Daytime Blue Light Enhances the Nighttime Circadian Melatonin Inhibition of Human Prostate Cancer Growth

Comparative Medicine

Volumn 65, Issue 6, 2015, Pages 473-485

  Dauchy, Robert T ^a   Hoffman, Aaron E ^b   Wren Dail, Melissa A ^a   Hanifin, John P ^c   Warfield, Benjamin ^c   Brainard, George C ^c   Xiang, Shulin ^a   Yuan, Lin ^a   Hill, Steven M ^a   Belancio, Victoria P ^a   Dauchy, Erin M ^a   Smith, Kara ^a   Blask, David E ^a  

^a Departments of Cellular and Structural Biology   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

13 hydroxyoctadecadienoic acid; TFA; A V; Arterial venous difference; IpRGC; Intrinsically photosensitive retinal ganglion cell; LA; Linoleic acid; 13 HODE; Total fatty acids

Indexed keywords

CORTICOSTERONE; CYCLIC AMP; GLUCOSE; INSULIN; LACTIC ACID; LINOLEIC ACID; MELATONIN; FATTY ACID; GLUCOSE BLOOD LEVEL; LEPTIN;

AEROBIC GLYCOLYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD OXYGEN TENSION; BLUE LIGHT; CANCER GROWTH; CARBON DIOXIDE TENSION; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN TISSUE; INSULIN BLOOD LEVEL; LIGHT DARK CYCLE; MALE; METABOLISM; NIGHT; NONHUMAN; NUDE RAT; PROSTATE CANCER; RAT; RED LIGHT; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANALYSIS; ANIMAL; BLOOD; CELL DIVISION; LIGHT; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR;

ANIMALS; BLOOD GLUCOSE; CELL DIVISION; CIRCADIAN RHYTHM; CORTICOSTERONE; FATTY ACIDS; HUMANS; INSULIN; LACTIC ACID; LEPTIN; LIGHT; MALE; MELATONIN; PROSTATIC NEOPLASMS; RATS; RATS, NUDE;

EID: 85008932669     PISSN: 15320820     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. Altimus CM, Guler AD, Alam NM, Arman AC, Prusky GT, Sampath AP, Hattar S. 2010. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci 13:1107-1112.
2. Aschoff J, editor. 1981. Handbook of behavioral neurobiology: biological rhythms. New York (NY): Plenum Press.
3. Bhatti P, Mirrick DK, Davis S. 2012. Invited commentary: shift work and cancer. Am J Epidemiol 176:760-763.
4. Blask DE, Brainard GC, Dauchy RT, Hanifin JP, Davidson LK, Krause JA, Sauer LA, Rivera-Bermudez MA, Dubocovich ML, Jasser SA, Lynch DT, Rollag MD, Zalatan F. 2005. Melatonindepleted blood from premenopausal women exposed to light at night stimulates growth of human breast cancer xenografts in nude rats. Cancer Res 65:11174-11184.
5. Blask DE, Dauchy RT, Dauchy EM, Mao L, Hill SM, Greene MW, Belancio VP, Sauer LA, Davidson L. 2014. Light exposure at night disrupts host/cancer circadian regulatory dynamics: impact on the Warburg effect, lipid signaling, and tumor growth prevention. PLOS ONE 9:e102776.
6. Blask DE, Sauer LA, Dauchy RT, Holowachuk EW, Ruhoff MS, Kopff HS. 1999. Melatonin inhibition of cancer growth in vivo involves suppression of tumor fatty acid metabolism receptormediated signal transduction events. Cancer Res 59:4693-4701.
7. Blask DE, Dauchy RT, Sauer LA, Krause JA. 2004. Melatonin uptake and growth prevention in rat hepatoma 7288CTC in response to dietary melatonin: melatonin receptor-mediated inhibition of tumor linoleic acid metabolism to the growth signaling molecule 13-hydroxyoctadecadienoic acid and the potential role of phytomelatonin. Carcinogenesis 25:951-960.
8. Brainard GC. 1989. Illumination of laboratory animal quarters: participation of light irradiance and wavelength in the regulation of the neuroendocrine system, p 69-74. In: Guttman HN, Mench JA, Simmonds RC, Scientists Center for Animal Welfare, editors. Science and animals: addressing contemporary issues. Presented at the Scientists Center for Animal Welfare, Washington DC, 22-25 June 1988. Bethesda (MD): Scientists Center for Animal Welfare.
9. Brainard GC, Hanifin JP. 2005. Photons, clocks, and consciousness. J Biol Rhythms 20:314-325.
10. Brainard GC, Hanifin JP, Rollag MD, Greeson JM, Byrne B, Glickman G, Gerner E, Sanford B. 2001. Human melatonin regulation is not mediated by the threecone photopic visual system. J Clin Endocrinol Metab 86:433-436.
11. Brainard GC, Richardson BA, King TS, Matthews SA, Reiter RJ. 1983. The suppression of pineal melatonin content and N-acetyltransferase activity by different light irradiances in the Syrian hamster: a dose-response relationship. Endocrinology 113:293-296.
12. Brainard GC, Richardson BA, King TS, Reiter RJ. 1984. The influence of different light spectra on the suppression of pineal melatonin content in the Syrian hamster. Brain Res 294:333-339.
13. Brainard GC, Vaughan MK, Reiter RJ. 1986. Effect of light irradiance and wavelength on the Syrian hamster reproductive system. Endocrinology 119:648-654.
14. Buhr ED, Yoo SH, Takahashi JS. 2010. Temperature as a universal resetting cue for mammalian oscillators. Science 330:379-385.
15. Commission International de L'Eclarirage. 2003. Ocular lighting effects on human physiology and behavior, p 1-54. In: Technical report 158. Vienna (Austria): Commission Internationale De L'Eclairage.
16. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KY, Gamlin PD. 2005. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:749-754.
17. Dauchy RT, Blask DE, Sauer LA, Brainard GC, Krause JA. 1999. Dim light during darkness stimulated tumor progression by enhancing tumor fatty acid uptake and metabolism. Cancer Lett 144:131-136.
18. Dauchy RT, Blask DE, Dauchy EM, Davidson LK, Tirrell PC, Greene MW, Tirrell RP, Hill CR, Sauer LA. 2009. Antineoplastic effects of melatonin on a rare malignancy of mesenchymal origin: melatonin receptor-mediated inhibition of signal transduction, linoleic acid metabolism, and growth in tissue-isolated human leiomyosarcoma xenografts. J Pineal Res 47:32-42.
19. Dauchy RT, Dauchy EM, Hanifin JP, Gauthreaux SL, Mao L, Belancio VP, Ooms TG, Dupepe LM, Jablonski MR, Warfield B, Wren MA, Brainard GC, Hill SM, Blask DE. 2013. Effects of spectral transmittance through standard laboratory cages on circadian metabolism and physiology in nude rats. J Am Assoc Lab Anim Sci 52:146-156.
20. Dauchy RT, Dauchy EM, Mao L, Belancio VP, Hill SM, Blask DE. 2012. A new apparatus and surgical technique for the dual perfusion of human tumor xenografts in situ in nude rats. Comp Med 62:99-108.
21. Dauchy RT, Dauchy EM, Tirrell RP, Hill CR, Davidson LK, Greene MW, Tirrell PC, Wu J, Sauer LA, Blask DE. 2010. Dark-phase light contamination disrupts circadian rhythms in plasma measures of endocrine physiology and metabolism in rats. Comp Med 60:348-356.
22. Dauchy RT, Dupepe LM, Ooms TG, Dauchy EM, Hill CR, Mao L, Belancio VP, Slakey LM, Hill SM, Blask DE. 2011. Eliminating animal facility light-at-night contamination and its effect on circadian regulation of rodent physiology, tumor growth, and metabolism: a challenge in the relocation of a cancer research laboratory. J Am Assoc Lab Anim Sci 50:326-336.
23. Dauchy RT, Sauer LA. 1986. Preparation of 'tissue-isolated' rat tumors for perfusion: a new surgical technique that preserves continuous blood flow. Lab Anim Sci 36:678-681.
24. Dauchy RT, Wren MA, Dauchy EM, Hanifin JP, Jablonski MR, Warfield B, Brainard GC, Hill SM, Mao L, Dupepe LM, Ooms TG, Blask DE. 2013. Effects of spectral transmittance through red-tinted cages on circadian metabolism and physiology in nude rats. J Am Assoc Lab Anim Sci 52:745-755.
25. Dauchy RT, Xiang S, Mao L, Brimer S, Wren MA, Yuan L, Anbalagan M, Hauch A, Frasch T, Rowan BG, Blask DE, Hill SM. 2014. Circadian and melatonin disruption by exposure to light at night drives intrinsic resistance to tamoxifen therapy in breast cancer. Cancer Res 74:4099-4110.
26. Davis S, Mirick DK, Stevens RG. 2001. Nightshift work, light at night, and the risk of breast cancer. J Natl Cancer Inst 93:1557-1562.
27. Diaz B, Blazquez E. 1986. Effect of pinealectomy on plasma glucose, insulin, and glucagon levels in the rat. Horm Metab Res 18:225-229.
28. Dijk DJ, von Schantz M. 2005. Timing and consolidation of human sleep, wakefulness, and performance by a symphony of oscillators. J Biol Rhythms 20:279-290.
29. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna JM, Prusky GT, Berson DM, Hattar S. 2010. Melanopsinexpressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67:49-60.
30. Gabel V, Maire M, Chellappa CF, Reichert SL, Schmidt C, Hommes V, Viola AU, Cajochen C. 2013. Effects of artificial dawn and morning blue light on daytime cognitive performance, wellbeing, cortisol, and melatonin levels. Chronobiol Int 30:988-997.
31. Gamlin PD, McDougal DH, Pokorny J, Smith VC, Yau KW, Dacey DM 2007. Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Res 47:946-954.
32. Ge D, Dauchy RT, Liu S, Zhang Q, Mao L, Dauchy EM, Blask DE, Hill SM, Rowan BG, Brainard GC, Hanifin JP, Cecil KS, Xiong Z, Myers L, You Z. 2013. Insulin and IGF1 enhance IL17-induced chemokine expression through a GSK3B-dependent mechanism. J Pineal Res 55:377-387.
33. Gooley JJ, Rajaratnam SM, Brainard GC, Kronauer RE, Czeisler CA, Lockley SW. 2010. Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci Transl Med 2:31ra33.
34. Hansen J. 2001. Increased breast cancer risk among women who work predominantly at night. Epidemiology 12:74-77.
35. Hansen T, Bratlid T, Lingjarde O, Brenn T. 1987. Midwinter insomnia in the subarctic region: evening levels of serum melatonin and cortisol before and after treatment with bright artificial light. Acta Psychiatr Scand 75:428-434.
36. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, Yau KW. 2003. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice photosensitivity. Nature 424:76-81.
37. Hughes ME, Hogenesch JB, Kornacker K. 2010. JKT-CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms 25:372-380.
38. Illnerova H, Vanecek J, Hoffman K. 1983. Regulation of the pineal melatonin concentration in the rat (Rattus norvegicus) and the Djungarian hamster (Phodopus sungorus). Comp Biochem Physiol A Comp Physiol 74:155-159.
39. Institute for Laboratory Animal Research. 2011. Guide for the care and use of laboratory animals, 8th ed. Washington (DC): National Academy Press.
40. Illuminating Engineering Society of North America. 2008. Light and human health: an overview of the impact of optical radiation on visual, circadian, neuroendocrine, and neurobehavioral responses. New York (NY): Illuminating Engineering Society of North America.
41. Jasser SA, Hanifin JP, Rollag MD, Brainard GC. 2006. Dim light adaptation attenuates acute melatonin suppression in humans. J Biol Rhythms 21:394-404.
42. Jung-Hynes B, Schmit TL, Reagan-Shaw SR, Siddiqui IA, Mukhtar H, Ahmad N. 2011. Melatonin, a novel Sirt1 inhibitor, imparts antiproliferation effects against prostate cancer in vitro in culture and in vivo in TRAMP model. J Pineal Res 50:140-149.
43. Kalsbeek A, Strubbe JH. 1998. Circadian control of insulin secretion is independent of the temporal distribution of feeding. Physiol Behav 63:553-558.
44. Kennaway DJ, Voultsios A, Varcoe TJ, Moyer RW. 2002. Melatonin in mice: rhythms, response to light, adrenergic stimulation, and metabolism. Am J Physiol Regul Integr Comp Physiol 282:R358-R365.
45. Klein DC, Weller JL. 1972. Rapid light-induced decrease in pineal serotonin N-acetyltransferase activity. Science 177:532-533.
46. Kubo T, Ozasa K, Mikami K, Wakai K, Fujino Y, Watanabe Y, Miki T, Nakao M, Hayashi K, Suzuki K, Mori M, Washio M, Sakauchi F, Ito Y Yoshimura T, Tamakoshi A. 2006. Prospective cohort study of the risk of prostate cancer among rotating-shift workers: findings from the Japan collaborative cohort study. Am J Epidemiol 164:549-555.
47. Laakso ML, Porkka-Heiskanen T, Alila A, Peder M, Johansson G. 1988. Twenty-four-hour patterns of pineal melatonin and pituitary and plasma prolactin in male rats under 'natural' and artificial lighting conditions. Neuroendocrinology 48:308-313.
48. Lima FB, Machado UF, Bartol I, Seraphim PM, Sumida DH, Moraes SM, Hell NS, Okamoto NM, Saad MJ, Carvalho CR, Cipolla-Neto J. 1998. Pinealectomy causes glucose intolerance and decreases adipose cell responsiveness to insulin in rats. Am J Physiol 275:E934-E941.
49. Lucas RJ, Pierson SN, Berson DM, Brown TM, Cooper HM, Czeisler CA, Figueiro MG, Gamlin PD, Lockely SW, O'Hagan JB, Price LLA, Provencio I, Skene DJ, Brainard GC. 2014. Measuring and using light in the melanopsin age. Trends Neurosci 37:1-9.
50. Mao L, Dauchy RT, Blask DE, Slakey LM, Xiang S, Yuan L, Dauchy EM, Shan B, Brainard GC, Hanifin JP, Frasch T, Duplessis TT, Hill SM. 2012. Circadian gating of epithelial-to-mesenchymal transition in breast cancer cells via melatonin-regulation of GSK3β. Mol Endocrinol 26.
51. Nelson DL, Cox MM. 2005. Hormonal regulation of food metabolism, p 881-992; In: Nelson DL, Cox MM, editors. Lehninger principles of biochemistry, 4th ed. New York (NY): WH Freeman.
52. Nuffield Department of Clinical Neurosciences Medical Sciences Division. [Internet]. 2015. Rodent Toolbox v1.xlsx. [Cited 12 March 2015]. Available at: http://www.ndcn.ox.ac.uk/team/stuartpeirson.
53. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, Pletcher MT, Sato TK, Wiltshire T, Andahazy M, Kay SA, Van Gelder RN, Hogenesch JB. 2003. Melanopsin is required for nonimage- forming photic responses in blind mice. Science 301:525-527.
54. Reiter RJ. 1991. Pineal gland interface between photoperiodic environment and the endocrine system. Trends Endocrinol Metab 2:13-19.
55. Rollag MD, Niswender GD. 1976. Radioimmunoassay of serum concentrations of melatonin in sheep exposed to different lighting regimens. Endocrinology 98:482-489.
56. Sainz RM, Mayo JC, Tan DX, Leon J, Manchester L, Reiter RJ. 2005. Melatonin reduces prostate cancer cell growth leading to neuroendocrine differentiation via a receptor- and PKA-independent mechanism. Prostate 63:29-43.
57. Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, Colditz GA. 2001. Rotating night shifts and risk of breast cancer in women participating in the nurses' health study. J Natl Cancer Inst 93:1563-1568.
58. Sigurdardottir LG, Valdimarsdottir UA, Fall K, Rider JR, , Lockley SW, Schernhammer E, Mucci LA. 2012. Circadian disruption, sleep loss, and prostate cancer risk: a systematic review of epidemiologic studies. Cancer Epidemiol Biomarkers Prev 21:1002-1011.
59. Weng S, Estevez ME, Berson DM. 2013. Mouse ganglion-cell photoreceptors are driven by the most sensitive rod pathway and by both types of cones. PLoS One 8:e66480.
60. Wren MA, Dauchy RT, Hanifin JP, Jablonski MR, Warfield B, Brainard GC, Blask DE, Hill SM, Ooms TG, Bohm RP Jr. 2014. Effect of different spectral transmittances through tinted animal cages on circadian metabolism and physiology in Sprague-Dawley rats. J Am Assoc Lab Anim Sci 53:44-51.
61. Wu J, Dauchy RT, Tirrell PC, Wu SS, Lynch DT, Jitawatanarat P, Burrington CM, Dauchy EM, Blask DE, Greene MW. 2011. Light at night activates IGF1R-PDK1 signaling and accelerates tumor growth in human breast cancer xenografts. Cancer Res 71:2622-2631.