Circadian and melatonin disruption by exposure to light at night drives intrinsic resistance to tamoxifen therapy in breast cancer

Cancer Research

Volumn 74, Issue 15, 2014, Pages 4099-4110

  Dauchy, Robert T ^a   Xiang, Shulin ^a   Mao, Lulu ^a   Brimer, Samantha ^a   Wren, Melissa A ^a,b   Yuan, Lin ^a   Anbalagan, Muralidharan ^a   Hauch, Adam ^a   Frasch, Tripp ^a   Rowan, Brian G ^a   Blask, David E ^a   Hill, Steven M ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TULANE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MELATONIN; TAMOXIFEN; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RESISTANCE; CANCER RISK; CELL PROLIFERATION; CELL SURVIVAL; CIRCADIAN RHYTHM; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; LIGHT DARK CYCLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ANIMAL; BLOOD; BREAST NEOPLASMS; DISEASE MODEL; DRUG RESISTANCE; DRUG SCREENING; LIGHT; MCF 7 CELL LINE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; RAT;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CIRCADIAN RHYTHM; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; LIGHT; MCF-7 CELLS; MELATONIN; MICE, NUDE; RANDOM ALLOCATION; RATS; TAMOXIFEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84905501655     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3156     Document Type: Article

References (48)

1. Ravdin PM, Green S, Dorr TM, McGuire WL, Fabian C, Pugh RP, et al. Prognostic significance of progesterone receptor levels in estrogen receptor-positive patients with metastatic breast cancer treated with tamoxifen: results of a prospective Southwest Oncology Group study. J Clin Oncol 1992;8:1284-91.
2. Lewis-Wambi JS, Jordan VC. Treatment of Postmenopausal Breast Cancer with Selective Estrogen Receptor Modulators (SERMs). Breast Dis 2006;24:93-105.
3. Lønning PE, Eikesdal HP. Aromatase inhibition 2013: clinical state of the art and questions that remain to be solved. Endocr Relat Cancer 2013;20:R183-201.
4. Jordan VC, Brodie AM. Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer. Steroids 2007;72:7-25.
5. Ingle JN. Endocrine therapy trials of aromatase inhibitors for breast cancer in the adjuvant and prevention settings. Clin Cancer Res 2005;11:900-5.
6. Sabnis G, Brodie A. Understanding resistance to endocrine agents: molecular mechanisms and potential for intervention. Clin Breast Cancer 2010;18:E6.
7. Werner H, Bruchi I. The insulin-like growth factor-1 receptor as an oncogene. Arch Physiol Biochem 2009;115:58-71.
8. Fagan DH, Yee D. Crosstalk between IGF1R and estrogen receptor signaling in breast cancer. J Mammary Gland Biol Neoplasia 2008;13:423-9.
9. Chen M, Cui YK, Huang WH, Man K, Zhang GJ. Phosphorylation of estrogen receptor a at serine 118 is correlated with breast cancer resistance to tamoxifen. Oncol Lett 2013;1:118-24.
10. Arpino G, Wiechmann L, Osborne CK, Schiff R. Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance. Endocr Rev 2008;29:1289-91.
11. deGraffenried LA, Chandrasekar B, Friedrichs WE, Donzis E, Silva J, Hildalgo M, et al. NF-kappa B inhibition markedly enhances sensitivity of resistant breast tumor cells to tamoxifen. Ann Oncol 2004;15:885-90.
12. Shah YM, Rowan BG. The Src kinase pathway promotes tamoxifen agonist action in Ishikawa endometrial cell through phosphorylationdependent stabilization of estrogen receptor (alpha) promoter interaction and elevated steroid receptor coactivator 1 activity. Mol Endocrinol 2005;19:732-48.
13. Vallabhaneni S, Nair BC, Cortez V, Challa R, Chakravarty D, Tekma RR, et al. Significance of ER-Src axis in hormonal therapy resistance. Breast Cancer Res Treat 2011;130:377-85.
14. EH Y, Lee CS, Lee JK, Lee YJ, Shin MK, Cho CH, et al. STAT3-RANTES autocrine signaling is essential for tamoxifen resistance in human breast cancer cells. Mol Cancer Res 2013;11:31-42.
15. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer. Int J Cancer 2010;127:2893-917.
16. Madigan MP, Ziegler RG, Benichou J, Byrne C, Hoover RN. Proportion of breast cancer cases in the United States explained by well-established risk factors. J. Natl Cancer Inst 1997;87:1681-5.
17. Hahn RA, Moolgavkar SH. Nulliparity, decade of first birth, and breast cancer in Connecticut cohorts, 1855-1945: an ecological study. Am J Public Health 1989;79:1503-7.
18. Stevens RG. Electric power used and breast cancer: a hypothesis. Am J Epidemiol 1987;125:556-61.
19. Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Bouvard V, et al. Carcinogenicity of shift work, painting, and fire fighting. Lancet Oncol 2007;8:1065-6.
20. Hardeland R, Madrid JA, Tan DX, Reiter RJ. Melatonin, the circadian multioscillator system and health: the need for detailed analysis of peripheral melatonin signaling. J Pineal Res 2012;52:139-66.
21. Stevens RG. Artificial lighting in the industrialized world: circadian disruption and breast cancer. Cancer Causes Control 2006;17:501-7.
22. Ruger M, St Hilaire MA, Brainard GC, Khalsa SB, Kronauer RE, Czeisler CA, et al. Human phase response curve to a single 6.5 h pulse of shortwavelength light. J Physiol 2013;591:353-63.
23. Hanifin JP, Brainard GC. Photoreception for circadian, neuroendocrine and neurobehavioral regulation. J Physiol Anthropol 2007;26:87-94.
24. Dauchy RT, Blask DE, Sauer LA, Brainard GC, Krause JA. Dim light during darkness stimulates tumor progression by enhancing tumor fatty acid uptake and metabolism. Cancer Lett 1999;144:131-6.
25. Blask DE, Hill SM, Dauchy RT, Xiang S, Yuan L, Duplesis T, et al. Circadian regulation of molecular, dietary, and metabolic signaling mechanisms of human breast cancer growth by the nocturnal melatonin signal and the consequences of its disruption by light at night. J Pineal Res 2011;51:259-69.
26. Blask DE, Dauchy RT, Sauer LA, Krause JA, Brainard GC. Growth and fatty acid metabolism of human breast cancer (MCF-7) xenografts in nude rats: impact of constant light-induced nocturnal melatonin suppression. Breast Cancer Res Treat 2003;279:313-20.
27. Wu J, Dauchy RT, Tirrell PC, Wu SS, Lynch DT, Jitawatanarat P, et al. Light at night activates IGF-1R/PDK1 signaling and accelerates tumor growth in human breast cancer xenografts. Cancer Res 2011;71:2622-31.
28. Mao L, Dauchy RT, Blask DE, Slakey LM, Xiang S, Yuan L, et al. Circadian gating of epithelial-to-mesenchymal transition in breast cancer cells via melatonin regulation of GSK3b. Mol Endocrinol 2012;26:1808-20.
29. Wilson ST, Blask DE, Lemus-Wilson AM. Melatonin augments the sensitivity of MCF-7 human breast cancer cells to tamoxifen in vitro. J Clin Endocrinol Metab 1992;75:669-70.
30. Dauchy RT, Dauchy EM, Tirrell RP, Hill CR, Davidson LK, Greene MW, et al. Dark-phase light contamination disrupts circadian rhythms in plasma measures of physiology and metabolism. Comp Med 2010;60:348-56.
31. Blask DE, Brainard GC, Dauchy RT, Hanifin JP, Davidson LK, Krause JA, et al. Melatonin-depleted blood from premenopausal women exposed to light at night stimulates growth of human breast cancer xenografts in nude rats. Cancer Res 2005;65:11174-84.
32. Anbalagan M, Carrier L, Glodowski S, Hangauer D, Shan B, Rowan BG. KX-01, a novel Src kinase inhibitor directed toward the peptide substrate site, synergizes with tamoxifen in estrogen receptor a positive breast cancer. Breast Cancer Res Treat 2012;132:391-409.
33. Lazennec G, Thomas JA, Katzenellenbogen BS. Involvement of the cAMP response element binding protein (CREB) and estrogen receptor phosphorylation in the synergistic action of the estrogen receptor by estradiol and protein kinase activators. J Steroid Biochem Mol Biol 2001;77:193-203.
34. Cho YS, Park YG, Lee YN, Kim MK, Bates S, Tan L, et al. Extracellular protein kinase A as a cancer biomarker: its expression by tumor cells and reversal by a myristate-lacking C alpha and RIIbeta subunit overexpression. Proc Natl Acad Sci U S A 2000;97:835-40.
35. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer 2011;11:85-95.
36. Blask DE, Dauchy RT, Dauchy EM, Mao L, Hill SM, Greene MW, et al. Light exposure at night disrupts host/cancer circadian regulatory dynamics: impact on the Warburg effect, lipid signaling and tumor growth prevention. PLoS ONE 2014 (in press).
37. Soga T. Cancer metabolism: key players in metabolic reprograming. Cancer Sci 2013;104:275-81.
38. Demaria M, Giorgi C, Lebiedzinska M, Esposito G, D'Angeli L, Bartoli A, et al. A Stat3-mediated metabolic switch is involved in tumor transformation and Stat3 addiction. Aging 2010;2:823-42.
39. Demaria M, Poli V. PMK2, Stat3 and HIF-1a: The Warburg's vicious circle. JAK-STAT 2012;1:194-6.
40. Martinez-Outschoorn UE, Lin Z, Ko YH, Goldberg AF, Flomenberg N, Wang C, et al. Understanding the metabolic basis of drug resistance: therapeutic induction of the Warburg effect kills cancer cells. Cell Cycle 2011;10:2521-8.
41. Browne BC, Hochgrafe F, Wu J, Millar EK, Barraclough J, Stone A, et al. Global characterization of signaling networks associated with tamoxifen resistance in breast cancer. FEBS J 2013;280:5237-57.
42. Garcia-Becerra R, Santos N, Diaz L, Comacho J. Mechanisms of resistance to endocrine therapy in breast cancer: focus on signaling pathways, miRNAs and genetically based resistance. Int J Mol Sci 2012;14:108-45.
43. Hiscox S, Morgan L, Green TP, Barrow D, Gee J, Nicholson RI. Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res Treat 2006;97:263-74.
44. Bowman T, Broome MA, Sinibaldi D, Wharton W, Pledger WJ, Sedivy JM, et al. Stat3-mediated Myc expression is required for Src transformation and PDGF-induced mitogenesis. Proc Natl Acad Sci U S A 2001;98:7319-24.
45. Grivennikov SI, Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev 2010;21:11-9.
46. Alvarez-Garcia V, Gonzalez A, Alonso-Gonzales C, Martinez-Campla C, Cos S. Melatonin interferes in the desmoplastic reaction in breast cancer by regulating cytokine production. J Pineal Res 2012;52:282-90.
47. Kiefer T, Ram PT, Yuan L, Hill SM. Melatonin inhibits estrogen receptor transactivation and cAMP levels in breast cancer cells. Breast Cancer Res 2002;71:37-48.
48. Del Rio B, Garcia Pedrero JM, Martinez-Campa C, Zuazua P, Lazo PS, Ramos S. Melatonin, an endogenous-specific inhibitor of estrogen receptor alpha via calmodulin. J Biol Chem 2004;279:38294-302.