The CC Chemokine MCP-1/CCL2 in Pancreatic Cancer Progression: Regulation of Expression and Potential Mechanisms of Antimalignant Activity

Cancer Research

Volumn 63, Issue 21, 2003, Pages 7451-7461

  Monti, Paolo ^a   Leone, Biagio Eugenio ^b   Marchesi, Federica ^c   Balzano, Gianpaolo ^d   Zerbi, Alessandro ^d   Scaltrini, Francesca ^d   Pasquali, Claudio ^e   Calori, Giliola ^f   Pessi, Francesca ^d   Sperti, Cosimo ^c   Di Carlo, Valerio ^d   Allavena, Paola ^c   Piemonti, Lorenzo ^a,d  

^a Laboratory of Experimental Surgery   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c Ist di Ric Farmacol Mario Negri ^*

^d VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^e UNIVERSITY OF PADOVA   (Italy)

^f SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CHEMOKINE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1BETA; KI 67 ANTIGEN; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BLOOD LEVEL; CANCER GROWTH; CELL CYCLE; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MONOCYTE; PANCREAS CANCER; PRIORITY JOURNAL; SURVIVAL RATE;

CARCINOMA, PANCREATIC DUCTAL; CELL DIVISION; CELL LINE, TUMOR; CHEMOKINE CCL2; DISEASE PROGRESSION; HUMANS; MACROPHAGES; PANCREATIC NEOPLASMS; PROGNOSIS;

EID: 10744234018     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. Parker, S. L., Tong, T., Bolden, S., and Wingo, P. A. Cancer statistics, 1997. CA - Cancer J. Clin., 47: 5-27, 1997.
2. Wanebo, H. J., and Vezeridis, M. P. Pancreatic carcinoma in perspective. A continuing challenge. Cancer (Phila.), 78: 580-591, 1996.
3. Gudjonsson, B. Management of patients with carcinoma of the pancreas. J. Am. Coll. Surg., 183: 290-291, 1996.
4. Heywood, G., Vezeridis, M. P., and Wanebo, H. J. Surgical therapy of pancreatic cancer. Front Biosci., 3: E175-E180, 1998.
5. Evans, D. B., Lee, J. E., Pisters, P. W., Charnsangavej, C., Ellis, L. M., Chiao, P. J., Lenzi, R., and Abbruzzese, J. L. Advances in the diagnosis and treatment of adenocarcinoma of the pancreas. Cancer Treat Res., 90: 109-125, 1997.
6. Breslin, T. M., Janjan, N. A., Lee, J. E., Pisters, P. W., Wolff, R. A., Abbruzzese, J. L., and Evans, D. B. Neoadjuvant chemoradiation for adenocarcinoma of the pancreas. Front Biosci., 3: E193-E203, 1998.
7. Bold, R. J., Hess, K. R., Pearson, A. S., Grau, A. M., Sinicrope, F. A., Jennings, M., McConkey, D. J., Bucana, C. D., Cleary, K. R., Hallin, P. A., Chiao, P. J., Abbruzzese, J. L., and Evans, D. B. Prognostic factors in resectable pancreatic cancer: p53 and bcl-2. J. Gastrointest. Surg., 3: 263-277, 1999.
8. Hawes, R. H., Xiong, Q., Waxman, I., Chang, K. J., Evans, D. B., and Abbruzzese, J. L. A multispecialty approach to the diagnosis and management of pancreatic cancer. Am. J. Gastroenterol., 95: 17-31, 2000.
9. Wolff, R. A., Chiao, P., Lenzi, R., Pisters, P. W., Lee, J. E., Janjan, N. A., Crane, C. H., Evans, D. B., and Abbruzzese, J. L. Current approaches and future strategies for pancreatic carcinoma. Investig. New Drugs, 18: 43-56, 2000.
10. Abbruzzese, J. L. New applications of gemcitabine and future directions in the management of pancreatic cancer. Cancer (Phila.), 95: 941-945, 2002.
11. Ozawa, F., Friess, H., Tempia-Caliera, A., Kleff, J., and Buchler, M. W. Growth factors and their receptors in pancreatic cancer. Teratog. Carcinog. Mutagen., 21: 27-44, 2001.
12. Shi, X., Friess, H., Kleeff, J., Ozawa, F., and Buchler, M. W. Pancreatic cancer: factors regulating tumor development, maintenance and metastasis. Pancreatology, 1: 517-524, 2001.
13. Farrow, B., and Evers, B. M. Inflammation and the development of pancreatic cancer. Surg. Oncol., 10: 153-169, 2002.
14. Mantovani, A. Chemokines. Introduction and overview. Chem. Immunol., 72: 1-6, 1999.
15. Shi, Q., Abbruzzese, J. L., Huang, S., Fidler, I. J., Xiong, Q., and Xie, K. Constitutive and inducible interleukin 8 expression by hypoxia and acidosis renders human pancreatic cancer cells more tumorigenic and metastatic. Clin. Cancer Res., 5: 3711-3721, 1999.
16. Miyamoto, M., Shimizu, Y., Okada, K., Kashii, Y., Higuchi, K., and Watanabe, A. Effect of interleukin-8 on production of tumor-associated substances and autocrine growth of human liver and pancreatic cancer cells. Cancer Immunol. Immunother., 47: 47-57, 1998.
17. Blanchard, J. A., II, Barve, S., Joshi-Barve, S., Talwalker, R., and Gates, L. K., Jr. Cytokine production by CAPAN-1 and CAPAN-2 cell lines. Dig. Dis. Sci., 45: 927-932, 2000.
18. Takamori, H., Oades, Z. G., Hoch, O. C., Burger, M., and Schraufstatter, I. U. Autocrine growth effect of IL-8 and GROα on a human pancreatic cancer cell line, Capan-1. Pancreas, 21: 52-56, 2000.
19. Shi, Q., Le, X., Wang, B., Xiong, Q., Abbruzzese, J. L., and Xie, K. Regulation of interleukin-8 expression by cellular pH in human pancreatic adenocarcinoma cells. J. Interferon. Cytokine. Res., 20: 1023-1028, 2000.
20. Xiong, Q., Shi, Q., Le, X., Wang, B., and Xie, K. Regulation of interleukin-8 expression by nitric oxide in human pancreatic adenocarcinoma. J. Interferon. Cytokine. Res., 21: 529-537, 2001.
21. Xie, K. Interleukin-8 and human cancer biology. Cytokine Growth Factor Rev., 12: 375-391, 2001.
22. Wigmore, S. J., Fearon, K. C., Sangster, K., Maingay, J. P., Garden, O. J., and Ross, J. A. Cytokine regulation of constitutive production of interleukin-8 and -6 by human pancreatic cancer cell lines and serum cytokine concentrations in patients with pancreatic cancer. Int. J. Oncol., 21: 881-886, 2002.
23. Shi, Q., Le, X., Abbruzzese, J. L., Wang, B., Mujaida, N., Matsushima, K., Huang, S., Xiong, Q., and Xie, K. Cooperation between transcription factor AP-1 and NF-κB in the induction of interleukin-8 in human pancreatic adenocarcinoma cells by hypoxia. J. Interferon. Cytokine. Res., 19: 1363-1371, 1999.
24. Le, X., Shi, Q., Wang, B., Xiong, Q., Qian, C., Peng, Z., Li, X. C., Tang, H., Abbruzzese, J. L., and Xie, K. Molecular regulation of constitutive expression of interleukin-8 in human pancreatic adenocarcinoma. J. Interferon. Cytokine. Res., 20: 935-946, 2000.
25. Wigmore, S. J., Fearon, K. C., Maingay, J. P., Lai, P. B., and Ross, J. A. Interleukin-8 can mediate acute-phase protein production by isolated human hepatocytes. Am. J. Physiol., 273: E720-E726, 1997.
26. Yamada, T., Okajima, F., Adachi, M., Ohwada, S., and Kondo, Y. Growth dependency of a new human pancreatic cancer cell line, YAPC, on autocrine interleukin-1α stimulation. Int. J. Cancer, 76: 141-147, 1998.
27. Takaya, H., Andoh, A., Shimada, M., Hata, K., Fujiyama, Y., and Bamba, T. The expression of chemokine genes correlates with nuclear factor-κB activation in human pancreatic cancer cell lines. Pancreas, 21: 32-40, 2000.
28. Shimada, M., Andoh, A., Araki, Y., Fujiyama, Y., and Bamba, T. Ligation of the Fas antigen stimulates chemokine secretion in pancreatic cancer cell line PANC-1. J. Gastroenterol. Hepatol., 16: 1060-1067, 2001.
29. Bottazzi, B., Polentarutti, N., Acero, R., Balsari, A., Boraschi, D., Ghezzi, P., Salmona, M., and Mantovani, A. Regulation of the macrophage content of neoplasms by chemoattractants. Science (Wash. DC), 220: 210-212, 1983.
30. Negus, R. P., Stamp, G. W., Hadley, J., and Balkwill, F. R. Quantitative assessment of the leukocyte infiltrate in ovarian cancer and its relationship to the expression of C-C chemokines. Am. J. Pathol., 150: 1723-1734, 1997.
31. Balkwill, F., and Mantovani, A. Inflammation and cancer: back to Virchow? Lancet, 357: 539-545, 2001.
32. Brigati, C., Noonan, D. M., Albini, A., and Benelli, R. Tumors and inflammatory infiltrates: friends or foes? Clin. Exp. Metastasis, 19: 247-258, 2002.
33. Mantovani, A., Bottazzi, B., Colotta, F., Sozzani, S., and Ruco, L. The origin and function of tumor-associated macrophages. Immunol. Today, 13: 265-270, 1992.
34. Mantovani, A. Tumor-associated macrophages in neoplastic progression: a paradigm for the in vivo function of chemokines. Lab. Investig., 71: 5-16, 1994.
35. Peri, G., Milanese, C., Matteucci, C., Ruco, L., Zhou, D., Sozzani, S., Coletta, I., and Mantovani, A. A new monoclonal antibody (5D3-F7) which recognizes human monocyte-chemotactic protein-1 but not related chemokines. Development of a sandwich ELISA and in situ detection of producing cells. J. Immunol. Methods, 174: 249-257, 1994.
36. Sironi, M., Pozzi, P., Polentarutti, N., Benigni, F., Coletta, I., Guglielmotti, A., Milanese, C., Ghezzi, P., Vecchi, A., Pinza, M., and Mantovani, A. Inhibition of inflammatory cytokine production and protection against endotoxin toxicity by benzydamine. Cytokine, 8: 710-716, 1996.
37. Polentarutti, N., Allavena, P., Bianchi, G., Giardina, G., Basile, A., Sozzani, S., Mantovani, A., and Introna, M. IL-2-regulated expression of the monocyte chemotactic protein-1 receptor (CCR2) in human NK cells: characterization of a predominant 3.4-kilobase transcript containing CCR2B and CCR2A sequences. J. Immunol., 158: 2689-2694, 1997.
38. Piemonti, L., Monti, P., Zerbi, A., Balzano, G., Allavena, P., and Di Carlo, V. Generation and functional characterization of dendritic cells from patients with pancreatic carcinoma with special regard to clinical applicability. Cancer Immunol. Immunother., 49: 544-550, 2000.
39. Negus, R. P., Stamp, G. W., Relf, M. G., Burke, F., Malik, S. T., Bernasconi, S., Allavena, P., Sozzani, S., Mantovani, A., and Balkwill, F. R. The detection and localization of monocyte chemoattractant protein-1 (MCP-1) in human ovarian cancer. J. Clin. Investig., 95: 2391-2396, 1995.
40. 1 arrest and an increase of the cyclin-dependent kinase inhibitor p21WAF1/CIP1. Cell Growth Differ., 9: 611-617, 1998.
41. Coussens, L. M., and Werb, Z. Inflammation and cancer. Nature (Lond.), 420: 860-867, 2002.
42. Ueno, T., Toi, M., Saji, H., Muta, M., Bando, H., Kuroi, K., Koike, M., Inadera, H., and Matsushima, K. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin. Cancer Res., 6: 3282-3289, 2000.
43. Goede, V., Brogelli, L., Ziche, M., and Augustin, H. G. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int. J. Cancer, 82: 765-770, 1999.
44. Salcedo, R., Ponce, M. L., Young, H. A., Wasserman, K., Ward, J. M., Kleinman, H. K., Oppenheim, J. J., and Murphy, W. J. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood, 96: 34-40, 2000.
45. Leek, R. D., Talks, K. L., Pezzella, F., Turley, H., Campo, L., Brown, N. S., Bicknell, R., Taylor, M., Gatter, K. C., and Harris, A. L. Relation of hypoxia-inducible factor-2α (HIF-2α) expression in tumor-infiltrative macrophages to tumor angiogenesis and the oxidative thymidine phosphorylase pathway in human breast cancer. Cancer Res., 62: 1326-1329, 2002.
46. Arlt, A., Vorndamm, J., Muerkoster, S., Yu, H., Schmidt, W. E., Folsch, U. R., and Schafer, H. Autocrine production of interleukin 1β confers constitutive nuclear factor κB activity and chemoresistance in pancreatic carcinoma cell lines. Cancer Res., 62: 910-916, 2002.
47. Engelken, F. J., Bettschart, V., Rahman, M. Q., Parks, R. W., and Garden, O. J. Prognostic factors in the palliation of pancreatic cancer. Eur. J. Surg. Oncol., 29: 368-373, 2003.
48. Ueno, H., Okada, S., Okusaka, T., and Ikeda, M. Prognostic factors in patients with metastatic pancreatic adenocarcinoma receiving systemic chemotherapy. Oncology, 59: 296-301, 2000.
49. Tsung, K., Dolan, J. P., Tsung, Y. L., and Norton, J. A. Macrophages as effector cells in interleukin 12-induced T-cell-dependent tumor rejection. Cancer Res., 62: 5069-5075, 2002.
50. Schoppmann, S. F., Birner, P., Stockl, J., Kalt, R., Ullrich, R., Caucig, C., Kriehuber, E., Nagy, K., Alitalo, K., and Kerjaschki, D. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am. J. Pathol., 161: 947-956, 2002.
51. Johnsen, M., Lund, L. R., Romer, J., Almholt, K., and Dano, K. Cancer invasion and tissue remodeling: common themes in proteolytic matrix degradation. Curr. Opin. Cell Biol., 10: 667-671, 1998.
52. Blasi, F. Proteolysis, cell adhesion, chemotaxis, and invasiveness are regulated by the u-PA-u-PAR-PAI-1 system. Thromb. Haemost., 82: 298-304, 1999.
53. Opdenakker, G., and Van Damme, J. Chemotactic factors, passive invasion and metastasis of cancer cells. Immunol. Today, 13: 463-464, 1992.
54. Paciucci, R., Tora, M., Diaz, V. M., and Real, F. X. The plasminogen activator system in pancreas cancer: role of t-PA in the invasive potential in vitro. Oncogene, 16: 625-633, 1998.
55. Paciucci, R., Vila, M. R., Adell, T., Diaz, V. M., Tora, M., Nakamura, T., and Real, F. X. Activation of the urokinase plasminogen activator/urokinase plasminogen activator receptor system and redistribution of E-cadherin are associated with hepatocyte growth factor-induced motility of pancreas tumor cells overexpressing Met. Am. J. Pathol., 153: 201-212, 1998.
56. Koshiba, T., Hosotani, R., Wada, M., Miyamoto, Y., Fujimoto, K., Lee, J. U., Doi, R., Arii, S., and Imamura, M. Involvement of matrix metalloproteinase-2 activity in invasion and metastasis of pancreatic carcinoma. Cancer (Phila.), 82: 642-650, 1998.
57. Huang, S., Singh, R. K., Xie, K., Gutman, M., Berry, K. K., Bucana, C. D., Fidler, I. J., and Bar-Eli, M. Expression of the JE/MCP-1 gene suppresses metastatic potential in murine colon carcinoma cells. Cancer Immunol. Immunother., 39: 231-238, 1994.
58. Nakashima, E., Mukaida, N., Kubota, Y., Kuno, K., Yasumoto, K., Ichimura, F., Nakanishi, I., Miyasaka, M., and Matsushima, K. Human MCAF gene transfer enhances the metastatic capacity of a mouse cachectic adenocarcinoma cell line in vivo. Pharm. Res., 12: 1598-1604, 1995.
59. Rollins, B. J., and Sunday, M. E. Suppression of tumor formation in vivo by expression of the JE gene in malignant cells. Mol. Cell. Biol., 11: 3125-3131, 1991.
60. Hirose, K., Hakozaki, M., Nyunoya, Y., Kobayashi, Y., Matsushita, K., Takenouchi, T., Mikata, A., Mukaida, N., and Matsushima, K. Chemokine gene transfection into tumour cells reduced tumorigenicity in nude mice in association with neutrophilic infiltration. Br. J. Cancer, 72: 708-714, 1995.
61. Manome, Y., Wen, P. Y., Hershowitz, A., Tanaka, T., Rollins, B. J., Kufe, D. W., and Fine, H. A. Monocyte chemoattractant protein-1 (MCP-1) gene transduction: an effective tumor vaccine strategy for non-intracranial tumors. Cancer Immunol. Immunother., 41: 227-235, 1995.
62. Zhang, L., Yoshimura, T., and Graves, D. T. Antibody to Mac-1 or monocyte chemoattractant protein-1 inhibits monocyte recruitment and promotes tumor growth. J. Immunol., 158: 4855-4861, 1997.
63. Tonouchi, H., Miki, C., Tanaka, K., and Kusunoki, M. Profile of monocyte chemoattractant protein-1 circulating levels in gastric cancer patients. Scand J. Gastroenterol., 37: 830-833, 2002.
64. Nesbit, M., Schaider, H., Miller, T. H., and Herlyn, M. Low-level monocyte chemoattractant protein-1 stimulation of monocytes leads to tumor formation in nontumorigenic melanoma cells. J. Immunol., 166: 6483-6490, 2001.
65. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., and Sica, A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23: 549-555, 2002.
66. Wright, P., Braun, R., Babiuk, L., Littel-van den Hurk, S. D., Moyana, T., Zheng, C., Chen, Y., and Xiang, J. Adenovirus-mediated TNF-α gene transfer induces significant tumor regression in mice. Cancer Biother. Radiopharm., 14: 49-57, 1999.
67. Stoelcker, B., Ruhland, B., Hehlgans, T., Bluethmann, H., Luther, T., and Mannel, D. N. Tumor necrosis factor induces tumor necrosis via tumor necrosis factor receptor type 1-expressing endothelial cells of the tumor vasculature. Am. J. Pathol., 156: 1171-1176, 2000.
68. Thomas, W. J., Thomas, D. L., Knezetic, J. A., and Adrian, T. E. The role of oxygen-derived free radicals and nitric oxide in cytokine-induced antiproliferation of pancreatic cancer cells. Pancreas, 24: 161-168, 2002.
69. Shen, W. H., Zhou, J. H., Broussard, S. R., Freund, G. G., Dantzer, R., and Kelley, K. W. Proinflammatory cytokines block growth of breast cancer cells by impairing signals from a growth factor receptor. Cancer Res., 62: 4746-4756, 2002.
70. Kong, G., Kim, E., Kim, W., Lee, Y., Lee, J., Paik, S., Rhee, J., Choi, K., and Lee, K. Inducible nitric oxide synthase (iNOS) immunoreactivity and its relationship to cell proliferation, apoptosis, angiogenesis, clinicopathologic characteristics, and patient survival in pancreatic cancer. Int. J. Gastrointest. Cancer, 29: 133-140, 2001.