Propranolol attenuates surgical stress-induced elevation of the regulatory T cell response in patients undergoing radical mastectomy

Journal of Immunology

Volumn 196, Issue 8, 2016, Pages 3460-3469

  Zhou, Lei ^a   Li, Yunli ^a   Li, Xiaoxiao ^a   Chen, Gong ^a   Liang, Huiying ^b   Wu, Yuhui ^c   Tong, Jianbin ^a   Ouyang, Wen ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; NORADRENALIN; PARECOXIB; PROPRANOLOL; PROSTAGLANDIN E2; TRANSCRIPTION FACTOR FOXP3; TUMOR ANTIGEN; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CATECHOLAMINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; GAMMA INTERFERON; ISOXAZOLE DERIVATIVE; MESSENGER RNA;

ADRENALIN BLOOD LEVEL; ADULT; AGED; ARTICLE; BLOOD LEVEL; BREAST CANCER; CANCER PATIENT; CD4+ T LYMPHOCYTE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MAJOR CLINICAL STUDY; MASTECTOMY; NORADRENALIN BLOOD LEVEL; PERIOPERATIVE PERIOD; PERIPHERAL BLOOD MONONUCLEAR CELL; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REGULATORY T LYMPHOCYTE; SURGICAL STRESS; BIOSYNTHESIS; BLOOD; BREAST NEOPLASMS; CELL CULTURE; CELL PROLIFERATION; CLINICAL TRIAL; DRUG EFFECTS; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INFLAMMATION; MIDDLE AGED; MONONUCLEAR CELL; PHYSIOLOGICAL STRESS; SECRETION (PROCESS);

ADRENERGIC BETA-ANTAGONISTS; ADULT; AGED; BREAST NEOPLASMS; CATECHOLAMINES; CELL PROLIFERATION; CELLS, CULTURED; DINOPROSTONE; EPINEPHRINE; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNE TOLERANCE; INFLAMMATION; INTERFERON-GAMMA; ISOXAZOLES; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE COUNT; MASTECTOMY, RADICAL; MIDDLE AGED; NOREPINEPHRINE; PROPRANOLOL; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES, REGULATORY;

EID: 84974822330     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501677     Document Type: Article

References (45)

1. Siegel, R., D. Naishadham, and A. Jemal. 2013. Cancer statistics, 2013. CA Cancer J. Clin. 63: 11-30.
2. Neeman, E., and S. Ben-Eliyahu. 2013. Surgery and stress promote cancer metastasis: new outlooks on perioperative mediating mechanisms and immune involvement. Brain Behav. Immun. 30: S32-S40.
3. Ben-Eliyahu, S. 2003. The promotion of tumor metastasis by surgery and stress: immunological basis and implications for psychoneuroimmunology. Brain Behav. Immun. 17(Suppl. 1): S27-S36.
4. Shakhar, G., and S. Ben-Eliyahu. 2003. Potential prophylactic measures against postoperative immunosuppression: could they reduce recurrence rates in oncological patients? Ann. Surg. Oncol. 10: 972-992.
5. Bartal, I., R. Melamed, K. Greenfeld, S. Atzil, A. Glasner, V. Domankevich, R. Naor, B. Beilin, I. Z. Yardeni, and S. Ben-Eliyahu. 2010. Immune perturbations in patients along the perioperative period: alterations in cell surface markers and leukocyte subtypes before and after surgery. Brain Behav. Immun. 24: 376-386.
6. Nelson, C. J., and D. T. Lysle. 1998. Severity, time, and beta-adrenergic receptor involvement in surgery-induced immune alterations. J. Surg. Res. 80: 115-122.
7. Ogawa, K., M. Hirai, T. Katsube, M. Murayama, K. Hamaguchi, T. Shimakawa, Y. Naritake, T. Hosokawa, and T. Kajiwara. 2000. Suppression of cellular immunity by surgical stress. Surgery 127: 329-336.
8. Tashiro, T., H. Yamamori, K. Takagi, N. Hayashi, K. Furukawa, H. Nitta, Y. Toyoda, W. Sano, T. Itabashi, K. Nishiya, et al. 1999. Changes in immune function following surgery for esophageal carcinoma. Nutrition 15: 760-766.
9. Fontenot, J. D., M. A. Gavin, and A. Y. Rudensky. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4: 330-336.
10. Nishikawa, H., and S. Sakaguchi. 2010. Regulatory T cells in tumor immunity. Int. J. Cancer 127: 759-767.
11. Watanabe, M. A., J. M. Oda, M. K. Amarante, and J. Cesar Voltarelli. 2010. Regulatory T cells and breast cancer: implications for immunopathogenesis. Cancer Metastasis Rev. 29: 569-579.
12. Gupta, S., K. Joshi, J. D. Wig, and S. K. Arora. 2007. Intratumoral FOXP3 expression in infiltrating breast carcinoma: its association with clinicopathologic parameters and angiogenesis. Acta Oncol. 46: 792-797.
13. Perez, S. A., M. V. Karamouzis, D. V. Skarlos, A. Ardavanis, N. N. Sotiriadou, E. G. Iliopoulou, M. L. Salagianni, G. Orphanos, C. N. Baxevanis, G. Rigatos, and M. Papamichail. 2007. CD4+CD25+ regulatory T-cell frequency in HER-2/ neu (HER)-positive and HER-negative advanced-stage breast cancer patients. Clin. Cancer Res. 13: 2714-2721.
14. Neeman, E., O. Zmora, and S. Ben-Eliyahu. 2012. A new approach to reducing postsurgical cancer recurrence: perioperative targeting of catecholamines and prostaglandins. Clin. Cancer Res. 18: 4895-4902.
15. Inbar, S., E. Neeman, R. Avraham, M. Benish, E. Rosenne, and S. Ben-Eliyahu. 2011. Do stress responses promote leukemia progression? An animal study suggesting a role for epinephrine and prostaglandin-E2 through reduced NK activity. PLoS One 6: e19246.
16. Glasner, A., R. Avraham, E. Rosenne, M. Benish, O. Zmora, S. Shemer, H. Meiboom, and S. Ben-Eliyahu. 2010. Improving survival rates in two models of spontaneous postoperative metastasis in mice by combined administration of a beta-adrenergic antagonist and a cyclooxygenase-2 inhibitor. J. Immunol. 184: 2449-2457.
17. Goldfarb, Y., L. Sorski, M. Benish, B. Levi, R. Melamed, and S. Ben-Eliyahu. 2011. Improving postoperative immune status and resistance to cancer metastasis: a combined perioperative approach of immunostimulation and prevention of excessive surgical stress responses. Ann. Surg. 253: 798-810.
18. Avraham, R., M. Benish, S. Inbar, I. Bartal, E. Rosenne, and S. Ben-Eliyahu. 2010. Synergism between immunostimulation and prevention of surgery-induced immune suppression: an approach to reduce post-operative tumor progression. Brain Behav. Immun. 24: 952-958.
19. Kohm, A. P., and V. M. Sanders. 2001. Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol. Rev. 53: 487-525.
20. Madden, K. S. 2003. Catecholamines, sympathetic innervation, and immunity. Brain Behav. Immun. 17(Suppl. 1): S5-S10.
21. Kalinski, P. 2012. Regulation of immune responses by prostaglandin E2. J. Immunol. 188: 21-28.
22. Xiang, L., and G. D. Marshall, Jr. 2011. Immunomodulatory effects of in vitro stress hormones on FoxP3, Th1/Th2 cytokine and costimulatory molecule mRNA expression in human peripheral blood mononuclear cells. Neuroimmunomodulation 18: 1-10.
23. Sood, A. K., G. N. Armaiz-Pena, J. Halder, A. M. Nick, R. L. Stone, W. Hu, A. R. Carroll, W. A. Spannuth, M. T. Deavers, J. K. Allen, et al. 2010. Adrenergic modulation of focal adhesion kinase protects human ovarian cancer cells from anoikis. J. Clin. Invest. 120: 1515-1523.
24. 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.
25. Guo, K., Q. Ma, L. Wang, H. Hu, J. Li, D. Zhang, and M. Zhang. 2009. Norepinephrine-induced invasion by pancreatic cancer cells is inhibited by propranolol. Oncol. Rep. 22: 825-830.
26. Barron, T. I., R. M. Connolly, L. Sharp, K. Bennett, and K. Visvanathan. 2011. Beta blockers and breast cancer mortality: a population-based study. J. Clin. Oncol. 29: 2635-2644.
27. Powe, D. G., M. J. Voss, K. S. Zänker, H. O. Habashy, A. R. Green, I. O. Ellis, and F. Entschladen. 2010. Beta-blocker drug therapy reduces secondary cancer formation in breast cancer and improves cancer specific survival. Oncotarget 1: 628-638.
28. Yokokawa, J., V. Cereda, C. Remondo, J. L. Gulley, P. M. Arlen, J. Schlom, and K. Y. Tsang. 2008. Enhanced functionality of CD4+CD25(high)FoxP3+ regulatory T cells in the peripheral blood of patients with prostate cancer. Clin. Cancer Res. 14: 1032-1040.
29. Clarke, S. L., G. J. Betts, A. Plant, K. L. Wright, T. M. El-Shanawany, R. Harrop, J. Torkington, B. I. Rees, G. T. Williams, A. M. Gallimore, and A. J. Godkin. 2006. CD4+CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS One 1: e129.
30. Betts, G., E. Jones, S. Junaid, T. El-Shanawany, M. Scurr, P. Mizen, M. Kumar, S. Jones, B. Rees, G. Williams, et al. 2012. Suppression of tumour-specific CD4+ T cells by regulatory T cells is associated with progression of human colorectal cancer. Gut 61: 1163-1171.
31. Kadoi, Y., and S. Saito. 2010. Possible indications of beta-blockers in the perioperative period other than prevention of cardiac ischemia. J. Anesth. 24: 81-95.
32. MacConmara, M. P., A. A. Maung, S. Fujimi, A. M. McKenna, A. Delisle, P. H. Lapchak, S. Rogers, J. A. Lederer, and J. A. Mannick. 2006. Increased CD4 + CD25+ T regulatory cell activity in trauma patients depresses protective Th1 immunity. Ann. Surg. 244: 514-523.
33. Marik, P. E., and M. Flemmer. 2012. The immune response to surgery and trauma: implications for treatment. J. Trauma Acute Care Surg. 73: 801-808.
34. Bhowmick, S., A. Singh, R. A. Flavell, R. B. Clark, J. O'Rourke, and R. E. Cone. 2009. The sympathetic nervous system modulates CD4(+)FoxP3(+) regulatory T cells via a TGF-beta-dependent mechanism. J. Leukoc. Biol. 86: 1275-1283.
35. Freier, E., C. S. Weber, U. Nowottne, C. Horn, K. Bartels, S. Meyer, Y. Hildebrandt, T. Luetkens, Y. Cao, C. Pabst, et al. 2010. Decrease of CD4(+) FOXP3(+) T regulatory cells in the peripheral blood of human subjects undergoing a mental stressor. Psychoneuroendocrinology 35: 663-673.
36. Fisher, S. A., and M. Absher. 1995. Norepinephrine and ANG II stimulate secretion of TGF-beta by neonatal rat cardiac fibroblasts in vitro. Am. J. Physiol. 268: C910-C917.
37. Nance, D. M., and V. M. Sanders. 2007. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav. Immun. 21: 736-745.
38. Dhabhar, F. S., A. N. Saul, C. Daugherty, T. H. Holmes, D. M. Bouley, and T. M. Oberyszyn. 2010. Short-term stress enhances cellular immunity and increases early resistance to squamous cell carcinoma. Brain Behav. Immun. 24: 127-137.
39. Tang, Q., E. K. Boden, K. J. Henriksen, H. Bour-Jordan, M. Bi, and J. A. Bluestone. 2004. Distinct roles of CTLA-4 and TGF-beta in CD4+CD25+ regulatory T cell function. Eur. J. Immunol. 34: 2996-3005.
40. Mays, L. E., and Y. H. Chen. 2007. Maintaining immunological tolerance with Foxp3. Cell Res. 17: 904-918.
41. Jonuleit, H., E. Schmitt, M. Stassen, A. Tuettenberg, J. Knop, and A. H. Enk. 2001. Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood. J. Exp. Med. 193: 1285-1294.
42. Lee, J. W., M. M. Shahzad, Y. G. Lin, G. Armaiz-Pena, L. S. Mangala, H. D. Han, H. S. Kim, E. J. Nam, N. B. Jennings, J. Halder, et al. 2009. Surgical stress promotes tumor growth in ovarian carcinoma. Clin. Cancer Res. 15: 2695-2702.
43. Cole, S. W., and A. K. Sood. 2012. Molecular pathways: beta-adrenergic signaling in cancer. Clin. Cancer Res. 18: 1201-1206.
44. Domschke, C., F. Schuetz, Y. Ge, T. Seibel, C. Falk, B. Brors, I. Vlodavsky, N. Sommerfeldt, H. P. Sinn, M. C. Kühnle, et al. 2009. Intratumoral cytokines and tumor cell biology determine spontaneous breast cancer-specific immune responses and their correlation to prognosis. Cancer Res. 69: 8420-8428.
45. Karyampudi, L., C. Formicola, C. L. Erskine, M. J. Maurer, J. N. Ingle, C. J. Krco, P. J. Wettstein, K. R. Kalli, J. D. Fikes, M. Beebe, et al. 2010. A degenerate HLA-DR epitope pool of HER-2/neu reveals a novel in vivo immunodominant epitope, HER-2/neu88-102. Clin. Cancer Res. 16: 825-834.