Src as the link between inflammation and cancer

Frontiers in Physiology

Volumn 4 JAN, Issue , 2014, Pages

  Liu, Sandy T ^a,b   Pham, Hung ^a   Pandol, Stephen J ^a,b,c   Ptasznik, Andrzej ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Veterans Affairs ^*  (United States)

Author keywords

Cancer; Chronic pancreatitis; Cytokines; Inflammation; Pancreatic cancer; Src

Indexed keywords

EID: 84893475696     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00416     Document Type: Review

References (73)

1. Abram, C. L., and Lowell, C. A. (2008). The diverse functions of Src family kinases in macrophages. Front. Biosci. 13, 4426-4450. doi: 10.2741/3015.
2. Aligayer, H., Boyd, D. D., Heiss, M. M., Abdalla, E. K., Curley, S. A., and Gallick, G. E. (2002). Activation of Src kinase in primary colorectal carcinoma: an indicator of poor clinical prognosis. Cancer 94, 344-351. doi: 10.1002/cncr.10221.
3. Balkwill, F. (2004). The significance of cancer cell expression of the chemokine receptor CXCR4. Semin. Cancer Biol. 14, 171-179. doi: 10.1016/j.semcancer.2003.10.003.
4. Balkwill, F., Charles, K. A., and Mantovani, A. (2005). Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7, 211-217. doi: 10.1016/j.ccr.2005.02.013.
5. Bernstein, C. N., Blanchard, J. F., Kliewer, E., and Wajda, A. (2001). Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 91, 854-862. doi: 10.1002/1097-0142(20010215)91:4<854::AID-CNCR1073>3.0.CO;2-Z.
6. Brugge, J. S., and Erikson, R. L. (1997). Identification of a transformation-specific antigen induced by an avian sarcome virus. Nature 269, 346-348. doi: 10.1038/269346a0.
7. Chen, Y. Y., Malik, M., Tomkowicz, B. E., Collman, R. G., and Ptasznik, A. (2008). BCR-ABL1 alters SDF-1alpha-mediated adhesive responses through the beta2 integrin LFA-1 in leukemia cells. Blood 111, 5182-5186. doi: 10.1182/blood-2007-10-117705.
8. Cheung, R., Malik, M., Ravyn, V., Tomkowicz, B., Ptasznik, A., and Collman, R. G. (2009). An arrestin-dependent multi-kinase signaling complex mediates MIP-1beta/CCL4 signaling and chemotaxis of primary human macrophages. J. Leukoc. Biol. 86, 833-845. doi: 10.1189/jlb.0908551.
9. Cheung, R., Ravyn, V., Wang, L., Ptasznik, A., and Collman, R. G. (2008). Signaling mechanism of HIV-1 gp120 and virion-induced IL-1beta release in primary human macrophages. J. Immunol. 180, 6675-6684.
10. Coppola, D. (2000). Molecular prognostic markers in pancreatic cancer. Cancer Control 7, 421-427.
11. Coussens, L. M., and Werb, Z. (2002). Inflammation and cancer. Nature 420, 860-867. doi: 10.1038/nature01322.
12. Díte, P., Hermanová, M., Trna, J., Novotnỳ, I., Ružièka, M., Liberda, M., et al. (2012). The role of chronic inflammation: chronic pancreatitis as a risk factor of pancreatic cancer. Dig. Dis. 30, 277-283. doi: 10.1159/000336991.
13. Duell, E. J., Casella, D. P., Burk, R. D., Kelsey, K. T., and Holly, E. A. (2006). Inflammation, genetic polymorphisms in proinflammatory genes TNF-A, RANTES, and CCR5, and risk of pancreatic adenocarcinoma. Cancer Epidemiol. Biomarkers Prev. 15, 726-731. doi: 10.1158/1055-9965.EPI-05-0797.
14. Eaden, J. A., Abrams, K. R., and Mayberry, J. F. (2001). The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48, 526-535. doi: 10.1136/gut.48.4.526.
15. Erkan, M., Hausmann, S., Michalski, C. W., Fingerle, A. A., Dobritz, M., Kleeff, J., et al. (2012). The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat. Rev. Gastroenterol. Hepatol. 9, 454-467. doi: 10.1038/nrgastro.2012.115.
16. Feig, C., Gopinathan, A., Neesse, A., Chan, D. S., Cook, N., and Tuveson, D. A. (2012). The pancreas cancer microenvironment. Clin. Cancer Res. 18, 4266-4276. doi: 10.1158/1078-0432.CCR-11-3114.
17. Fu, Y., Zagozdzon, R., Avraham, R., and Avraham, H. K. (2006). CHK negatively regulates Lyn kinase and suppresses pancreatic cancer invasion. Int. J. Oncol. 29, 1453-1458.
18. Gao, Z., Wang, X., Wu, K., Zhao, Y., and Hu, G. (2010). Pancreatic stellate cells increase the invasion of human pancreatic cancer cells through the stromal cell-derived factor-1/CXCR4 axis. Pancreatology 10, 186-193. doi: 10.1159/000236012.
19. Go, V. L., Gukovskaya, A., and Pandol, S. J. (2005). Alcohol and pancreatic cancer. Alcohol 35, 205-211. doi: 10.1016/j.alcohol.2005.03.010.
20. Goecke, H., Forssmann, U., Uguccioni, M., Friess, H., Conejo-Garcia, J. R., Zimmermann, A., et al. (2000). Macrophages infiltrating the tissue in chronic pancreatitis express the chemokine receptor CCR5. Surgery 128, 806-814. doi: 10.1067/msy.2000.108613.
21. Guerra, C., Schuhmacher, A. J., Cañamero, M., Grippo, P. J., Verdaguer, L., Pérez-Gallego, L., et al. (2007). Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 11, 291-302. doi: 10.1016/j.ccr.2007.01.012.
22. Hallek, M., Neumann, C., Schäffer, M., Danhauser-Riedl, S., von Bubnoff, N., de Vos, G., et al. (1997). Signal transduction of interleukin-6 involves tyrosine phosphorylation of multiple cytosolic proteins and activation of Src-family kinases Fyn, Hck, and Lyn in multiplemyeloma cell lines. Exp. Hematol. 25, 1367-1377.
23. Howes, N., Lerch, M. M., Greenhalf, W., Stocken, D. D., Ellis, I., Simon, P., et al. (2004). Clinical and genetic characteristics of hereditary pancreatitis in Europe. Clin. Gastroenterol. Hepatol. 2, 252-261. doi: 10.1016/S1542-3565(04)00013-8.
24. Hunter, T., and Sefton, B. M. (1980). Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc. Natl. Acad. Sci. U.S.A. 77, 1311-1315. doi: 10.1073/pnas.77.3.1311.
25. Inngjerdingen, M., Torgersen, K. M., and Maghazachi, A. A. (2002). Lck is required for stromal cell-derived factor 1 alpha (CXCL12)-induced lymphoid cell chemotaxis. Blood. 15, 99, 4318-4325. doi: 10.1182/blood.V99.12.4318.
26. Ito, Y., Lugea, A., Pandol, S. J., and McCuskey, R. S. (2007). Substance P mediates cerulein-induced pancreatic microcirculatory dysfunction in mice. Pancreas 34, 138-143. doi: 10.1097/01.mpa.0000246663.30751.24.
27. Itzkowitz, S. H., and Yio, X. (2004). Inflammation and cancer IV. colorectal cancer in inflammatory bowel disease: the role of inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G7-G17. doi: 10.1152/ajpgi.00079.2004.
28. Kayali, A. G., Van Gunst, K., Campbell, I. L., Stotland, A., Kritzik, M., Liu, G., et al. (2003). The stromal cell-derived factor-1alpha/CXCR4 ligand-receptor axis is critical for progenitor survival and migration in the pancreas. J. Cell Biol. 163, 859-869. doi: 10.1083/jcb.200304153.
29. Kulbe, H., Levinson, N. R., Balkwill, F., and Wilson, J. L. (2004). The chemokine network in cancer-much more than directing cell movement. Int. J. Dev. Biol. 48, 489-496. doi: 10.1387/ijdb.041814hk.
30. Lin, M. T., Lin, B. R., Chang, C. C., Chu, C. Y., Su, H. J., Chen, S. T., et al. (2007). IL-6 induces AGS gastric cancer cell invasion via activation of the c-Src/RhoA/ROCK signaling pathway. Int. J. Cancer. 120, 2600-2608. doi: 10.1002/ijc.22599.
31. Liou, G. Y., Döppler, H., Necela, B., Krishna, M., Crawford, H. C., Raimondo, M., et al. (2013). Macrophage-secreted cytokines drive pancreatic acinar-to-ductal metaplasia through NF-κB and MMPs. J. Cell Biol. 202, 563-577. doi: 10.1083/jcb.201301001.
32. Lowenfels, A. B., Maisonneuve, P., Whitcomb, D. C., Lerch, M. M., and DiMagno, E. P. (2001). Cigarette smoking as a risk factor for pancreatic cancer in patients with hereditary pancreatitis. JAMA 286, 169-170. doi: 10.1001/jama.286.2.169.
33. Lutz, M. P., Esser, I. B., Flossmann-Kast, B. B., Vogelmann, R., Lührs, H., Friess, H., et al. (1998). Overexpression and activation of the tyrosine kinase Src in human pancreatic carcinoma. Biochem. Biophys. Res. Commun. 243, 503-508. doi: 10.1006/bbrc.1997.8043.
34. Maisonneuve, P., Lowenfels, A. B., Müllhaupt, B., Cavallini, G., Lankisch, P. G., Andersen, J. R., et al. (2005). Cigarette smoking accelerates progression of alcoholic chronic pancreatitis. Gut 54, 510-514. doi: 10.1136/gut.2004.039263.
35. Malik, M., Chen, Y. Y., Kienzle, M. F., Tomkowicz, B. E., Collman, R. G., and Ptasznik, A. (2008). Monocyte migration and LFA-1-mediated attachment to brain microvascular endothelia is regulated by SDF-1 alpha through Lyn kinase. J. Immunol. 181, 4632-4637.
36. Mantovani, A., Allavena, P., Sica, A., and Balkwill, F. (2008). Cancer-related inflammation. Nature 454, 436-444. doi: 10.1038/nature07205.
37. Momi, N., Kaur, S., Ponnusamy, M. P., Kumar, S., Wittel, U. A., and Batra, S. K. (2012). Interplay between smoking-induced genotoxicity and altered signaling in pancreatic carcinogenesis. Carcinogenesis 33, 1617-1628. doi: 10.1093/carcin/bgs186.
38. Nakata, Y., Tomkowicz, B., Gewirtz, A. M., and Ptasznik, A. (2006). Integrin inhibition through Lyn-dependent cross talk from CXCR4 chemokine receptors in normal human CD34+ marrow cells. Blood 107, 4234-4239. doi: 10.1182/blood-2005-08-3343.
39. Nordskog, B. K., Blixt, A. D., Morgan, W. T., Fields, W. R., and Hellmann, G. M. (2003). Matrix-degrading and pro-inflammatory changes in human vascular endothelial cells exposed to cigarette smoke condensate. Cardiovasc. Toxicol. 3, 101-117. doi: 10.1385/CT:3:2:101.
40. Okenwa, C., Kumar, A., Rego, D., Konarski, Y., Nilchi, L., Wright, K., et al. (2013). SHP-1-Pyk2-Src protein complex and p38 MAPK pathways independently regulate IL-10 production in lipopolysaccharide-stimulated macrophages. J. Immunol. 191, 2589-2603. doi: 10.4049/jimmunol.1300466.
41. Orlicek, S. L., Hanke, J. H., and English, B. K. (1999). The src family-selective tyrosine kinase inhibitor PP1 blocks LPS and IFN-gamma-mediated TNF and iNOS production in murine macrophages. Shock 12, 350-354. doi: 10.1097/00024382-199911000-00004.
42. Pannala, R., Basu, A., Petersen, G. M., and Chari, S. T. (2009). New-onset diabetes: a potential clue to the early diagnosis of pancreatic cancer. Lancet Oncol. 10, 88-95. doi: 10.1016/S1470-2045(08)70337-1.
43. Peruzzi, B., Cappariello, A., Del Fattore, A., Rucci, N., De Benedetti, F., and Teti, A. (2012). c-Src and IL-6 inhibit osteoblast differentiation and integrate IGFBP5 signalling. Nat. Commun. 3, 630. doi: 10.1038/ncomms1651.
44. Podar, K., Mostoslavsky, G., Sattler, M., Tai, Y. T., Hayashi, T., Catley, L. P., et al. (2004). Critical role for hematopoietic cell kinase (Hck)-mediated phosphorylation of Gab1 and Gab2 docking proteins in interleukin 6-induced proliferation and survival of multiple myeloma cells. J. Biol. Chem. 279, 21658-21665. doi: 10.1074/jbc.M305783200.
45. Ptasznik, A., Prossnitz, E. R., Yoshikawa, D., Smrcka, A., Traynor-Kaplan, A. E., and Bokoch, G. M. (1996). A tyrosine kinase signaling pathway accounts for the majority of phosphatidylinositol 3,4,5-trisphosphate formation in chemoattractant-stimulated human neutrophils. J. Biol. Chem. 271, 25204-25207. doi: 10.1074/jbc.271.41.25204.
46. Ptasznik, A., Traynor-Kaplan, A., and Bokoch, G. M. (1995). G protein-coupled chemoattractant receptors regulate Lyn tyrosine kinase.Shc adapter protein signaling complexes. J. Biol. Chem. 270, 19969-19973. doi: 10.1074/jbc.270.34.19969.
47. Ramnath, R. D., and Bhatia, M. (2006). Substance P treatment stimulates chemokine synthesis in pancreatic acinar cells via the activation of NF-kappaB. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G1113-G1119. doi: 10.1152/ajpgi.00177.2006.
48. Ramnath, R. D., Sun, J., and Bhatia, M. (2009). Involvement of SRC family kinases in substance P-induced chemokine production in mouse pancreatic acinar cells and its significance in acute pancreatitis. J. Pharmacol. Exp. Ther. 329, 418-428. doi: 10.1124/jpet.108.148684.
49. Rebours, V., Boutron-Ruault, M. C., Schnee, M., Férec, C., Le Maréchal, C., Hentic, O., et al. (2009). The natural history of hereditary pancreatitis: a national series. Gut 58, 97-103. doi: 10.1136/gut.2008.149179.
50. Rous, P. (1911). A sarcoma of the fowl transmissible by an aget seperable from the tumor cells. J Exp. Med. 13, 397-411. doi: 10.1084/jem.13.4.397.
51. Sarang, Z., Koroskenyi, K., Pallai, A., Duro, E., Melino, G., Griffin, M., et al. (2011). Translutaminase 2 null macrophages respond to lipopolysaccharide stimulation by elevated proinflammatory ctyokine production due to an enhanced a?β3 integrin-induced Src tyrosine kinase sinaling. Immunol. Lett. 138, 71-78. doi: 10.1016/j.imlet.2011.03.004.
52. Satoh, A., Gukovskaya, A. S., Edderkaoui, M., Daghighian, M. S., Reeve, J. R. Jr, Shimosegawa, T., et al. (2005). Tumor necrosis factor-alpha mediates pancreatitis responses in acinar cells via protein kinase C and proline-rich tyrosine kinase 2. Gastroenterology 129, 639-651. doi: 10.1016/j.gastro.2005.05.005.
53. Sell, H., Habich, C., and Eckel, J. (2012). Adaptive immunity in obesity and insulin resistance. Nat. Rev. Endocrinol. 8, 709-716. doi: 10.1038/nrendo.2012.114.
54. Shi, C., Andersson, R., Zhao, X., and Wang, X. (2005). Potential role of reactive oxygen species in pancreatitis-associated multiple organ dysfunction. Pancreatology 5, 492-500. doi: 10.1159/000087063.
55. Shields, D. J., Murphy, E. A., Desgrosellier, J. S., Mielgo, A., Lau, S. K., Barnes, L. A., et al. (2011). Oncogenic Ras/Src cooperativity in pancreatic neoplasia. Oncogene 30, 2123-2134. doi: 10.1038/onc.2010.589.
56. Shoelson, S. E., Herrero, L., and Naaz, A. (2007). Obesity, inflammation, and insulin resistance. Gastroenterology 132, 2169-2180. doi: 10.1053/j.gastro.2007.03.059.
57. Smolinska, M. J., Page, T. H., Urbaniak, A. M., Mutch, B. E., and Horwood, N. J. (2011). Hck tyrosine kinase regulates TLR4-induced TNF and IL-6 production via AP-1. J. Immunol. 187, 6043-6051. doi: 10.4049/jimmunol.1100967.
58. Spaeth, E., Klopp, A., Dembinski, J., Andreeff, M., and Marini, F. (2008). Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther. 15, 730-738. doi: 10.1038/gt.2008.39.
59. Staley, C. A., Parikh, N. U., and Gallick, G. E. (1997). Decreased tumorigenicity of a human colon adenocarcinoma cell line by an antisense expression vector specific for c-Src. Cell Growth Differ. 8, 269-274.
60. Stehelin, D., Varmus, H. E., Bishop, J. M., and Vogt, P. K. (1976). DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature 260, 170-173. doi: 10.1038/260170a0.
61. Summy, J. M., Trevino, J. G., Baker, C. H., and Gallick, G. E. (2005). c-Src regulates constitutive and EGF-mediated VEGF expression in pancreatic tumor cells through activation of phosphatidyl inositol-3 kinase and p38 MAPK. Pancreas 31, 263-274. doi: 10.1097/01.mpa.0000178280.50534.0c.
62. Takatomo, K., Ryo, H., Yoshiharu, M., Jun, I., Shoichiro, T., Sanae, N., et al. (2000). Expression of stromal cell-derived factor 1 and CXCR4 ligand receptor system in pancreatic cancer: a possible role for tumor progression. Clin. Cancer Res. 6, 3530-3535.
63. Talamini, G., Bassi, C., Falconi, M., Sartori, N., Salvia, R., Rigo, L., et al. (1999). Alcohol and smoking as risk factors in chronic pancreatitis and pancreatic cancer. Dig. Dis. Sci. 44, 1303-1311. doi: 10.1023/A:1026670911955.
64. Terzic, J., Grivennikov, S., Karin, E., and Karin, M. (2010). Inflammation and colon cancer. Gastroenterology 138, 2101-2114. doi: 10.1053/j.gastro.2010.01.058.
65. Tomkowicz, B., Lee, C., Ravyn, V., Cheung, R., Ptasznik, A., and Collman, R. G. (2006). The Src kinase Lyn is required for CCR5 signaling in response to MIP-1beta and R5 HIV-1 gp120 in human macrophages. Blood 108, 1145-1150. doi: 10.1182/blood-2005-12-012815.
66. Trevino, J. G., Summy, J. M., Lesslie, D. P., Parikh, N. U., Hong, D. S., Lee, F. Y., et al. (2006). Inhibition of SRC expression and activity inhibits tumor progression and metastasis of human pancreatic adenocarcinoma cells in an orthotopic nude mouse model. Am. J. Pathol. 168, 962-972. doi: 10.2353/ajpath.2006.050570.
67. Trinchieri, G. (2012). Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu. Rev. Immunol. 30, 677-706. doi: 10.1146/annurev-immunol-020711-075008.
68. Ullman, T. A., and Itzkowitz, S. H. (2011). Intestinal inflammation and cancer. Gastroenterology 140, 1807-1816. doi: 10.1053/j.gastro.2011.01.057.
69. Ungefroren, H., Sebens, S., Groth, S., Gieseler, F., and Fändrich, F. (2011). Differential roles of Src in transforming growth factor-β regulation of growth arrest, epithelial-to-mesenchymal transition and cell migration in pancreatic ductal adenocarcinoma cells. Int. J. Oncol. 38, 797-805. doi: 10.3892/ijo.2011.897.
70. Wisniewska, E., Dylik, A., Kulza, M., Florek, E., Piekoszewski, W., Señczuk-Przybylowska, M., et al. (2013). Exposure to ethanol and tobacco smoke in relation to level of PCNA antigen expression in pancreatic and hepatic rat cells. Pharmacol. Rep. 65, 914-926.
71. Yadav, D., Timmons, L., Benson, J. T., Dierkhising, R. A., and Chari, S. T. (2011). Incidence, prevalence, and survival of chronic pancreatitis: a population-based study. Am. J. Gastroenterol. 106, 2192-2199. doi: 10.1038/ajg.2011.328.
72. Yokoi, K., Hawke, D., Oborn, C. J., Jang, J. Y., Nishioka, Y., Fan, D., et al. (2011). Identification and validation of SRC and phospho-SRC family proteins in circulating mononuclear cells as novel biomarkers for pancreatic cancer. Transl. Oncol. 4, 83-91.
73. Zhang, Y., Yan, W., Collin, M., Bednar, F., Rakshit, S., Zetter, B., et al. (2013). Interleukin-6 is required for pancreatic cancer progression by promoting MAPK signaling activation and oxidative stress resistance. Cancer Res. 73, 6359-6374. doi: 10.1158/0008-5472.CAN-13-1558-T.