Can CoQ10 cause eye problems?

The CoQ10 plays an important role in the biological and medical fields. In human eyes, the consequences of CoQ10 deficiency are closely associated with aging-associated diseases, such as age-related macular degeneration and glaucoma 40.

nature.com - Coenzyme Q10 in the eye isomerizes by sunlight irradiation - Nature

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Exploration of potential photoisomerizable lipids in the eyeball

We irradiated six paired eyeball lipid extracts in the sunlight for over a day in order to explore any photoisomerizable lipids in the eyeball (Fig. S1). Interestingly, the light irradiation decreased the darkness of the extract (Fig. S1). The total ion chromatogram (TIC) obtained from liquid chromatography-mass spectrometry (LC/MS) analysis showed a similar pattern in nonirradiated and irradiated extracts (Fig. 1A,B). To explore the potential photoisomerizable lipid molecules, we first identified the decreased molecular species by volcano plot analysis. Surprisingly, the volcano plot showed a decrease of more than nine hundred lipid-associated ions (including both positive and negative ions) in the sunlight-irradiated samples (Fig. 1C, Supplementary file 1). Of these, four positive ions at m/z 880.72, 863.69, 956.86, and 812.65 were decreased both significantly (p < 0.05) and by more than two-fold in irradiated samples compared to the nonirradiated ones (Fig. 1C). The first two ions (m/z 880.72 and 863.69) were tentatively assigned as [M + NH 4 ]+ and [M + H]+ adduct of CoQ10 (oxidized), respectively (Fig. 1C, Table S1, Supplementary file 1). The other two ions (m/z 956.86 and 812.65) were associated with [M + NH 4 ]+ adduct of triglyceride (58:4) and coenzyme Q9, respectively (Fig. 1C, Table S1, Supplementary file 1). In the current study, we further focused on CoQ10, which may have the strong potentiality of isomerization, as it showed the most significant decrease among those three lipids of interest. The dot plot showed that both ions (protonated and ammonium adduct) associated with CoQ10 decreased (ranging between 2 to 10-folds) in all six paired eyeball extracts upon sunlight irradiation (Fig. 1D). It is important to note that the reduced form of CoQ10 (CoQ10H2) was not detected in the LC/MS data of the eyeball extract sample. Figure 1 Exploration of potential isomerizable lipids in eyeballs upon sunlight irradiation. Total ion chromatogram (TIC) was obtained from the (A) nonirradiated and (B) irradiated eyeball extract (data of the first paired sample was shown here). Both positive and negative ion mode data were shown in the TIC. (C) Volcano plots of 1001 identified lipid species in the eyeball extracts. The dashed orange line show where p = 0.05. The dashed purple lines at the right and left show where fold change (irradiated/nonirradiated) = 2 and 0.5, respectively. The ions-of-interest that showed both large magnitude fold changes (x-axis) and high statistical significance (y-axis) were annotated. (D) Distributions of fold changes (irradiated/nonirradiated) of ions associated with CoQ10. A single dot in the dot plot indicates the fold change of one paired sample. The average retention time for [M + H]+ and [M + NH 4 ]+ of CoQ10 shown here was 45.69 min and 45.70 min, respectively. CoQ10 Coenzyme Q10, CoQ9 Coenzyme Q9, TG(58:4) triglyceride(58:4). Full size image

Assignment of CoQ10 in eyeball extract

As already described, the LipidSearch™ assigned the m/z 863.69 and m/z 880.72 in the eyeball extract data as [M + H]+ and [M + NH 4 ]+ adduct of CoQ10, respectively. To verify the assignment of CoQ10, we investigated the mass spectra and MS/MS spectra observed in eyeball extract and compared them with those of pure compounds. As is seen in Fig. S2, the ion at m/z 863.69 and m/z 880.72 were detected as the monoisotopic peak in both nonirradiated and irradiated eyeball extract. The nonirradiated pure CoQ10 (oxidized form and all-trans-isomer) was also detected at m/z 863.69 and m/z 880.72, which belong to [M + H]+ and [M + NH 4 ]+ adducts, respectively (Fig. S2C). The isotopic distribution of these two ions in pure CoQ10 data was consistent with those of eyeball extract data (Fig. S2). Of the ions at m/z 863.69 and m/z 880.72, the latter showed a higher signal intensity in the mass spectra of both eyeball extract and pure CoQ10 (Fig. S2). In this study, we investigated the fragments of the molecular ion at m/z 880.72 to visualize the clearer MS/MS spectra. Interestingly, we observed similar fragmentation patterns between the spectra obtained from the eyeball extracts and pure CoQ10 (Fig. S3, Fig. 2). Upon tandem MS of CoQ (regardless of the length of isoprene tail), two fragment ions, namely tropylium ion (m/z 197.08) and chromenylium ion (m/z 237.11) are known to derive from the quinone head group, which is shared by all CoQ species21,22,23,24. Consistently, both of those fragments were seen in the MS/MS spectra of eyeball extract and pure CoQ10 (Fig. 2). The tropylium ion (m/z 197.08) was detected as the most abundant fragment in both MS/MS spectra (Fig. S3). In addition, a number of fragments (m/z 149.13, m/z 135.12, m/z 121.10, m/z 109.10, m/z 95.09, m/z 81.07, and m/z 69.07) that are associated with the isoprene chain were prominent in both MS/MS spectra (Fig. 2). These data made the assignment of CoQ10 unambiguous. Figure 2 Structural analysis of ion at m/z 880.72. (A) The structure of natural CoQ10 (all-trans form) with known and possible fragment ions (a–j). (B) MS/MS spectra of nonirradiated pure CoQ10. (C) MS/MS spectra of the molecular ion at m/z 880.72 (tentatively assigned as [CoQ10 + NH 4 ]+) were observed in nonirradiated eyeball lipid extract data. The fragments of CoQ10 shown in (A) were marked in the MS/MS spectra. Full size image

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CoQ10 in sunlight-irradiated eyeball extract was isomerized

Next, we analyzed the extracted ion chromatogram (EIC) for the ion of m/z 880.72 of the eyeball extract data in order to investigate the isomeric CoQ10 molecules. Interestingly, we observed two distinct peaks at two different retention times (RT) in the irradiated sample (Fig. 3B), whereas a single peak was found in the nonirradiated one (Fig. 3A). For the EIC of CoQ10, the single peak in the nonirradiated sample and the right peak in the irradiated sample will be termed the “original peak” in this article. The MS/MS spectra (molecular ion at m/z 880.72) acquired at two RT (RT 45.20 min and RT 45.61 min) in the irradiated sample showed a similar pattern (Fig. 3) with some characteristic fragment ions (Fig. 3C,D). The fragment ions of m/z 249.91, m/z 277.14, and m/z 303.16 were exclusively observed at RT 45.20 (Fig. 3C). On the other hand, the characteristic fragment ions observed at RT 45.61 were m/z 201.17, m/z 219.10, m/z 231.10, and m/z 245.12 (Fig. 3D). These results indicated that CoQ10 in eyeball extract was isomerized by sunlight irradiation. Figure 3 EIC and MS/MS spectra of coenzyme Q10 (CoQ10) in sunlight-irradiated eyeball extract. The EICs were observed in the (A) nonirradiated and (B) irradiated extract. MS/MS spectra of CoQ10 at (C) RT 45.20 min and (D) RT 45.61 min in the irradiated extract. Arrows indicate the fragmentations exclusively observed at RT 45.20 min or RT 45.61 min. Full size image

Pure CoQ10 was isomerized along with altered physical properties by sunlight irradiation

To confirm the photoisomerization of CoQ10 in the eyeball, we prepared the solution of the pure compound, irradiated it in the sunlight similarly, and then analyzed it by LC–MS/MS. As expected, a single peak at 45.3 min (excluding the peak which generally appears at the beginning due to the elution of highly hydrophilic compounds that do not bind to the column) was mainly observed in the TIC of the nonirradiated pure CoQ10 (Fig. S4A). On the other hand, in addition to the peak at 45.3 min, a number of peaks were observed in the TIC of sunlight-irradiated pure CoQ10 (Fig. S4B), indicating that the isomerization and/or any other phenomena (e.g., degradation) of some CoQ10 molecules has occurred. Similar to the results of eyeball extract, an additional peak (at RT 44.8 min) at the left of the original peak (RT 45.3 min) was observed in the EIC of CoQ10 in the irradiated pure sample (Fig. 4B). Interestingly, the left peak of CoQ10 showed a larger area than the right peak. It is also noteworthy that the isomeric peak (at RT 44.8 min) of CoQ10 was the most prominent among the additional peaks in the TIC of irradiated pure CoQ10 (Fig. S4, Fig. 4). The MS/MS spectra at two different RT showed a similar pattern with several characteristic fragment ions, which were exclusively observed at RT 44.86 min or 45.17 min (Fig. S5, Fig. 4C,D). These results indicated that pure CoQ10 was isomerized by sunlight irradiation. It is to be noted that CoQ10H2 was not detected in this data (Fig. S6), meaning that sunlight did not mediate the reduction of CoQ10 to CoQ10H2. Figure 4 EIC and MS/MS spectra of pure coenzyme Q10 (CoQ10). EICs were observed in the (A) nonirradiated and (B) sunlight-irradiated samples. MS/MS spectra of CoQ10 at (C) RT 44.86 min and (D) RT 45.17 min in the sunlight-irradiated sample. Arrows indicate the fragmentations exclusively observed at RT 44.86 min or RT 45.17 min. Full size image We also performed LC separations in conjunction with ion mobility spectrometry-mass spectrometry (LC-IMS-MS). Consistently, a difference in drift time of 0.05 ms was observed between the isomeric peaks of sunlight-irradiated pure CoQ10 (Fig. S7). Next, we examined the physical properties of the nonirradiated and sunlight-irradiated CoQ10 through direct visualization and turbidity measurement. Before irradiation, the pure CoQ10 in Bligh and Dyer solvent produced a yellow-colored solution (Fig. S8A). Interestingly, the sunlight exposure turned the color of the solution from yellow to orange (Fig. S8B). The solutions were then dried and re-dissolved in 100% methanol, where we observed a cloudy and transparent solution of the nonirradiated and sunlight-irradiated CoQ10, respectively (Fig. S8C). Consistently, the turbidity of the nonirradiated solution in methanol was much higher than that of the irradiated solution (Table S2). These altered physical properties might be attributed to the isomeric CoQ10 produced upon irradiation.

CoQ10 in sunlight-irradiated fresh eyeball was also isomerized

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Next, we investigated whether sunlight irradiation is capable of producing an isomer of CoQ10 in the freshly-prepared eyeball. For this purpose, the fresh eyeballs were irradiated in the sunlight, followed by lipid extraction and LC/MS analysis. Pure CoQ10 was also analyzed under the same conditions to confirm the consistency of RT. The TIC of nonirradiated and irradiated fresh eyeballs showed a similar pattern (Fig. 5A,B). Also, the EIC of CoQ10 in the nonirradiated fresh eyeball data showed a single peak (at RT 45.32), whereas the irradiated fresh eyeball data showed an additional peak (RT 44.88 min) at the left side of the original peak (Fig. 5C,D). The retention time was consistent with that of pure CoQ10 data (Fig. 5C–F). These results indicated that the CoQ10 in the fresh eyeball was also isomerized upon sunlight irradiation. Figure 5 LC/MS data of fresh eyeball and pure CoQ10. TIC of (A) nonirradiated and (B) sunlight-irradiated fresh eyeball. The data shown here were obtained in positive ion mode. EIC of CoQ10 in (C) nonirradiated and (D) sunlight-irradiated fresh eyeball. EIC of CoQ10 in (E) nonirradiated and (F) sunlight-irradiated pure CoQ10. Full size image

Ultraviolet (UV) radiation mediated photoisomerization of CoQ10 rapidly

Next, we irradiated pure CoQ10 solution with laser (UV and visible light) followed by LC/MS analysis in order to identify the range of the light spectrum that induces photoisomerization. Compared to the TIC of the nonirradiated pure CoQ10, the laser-irradiated pure CoQ10 showed a number of additional peaks (Fig. S9). Similar to the data in Figs. 3, 4, and 5, a single peak at RT 45.1 min was observed in the EIC of the nonirradiated sample (Fig. 6A). As expected, an additional peak at RT 44.6 min (left to the original peak at RT 45.1 min) appeared in the EIC of laser-irradiated pure CoQ10 solution (irradiated for 1 min, 2 min, and 5 min with 266 nm laser light) (Fig. 6B). A similar phenomenon was observed when the solution was treated for 15 min with a laser beam at 355 nm (Fig. 6C). The higher the duration of irradiation and the shorter the wavelength of UV light, the greater the isomeric peak area (at RT 44.6 min). On the other hand, 60 min of irradiation with visible light (488 nm but not 532 nm) was capable of producing an isomeric peak of CoQ10 (Fig. 6D). Consistently, we observed a decrease in the absorbance spectra of CoQ10 with the increase in irradiation time by UV light (Fig. S10). It is also to be noted that the isomeric peak was the most abundant among the additional peaks in the TIC, which was consistent with the data of sunlight-irradiated pure CoQ10. These results suggested that UV radiation was the main culprit that mediates the photoisomerization of CoQ10 rapidly (within minutes). The lower the wavelength, the higher the rate of isomerization (Fig. 6B–E).

nature.com - Coenzyme Q10 in the eye isomerizes by sunlight irradiation - Nature

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