Catecholamine-induced β2-adrenergic receptor activation mediates desensitization of gastric cancer cells to trastuzumab by upregulating MUC4 expression

Journal of Immunology

Volumn 190, Issue 11, 2013, Pages 5600-5608

  Shi, Ming ^a   Yang, Zhengyan ^b   Hu, Meiru ^a   Liu, Dan ^a   Hu, Yabin ^a   Qian, Lu ^a   Zhang, Wei ^b   Chen, Hongyu ^a   Guo, Liang ^a   Yu, Ming ^a   Song, Lun ^a   Ma, Yuanfang ^b   Guo, Ning ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b HENAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 ISOPROPYLAMINO 1 (7 METHYL 4 INDANYLOXY) 2 BUTANOL; BETA 2 ADRENERGIC RECEPTOR; IMMUNOGLOBULIN G; ISOPRENALINE; MITOGEN ACTIVATED PROTEIN KINASE; MUCIN 4; STAT3 PROTEIN; TRASTUZUMAB;

ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CONTROLLED STUDY; DESENSITIZATION; DRUG BINDING; DRUG PROTEIN BINDING; DRUG RESISTANCE; ENZYME ACTIVATION; ENZYME INDUCTION; FEMALE; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; STOMACH CANCER; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CATECHOLAMINES; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ISOPROTERENOL; MICE; MUCIN-4; PROTEIN BINDING; RECEPTOR, ERBB-2; RECEPTORS, ADRENERGIC, BETA-2; STAT3 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS; TRANSCRIPTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84878026061     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202364     Document Type: Article

References (46)

1. Siegel, R., E. Ward, O. Brawley, and A. Jemal. 2011. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J. Clin. 61: 212-236.
2. Polk, D. B., and R. M. Peek, Jr. 2010. Helicobacter pylori: gastric cancer and beyond. Nat. Rev. Cancer 10: 403-414.
3. De Vita, F., F. Giuliani, N. Silvestris, G. Catalano, F. Ciardiello, and M. Orditura. 2010. Human epidermal growth factor receptor 2 (HER2) in gastric cancer: a new therapeutic target. Cancer Treat. Rev. 36(Suppl. 3): S11-S15.
4. Fornaro, L., M. Lucchesi, C. Caparello, E. Vasile, S. Caponi, L. Ginocchi, G. Masi, and A. Falcone. 2011. Anti-HER agents in gastric cancer: from bench to bedside. Nat. Rev. Gastroenterol. Hepatol. 8: 369-383.
5. Stern, H. M. 2012. Improving treatment of HER2-positive cancers: opportunities and challenges. Sci. Transl. Med. 4: 127rv122.
6. Yoshida, R., H. Tazawa, Y. Hashimoto, S. Yano, T. Onishi, T. Sasaki, Y. Shirakawa, H. Kishimoto, F. Uno, M. Nishizaki, et al. 2012. Mechanism of resistance to trastuzumab and molecular sensitization via ADCC activation by exogenous expression of HER2-extracellular domain in human cancer cells. Cancer Immunol. Immunother. 61: 1905-1916.
7. Arteaga, C. L., M. X. Sliwkowski, C. K. Osborne, E. A. Perez, F. Puglisi, and L. Gianni. 2012. Treatment of HER2-positive breast cancer: current status and future perspectives. Nat. Rev. Clin. Oncol. 9: 16-32.
8. Jones, K. L., and A. U. Buzdar. 2009. Evolving novel anti-HER2 strategies. Lancet Oncol. 10: 1179-1187.
9. Spector, N. L., and K. L. Blackwell. 2009. Understanding the mechanisms behind trastuzumab therapy for human epidermal growth factor receptor 2-positive breast cancer. J. Clin. Oncol. 27: 5838-5847.
10. Zhang, S., W. C. Huang, P. Li, H. Guo, S. B. Poh, S. W. Brady, Y. Xiong, L. M. Tseng, S. H. Li, Z. Ding, et al. 2011. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat. Med. 17: 461-469.
11. Berns, K., H. M. Horlings, B. T. Hennessy, M. Madiredjo, E. M. Hijmans, K. Beelen, S. C. Linn, A. M. Gonzalez-Angulo, K. Stemke-Hale, M. Hauptmann, et al. 2007. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 12: 395-402. (Pubitemid 47539306)
12. Hynes, N. E., and J. H. Dey. 2009. PI3K inhibition overcomes trastuzumab resistance: blockade of ErbB2/ErbB3 is not always enough. Cancer Cell 15: 353-355.
13. Nagata, Y., K. H. Lan, X. Zhou, M. Tan, F. J. Esteva, A. A. Sahin, K. S. Klos, P. Li, B. P. Monia, N. T. Nguyen, et al. 2004. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6: 117-127. (Pubitemid 39485684)
14. Liang, K., F. J. Esteva, C. Albarracin, K. Stemke-Hale, Y. Lu, G. Bianchini, C. Y. Yang, Y. Li, X. Li, C. T. Chen, et al. 2010. Recombinant human erythropoietin antagonizes trastuzumab treatment of breast cancer cells via Jak2-mediated Src activation and PTEN inactivation. Cancer Cell 18: 423-435.
15. Arribas, J., J. Baselga, K. Pedersen, and J. L. Parra-Palau. 2011. p95HER2 and breast cancer. Cancer Res. 71: 1515-1519.
16. Cao, L., and M. J. During. 2012. What is the brain-cancer connection? Annu. Rev. Neurosci. 35: 331-345.
17. Armaiz-Pena, G. N., S. W. Cole, S. K. Lutgendorf, and A. K. Sood. 2013. Neuroendocrine influences on cancer progression. Brain Behav. Immun. 30 (Suppl.): S19-S25.
18. Antoni, M. H., S. K. Lutgendorf, S. W. Cole, F. S. Dhabhar, S. E. Sephton, P. G. McDonald, M. Stefanek, and A. K. Sood. 2006. The influence of bio-behavioural factors on tumour biology: pathways and mechanisms. Nat. Rev. Cancer 6: 240-248. (Pubitemid 43292567)
19. Cole, S. W., and A. K. Sood. 2012. Molecular pathways: beta-adrenergic signaling in cancer. Clin. Cancer Res. 18: 1201-1206.
20. Shi, M., D. Liu, H. Duan, C. Han, B. Wei, L. Qian, C. Chen, L. Guo, M. Hu, M. Yu, et al. 2010. Catecholamine up-regulates MMP-7 expression by activating AP-1 and STAT3 in gastric cancer. Mol. Cancer 9: 269.
21. Shi, M., D. Liu, H. Duan, L. Qian, L. Wang, L. Niu, H. Zhang, Z. Yong, Z. Gong, L. Song, et al. 2011. The β2-adrenergic receptor and Her2 comprise a positive feedback loop in human breast cancer cells. Breast Cancer Res. Treat. 125: 351-362.
22. Nagy, P., E. Friedländer, M. Tanner, A. I. Kapanen, K. L. Carraway, J. Isola, and T. M. Jovin. 2005. Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res. 65: 473-482.
23. Lu, H., M. Shi, M. Wang, Z. Xie, M. Hu, M. Yu, B. Shen, Y. Ma, and N. Guo. 2008. In vitro and in vivo antitumor effect of a trivalent bispecific antibody targeting ErbB2 and CD16. Cancer Biol. Ther. 7: 1744-1750.
24. Landen, C. N., Jr., Y. G. Lin, G. N. Armaiz Pena, P. D. Das, J. M. Arevalo, A. A. Kamat, L. Y. Han, N. B. Jennings, W. A. Spannuth, P. H. Thaker, et al. 2007. Neuroendocrine modulation of signal transducer and activator of transcription-3 in ovarian cancer. Cancer Res. 67: 10389-10396.
25. Yang, E. V., S. J. Kim, E. L. Donovan, M. Chen, A. C. Gross, J. I. Webster Marketon, S. H. Barsky, and R. Glaser. 2009. Norepinephrine upregulates VEGF, IL-8, and IL-6 expression in human melanoma tumor cell lines: implications for stress-related enhancement of tumor progression. Brain Behav. Immun. 23: 267-275.
26. Shahzad, M. M., J. M. Arevalo, G. N. Armaiz-Pena, C. Lu, R. L. Stone, M. Moreno-Smith, M. Nishimura, J. W. Lee, N. B. Jennings, J. Bottsford-Miller, et al. 2010. Stress effects on FosB- and interleukin-8 (IL8)-driven ovarian cancer growth and metastasis. J. Biol. Chem. 285: 35462-35470.
27. Thaker, P. H., L. Y. Han, A. A. Kamat, J. M. Arevalo, R. Takahashi, C. Lu, N. B. Jennings, G. Armaiz-Pena, J. A. Bankson, M. Ravoori, et al. 2006. Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat. Med. 12: 939-944. (Pubitemid 44175146)
28. Glaser, R., and J. K. Kiecolt-Glaser. 2005. Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol. 5: 243-251. (Pubitemid 40364825)
29. Gan, X., L. Zhang, G. F. Solomon, and B. Bonavida. 2002. Mechanism of norepinephrine-mediated inhibition of human NK cytotoxic functions: inhibition of cytokine secretion, target binding, and programming for cytotoxicity. Brain Behav. Immun. 16: 227-246. (Pubitemid 35425562)
30. Sloan, E. K., S. J. Priceman, B. F. Cox, S. Yu, M. A. Pimentel, V. Tangkanangnukul, J. M. Arevalo, K. Morizono, B. D. Karanikolas, L. Wu, et al. 2010. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res. 70: 7042-7052.
31. Mukhopadhyay, P., S. Chakraborty, M. P. Ponnusamy, I. Lakshmanan, M. Jain, and S. K. Batra. 2011. Mucins in the pathogenesis of breast cancer: implications in diagnosis, prognosis and therapy. Biochim. Biophys. Acta 1815: 224-240.
32. Senapati, S., P. Chaturvedi, P. Sharma, G. Venkatraman, J. L. Meza, W. El-Rifai, H. K. Roy, and S. K. Batra. 2008. Deregulation of MUC4 in gastric adenocarcinoma: potential pathobiological implication in poorly differentiated non-signet ring cell type gastric cancer. Br. J. Cancer 99: 949-956.
33. Mejías-Luque, R., S. K. Lindén, M. Garrido, H. Tye, M. Najdovska, B. J. Jenkins, M. Iglesias, M. Ernst, and C. de Bolós. 2010. Inflammation modulates the expression of the intestinal mucins MUC2 and MUC4 in gastric tumors. Oncogene 29: 1753-1762.
34. Mejías-Luque, R., S. Peiró, A. Vincent, I. Van Seuningen, and C. de Bolós. 2008. IL-6 induces MUC4 expression through gp130/STAT3 pathway in gastric cancer cell lines. Biochim. Biophys. Acta 1783: 1728-1736.
35. Mukohara, T. 2011. Mechanisms of resistance to anti-human epidermal growth factor receptor 2 agents in breast cancer. Cancer Sci. 102: 1-8.
36. Collins, D. M., N. O'Donovan, P. M. McGowan, F. O'Sullivan, M. J. Duffy, and J. Crown. 2012. Trastuzumab induces antibody-dependent cell-mediated cytotoxicity (ADCC) in HER-2-non-amplified breast cancer cell lines. Ann. Oncol. 23: 1788-1795.
37. Shakhar, G., and S. Ben-Eliyahu. 1998. In vivo beta-adrenergic stimulation suppresses natural killer activity and compromises resistance to tumor metastasis in rats. J. Immunol. 160: 3251-3258. (Pubitemid 28164714)
38. Watabe, K., M. Nishi, H. Miyake, and K. Hirata. 1998. Lifestyle and gastric cancer: a case-control study. Oncol. Rep. 5: 1191-1194. (Pubitemid 28372585)
39. Tian, J., Z. C. Chen, and L. F. Hang. 2009. Effects of nutritional and psychological status of the patients with advanced stomach cancer on physical performance status. Support. Care Cancer 17: 1263-1268.
40. Verhaak, P. F. 1997. Somatic disease and psychological disorder. J. Psychosom. Res. 42: 261-273. (Pubitemid 27186878)
41. Bafna, S., S. Kaur, and S. K. Batra. 2010. Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 29: 2893-2904.
42. Ponnusamy, M. P., A. P. Singh, M. Jain, S. Chakraborty, N. Moniaux, and S. K. Batra. 2008. MUC4 activates HER2 signalling and enhances the motility of human ovarian cancer cells. Br. J. Cancer 99: 520-526.
43. Chaturvedi, P., A. P. Singh, S. Chakraborty, S. C. Chauhan, S. Bafna, J. L. Meza, P. K. Singh, M. A. Hollingsworth, P. P. Mehta, and S. K. Batra. 2008. MUC4 mucin interacts with and stabilizes the HER2 oncoprotein in human pancreatic cancer cells. Cancer Res. 68: 2065-2070. (Pubitemid 351521776)
44. Singh, A. P., P. Chaturvedi, and S. K. Batra. 2007. Emerging roles of MUC4 in cancer: a novel target for diagnosis and therapy. Cancer Res. 67: 433-436. (Pubitemid 46192176)
45. Yokoyama, A., B. H. Shi, T. Kawai, H. Konishi, R. Andoh, H. Tachikawa, S. Ihara, and Y. Fukui. 2007. Muc4 is required for activation of ErbB2 in signet ring carcinoma cell lines. Biochem. Biophys. Res. Commun. 355: 200-203. (Pubitemid 46273387)
46. Price-Schiavi, S. A., S. Jepson, P. Li, M. Arango, P. S. Rudland, L. Yee, and K. L. Carraway. 2002. Rat Muc4 (sialomucin complex) reduces binding of anti-ErbB2 antibodies to tumor cell surfaces, a potential mechanism for herceptin resistance. Int. J. Cancer 99: 783-791. (Pubitemid 34575694)