. Fox JM, Chamberlain G, Ashton BA, Middleton J, (2007) Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol 137: 491-502.
13. Hutchinson L, Stenstrom B, Chen D, Piperdi B, Levey S, et al. (2010) Human Barrett's Adenocarcinoma of the Esophagus, Associated Myofibroblasts, and Endothelium Can Arise from Bone Marrow-Derived Cells After Allogeneic Stem Cell Transplant. Stem Cells Dev 20: 11-17.
14. Li H, Fan X, Kovi RC, Jo Y, Moquin B, et al. (2007) Spontaneous expression of embryonic factors and p53 point mutations in aged mesenchymal stem cells: a model of age-related tumorigenesis in mice. Cancer Res 67: 10889-10898.
15. Sarosi G, Brown G, Jaiswal K, Feagins LA, Lee E, et al. (2008) Bone marrow progenitor cells contribute to esophageal regeneration and metaplasia in a rat model of Barrett's esophagus. Dis Esophagus 21: 43-50.
16. Tirode F, Laud-Duval K, Prieur A, Delorme B, Charbord P, et al. (2007) Mesenchymal stem cell features of Ewing tumors. Cancer Cell 11: 421-429.
17. Correa P, Houghton J, (2007) Carcinogenesis of Helicobacter pylori. Gastroenterology 133: 659-672.
18. Kuipers EJ, (1999) Review article: exploring the link between Helicobacter pylori and gastric cancer. Aliment Pharmacol Ther 13 (Suppl 1): 3-11.
19. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, et al. (2007) Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449: 862-866.
20. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, et al. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5: 1166-1174.
21. Dwyer RM, Potter-Beirne SM, Harrington KA, Lowery AJ, Hennessy E, et al. (2007) Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res 13: 5020-5027.
22. Mishima Y, Lotz M, (2008) Chemotaxis of human articular chondrocytes and mesenchymal stem cells. J Orthop Res.
23. Ponte AL, Marais E, Gallay N, Langonne A, Delorme B, et al. (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25: 1737-1745.
24. Ries C, Egea V, Karow M, Kolb H, Jochum M, et al. (2007) MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines. Blood 109: 4055-4063.
25. Secchiero P, Melloni E, Corallini F, Beltrami AP, Alviano F, et al. (2008) Tumor necrosis factor-related apoptosis-inducing ligand promotes migration of human bone marrow multipotent stromal cells. Stem Cells 26: 2955-2963.
26. Sordi V, (2009) Mesenchymal stem cell homing capacity. Transplantation 87: S42-45.
27. Spaeth E, Klopp A, Dembinski J, Andreeff M, Marini F, (2008) Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther 15: 730-738.
28. Wang L, Li Y, Chen X, Chen J, Gautam SC, et al. (2002) MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology 7: 113-117.
29. Bauer B, Moese S, Bartfeld S, Meyer TF, Selbach M, (2005) Analysis of cell type-specific responses mediated by the type IV secretion system of Helicobacter pylori. Infect Immun 73: 4643-4652.
30. Futagami S, Hiratsuka T, Tatsuguchi A, Suzuki K, Kusunoki M, et al. (2003) Monocyte chemoattractant protein 1 (MCP-1) released from Helicobacter pylori stimulated gastric epithelial cells induces cyclooxygenase 2 expression and activation in T cells. Gut 52: 1257-1264.
31. Kudo T, Lu H, Wu JY, Graham DY, Casola A, et al. (2005) Regulation of RANTES promoter activation in gastric epithelial cells infected with Helicobacter pylori. Infect Immun 73: 7602-7612.
32. Kundu P, Mukhopadhyay AK, Patra R, Banerjee A, Berg DE, et al. (2006) Cag pathogenicity island-independent up-regulation of matrix metalloproteinases-9 and-2 secretion and expression in mice by Helicobacter pylori infection. J Biol Chem 281: 34651-34662.
33. Kusugami K, Ando T, Imada A, Ina K, Ohsuga M, et al. (1999) Mucosal macrophage inflammatory protein-1alpha activity in Helicobacter pylori infection. J Gastroenterol Hepatol 14: 20-26.
34. Peek RM Jr, Miller GG, Tham KT, Perez-Perez GI, Zhao X, et al. (1995) Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab Invest 73: 760-770.
35. Wang G, Yu D, Tan W, Zhao D, Wu C, et al. (2009) Genetic polymorphism in chemokine CCL22 and susceptibility to Helicobacter pylori infection-related gastric carcinoma. Cancer 115: 2430-2437.
36. Yamaoka Y, Kita M, Kodama T, Sawai N, Imanishi J, (1996) Helicobacter pylori cagA gene and expression of cytokine messenger RNA in gastric mucosa. Gastroenterology 110: 1744-1752.
37. Yamaoka Y, Kita M, Kodama T, Sawai N, Kashima K, et al. (1997) Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains. Gut 41: 442-451.
38. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
39. Goso Y, Nakano S, Sugiyama N, Tabuchi Y, Horiuchi T, et al. (1997) Immortalized gastric epithelial cell line GSM06 synthesizes hyaluronan under the influence of simian virus 40 large T-antigen expression. J Biochem 122: 96-100.
40. Hollande F, Blanc EM, Bali JP, Whitehead RH, Pelegrin A, et al. (2001) HGF regulates tight junctions in new nontumorigenic gastric epithelial cell line. Am J Physiol Gastrointest Liver Physiol 280: G910-921.
41. Bens M, Bogdanova A, Cluzeaud F, Miquerol L, Kerneis S, et al. (1996) Transimmortalized mouse intestinal cells (m-ICc12) that maintain a crypt phenotype. Am J Physiol 270: C1666-1674.
42. Kotarsky K, Sitnik KM, Stenstad H, Kotarsky H, Schmidtchen A, et al. (2010) A novel role for constitutively expressed epithelial-derived chemokines as antibacterial peptides in the intestinal mucosa. Mucosal Immunol 3: 40-48.
43. Chaouche-Drider N, Kaparakis M, Karrar A, Fernandez MI, Carneiro LA, et al. (2009) A commensal Helicobacter sp. of the rodent intestinal flora activates TLR2 and NOD1 responses in epithelial cells. PLoS One 4: e5396.
44. Sterzenbach T, Lee SK, Brenneke B, von Goetz F, Schauer DB, et al. (2007) Inhibitory effect of enterohepatic Helicobacter hepaticus on innate immune responses of mouse intestinal epithelial cells. Infect Immun 75: 2717-2728.
45. Kaparakis M, Turnbull L, Carneiro L, Firth S, Coleman HA, et al. (2010) Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol 12: 372-385.
46. Suganuma M, Kurusu M, Suzuki K, Nishizono A, Murakami K, et al. (2005) New tumor necrosis factor-alpha-inducing protein released from Helicobacter pylori for gastric cancer progression. J Cancer Res Clin Oncol 131: 305-313.
47. Smith MF Jr, Mitchell A, Li G, Ding S, Fitzmaurice AM, et al. (2003) Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J Biol Chem 278: 32552-32560.
48. Torok AM, Bouton AH, Goldberg JB, (2005) Helicobacter pylori induces interleukin-8 secretion by Toll-like receptor 2- and Toll-like receptor 5-dependent and-independent pathways. Infect Immun 73: 1523-1531.
49. Fukata M, Abreu MT, (2008) Role of Toll-like receptors in gastrointestinal malignancies. Oncogene 27: 234-243.
50. Backhed F, Rokbi B, Torstensson E, Zhao Y, Nilsson C, et al. (2003) Gastric mucosal recognition of Helicobacter pylori is independent of Toll-like receptor 4. J Infect Dis 187: 829-836.
51. Ishihara S, Rumi MA, Kadowaki Y, Ortega-Cava CF, Yuki T, et al. (2004) Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J Immunol 173: 1406-1416.
52. Lee SK, Stack A, Katzowitsch E, Aizawa SI, Suerbaum S, et al. (2003) Helicobacter pylori flagellins have very low intrinsic activity to stimulate human gastric epithelial cells via TLR5. Microbes Infect 5: 1345-1356.
53. Su B, Ceponis PJ, Lebel S, Huynh H, Sherman PM, (2003) Helicobacter pylori activates Toll-like receptor 4 expression in gastrointestinal epithelial cells. Infect Immun 71: 3496-3502.
54. Ferrand J, Noel D, Lehours P, Prochazkova-Carlotti M, Chambonnier L, et al. (2011) Human Bone Marrow-Derived Stem Cells Acquire Epithelial Characteristics through Fusion with Gastrointestinal Epithelial Cells. PLoS One 6: e19569.
55. Franco AT, Johnston E, Krishna U, Yamaoka Y, Israel DA, et al. (2008) Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res 68: 379-387.
56. Tatin F, Varon C, Genot E, Moreau V, (2006) A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J Cell Sci 119: 769-781.
57. Varon C, Tatin F, Moreau V, Van Obberghen-Schilling E, Fernandez-Sauze S, et al. (2006) Transforming growth factor beta induces rosettes of podosomes in primary aortic endothelial cells. Mol Cell Biol 26: 3582-3594.