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, 69 (5), 350-373

Influence of Daytime LED Light Exposure on Circadian Regulatory Dynamics of Metabolism and Physiology in Mice

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Influence of Daytime LED Light Exposure on Circadian Regulatory Dynamics of Metabolism and Physiology in Mice

Robert T Dauchy et al. Comp Med.

Abstract

Light is a potent biologic force that profoundly influences circadian, neuroendocrine, and neurobehavioral regulation in animals. Previously we examined the effects of light-phase exposure of rats to white light-emitting diodes (LED), which emit more light in the blue-appearing portion of the visible spectrum (465 to 485 nm) than do broad-spectrum cool white fluorescent (CWF) light, on the nighttime melatonin amplitude and circadian regulation of metabolism and physiology. In the current studies, we tested the hypothesis that exposure to blue-enriched LED light at day (bLAD), compared with CWF, promotes the circadian regulation of neuroendocrine, metabolic, and physiologic parameters that are associated with optimizing homeostatic regulation of health and wellbeing in 3 mouse strains commonly used in biomedical research (C3H [melatonin-producing], C57BL/6, and BALB/c [melatonin-non-producing]). Compared with male and female mice housed for 12 wk under 12:12-h light:dark (LD) cycles in CWF light, C3H mice in bLAD evinced 6-fold higher peak plasma melatonin levels at the middark phase; in addition, high melatonin levels were prolonged 2 to 3 h into the light phase. C57BL/6 and BALB/c strains did not produce nighttime pineal melatonin. Body growth rates; dietary and water intakes; circadian rhythms of arterial blood corticosterone, insulin, leptin, glucose, and lactic acid; pO₂ and pCO₂; fatty acids; and metabolic indicators (cAMP, DNA, tissue DNA 3H-thymidine incorporation, fat content) in major organ systems were significantly lower and activation of major metabolic signaling pathways (mTOR, GSK3β, and SIRT1) in skeletal muscle and liver were higher only in C3H mice in bLAD compared with CWF. These data show that exposure of C3H mice to bLAD compared with CWF has a marked positive effect on the circadian regulation of neuroendocrine, metabolic, and physiologic parameters associated with the promotion of animal health and wellbeing that may influence scientific outcomes. The absence of enhancement in amelatonic strains suggests hyperproduction of nighttime melatonin may be a key component of the physiology.

Figures

Figure 1.
Figure 1.
Normalized spectral power distributions of the polychromatic blue-enriched LED (blue) and fluorescent lamp (red) light as transmitted through a standard polycarbonate, translucent laboratory mouse cage.
Figure 2.
Figure 2.
Circadian plasma melatonin levels (mean ± 1 SD) of male and female pigmented (A) C3H and (B) C57BL/6 and nonpigmented BALB/c (C) mice maintained for 12 wk in standard, polycarbonate, translucent, clear cages under CWF (controls, solid black circles) or bLAD (experimental, solid blue squares) lighting with a 12:12-h light:dark phase (300 lx; 123 µW/cm2). During the 12-h dark phase lighting conditions from 1800 to 0600 (dark bars), animals were exposed to no light at night. Data are plotted twice in panels to better demonstrate rhythmicity and clarity of scale. Rhythmicity analysis (Table 3) revealed robust and highly significant (P < 0.0001) rhythmic patterns under control lighting conditions for both groups of C3H mice but not for C57BL/6 and BALB/c mice, with 31.9-fold and 230.9-fold increases in nighttime amplitudes compared with daytime in CWF and bLAD in C3H mice, respectively, and a 5.2-fold increase in amplitude observed in bLAD-exposed C3H mice compared with controls at 2400 (P < 0.001; Student t test). Concentrations with asterisks (black, CWF peaks; blue, bLAD peaks) differ (P < 0.05) from concentrations without asterisks.
Figure 3.
Figure 3.
Circadian changes in the blood plasma total fatty (TFA) levels (µg/mL; mean ± 1 SD) of male and female (A) C3H, (B) C57BL/6, and (C) BALB/c mice fed normal chow without restriction and maintained under either control CWF (TFA, male, solid black circles; female solid amber triangles) or experimental bLAD (TFA, male, solid blue squares; female, inverted green triangles) lighting conditions. Mice were exposed to dark-phase lighting conditions (see Methods) from 1800 to 0600 (dark bars). TFA values (mean ± 1 SD; n = 60 per group) are the sums of myristic, palmitic, palmitoleic, stearic, oleic, linoleic, and arachidonic acid concentrations collected at the various time points. Data are plotted twice to better demonstrate rhythmicity. Rhythmicity analysis (Table 3) revealed robust and highly significant (P < 0.0001) rhythmic patterns under control lighting conditions for both groups, with a more than a 6-fold increase in nighttime amplitude in CWF control and bLAD experimental groups. Concentrations indicated by asterisks are different (P < 0.05) from those without asterisks.
Figure 4.
Figure 4.
Circadian changes in the arterial blood glucose, lactate, pO2, and pCO2 levels of male and female (A) C3H, (B) C57BL/6, and (C) BALB/c mice maintained under either control (solid black circles) or experimental (solid blue squares) lighting conditions (mean ± 1 SD; n = 120 per group). Mice were exposed to dark-phase lighting conditions from 1800 to 0600 (dark bars). Data are plotted twice to better visualize rhythmicity. Rhythmicity analysis (Table 3) revealed robust and highly significant (P < 0.0001) rhythmic patterns for both control CWF and experimental bLAD groups but a significantly disrupted (P < 0.05) phase pattern for bLAD group animals of the C3H but not C57BL/6 or BALB/c strain. *, Value differs significantly (P < 0.001) between experimental and control conditions (Student t test).
Figure 5.
Figure 5.
Circadian changes in plasma corticosterone in the arterial blood of (A) C3H, (B) C57BL/6, and (C) BALB/c mice maintained under either CWF control (male, solid black circles; female, solid amber squares) or experimental bLAD (male, solid blue triangles; female, solid green inverted triangles) lighting conditions. Data are plotted twice to better demonstrate rhythmicity. Dark bars represent dark-phase lighting conditions from 1800 to 0600. Rhythmicity analysis (Table 3) revealed robust and highly significant (P < 0.0001) rhythmic patterns under control conditions, with significant (P < 0.05) but disrupted rhythmic patterns under experimental conditions for corticosterone (*, P < 0.001) in C3H but not C57BL/6 and BALB/c mice.
Figure 6.
Figure 6.
Circadian changes in plasma insulin in the arterial blood of (A) C3H, (B) C57BL/6, and (C) BALB/c mice maintained under either CWF control (male, solid black circles; female, solid amber squares) or experimental bLAD (male, solid blue triangles; female, solid green inverted triangles) lighting conditions. Data are plotted twice to better demonstrate rhythmicity. Mice were exposed to dark-phase lighting conditions from 1800 to 0600 (dark bars). Rhythmicity analysis (Table 3) revealed robust and highly significant (P < 0.0001) rhythmic patterns under control conditions, with significant (P < 0.05) but disrupted rhythmic patterns under experimental conditions for insulin (*, P < 0.001) in C3H but not C57BL/6 and BALB/c mice.
Figure 7.
Figure 7.
Circadian changes in plasma leptin in the arterial blood of (A) C3H, (B) C57BL/6, and (C) BALB/c mice maintained under either CWF control (male, solid black circles; female, solid amber squares) or experimental bLAD (male, solid blue triangles; female, solid green inverted triangles) lighting conditions. Data are plotted twice to better demonstrate rhythmicity. Black bars represent dark-phase lighting conditions from 1800 to 0600. Rhythmicity analysis (Table 3) revealed robust and highly significant (P < 0.0001) rhythmic patterns under control conditions, with significant (P < 0.05) but disrupted rhythmic patterns under experimental conditions for leptin (*, P < 0.001) in C3H but not C57BL/6 and BALB/c mice.
Figure 8.
Figure 8.
Circadian alterations in skeletal muscle cAMP levels (nmol/g) in (A) C3H, (B) C57BL/6, and (C) BALB/c mice maintained under either CWF control (male, solid black circles; female, solid amber squares) or experimental bLAD (male, solid blue triangles; female, solid green inverted triangles) lighting conditions. Data are plotted twice to better demonstrate rhythmicity. Dark bars represent dark-phase lighting conditions from 1800 to 0600. Rhythmicity analysis revealed robust and highly significant (P < 0.0001) rhythmic patterns under control conditions, with significant (P < 0.05) but disrupted rhythmic patterns under experimental conditions for skeletal muscle cAMP levels (*, P < 0.001) in C3H but not C57BL/6 and BALB/c mice.
Figure 9.
Figure 9.
Circadian alterations in liver cAMP levels (nmol/g), in (A) C3H, (B) C57BL/6, and (C) BALB/c mice maintained on either CWF control (male, solid black circles; female, solid amber squares) or experimental bLAD (male, solid blue triangles; female, solid green inverted triangles) lighting conditions. Data are plotted twice to better demonstrate rhythmicity. Dark bars represent dark-phase lighting conditions from 1800 to 0600. Concentrations with asterisks are different (P < 0.05) from those without asterisks.
Figure 10.
Figure 10.
Circadian alterations in [3H]thymidine into skeletal muscle DNA in (A) C3H, (B) C57BL/6, and (C) BALB/c mice male maintained on either CWF control (male, solid black circles; female, solid amber squares) or experimental bLAD (male, solid blue triangles; female, solid green inverted triangles) lighting conditions. Data are plotted twice to better demonstrate rhythmicity. Dark bars represent dark-phase lighting conditions from 1800 to 0600. Concentrations with asterisks are different (P < 0.05) from those without asterisks.
Figure 11.
Figure 11.
Circadian alterations in [3H]thymidine into liver tissue DNA in (A) C3H, (B) C57BL/6, and (C) BALB/c male maintained on either CWF control (male, solid black circles; female, solid amber squares) or experimental bLAD (male, solid blue triangles; female, solid green inverted triangles) lighting conditions. Data are plotted twice to better demonstrate rhythmicity. Dark bars represent dark-phase lighting conditions from 1800 to 0600. Concentrations with asterisks are different (P < 0.05) from those without asterisks.
Figure 12.
Figure 12.
Western blot analysis of the expression of phosphorylated (p) and total (t) forms of GSK3β, SIRT1, and mTOR in (A) skeletal muscle from male and female C3H and C57BL/6 mice exposed to either control CWF or experimental bLAD daytime light at 1200 (CWF, lanes 1, 5, 9, and 13; bLAD, lanes 2, 6, 10, and 14) or 2400 (CWF, lanes 3, 7, 11, and 15; bLAD, lanes 4, 8, 12, and 16); each lane represents results from 5 mouse tissue samples combined. Relative expression (mean ± 1 SD; derived from the densitometric quantitation of the immunoblots) as phosphorylated GSK3β to total protein in C3H (B) C57BL/6 mouse (C) skeletal muscle. Significant (P < 0.05) differences from CWF 1200 are indicated as: aCWF male (M) 1200, bbLAD (M) 1200, cCWF female (F) 1200, dbLAD F 1200, eCWF M 2400, fbLAD M 2400, gCWF F 2400, and hbLAD F 2400. Relative expression (mean ± 1 SD; derived from the densitometric quantitation of the immunoblots) of SIRT1 total protein in (D) C3H and (E) C57BL/6 mouse skeletal muscle. Significant (P < 0.05) differences from CWF 1200 are indicated as: aCWF male (M) 1200, bbLAD (M) 1200, cCWF female (F) 1200, dbLAD F 1200, eCWF (M) 2400, fbLAD (M) 2400, gCWF (F) 2400, and hbLAD (F) 2400. Relative expression (mean ± 1 SD; derived from the densitometric quantitation of the immunoblots) as phosphorylated mTOR to total protein in (F) C3H and (G) C57BL/6 mouse skeletal muscle. Significant (P < 0.05) differences from CWF 1200 are indicated as: aCWF male (M) 1200, bbLAD M 1200, cCWF female (F) 1200, dbLAD F 1200, eCWF (M) 2400, fbLAD (M) 2400, gCWF (F) 2400, and hbLAD (F) 2400.
Figure 13.
Figure 13.
Western blot analysis of the expression of phosphorylated (p) and total (t) forms of GSK3β, SIRT1, and mTOR in (A) liver from male and female C3H and C57BL/6 mice exposed to either control CWF or experimental bLAD daytime light at 1200 (CWF, lanes 1, 5, 9, and 13; bLAD, lanes 2, 6, 10, and 14) or 2400 (CWF, lanes 3, 7, 11, and 15; bLAD, lanes 4, 8, 12, and 16); each lane represents results from 5 mouse tissue samples combined. Relative expression (mean ± 1 SD; derived from the densitometric quantitation of the immunoblots) as phosphorylated GSK3β to total protein in (B) C3H and (C) C57BL/6 mouse liver. Significant (P < 0.05) differences from CWF 1200 are indicated as: aCWF male (M) 1200, bbLAD (M) 1200, cCWF female (F) 1200, dbLAD F 1200, eCWF (M) 2400, fbLAD (M) 2400, gCWF (F) 2400, and hbLAD F 2400. Relative expression (mean ± 1 SD; derived from the densitometric quantitation of the immunoblots) of SIRT1 total protein in (D) C3H and (E) C57BL/6 mouse liver. Significant (P < 0.05) differences from CWF 1200 are indicated as: aCWF male (M) 1200, bbLAD (M) 1200, cCWF female (F) 1200, dbLAD (F) 1200, eCWF (M) 2400, fbLAD (M) 2400, gCWF (F) 2400, and hbLAD (F) 2400. Relative expression (mean ± 1 SD; derived from the densitometric quantitation of the immunoblots) as phosphorylated mTOR to total protein in (F) C3H and (G) C57BL/6 mouse and liver. Significant (P < 0.05) differences from CWF 1200 are indicated as: aCWF male (M) 1200, bbLAD M 1200, cCWF female (F) 1200, dbLAD (F) 1200, eCWF (M) 2400, fbLAD (M) 2400, gCWF (F) 2400, and hbLAD (F) 2400.

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