Housing temperature-induced stress drives therapeutic resistance in murine tumour models through β2-adrenergic receptor activation

Nature Communications

Volumn 6, Issue , 2015, Pages

  Eng, Jason W L ^a   Reed, Chelsey B ^a   Kokolus, Kathleen M ^a   Pitoniak, Rosemarie ^a   Utley, Adam ^a   Bucsek, Mark J ^a   Ma, Wen Wee ^a   Repasky, Elizabeth A ^a   Hylander, Bonnie L ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CASPASE 3; CISPLATIN; NORADRENALIN; PACLITAXEL; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; 130-NM ALBUMIN-BOUND PACLITAXEL; ALBUMINOID; ANTINEOPLASTIC AGENT; BCL2 PROTEIN, MOUSE; BCL2L1 PROTEIN, MOUSE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; ISOPRENALINE; PROTEIN BCL X; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; CANCER; DISEASE TREATMENT; ENVIRONMENTAL STRESS; RODENT; TEMPERATURE EFFECT; TUMOR;

ADRENERGIC RECEPTOR BLOCKING; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RESEARCH; CELL SURVIVAL; COLD STRESS; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; FEMALE; HOUSING; HUMAN; HUMAN CELL; MOUSE; MURINE MODEL; NONHUMAN; PANCREAS TUMOR; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR MODEL; TUMOR XENOGRAFT; ANIMAL; C57BL MOUSE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; PHYSIOLOGICAL STRESS; SCID MOUSE; TEMPERATURE; TUMOR CELL LINE;

MURINAE; MUS;

ADRENERGIC BETA-AGONISTS; ALBUMINS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-X PROTEIN; CELL LINE, TUMOR; CISPLATIN; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ISOPROTERENOL; MICE; MICE, INBRED C57BL; MICE, SCID; PACLITAXEL; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TEMPERATURE; TNF-RELATED APOPTOSIS-INDUCING LIGAND; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84924390520     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7426     Document Type: Article

References (70)

1. Buttles, S. S., Newell, D. R., Henrar, R. E. C. & Connors, T. A. Revisions of general guidelines for the preclinical toxicology of new cytotoxic anticancer agents in Europe. Eur. J. Cancer 31, 408-410.
2. Talmadge, J. E., Singh, R. K., Fidler, I. J. & Raz, A. Murine models to evaluate novel and conventional therapeutic strategies for cancer. Am. J. Pathol. 170, 793-804 (2007).
3. Schein, P. S. & Scheffler, B. Barriers to efficient development of cancer therapeutics. Clin. Cancer Res. 12, 3243-3248 (2006).
4. Newell, D., Burtles, S., Fox, B., Jodrell, D. & Connors, T. Evaluation of rodentonly toxicology for early clinical trials with novel cancer therapeutics. Br. J. Cancer 81, 760-768 (1999).
5. National Research Council (US). Committee for the Update of the Guide for the Care and Use of Laboratory Animals (National Academy of Sciences, 2011).
6. Eng, J. W., Reed, C. B., Kokolus, K. M. & Repasky, E. A. Housing temperature influences the pattern of heat shock protein induction in mice following mild whole body hyperthermia. Int. J. Hyperthermia 30, 540-546 (2014).
7. Kokolus, K. M. et al. Stressful presentations: mild chronic cold stress in mice influences baseline properties of dendritic cells. Front. Immunol. 5, 23 (2014).
8. Kokolus, K. M. et al. Baseline tumor growth and immune control in laboratory mice are significantly influenced by subthermoneutral housing temperature. Proc. Natl Acad. Sci. USA 110, 20176-20181 (2013).
9. Conley, K. E. & Porter, W. P. Heat loss from deer mice (Peromyscus): evaluation of seasonal limits to thermoregulation. J. Exp. Biol. 126, 249-269 (1986).
10. Cannon, B. & Nedergaard, J. Nonshivering thermogenesis and its adequate measurement in metabolic studies. J. Exp. Biol. 214, 242-253 (2011).
11. Silva, J. E. Physiological importance and control of non-shivering facultative thermogenesis. Front. Biosci. (Schol. Ed.) 3, 352-371 (2011).
12. Hsieh, A. C. & Carlson, L. D. Role of adrenaline and noradrenaline in chemical regulation of heat production. Am. J. Physiol. 190, 243-246 (1957).
13. Cakir, Y., Plummer, H., Tithof, P. & Schuller, H. Beta-adrenergic and arachidonic acid-mediated growth regulation of human breast cancer cell lines. Int. J. Oncol. 21, 153-157 (2002).
14. Thaker, P. H. et al. Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat. Med. 12, 939-944 (2006).
15. Palm, D. et al. The norepinephrine-driven metastasis development of PC-3 human prostate cancer cells in BALB/c nude mice is inhibited by b-blockers. Int. J. Cancer 118, 2744-2749 (2006).
16. Sastry, K. S. R. et al. Epinephrine protects cancer cells from apoptosis via activation of cAMP-dependent protein kinase and BAD phosphorylation. J. Biol. Chem. 282, 14094-14100 (2007).
17. Sood, A. K. et al. Adrenergic modulation of focal adhesion kinase protects human ovarian cancer cells from anoikis. J. Clin. Invest. 120, 1515-1523 (2010).
18. Shahzad, M. M. K. et al. Stress effects on FosB-and interleukin-8 (IL8)-driven ovarian cancer growth and metastasis. J. Biol. Chem. 285, 35462-35470 (2010).
19. Hassan, S. et al. Behavioral stress accelerates prostate cancer development in mice. J. Clin. Invest. 123, 874-886 (2013).
20. Lutgendorf, S. K. et al. Social isolation is associated with elevated tumor norepinephrine in ovarian carcinoma patients. Brain Behav. Immun. 25, 250-255 (2011).
21. Armaiz-Pena, G. N. et al. Src activation by beta-adrenoreceptors is a key switch for tumour metastasis. Nat. Commun. 4, 1403 (2013).
22. Zhang, D. et al. b2-adrenoceptor blockage induces G1/S phase arrest and apoptosis in pancreatic cancer cells via Ras/Akt/NFkB pathway. Mol. Cancer. 10, 146 (2011).
23. Zhang, D., Ma, Q. Y., Hu, H. T. & Zhang, M. beta2-adrenergic antagonists suppress pancreatic cancer cell invasion by inhibiting CREB, NFkappaB and AP-1. Cancer Biol. Ther. 10, 19-29 (2010).
24. Yang, E. V. et al. 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 (2009).
25. Park, S. Y. et al. Norepinephrine induces VEGF expression and angiogenesis by a hypoxia-inducible factor-1a protein-dependent mechanism. Int. J. Cancer 128, 2306-2316 (2011).
26. Diaz, E. S., Karlan, B. Y. & Li, A. J. Impact of beta blockers on epithelial ovarian cancer survival. Gynecol. Oncol. 127, 375-378 (2012).
27. Barron, T. I., Connolly, R. M., Sharp, L., Bennett, K. & Visvanathan, K. Beta blockers and breast cancer mortality: a population-based study. J. Clin. Oncol. 29, 2635-2644 (2011).
28. Melhem-Bertrandt, A. et al. Beta-blocker use is associated with improved relapse-free survival in patients with triple-negative breast cancer. J. Clin. Oncol. 29, 2645-2652 (2011).
29. Wang, H. M. et al. Improved survival outcomes with the incidental use of betablockers among patients with non-small-cell lung cancer treated with definitive radiation therapy. Ann. Oncol. 24, 1312-1319 (2013).
30. Powe, D. G. et al. Beta-blocker drug therapy reduces secondary cancer formation in breast cancer and improves cancer specific survival. Oncotarget 1, 628-638 (2010).
31. McCourt, C. et al. Beta-blocker usage after malignant melanoma diagnosis and survival: a population-based nested case-control study. Br. J. Dermatol. 170, 930-938 (2014).
32. Cardwell, C. R., Coleman, H. G., Murray, L. J., Entschladen, F. & Powe, D. G. Beta-blocker usage and breast cancer survival: a nested case-control study within a UK Clinical Practice Research Datalink cohort. Int. J. Epidemiol. 42, 1852-1861 (2013).
33. Cardwell, C. R., Coleman, H. G., Murray, L. J., O'Sullivan, J. M. & Powe, D. G. Beta-blocker usage and prostate cancer survival: a nested case-control study in the UK Clinical Practice Research Datalink cohort. Cancer Epidemiol. 38, 279-285 (2014).
34. Pitti, R. M. et al. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271, 12687-12690 (1996).
35. Ashkenazi, A., Holland, P. & Eckhardt, S. G. Ligand-based targeting of apoptosis in cancer: The potential of recombinant human apoptosis ligand 2/tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J. Clin. Oncol. 26, 3621-3630 (2008).
36. Ling, Y. H., Lin, R. & Perez-Soler, R. Erlotinib induces mitochondrial-mediated apoptosis in human H3255 non-small-cell lung cancer cells with epidermal growth factor receptorL858R mutation through mitochondrial oxidative phosphorylation-dependent activation of BAX and BAK. Mol. Pharmacol. 74, 793-806 (2008).
37. Dasari, S. & Tchounwou, P. B. Cisplatin in cancer therapy: molecular mechanisms of action. Eur. J. Pharmacol. 740, 364-378 (2014).
38. Awasthi, N. et al. Comparative benefits of Nab-paclitaxel over gemcitabine or polysorbate-based docetaxel in experimental pancreatic cancer. Carcinogenesis 34, 2361-2369 (2013).
39. Weddle, D. L., Tithoff, P., Williams, M. & Schuller, H. M. Beta-adrenergic growth regulation of human cancer cell lines derived from pancreatic ductal carcinomas. Carcinogenesis 22, 473-479 (2001).
40. Schuller, H. M. Mechanisms of smoking-related lung and pancreatic adenocarcinoma development. Nat. Rev. Cancer 2, 455-463 (2002).
41. Zitvogel, L., Kepp, O. & Kroemer, G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat. Rev. Clin. Oncol. 8, 151-160 (2011).
42. Apetoh, L. et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13, 1050-1059 (2007).
43. Ashkenazi, A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat. Rev. Drug Discov. 7, 1001-1012 (2008).
44. Ashkenazi, A. et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104, 155-162 (1999).
45. Hylander, B. L. et al. The anti-tumor effect of Apo2L/TRAIL on patient pancreatic adenocarcinomas grown as xenografts in SCID mice. J. Transl. Med. 3, 22 (2005).
46. Cannon, B. & Nedergaard, J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359 (2004).
47. Uchida, K., Shiuchi, T., Inada, H., Minokoshi, Y. & Tominaga, M. Metabolic adaptation of mice in a cool environment. Pflugers Arch. 459, 765-774 (2010).
48. Nguyen, K. D. et al. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 480, 104-108 (2011).
49. Pasquier, E. et al. b-blockers increase response to chemotherapy via direct antitumour and anti-angiogenic mechanisms in neuroblastoma. Br. J. Cancer 108, 2485-2494 (2013).
50. Pasquier, E. et al. Propranolol potentiates the anti-angiogenic effects and antitumor efficacy of chemotherapy agents: implication in breast cancer treatment. Oncotarget 2, 797-809 (2011).
51. Guo, K. et al. Norepinephrine-induced invasion by pancreatic cancer cells is inhibited by propranolol. Oncol. Rep. 22, 825-830 (2009).
52. Huang, X. Y., Wang, H. C., Yuan, Z., Huang, J. & Zheng, Q. Norepinephrine stimulates pancreatic cancer cell proliferation, migration and invasion via beta-adrenergic receptor-dependent activation of P38/MAPK pathway. Hepatogastroenterology 59, 889-893 (2012).
53. Schuller, H., Porter, B. & Riechert, A. Beta-adrenergic modulation of NNK-induced lung carcinogenesis in hamsters. J. Cancer Res. Clin. Oncol. 126, 624-630 (2000).
54. Wang, L. et al. Immune sculpting of norepinephrine on MHC-I, B7-1, IDO and B7-H1 expression and regulation of proliferation and invasion in pancreatic carcinoma cells. PLoS ONE 7, e45491 (2012).
55. Bekasi, S. & Zalatnai, A. Overexpression of glucocorticoid receptor in human pancreatic cancer and in xenografts. An immunohistochemical study. Pathol. Oncol. Res. 15, 561-566 (2009).
56. Norman, J. et al. Functional glucocorticoid receptor modulates pancreatic carcinoma growth through an autocrine loop. J. Surg. Res. 57, 33-38 (1994).
57. Nobles, K. N. et al. Distinct phosphorylation sites on the beta(2)-adrenergic receptor establish a barcode that encodes differential functions of beta-arrestin. Sci. Signal 4, ra51 (2011).
58. Martin, B., Ji, S., Maudsley, S. & Mattson, M. P. 'Control' laboratory rodents are metabolically morbid: why it matters. Proc. Natl Acad. Sci. USA 107, 6127-6133 (2010).
59. Paigen, B. et al. Physiological effects of housing density on C57BL/6J mice over a 9-month period. J. Anim. Sci. 90, 5182-5192 (2012).
60. Gordon, C. J. Thermal physiology of laboratory mice: Defining thermoneutrality. J. Therm. Biol. 37, 654-685 (2012).
61. Karp, C. L. Unstressing intemperate models: how cold stress undermines mouse modeling. J. Exp. Med. 209, 1069-1074 (2012).
62. Cole, S. W. & Sood, A. K. Molecular pathways: beta-adrenergic signaling in cancer. Clin. Cancer Res. 18, 1201-1206 (2012).
63. Shan, T. et al. b2-adrenoceptor blocker synergizes with gemcitabine to inhibit the proliferation of pancreatic cancer cells via apoptosis induction. Eur. J. Pharmacol. 665, 1-7 (2011).
64. Magnon, C. et al. Autonomic nerve development contributes to prostate cancer progression. Science 341, 1236361 (2013).
65. Masur, K., Niggemann, B., Zanker, K. S. & Entschladen, F. Norepinephrineinduced migration of SW 480 colon carcinoma cells is inhibited by b-blockers. Cancer Res. 61, 2866-2869 (2001).
66. Shi, M. et al. Catecholamine-Induced beta2-adrenergic receptor activation mediates desensitization of gastric cancer cells to trastuzumab by upregulating MUC4 expression. J. Immunol. 190, 5600-5608 (2013).
67. Dal Monte, M. et al. b3-adrenergic receptor activity modulates melanoma cell proliferation and survival through nitric oxide signaling. Naunyn Schmiedebergs Arch. Pharmacol. 387, 533-543 (2014).
68. Eng, J. W. et al. A nervous tumor microenvironment: the impact of adrenergic stress on cancer cells, immunosuppression, and immunotherapeutic response. Cancer Immunol. Immunother. 63, 1115-1128 (2014).
69. Madden, K. S., Szpunar, M. J. & Brown, E. B. Early impact of social isolation and breast tumor progression in mice. Brain Behav. Immun. 30 Suppl, S135-S141 (2013).
70. Gordon, C. J. et al. Thermoregulation and its influence on toxicity assessment. Toxicology 244, 87-97 (2008).