Promoting MΦ transepithelial migration by stimulating the epithelial cell P2Y2 receptor

European Journal of Immunology

Volumn 39, Issue 10, 2009, Pages 2895-2905

  Langlois, Christine ^a   Gendron, Fernand Pierre ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Adhesion; Inflammation; Intestinal epithelial cells; Leukocytes; P2Y

Indexed keywords

ADENOSINE TRIPHOSPHATE; INTERCELLULAR ADHESION MOLECULE 1; NUCLEOTIDE; PURINERGIC P2Y2 RECEPTOR; URIDINE TRIPHOSPHATE; ANTIBODY; DRUG DERIVATIVE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PURINERGIC P2 RECEPTOR; SURAMIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STIMULATION; CELL STRAIN CACO 2; COLITIS; COLON MUCOSA; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENTERITIS; EPITHELIUM CELL; GASTROINTESTINAL DISEASE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; INTESTINE CELL; INTESTINE EPITHELIUM; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPLEEN; WESTERN BLOTTING; ANIMAL; CELL LINE; CELL MOTION; CELL STRAIN U937; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION; GENETICS; IMMUNOLOGY; IMPEDANCE; INTESTINE MUCOSA; MACROPHAGE; METABOLISM; MOUSE STRAIN; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIBODIES; CACO-2 CELLS; CELL ADHESION; CELL LINE; CELL MOVEMENT; ELECTRIC IMPEDANCE; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; INTESTINAL MUCOSA; MACROPHAGES; MICE; MICE, INBRED STRAINS; NEUTROPHILS; NF-KAPPA B; NUCLEOTIDES; RATS; RECEPTORS, PURINERGIC P2; SURAMIN; U937 CELLS; URIDINE TRIPHOSPHATE;

EID: 70350526985     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939369     Document Type: Article

References (64)

1. Seidel, E. and Long, M., Gastrointestinal System, 1st Edn. Elsevier, Philadelphia 2006.
2. Grbic, D. M., Degagne, E., Langlois, C., Dupuis, A. A. and Gendron, F. P., Intestinal inflammation increases the expression of the P2Y6 receptor on epithelial cells and the release of CXC chemokine ligand 8 by UDP. J. Immunol. 2008. 180: 2659-2668.
3. Kelsall, B. L., Innate and adaptive mechanisms to control of pathological intestinal inflammation. J. Pathol. 2008. 214: 242-259.
4. Stadnyk, A. W., Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can. J. Gastroenterol. 2002. 16: 241-246.
5. Parkos, C. A., Delp, C., Arnaout, M. A. and Madara, J. L., Neutrophil migration across a cultured intestinal epithelium. Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J. Clin. Invest. 1991. 88: 1605-1612.
6. Reaves, T. A., Colgan, S. P., Selvaraj, P., Pochet, M. M., Walsh, S., Nusrat, A., Liang, T. W. et al., Neutrophil transepithelial migration: regulation at the apical epithelial surface by Fc-mediated events. Am. J. Physiol. Gastrointest. Liver Physiol. 2001. 280: G746-G754.
7. Parkos, C. A., Cell adhesion and migration. I. Neutrophil adhesive interactions with intestinal epithelium. Am. J. Physiol. 1997. 273: G763-G768.
8. Dippold, W., Wittig, B., Schwaeble, W., Mayet, W. and Meyer zum Buschenfelde, K. H., Expression of intercellular adhesion molecule 1 (ICAM-1, CD54) in colonic epithelial cells. Gut 1993. 34: 1593-1597.
9. Maaser, C., Schoeppner, S., Kucharzik, T., Kraft, M., Schoenherr, E., Domschke, W. and Luegering, N., Colonic epithelial cells induce endothelial cell expression of ICAM-1 and VCAM-1 by a NF-kappaB-dependent mechanism. Clin. Exp. Immunol. 2001. 124: 208-213.
10. Parkos, C. A., Colgan, S. P., Diamond, M. S., Nusrat, A., Liang, T. W., Springer, T. A. and Madara, J. L., Expression and polarization of intercellular adhesion molecule-1 on human intestinal epithelia: consequences for CD11b/CD18-mediated interactions with neutrophils. Mol. Med. 1996. 2: 489-505.
11. Vainer, B., Intercellular adhesion molecule-1 (ICAM-1) in ulcerative colitis: presence, visualization, and significance. Inflamm. Res. 2005. 54: 313-327.
12. Vainer, B., Brimnes, J., Claesson, M. H. and Nielsen, O. H., Impaired sensitivity to beta 2 integrin-blocking in ICAM-1-mediated neutrophil migration in ulcerative colitis. Scand. J. Gastroenterol. 2001. 36: 621-629.
13. Vainer, B., Horn, T. and Nielsen, O. H., Colonic epithelial cell expression of ICAM-1 relates to loss of surface continuity: a comparative study of inflammatory bowel disease and colonic neoplasms. Scand. J. Gastroenterol. 2006. 41: 318-325.
14. Beigi, R., Kobatake, E., Aizawa, M. and Dubyak, G. R., Detection of local ATP release from activated platelets using cell surface-attached firefly luciferase. Am. J. Physiol. 1999. 276: C267-C278.
15. Lazarowski, E. R. and Boucher, R. C., UTP as an extracellular signaling molecule. News Physiol. Sci. 2001. 16: 1-5.
16. Lazarowski, E. R. and Harden, T. K., Quantitation of extracellular UTP using a sensitive enzymatic assay. Br. J. Pharmacol. 1999. 127: 1272-1278.
17. Lazarowski, E. R., Tarran, R., Grubb, B. R., van Heusden, C. A., Okada, S. and Boucher, R. C., Nucleotide release provides a mechanism for airway surface liquid homeostasis. J. Biol. Chem. 2004. 279: 36855-36864.
18. Ivanova, E. P., Alexeeva, Y. V., Pham, D. K.,Wright, J. P. and Nicolau, D. V., ATP level variations in heterotrophic bacteria during attachment on hydrophilic and hydrophobic surfaces. Int. Microbiol. 2006. 9: 37-46.
19. Ghanem, E., Robaye, B., Leal, T., Leipziger, J., Van Driessche, W., Beauwens, R. and Boeynaems, J. M., The role of epithelial P2Y(2) and P2Y(4) receptors in the regulation of intestinal chloride secretion. Br. J. Pharmacol. 2005. 146: 364-369.
20. Kerstan, D., Gordjani, N., Nitschke, R., Greger, R. and Leipziger, J., Luminal ATP induces K+ secretion via a P2Y2 receptor in rat distal colonic mucosa. Pflugers Arch. 1998. 436: 712-716.
21. Kottgen, M., Loffler, T., Jacobi, C., Nitschke, R., Pavenstadt, H., Schreiber, R., Frische, S. et al., P2Y6 receptor mediates colonic NaCl secretion via differential activation of cAMP-mediated transport. J. Clin. Invest. 2003. 111: 371-379.
22. Matos, J. E., Robaye, B., Boeynaems, J. M., Beauwens, R. and Leipziger, J., K+ secretion activated by luminal P2Y2 and P2Y4 receptors in mouse colon. J. Physiol. 2005. 564: 269-279.
23. Robaye, B., Ghanem, E., Wilkin, F., Fokan, D., Van Driessche, W., Schurmans, S., Boeynaems, J. M. and Beauwens, R., Loss of nucleotide regulation of epithelial chloride transport in the jejunum of P2Y4-null mice. Mol. Pharmacol. 2003. 63: 777-783.
24. la Sala, A., Ferrari, D., Di Virgilio, F., Idzko, M., Norgauer, J. and Girolomoni, G., Alerting and tuning the immune response by extracellular nucleotides. J. Leukoc. Biol. 2003. 73: 339-343.
25. Myrtek, D. and Idzko, M., Chemotactic activity of extracellular nucleotides on human immune cells. Purinergic Signal. 2007. 3: 5-11.
26. Oshimi, Y., Miyazaki, S. and Oda, S., ATP-induced Ca2+ response mediated by P2U and P2Y purinoceptors in human macrophages: signalling from dying cells to macrophages. Immunology 1999. 98: 220-227. (Pubitemid 29487643)
27. Wu, L. J., Vadakkan, K. I. and Zhuo, M., ATP-induced chemotaxis of microglial processes requires P2Y receptor-activated initiation of outward potassium currents. Glia 2007. 55: 810-821. (Pubitemid 46787192)
28. Bagchi, S., Liao, Z., Gonzalez, F. A., Chorna, N. E., Seye, C. I., Weisman, G. A. and Erb, L., The P2Y2 nucleotide receptor interacts with alpha v integrins to activate Go and induce cell migration. J. Biol. Chem. 2005. 280: 39050-39057.
29. Baker, O. J., Camden, J. M., Rome, D. E., Seye, C. I. and Weisman, G. A., P2Y2 nucleotide receptor activation up-regulates vascular cell adhesion molecular-1 expression and enhances lymphocyte adherence to a human submandibular gland cell line. Mol. Immunol. 2008. 45: 65-75.
30. Seye, C. I., Kong, Q., Erb, L., Garrad, R. C., Krugh, B.,Wang, M., Turner, J. T. et al., Functional P2Y2 nucleotide receptors mediate uridine 5′-triphosphate-induced intimal hyperplasia in collared rabbit carotid arteries. Circulation 2002. 106: 2720-2726. (Pubitemid 35364928)
31. Zen, K. and Parkos, C. A., Leukocyte-epithelial interactions. Curr. Opin. Cell Biol. 2003. 15: 557-564.
32. Chen, Y., Corriden, R., Inoue, Y., Yip, L., Hashiguchi, N., Zinkernagel, A., Nizet, V. et al., ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 2006. 314: 1792-1795. (Pubitemid 44969094)
33. Migliorisi, G., Folkes, E. and Cramer, E. B., Differences in the ability of neutrophils and monocytes to traverse epithelial occluding junctions. J. Leukoc. Biol. 1988. 44: 485-492.
34. Martin, C. A., el-Sabban, M. E., Zhao, L., Burakoff, R. and Homaidan, F. R., Adhesion and cytosolic dye transfer between macrophages and intestinal epithelial cells. Cell Adhes. Commun. 1998. 5: 83-95.
35. Seye, C. I., Yu, N., Jain, R., Kong, Q., Minor, T., Newton, J., Erb, L. et al., The P2Y2 nucleotide receptor mediates UTP-induced vascular cell adhesion molecule-1 expression in coronary artery endothelial cells. J. Biol. Chem. 2003. 278: 24960-24965.
36. Ivanov, A. A., Ko, H., Cosyn, L., Maddileti, S., Besada, P., Fricks, I., Costanzi, S. et al., Molecular modeling of the human P2Y2 receptor and design of a selective agonist, 2′-amino-2′-deoxy-2-thiouridine 5′-triphosphate. J. Med. Chem. 2007. 50: 1166-1176.
37. Zen, K., Liu, Y., McCall, I. C.,Wu, T., Lee,W., Babbin, B. A., Nusrat, A. and Parkos, C. A., Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils. Mol. Biol. Cell 2005. 16: 2694-2703.
38. Dubyak, G. R. and el-Moatassim, C., Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am. J. Physiol. 1993. 265: C577-C606.
39. Smythies, L. E., Sellers, M., Clements, R. H., Mosteller-Barnum, M., Meng, G., Benjamin, W. H., Orenstein, J. M. and Smith, P. D., Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 2005. 115: 66-75.
40. Mahida, Y. R., Galvin, A. M., Gray, T., Makh, S., McAlindon, M. E., Sewell, H. F. and Podolsky, D. K., Migration of human intestinal lamina propria lymphocytes, macrophages and eosinophils following the loss of surface epithelial cells. Clin. Exp. Immunol. 1997. 109: 377-386.
41. Grimm, M. C., Pullman, W. E., Bennett, G. M., Sullivan, P. J., Pavli, P. and Doe, W. F., Direct evidence of monocyte recruitment to inflammatory bowel disease mucosa. J. Gastroenterol. Hepatol. 1995. 10: 387-395.
42. Spottl, T., Hausmann, M., Kreutz, M., Peuker, A., Vogl, D., Scholmerich, J., Falk, W. et al., Monocyte differentiation in intestine-like macro-phage phenotype induced by epithelial cells. J. Leukoc. Biol. 2001. 70: 241-251.
43. Herold, S., von Wulffen, W., Steinmueller, M., Pleschka, S., Kuziel, W. A., Mack, M., Srivastava, M. et al., Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J. Immunol. 2006. 177: 1817-1824. (Pubitemid 44092519)
44. Platt, A. M. and Mowat, A. M., Mucosal macrophages and the regulation of immune responses in the intestine. Immunol. Lett. 2008. 119: 22-31.
45. Baumgart, D. C. and Carding, S. R., Inflammatory bowel disease: cause and immunobiology. Lancet 2007. 369: 1627-1640. (Pubitemid 46722636)
46. Burgio, V. L., Fais, S., Boirivant, M., Perrone, A. and Pallone, F., Peripheral monocyte and naive T-cell recruitment and activation in Crohn's disease. Gastroenterology 1995. 109: 1029-1038.
47. Sartor, R. B. and Sandborn,W., (Eds.) Kirsner's Inflammatory Bowel Diseases. Elsevier, 6th Edn., Philadelphia 2004.
48. Savill, J. S., Wyllie, A. H., Henson, J. E., Walport, M. J., Henson, P. M. and Haslett, C., Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 1989. 83: 865-875.
49. Kolachala, V. L., Bajaj, R., Chalasani, M. and Sitaraman, S. V., Purinergic receptors in gastrointestinal inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 2008. 294: G401-G410.
50. Baker, O. J., Camden, J. M., Redman, R. S., Jones, J. E., Seye, C. I., Erb, L. and Weisman, G. A., Proinflammatory cytokines tumor necrosis factor-alpha and interferon-gamma alter tight junction structure and function in the rat parotid gland Par-C10 cell line. Am. J. Physiol. Cell Physiol. 2008. 295: C1191-C1201.
51. Forbes, E., Hulett, M., Ahrens, R., Wagner, N., Smart, V., Matthaei, K. I., Brandt, E. B. et al., ICAM-1-dependent pathways regulate colonic eosinophilic inflammation. J. Leukoc. Biol. 2006. 80: 330-341.
52. Nakamura, K., Honda, K., Mizutani, T., Akiho, H. and Harada, N., Novel strategies for the treatment of inflammatory bowel disease: Selective inhibition of cytokines and adhesion molecules. World J. Gastroenterol. 2006. 12: 4628-4635.
53. Vainer, B., Nielsen, O. H. and Horn, T., Comparative studies of the colonic in situ expression of intercellular adhesion molecules (ICAM-1, -2, and -3), beta2 integrins (LFA-1, Mac-1, and p150,95), and PECAM-1 in ulcerative colitis and Crohn's disease. Am. J. Surg. Pathol. 2000. 24: 1115-1124.
54. Morise, K., Yamaguchi, T., Kuroiwa, A., Kanayama, K., Matsuura, T., Shinoda, M., Yamamoto, H. et al., Expression of adhesion molecules and HLA-DR by macrophages and dendritic cells in aphthoid lesions of Crohn's disease: an immunocytochemical study. J. Gastroenterol. 1994. 29: 257-264. (Pubitemid 24188650)
55. Korcok, J., Raimundo, L. N., Du, X., Sims, S. M. and Dixon, S. J., P2Y6 nucleotide receptors activate NF-kappaB and increase survival of osteoclasts. J. Biol. Chem. 2005. 280: 16909-16915.
56. Roebuck, K. A. and Finnegan, A., Regulation of intercellular adhesion molecule-1 (CD54) gene expression. J. Leukoc. Biol. 1999. 66: 876-888.
57. Blake, K. M., Carrigan, S. O., Issekutz, A. C. and Stadnyk, A. W., Neutrophils migrate across intestinal epithelium using beta2 integrin (CD11b/CD18)-independent mechanisms. Clin. Exp. Immunol. 2004. 136: 262-268.
58. Huang, G. T., Eckmann, L., Savidge, T. C. and Kagnoff, M. F., Infection of human intestinal epithelial cells with invasive bacteria upregulates apical intercellular adhesion molecule-1 (ICAM)-1) expression and neutrophil adhesion. J. Clin. Invest. 1996. 98: 572-583.
59. Burnstock, G., Purinergic receptors as future targets for treatment of functional GI disorders. Gut 2008. 57: 1193-1194.
60. Gendron, F. P., Mongrain, S., Laprise, P., McMahon, S., Dubois, C. M., Blais, M., Asselin, C. and Rivard, N., The CDX2 transcription factor regulates furin expression during intestinal epithelial cell differentiation. Am. J. Physiol. Gastrointest. Liver Physiol. 2006. 290: G310-G318.
61. Shelley, C. S., Teodoridis, J. M., Park, H., Farokhzad, O. C., Bottinger, E. P. and Arnaout, M. A., During differentiation of the monocytic cell line U937, Pur alpha mediates induction of the CD11c beta 2 integrin gene promoter. J. Immunol. 2002. 168: 3887-3893.
62. Ear, T. and McDonald, P. P., Cytokine generation, promoter activation, and oxidant-independent NF-kappaB activation in a transfectable human neutrophilic cellular model. BMC Immunol. 2008. 9: 14. (Pubitemid 351566887)
63. Lavastre, V., Chiasson, S., Cavalli, H. and Girard, D., Viscum album agglutinin-I (VAA-I) induces apoptosis and degradation of cytoskeletal proteins in human leukemia PLB-985 and X-CGD cells via caspases: lamin B1 is a novel target of VAA-I. Leuk. Res. 2005. 29: 1443-1453.
64. Benrezzak, O., Grondin, G., Sevigny, J., Gendron, F. P., Rousseau, E., D'Orleans-Juste, P. and Beaudoin, A. R., Identification and immunolocalization of two isoforms of ATP-diphosphohydrolase (ATPDase) in the pig immune system. Arch. Biochem. Biophys. 1999. 370: 314-322.