Macrophage-inflammatory protein-3α mediates epidermal growth factor receptor transactivation and ERK1/2 MAPK signaling in Caco-2 colonic epithelial cells via metalloproteinase-dependent release of amphiregulin

Journal of Immunology

Volumn 178, Issue 12, 2007, Pages 8013-8021

  Keates, Sarah ^a   Han, Xinbing ^a   Kelly, Ciarán P ^a   Keates, Andrew C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIREGULIN; CHEMOKINE RECEPTOR CCR6; EPIDERMAL GROWTH FACTOR RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUTRALIZING ANTIBODY;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CELL STRAIN CACO 2; CELL STRAIN HT29; CELL TYPE; COLON MUCOSA; CONTROLLED STUDY; ENTERITIS; EPITHELIUM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; MITOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSACTIVATION;

EID: 34250202474     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.12.8013     Document Type: Article

References (50)

1. Rossi, D., and A. Zlotnik. 2000. The biology of chemokines and their reeeptors. Annu. Rev. Immunol. 18: 217-242.
2. Mackay, C. R. 2001. Chemokines: immunology's high impact factors. Nat. Immunol. 2: 95-101.
3. 3C motif. Nature 385: 640-644.
4. Kelner, G. S., J. Kennedy, K. B. Bacon, S. Kleyensteuber, D. A. Largaespada, N. A. Jenkins, N. G. Copeland, J. F. Bazan, K. W. Moore, and T. J. Schall. 1994. Lymphotactin: a cytokine that represents a new class of chemokine. Science 266: 1395-1399.
5. Pan, Y., C. Lloyd, H. Zhou, S. Dolich, J. Deeds, J. A. Gonzalo, J. Vath, M. Gosselin, J. Ma, B. Dussault, et al. 1997. Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature 387: 611-617.
6. Tanaka, Y., T. Imai, M. Baba, I. Ishikawa, M. Uehira, H. Nomiyama, and O. Yoshie. 1999. Selective expression of liver and activation-regulated chemokine (LARC) in intestinal epithelium in mice and humans. Eur. J. Immunol. 29: 633-642.
7. Kwon, J. H., S. Keates, L. Bassani, L. F. Mayer, and A. C. Keates. 2002. Colonic epithelial cells are a major site of macrophage inflammatory protein 3α (MIP-3α) production in normal colon and inflammatory bowel disease. Gut 51: 818-826.
8. Fujiie, S., K. Hieshima, D. Izawa, T. Nakayama, R. Fujisawa, H. Ohyanagi, and O. Yoshie. 2001. Proinflammatory cytokines induce liver and activation-regulated chemokine/macrophage inflammatory protein-3α/CCL20 in mucosal epithelial cells through NF-κB. Int. Immunol. 13: 1255-1263.
9. Liao, F., R. L. Rabin, C. S. Smith, G. Sharma, T. B. Nutman, and J. M. Farber. 1999. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3α. J. Immunol. 162: 186-194.
10. Campbell, J. J., J. Hedrick, A. Zlotnik, M. A. Siani, D. A. Thompson, and E. C. Butcher. 1998. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 279: 381-384.
11. Dieu, M. C., B. Vanbervliet, A. Vicari, J. M. Bridon, E. Oldham, S. Ait-Yahia, F. Briere, A. Zlotnik, S. Lebecque, and C. Caux. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188: 373-386.
12. Power, C. A., D. J. Church, A. Meyer, S. Alouani, A. E. Proudfoot, I. Clark-Lewis, S. Sozzani, A. Mantovani, and T. N. Wells. 1997. Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3α from lung dendritic cells. J. Exp. Med. 186: 825-835.
13. Kaser, A., O. Ludwiczek, S. Holzmann, A. R. Moschen, G. Weiss, B. Enrich, I. Graziadei, S. Dunzendorfer, C. J. Wiedermann, E. Murzl, et al. 2004. Increased expression of CCL20 in human inflammatory bowel disease. J. Clin. Immunol. 24: 74-85.
14. Izadpanah, A., M. B. Dwinell, L. Eckmann, N. M. Varki, and M. F. Kagnoff. 2001. Regulated MIP-3α/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. 280: G710-G719.
15. Le, Y., Y. Zhou, P. Iribarren, and J. Wang. 2004. Chemokines and chemokine receptors: their manifold roles in homeostasis and disease. Cell Mol. Immunol. 1: 95-104.
16. Driscoll, K. E., D. G. Hassenbein, B. W. Howard, R. J. Isfort, D. Cody, M. H. Tindal, M. Suchanek, and J. M. Carter. 1995. Cloning, expression, and functional characterization of rat MIP-2: a neutrophil chemoattractant and epithelial cell mitogen. J. Leukocyte Biol. 58: 359-364.
17. Suzuki, H., M. Mori, K. Seto, F. Shibata, S. Nagahashi, C. Kawaguchi, M. Suzuki, H. Matsui, K. Watanabe, S. Miura, and H. Ishii. 2000. Rat CXC chemokine GRO/CINC-1 paradoxically stimulates the growth of gastric epithelial cells. Aliment Pharmacol. Ther. 14: 94-100.
18. Lundien, M. C., K. A. Mohammed, N. Nasreen, R. S. Tepper, J. A. Hardwick, K. L. Sanders, R. D. Van Horn, and V. B. Antony. 2002. Induction of MCP-1 expression in airway epithelial cells: role of CCR2 receptor in airway epithelial injury. J. Clin. Immunol. 22: 144-152.
19. Dwinell, M. B., L. Eckmann, J. D. Leopard, N. M. Varki, and M. F. Kagnoff. 1999. Chemokine receptor expression by human intestinal epithelial cells. Gastroenterology 117: 359-367.
20. Pearson, G., F. Robinson, T. Beers Gibson, B. E. Xu, M. Karandikar, K. Berman, and M. H. Cobb. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22: 153-183.
21. Yoon, S., and R. Seger. 2006. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 24: 21-44.
22. Pai, R., B. Soreghan, I. L. Szabo, M. Pavelka, D. Baatar, and A. S. Tarnawski. 2002. Prostaglandin E2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy. Nat. Med. 8: 289-293.
23. Keely, S. J., J. M. Uribe, and K. E. Barrett. 1998. Carbachol stimulates transactivation of epidermal growth factor receptor and mitogen-activated protein kinase in T84 cells: implications for carbachol-stimulated chloride secretion. J. Biol. Chem. 273: 27111-27117.
24. Koon, H. W., D. Zhao, X. Na, M. P. Moyer, and C. Pothoulakis. 2004. Metalloproteinases and transforming growth factor-α mediate substance P-induced mitogen-activated protein kinase activation and proliferation in human colonocytes. J. Biol. Chem. 279: 45519-45527.
25. Zhao, D., Y. Zhan, H. W. Koon, H. Zeng, S. Keates, M. P. Moyer, and C. Pothoulakis. 2004. Metalloproteinase-dependent transforming growth factor-α release mediates neurotensin-stimulated MAP kinase activation in human colonic epithelial cells. J. Biol. Chem. 279: 43547-43554.
26. Blobel, C. P. 2005. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 6: 32-43.
27. Fischer, O. M., S. Hart, A. Gschwind, and A. Ullrich. 2003. EGFR signal transactivation in cancer cells. Biochem. Soc. Trans. 31: 1203-1208.
28. Baba, M., T. Imai, M. Nishimura, M. Kakizaki, S. Takagi, K. Hieshima, H. Nomiyama, and O. Yoshie. 1997. Identification of CCR6, the specific receptor for a novel lymphocyte-directed CC chemokine LARC. J. Biol. Chem. 272: 14893-14898.
29. Greaves, D. R., W. Wang, D. J. Dairaghi, M. C. Dieu, B. Saint-Vis, K. Franz-Bacon, D. Rossi, C. Caux, T. McClanahan, S. Gordon, et al. 1997. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3α and is highly expressed in human dendritic cells. J. Exp. Med. 186: 837-844.
30. Devalaraja, R. M., L. B. Nanney, J. Du, Q. Qian, Y. Yu, M. N. Devalaraja, and A. Richmond. 2000. Delayed wound healing in CXCR2 knockout mice. J. Invest. Dermatol. 115: 234-244.
31. Ottaiano, A., A. di Palma, M. Napolitano, C. Pisano, S. Pignata, F. Tatangelo, G. Botti, A. M. Acquaviva, G. Castello, P. A. Ascierto, et al. 2005. Inhibitory effects of anti-CXCR4 antibodies on human colon cancer cells. Cancer Immunol. Immunother. 54: 781-791.
32. Aksoy, M. O., Y. Yang, R. Ji, P. J. Reddy, S. Shahabuddin, J. Litvin, T. J. Rogers, and S. G. Kelsen, 2006. CXCR3 surface expression in human airway epithelial cells: cell cycle dependence and effect on cell proliferation. Am. J. Physiol. 290: L909-L918.
33. Brand, S., T. Olszak, F. Beigel, J. Diebold, J.-M. Otte, S. T. Eichhorst, B. Göke, and J. Dambacher. 2005. Cell differentiation dependent expressed CCR6 mediates ERK-1/2, SAPK/JNK, and Akt signaling resulting in proliferation and migration of colorectal cancer cells. J. Cell. Biochem. 97: 709-723.
34. Yang, C. C., H. Ogawa, M. B. Dwinell, D. F. McCole, L. Eckmann, and M. F. Kagnoff. 2005. Chemokine receptor CCR6 transduces signals that activate p130Cas and alter cAMP-stimulated ion transport in human intestinal epithelial cells. Am. J. Physiol. 288: C321-C328.
35. Na, X., D. Zhao, H. W. Koon, H. Kim, J. Husmark, M. P. Moyer, C. Pothoulakis, and J. T. LaMont. 2005. Clostridium difficile toxin B activates the EGF receptor and the ERK/MAP kinase pathway in human colonocytes. Gastroenterology 128: 1002-1011.
36. + Helicobacter pylori induce transactivation of the epidermal growth factor receptor in AGS gastric epithelial cells. J. Biol. Chem. 276: 48127-48134.
37. Adachi, T., C. H. Cui, A. Kanda, H. Kayaba, K. Ohta, and J. Chihara. 2004. Activation of epidermal growth factor receptor via CCR3 in bronchial epithelial cells. Biochem. Biophys. Res. Commun. 320: 292-296.
38. Venkatakrishnan, G., R. Salgia, and J. E. Groopman. 2000. Chemokine receptors CXCR-1/2 activate mitogen-activated protein kinase via the epidermal growth factor receptor in ovarian cancer cells. J. Biol. Chem. 275: 6868-6875.
39. Tanida, S., T. Joh, K. Itoh, H. Kataoka, M. Sasaki, H. Ohara, T. Nakazawa, T. Nomura, Y. Kinugasa, H. Ohmoto, et al. 2004. The mechanism of cleavage of EGFR ligands induced by inflammatory cytokines in gastric cancer cells. Gastroenterology 127: 559-569.
40. Itoh, Y., T. Joh, S. Tanida, M. Sasaki, H. Kataoka, K. Itoh, T. Oshima, N. Ogasawara, S. Togawa, T. Wada, et al. 2005. IL-8 promotes cell proliferation and migration through metalloproteinase-cleavage proHB-EGF in human colon carcinoma cells. Cytokine 29: 275-282.
41. Gschwind, A., S. Hart, O. M. Fischer, and A. Ullrich. 2003. TACE cleavage of proamphiregulin regulates GPCR-induccd proliferation and motility of cancer cells. EMBO J. 22: 2411-2421.
42. Gschwind, A., N. Prenzel, and A. Ullrich. 2002. Lysophosphatidic acid-induced squamous cell carcinoma cell proliferation and motility involves epidermal growth factor receptor signal transactivation. Cancer Res. 62: 6329-6336.
43. Lemjabbar, H., D. Li, M. Gallup, S. Sidhu, E. Drori, and C. Basbaum. 2003. Tobacco smoke-induced lung cell proliferation mediated by tumor necrosis factor α-converting enzyme and amphiregulin. J. Biol. Chem. 278: 26202-26207.
44. Seals, D. F., and S. A. Courtneidge. 2003. The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17: 7-30.
45. Fan, H., and R. Derynck. 1999. Ectodomain shedding of TGF-α and other transmembrane proteins is induced by receptor tyrosine kinase activation and MAP kinase signaling cascades. EMBO J. 18: 6962-6972.
46. Díaz-Rodríguez, E., J. C. Montero, A. Esparis-Ogando, L. Yuste, and A. Pandiella. 2002. Extracellular signal-regulated kinase phosphorylates tumor necrosis factor α-converting enzyme at threonine 735: a potential role in regulated shedding. Mol. Biol. Cell 13: 2031-2044.
47. Fan, H., C. W. Turck, and R. Derynck. 2003. Characterization of growth factor-induced serine phosphorylation of tumor necrosis factor-α converting enzyme and of an alternatively translated polypeptide. J. Biol. Chem. 278: 18617-18627.
48. Peiretti, F., P. Deprez-Beauclair, B. Bonardo, H. Aubert, I. Juhan-Vague, and G. Nalbone. 2003. Identification of SAP97 as an intracellular binding partner of TACE. J. Cell Sci. 116: 1949-1957.
49. Zheng, Y., J. Schlondorff, and C. P. Blobel. 2002. Evidence for regulation of the tumor necrosis factor α-convertase (TACE) by protein-tyrosine phosphatase PTPH1. J. Biol. Chem. 277: 42463-42470.
50. Nelson, K. K., J. Schlondorff, and C. P. Blobel. 1999. Evidence for an interaction of the metalloprotease-disintegrin tumour necrosis factor α convertase (TACE) with mitotic arrest deficient 2 (MAD2), and of the metalloprotease-disintegrin MDC9 with a novel MAD2-related protein, MAD2β. Biochem. J. 343: 673-680.