Exogenous norepinephrine attenuates the efficacy of sunitinib in a mouse cancer model

Journal of Experimental and Clinical Cancer Research

Volumn 33, Issue 1, 2014, Pages

  Deng, Guo Hua ^a   Liu, Jie ^a   Zhang, Jie ^a   Wang, Ying ^a   Peng, Xing Chen ^a   Wei, Yu Quan ^a   Jiang, Yu ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

Chronic stress; Norepinephrine; Propranolol; Sunitinib; Tumor

Indexed keywords

DOBUTAMINE; FORSKOLIN; INTERLEUKIN 6; INTERLEUKIN 8; ISOPRENALINE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NORADRENALIN; PHENTOLAMINE; PROPRANOLOL; SUNITINIB; TERBUTALINE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER MODEL; CHRONIC STRESS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG INHIBITION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; LUNG ADENOCARCINOMA; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; UPREGULATION;

ADRENERGIC ALPHA-AGONISTS; ANGIOGENESIS INHIBITORS; ANIMALS; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; HUMANS; INDOLES; INHIBITORY CONCENTRATION 50; INTERLEUKIN-6; INTERLEUKIN-8; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; NOREPINEPHRINE; PROPRANOLOL; PYRROLES; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION; TUMOR BURDEN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84895923500     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/1756-9966-33-21     Document Type: Article

References (70)

1. Effects of combined stress during intense training on cellular immunity, hormones and respiratory infections. Gomez-Merino D, Drogou C, Chennaoui M, et al. Neuroimmunomodulation 2005 12 164 172 10.1159/000084849 15905625
2. Stress-induced immune dysfunction: implications for health. Glaser R, Kiecolt-Glaser JK, Nat Rev Immunol 2005 5 243 251 10.1038/nri1571 15738954
3. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Johnson JD, Campisi J, Sharkey CM, Kennedy SL, Nickerson M, Greenwood BN, Fleshner M, Neuroscience 2005 135 1295 1307 10.1016/j.neuroscience.2005.06.090 16165282
4. Stress, depression, the immune system, and cancer. Reiche EM, Nunes SO, Morimoto HK, Lancet Oncol 2004 5 617 625 10.1016/S1470-2045(04)01597-9 15465465
5. Immune microenvironments in solid tumors: new targets for therapy. Shiao SL, Ganesan AP, Rugo HS, Coussens LM, Genes Dev 2011 25 2559 2572 10.1101/gad.169029.111 22190457
6. The complex interplay between stress and bacterial infections in animals. Verbrugghe E, Boyen F, Gaastra W, Bekhuis L, Leyman B, Van Parys A, Haesebrouck F, Pasmans F, Vet Microbiol 2012 155 115 127 10.1016/j.vetmic.2011.09.012 21963418
7. Norepinephrine-induced migration of SW 480 colon carcinoma cells is inhibited by beta-blockers. Masur K, Niggemann B, Zanker KS, Entschladen F, Cancer Res 2001 61 2866 2869 11306460
8. Stress-related mediators stimulate vascular endothelial growth factor secretion by two ovarian cancer cell lines. Lutgendorf SK, Cole S, Costanzo E, Bradley S, Coffin J, Jabbari S, Rainwater K, Ritchie JM, Yang M, Sood AK, Clin Cancer Res 2003 9 4514 4521 14555525
9. Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Thaker PH, Han LY, Kamat AA, Arevalo JM, Takahashi R, Lu C, Jennings NB, Armaiz-Pena G, Bankson JA, Ravoori M, et al. Nat Med 2006 12 939 944 10.1038/nm1447 16862152
10. Tumour-cell migration, invasion, and metastasis: navigation by neurotransmitters. Entschladen F, Drell TL 4th, Lang K, Joseph J, Zaenker KS, Lancet Oncol 2004 5 254 258 10.1016/S1470-2045(04)01431-7 15050959
11. Hostile marital interactions, proinflammatory cytokine production, and wound healing. Kiecolt-Glaser JK, Loving TJ, Stowell JR, Malarkey WB, Lemeshow S, Dickinson SL, Glaser R, Arch Gen Psychiatry 2005 62 1377 1384 10.1001/archpsyc.62.12.1377 16330726
12. Adrenergic activation of vascular endothelial growth factor mRNA expression in rat brown adipose tissue: implication in cold-induced angiogenesis. Asano A, Morimatsu M, Nikami H, Yoshida T, Saito M, Biochem J 1997 328 Pt 1 179 183 9359850
13. Behavioral stress accelerates prostate cancer development in mice. Hassan S, Karpova Y, Baiz D, Yancey D, Pullikuth A, Flores A, Register T, Cline JM, D'Agostino R Jr, Danial N, et al. J Clin Invest 2013 123 874 886 23348742
14. The norepinephrine-driven metastasis development of PC-3 human prostate cancer cells in BALB/c nude mice is inhibited by beta-blockers. Palm D, Lang K, Niggemann B, Drell TL 4th, Masur K, Zaenker KS, Entschladen F, Int J Cancer 2006 118 2744 2749 10.1002/ijc.21723 16381019
15. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Sloan EK, Priceman SJ, Cox BF, Yu S, Pimentel MA, Tangkanangnukul V, Arevalo JM, Morizono K, Karanikolas BD, Wu L, et al. Cancer Res 2010 70 7042 7052 10.1158/0008-5472.CAN-10-0522 20823155
16. Norepinephrine inhibits the migratory activity of pancreatic cancer cells. Stock AM, Powe DG, Hahn SA, Troost G, Niggemann B, Zanker KS, Entschladen F, Exp Cell Res 2013 319 1744 1758 10.1016/j.yexcr.2013.04.015 23639786
17. Norepinephrine upregulates VEGF, IL-8, and IL-6 expression in human melanoma tumor cell lines: implications for stress-related enhancement of tumor progression. Yang EV, Kim SJ, Donovan EL, Chen M, Gross AC, Webster MJI, Barsky SH, Glaser R, Brain Behav Immun 2009 23 267 275 10.1016/j.bbi.2008.10.005 18996182
18. Norepinephrine up-regulates the expression of vascular endothelial growth factor, matrix metalloproteinase (MMP)-2, and MMP-9 in nasopharyngeal carcinoma tumor cells. Yang EV, Sood AK, Chen M, Li Y, Eubank TD, Marsh CB, Jewell S, Flavahan NA, Morrison C, Yeh PE, et al. Cancer Res 2006 66 10357 10364 10.1158/0008-5472.CAN-06-2496 17079456
19. Norepinephrine antagonists and cancer risk. Friedman GD, Udaltsova N, Habel LA, Int J Cancer 2011 128 737 738 author reply 739 20333678
20. Beta blockers and breast cancer mortality: a population- based study. Barron TI, Connolly RM, Sharp L, Bennett K, Visvanathan K, J Clin Oncol 2011 29 2635 2644 10.1200/JCO.2010.33.5422 21632503
21. Beta-blocker use is associated with improved relapse-free survival in patients with triple-negative breast cancer. Melhem-Bertrandt A, Chavez-Macgregor M, Lei X, Brown EN, Lee RT, Meric-Bernstam F, Sood AK, Conzen SD, Hortobagyi GN, Gonzalez-Angulo AM, J Clin Oncol 2011 29 2645 2652 10.1200/JCO.2010.33.4441 21632501
22. Beta-blocker drug therapy reduces secondary cancer formation in breast cancer and improves cancer specific survival. Powe DG, Voss MJ, Zanker KS, Habashy HO, Green AR, Ellis IO, Entschladen F, Oncotarget 2010 1 628 638 21317458
23. Antitumor effect of vascular endothelial growth factor inhibitor sunitinib in preclinical models of hepatocellular carcinoma. Bagi CM, Gebhard DF, Andresen CJ, Eur J Gastroenterol Hepatol 2012 24 563 574 10.1097/MEG.0b013e328350916f 22314934
24. Contrasting effects of sunitinib within in vivo models of metastasis. Welti JC, Powles T, Foo S, Gourlaouen M, Preece N, Foster J, Frentzas S, Bird D, Sharpe K, van Weverwijk A, et al. Angiogenesis 2012 15 623 641 10.1007/s10456-012-9291-z 22843200
25. Magnetic resonance imaging identifies early effects of sunitinib treatment in human melanoma xenografts. Gaustad JV, Pozdniakova V, Hompland T, Simonsen TG, Rofstad EK, J Exp Clin Cancer Res 2013 32 93 10.1186/1756-9966-32- 93 24245934
26. Antitumor efficacy of a thrombospondin 1 mimetic CovX-body. Li L, Leedom TA, Do J, Huang H, Lai J, Johnson K, Osothprarop TF, Rizzo JD, Doppalapudi VR, Bradshaw CW, et al. Transl Oncol 2011 4 249 257 21804921
27. HGF/c-Met acts as an alternative angiogenic pathway in sunitinib-resistant tumors. Shojaei F, Lee JH, Simmons BH, Wong A, Esparza CO, Plumlee PA, Feng J, Stewart AE, Hu-Lowe DD, Christensen JG, Cancer Res 2010 70 10090 10100 10.1158/0008-5472.CAN-10-0489 20952508
28. Rlip76 transports sunitinib and sorafenib and mediates drug resistance in kidney cancer. Singhal SS, Sehrawat A, Sahu M, Singhal P, Vatsyayan R, Rao LPC, Yadav S, Awasthi S, Int J Cancer 2010 126 1327 1338 19626587
29. Efficient inhibition of lung cancer in murine model by plasmid-encoding VEGF short hairpin RNA in combination with low-dose DDP. Ma YP, Yang Y, Zhang S, Chen X, Zhang N, Wang W, Cao ZX, Jiang Y, Zhao X, Wei YQ, et al. J Exp Clin Cancer Res 2010 29 56 10.1186/1756-9966-29-56 20497582
30. Gene therapy with the angiogenesis inhibitor endostatin in an orthotopic lung cancer murine model. Ning T, Yan X, Lu ZJ, Wang GP, Zhang NG, Yang JL, Jiang SS, Wu Y, Yang L, Guan YS, et al. Hum Gene Ther 2009 20 103 111 10.1089/hum.2008.098 18939902
31. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection versus immunopathology. Dhabhar FS, Allergy Asthma Clin Immunol 2008 4 2 11 10.1186/1710-1492-4-1-2 20525121
32. Neuroendocrine-immune mechanisms of behavioral comorbidities in patients with cancer. Miller AH, Ancoli-Israel S, Bower JE, Capuron L, Irwin MR, J Clin Oncol 2008 26 971 982 10.1200/JCO.2007.10.7805 18281672
33. Different attitudes of chinese patients and their families toward truth telling of different stages of cancer. Jiang Y, Liu C, Li JY, Huang MJ, Yao WX, Zhang R, Yao B, Du XB, Chen J, Xie K, Zhao X, Wei YQ, Psychooncology 2007 16 10 928 936 10.1002/pon.1156 17285684
34. PinX1 regulation of telomerase activity and apoptosis in nasopharyngeal carcinoma cells. Lai XF, Shen CX, Wen Z, Qian YH, Yu CS, Wang JQ, Zhong PN, Wang HL, J Exp Clin Cancer Res 2012 31 12 10.1186/1756-9966-31-12 22316341
35. Vascular endothelial cells facilitated HCC invasion and metastasis through the Akt and NF-kappaB pathways induced by paracrine cytokines. Wang YH, Dong YY, Wang WM, Xie XY, Wang ZM, Chen RX, Chen J, Gao DM, Cui JF, Ren ZG, J Exp Clin Cancer Res 2013 32 51 10.1186/1756-9966-32-51 23941552
36. Pro-death and pro-survival properties of ouabain in U937 lymphoma derived cells. Cuozzo F, Raciti M, Bertelli L, Parente R, Di RL, J Exp Clin Cancer Res 2012 31 95 10.1186/1756-9966-31-95 23153195
37. Microvessel density and heparanase over-expression in clear cell renal cell cancer: correlations and prognostic significances. Ren J, Liu H, Yan L, Tian S, Li D, Xu Z, World J Surg Oncol 2011 9 158 10.1186/1477-7819-9-158 22133010
38. Reduced expression of tissue factor pathway inhibitor-2 contributes to apoptosis and angiogenesis in cervical cancer. Zhang Q, Zhang Y, Wang SZ, Wang N, Jiang WG, Ji YH, Zhang SL, J Exp Clin Cancer Res 2012 31 1 10.1186/1756-9966-31-1 22208663
39. Celecoxib alleviates tamoxifen-instigated angiogenic effects by ROS-dependent VEGF/VEGFR2 autocrine signaling. Kumar BN, Rajput S, Dey KK, Parekh A, Das S, Mazumdar A, Mandal M, BMC Cancer 2013 13 273 10.1186/1471-2407-13-273 23731702
40. Interleukin-6: a potential biomarker of resistance to multitargeted receptor tyrosine kinase inhibitors in castration-resistant prostate cancer. Kutikov A, Makhov P, Golovine K, Canter DJ, Sirohi M, Street R, Simhan J, Uzzo RG, Kolenko VM, Urology 2011 78 968 7 e11
41. Predominant mucosal IL-8 mRNA expression in non-cagA Thais is risk for gastric cancer. Yamada S, Kato S, Matsuhisa T, Makonkawkeyoon L, Yoshida M, Chakrabandhu T, Lertprasertsuk N, Suttharat P, Chakrabandhu B, Nishiumi S, et al. World J Gastroenterol 2013 19 2941 2949 23704827
42. Molecular pathways: beta-adrenergic signaling in cancer. Cole SW, Sood AK, Clin Cancer Res 2012 18 1201 1206 10.1158/1078-0432.CCR-11-0641 22186256
43. Animal models of social stress: effects on behavior and brain neurochemical systems. Blanchard RJ, McKittrick CR, Blanchard DC, Physiol Behav 2001 73 261 271 10.1016/S0031-9384(01)00449-8 11438351
44. Differential effects of social defeat in rats with high and low locomotor response to novelty. Calvo N, Cecchi M, Kabbaj M, Watson SJ, Akil H, Neuroscience 2011 183 81 89 21453756
45. Adrenocortical and behavioural response to chronic restraint stress in neurokinin-1 receptor knockout mice. Delgado-Morales R, del Rio E, Gomez-Roman A, Bisagno V, Nadal R, de Felipe C, Armario A, Physiol Behav 2012 105 669 675 10.1016/j.physbeh.2011.10.008 22019828
46. Social isolation dysregulates endocrine and behavioral stress while increasing malignant burden of spontaneous mammary tumors. Hermes GL, Delgado B, Tretiakova M, Cavigelli SA, Krausz T, Conzen SD, McClintock MK, Proc Natl Acad Sci USA 2009 106 22393 22398 10.1073/pnas.0910753106 20018726
47. Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Li S, Wang C, Wang W, Dong H, Hou P, Tang Y, Life Sci 2008 82 934 942 10.1016/j.lfs.2008.02.010 18402983
48. Reduction of the olfactory cognitive ability in horses during preslaughter: stress-related hormones evaluation. Micera E, Moramarco AM, Zarrilli A, Meat Sci 2012 90 272 275 21775068
49. Functional status of somatodendritic serotonin 1A autoreceptor after long-term treatment with fluoxetine in a mouse model of anxiety/depression based on repeated corticosterone administration. Rainer Q, Nguyen HT, Quesseveur G, Gardier AM, David DJ, Guiard BP, Mol Pharmacol 2012 81 106 112 10.1124/mol.111.075796 22031471
50. VEGF is an important mediator of tumor angiogenesis in malignant lesions in a genetically engineered mouse model of lung adenocarcinoma. Majeti BK, Lee JH, Simmons BH, Shojaei F, BMC Cancer 2013 13 213 10.1186/1471-2407-13-213 23627488
51. Interleukin-8 is associated with proliferation, migration, angiogenesis and chemosensitivity in vitro and in vivo in colon cancer cell line models. Ning Y, Manegold PC, Hong YK, Zhang W, Pohl A, Lurje G, Winder T, Yang D, LaBonte MJ, Wilson PM, et al. Int J Cancer 2011 128 2038 2049 10.1002/ijc.25562 20648559
52. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF, Science 1983 219 983 985 10.1126/science.6823562 6823562
53. Angiogenesis as a strategic target for ovarian cancer therapy. Spannuth WA, Sood AK, Coleman RL, Nat Clin Pract Oncol 2008 5 194 204 18268546
54. Simultaneous blockade of VEGFR-1 and VEGFR-2 activation is necessary to efficiently inhibit experimental melanoma growth and metastasis formation. Gille J, Heidenreich R, Pinter A, Schmitz J, Boehme B, Hicklin DJ, Henschler R, Breier G, Int J Cancer 2007 120 1899 1908 10.1002/ijc.22531 17230507
55. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Tammela T, Zarkada G, Wallgard E, Murtomaki A, Suchting S, Wirzenius M, Waltari M, Hellstrom M, Schomber T, Peltonen R, et al. Nature 2008 454 656 660 10.1038/nature07083 18594512
56. Combination therapy using imatinib and vatalanib improves the therapeutic efficiency of paclitaxel towards a mouse melanoma tumor. Klosowska-Wardega A, Hasumi Y, Ahgren A, Heldin CH, Hellberg C, Melanoma Res 2010 21 57 65
57. Resveratrol inhibits alpha-melanocyte-stimulating hormone signaling, viability, and invasiveness in melanoma cells. Chen YJ, Chen YY, Lin YF, Hu HY, Liao HF, Evid Based Complement Alternat Med 2013 2013 632121 23762150
58. Use of ss-blockers and mortality following ovarian cancer diagnosis: a population-based cohort study. Johannesdottir SA, Schmidt M, Phillips G, Glaser R, Yang EV, Blumenfeld M, Lemeshow S, BMC Cancer 2013 13 85 10.1186/1471-2407- 13-85 23433478
59. Expression of vascular endothelial growth factor (VEGF) and its receptors VEGFR1 and VEGFR2 in primary and recurrent WHO grade III meningiomas. Baumgarten P, Brokinkel B, Zinke J, Zachskorn C, Ebel H, Albert FK, Stummer W, Plate KH, Harter PN, Hasselblatt M, et al. Histol Histopathol 2013 28 1157 1165 23475388
60. Evaluation of potentially predictive markers for anti-angiogenic therapy with sunitinib in recurrent ovarian cancer patients. Bauerschlag DO, Hilpert F, Meier W, Rau J, Meinhold-Heerlein I, Maass N, Dubois A, Sehouli J, Arnold N, Schem C, et al. Transl Oncol 2013 6 305 310 23730410
61. Antitumor activity and biomarker analysis of sunitinib in patients with bevacizumab-refractory metastatic renal cell carcinoma. Rini BI, Michaelson MD, Rosenberg JE, Bukowski RM, Sosman JA, Stadler WM, Hutson TE, Margolin K, Harmon CS, DePrimo SE, et al. J Clin Oncol 2008 26 3743 3748 10.1200/JCO.2007.15.5416 18669461
62. Phase II study of sunitinib as first-line treatment of urothelial cancer patients ineligible to receive cisplatin-based chemotherapy: baseline interleukin-8 and tumor contrast enhancement as potential predictive factors of activity. Bellmunt J, Gonzalez-Larriba JL, Prior C, Maroto P, Carles J, Castellano D, Mellado B, Gallardo E, Perez-Gracia JL, Aguilar G, et al. Ann Oncol 2011 22 2646 2653 10.1093/annonc/mdr023 21427062
63. Identification of soluble candidate biomarkers of therapeutic response to sunitinib in medullary thyroid carcinoma in preclinical models. Broutin S, Ameur N, Lacroix L, Robert T, Petit B, Oumata N, Talbot M, Caillou B, Schlumberger M, Dupuy C, et al. Clin Cancer Res 2011 17 2044 2054 10.1158/1078-0432.CCR-10-2041 21325074
64. Efficacy, safety, and potential biomarkers of sunitinib monotherapy in advanced hepatocellular carcinoma: a phase II study. Zhu AX, Sahani DV, Duda DG, di Tomasco E, Ancukiewicz M, Catalano OA, Sindhwani V, Blaszkowsky LS, Yoon SS, Lahdenranta J, et al. J Clin Oncol 2009 27 3027 3035 10.1200/JCO.2008.20.9908 19470923
65. Dynamics of beta2-adrenergic receptor-ligand complexes on living cells. Hegener O, Prenner L, Runkel F, Baader SL, Kappler J, Haberlein H, Biochemistry 2004 43 6190 6199 10.1021/bi035928t 15147203
66. Terbutaline causes immobilization of single beta2-adrenergic receptor-ligand complexes in the plasma membrane of living A549 cells as revealed by single-molecule microscopy. Sieben A, Kaminski T, Kubitscheck U, Haberlein H, J Biomed Opt 2011 16 026013 10.1117/1.3540670 21361697
67. Enhancing versus suppressive effects of stress hormones on skin immune function. Dhabhar FS, McEwen BS, Proc Natl Acad Sci USA 1999 96 1059 1064 10.1073/pnas.96.3.1059 9927693
68. Impact of stress on cancer metastasis. Moreno-Smith M, Lutgendorf SK, Sood AK, Future Oncol 2010 6 1863 1881 10.2217/fon.10.142 21142861
69. Alpha- and beta-adrenergic receptor (AR) protein expression is associated with poor clinical outcome in breast cancer: an immunohistochemical study. Powe DG, Voss MJ, Habashy HO, Zanker KS, Green AR, Ellis IO, Entschladen F, Breast Cancer Res Treat 2011 130 457 463 10.1007/s10549-011-1371-z 21298476
70. Beta-adrenergic signaling, a novel target for cancer therapy. Schuller HM, Oncotarget 2010 1 466 469 21317444