Araştırma Makalesi
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Effects of various conditions related to circadian rhythm disturbances on plasma and erythrocyte lipids in rats: a peroxisomal perspective

Yıl 2024, Cilt: 17 Sayı: 1, 87 - 98, 01.01.2024
https://doi.org/10.31362/patd.1327736

Öz

Purpose: Lipidomics studies of sleep restriction, which is known to be associated with circadian perturbations, revealed alterations in some plasma phospholipid levels including plasmalogens which are partly synthesized in liver peroxisomes. To this end it was aimed to investigate effects of various conditions known to cause circadian
rhythm disturbances on various peroxisomal parameters and to compare those effects with that of fenofibrate, a peroxisome proliferator-activated receptor alpha agonist.
Materials and methods: Plasmalogens and some fatty acids in erythrocyte lysates were analyzed by GC. Peroxisomal metabolites including very long chain fatty acids as well as phytanic and pristanic acids in plasma were measured by GC-MS. Immunohistological analyses by catalase antibodies were conducted on liver
sections.
Results: All the conditions tested exhibited increased catalase immunoreactivity in liver sections compared to that of controls. Both calorie restriction, time-restricted feeding, as well as fenofibrate treatment exhibited lower C18:0 plasmalogen contents of erythrocyte lysates. As plasmalogens are known to be synthesized by peroxisomes, the present results suggest that the peroxisomal lipid content in membranes might be affected by conditions co-occuring with circadian perturbations.
Conclusion: Shared effects of conditions associated with circadian rhythm disturbances and peroxisomal induction by fenofibrate on erythrocyte membrane lipids might indicate a link between them.

Destekleyen Kurum

İnonu University, Scientific Research Unit

Teşekkür

We thank, İnönü University, Scientific Research Unit

Kaynakça

  • 1. Weljie AM, Meerlo P, Goel N, et al. Oxalic acid and diacylglycerol 36:3 are cross-species markers of sleep debt. PNAS 2015;112:2569-2574. https://doi.org/10.1073/pnas.1417432112
  • 2. Froy O, Miskin R. The interrelations among feeding, circadian rhythms and ageing. Prog Neurobiol 2007;82:142-150. https://doi.org/10.1016/j.pneurobio.2007.03.002
  • 3. Zvonic S, Ptitsyn AA, Conrad SA, et al. Characterization of peripheral circadian clocks in adipose tissues. Diabetes 2006;55:962-970. https://doi.org/10.2337/diabetes.55.04.06.db05-0873
  • 4. Froy O. The relationship between nutrition and circadian rhythms in mammals. Front Neuroendocrin 2007;28:61-71. https://doi.org/10.1016/j.yfrne.2007.03.001
  • 5. Fonken LK, Nelson RJ. The effects of light at night on circadian clocks and metabolism. Endocr Rev 2014;35:648-670. https://doi.org/10.1210/er.2013-1051
  • 6. Wideman CH, Murphy HM. Constant light induces alterations in melatonin levels, food intake, feed efficiency, visceral adiposity, and circadian rhythms in rats. Nutr Neurosci 2009;12:233-240. https://doi.org/10.1179/147683009x423436
  • 7. Charoensuksai P, Xu W. PPARs in rhythmic metabolic regulation and ımplications in health and disease. Ppar Res 2010;2010;243643(e1-9). https://doi.org/10.1155/2010/243643
  • 8. Çolak C, Parlakpinar H. Hayvan Deneyleri: In Vivo Denemelerin Bildirimi: ARRIVE Kılavuzu-Derleme. İnönü Üniversitesi Tıp Fakültesi Dergisi 2012;19:128-131. https://doi.org/10.7247/jiumf.19.2.14
  • 9. Taslidere E, Dogan Z, Elbe H, Vardi N, Cetin A, Turkoz Y. Quercetin protection against ciprofloxacin induced liver damage in rats. Biotech Histochem 2016;91:116-121. https://doi.org/10.3109/10520295.2015.1085093
  • 10. Parlakpinar H, Ozhan O, Ermis N, et al. Acute and subacute effects of low versus high doses of standardized panax ginseng extract on the heart: an experimental study. Cardiovasc Toxicol 2019;19:306-320. https://doi.org/10.1007/s12012-019-09512-1
  • 11. Duran M, Wanders RJA. Plasmalogens and polyunsaturated fatty acids. In: Duran M, Wanders RJA eds. Laboratory guide to the methods in biochemical genetics. 1st ed. Berlin: Springer, 2008:207-220. Available at: https://link.springer.com/chapter/10.1007/978-3-540-76698-8_11. Accessed March 13, 2019
  • 12. Horta Remedios M, Liang W, Gonzalez LN, Li V, Da Ros VG, Cohen DJ, et al. Ether lipids and a peroxisomal riddle in sperm. Front Cell Dev Biol 2023;11:1166232. https://doi.org/10.3389/fcell.2023.1166232
  • 13. Astudillo AM, Balboa MA, Balsinde J. Compartmentalized regulation of lipid signaling in oxidative stress and inflammation: Plasmalogens, oxidized lipids and ferroptosis as new paradigms of bioactive lipid research. Prog Lipid Res 2023;89:101207. https://doi.org/10.1016/j.plipres.2022.101207
  • 14. Collet TH, Sonoyama T, Henning E, et al. A metabolomic signature of acute caloric restriction. J Clin Endocr Metab 2017;102:4486-4495. https://doi.org/10.1210/jc.2017-01020
  • 15. Morand OH, Zoeller RA, Raetz CRH. Disappearance of plasmalogens from membranes of animal-cells subjected to photosensitized oxidation. J Biol Chem 1988;263:11597-11606.
  • 16. Braverman NE, Moser AB. Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta 2012;1822:1442-1452. https://doi.org/10.1016/j.bbadis.2012.05.008
  • 17. Adam M, Gajdova S, Kolarova H, et al. Red blood cells serve as intravascular carriers of myeloperoxidase. J Mol Cell Cardiol 2014;74:353-363. https://doi.org/10.1016/j.yjmcc.2014.06.009
  • 18. van Veldhoven PP, Baes M. Peroxisome deficient invertebrate and vertebrate animal models. Front Physiol 2013;4:335(e1-19). https://doi.org/10.3389/fphys.2013.00335
  • 19. Kleiboeker B, Lodhi IJ. Peroxisomal regulation of energy homeostasis: effect on obesity and related metabolic disorders. Mol Metab 2022;65:101577. https://doi.org/10.1016/j.molmet.2022.101577
  • 20. Malhi H, Barreyro FJ, Isomoto H, Bronk SF, Gores GJ. Free fatty acids sensitise hepatocytes to TRAIL mediated cytotoxicity. Gut 2007;56:1124-1131. https://doi.org/10.1136/gut.2006.118059
  • 21. Malhi H, Bronk SF, Werneburg NW, Gores GJ. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 2006;281:12093-12101. https://doi.org/10.1074/jbc.M510660200
  • 22. Moravcova A, Cervinkova Z, Kucera O, Mezera V, Rychtrmoc D, Lotkova H. The effect of oleic and palmitic acid on ınduction of steatosis and cytotoxicity on rat hepatocytes in primary culture. Physiol Res 2015;64:627-636. https://doi.org/10.33549/physiolres.933224
  • 23. Burri L, Thoresen GH, Berge RK. The Role of PPAR alpha activation in liver and muscle. Ppar Res 2010;2010:542359. https://doi.org/10.1155/2010/542359
  • 24. Sanchez Aguilar M, Ibarra Lara L, Cano Martinez A, et al. PPAR alpha activation by clofibrate alleviates ıschemia/reperfusion ınjury in metabolic syndrome rats by decreasing cardiac ınflammation and remodeling and by regulating the atrial natriuretic peptide compensatory response. Int J Mol Sci 2023;24:5321. https://doi.org/10.3390/ijms24065321
  • 25. Di Cara F, Savary S, Kovacs WJ, Kim P, Rachubinski RA. The peroxisome: an up-and-coming organelle in immunometabolism. Trends Cell Biol 2023;33:70-86. https://doi.org/10.1016/j.tcb.2022.06.001
  • 26. Halliwell B, Gutteridge J. Oxygen: boon yet bane—introducing oxygen toxicity and reactive species. In: Halliwell B, Gutteridge J eds. Free radicals in biology and medicine. 5th ed. New York: Oxford University Press, 2015;29-35. Available at: https://books.google.com/books?id=HABlCgAAQBAJ&printsec=frontcover&hl=tr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false. Accessed November 20, 2019
  • 27. Pascual P, Pedrajas JR, Toribio F, Lopez Barea J, Peinado J. Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem-Biol Interact 2003;145:191-199. https://doi.org/10.1016/S0009-2797(03)00002-4
  • 28. Wohaieb SA, Godin DV. Starvation-related alterations in free-radical tissue defense-mechanisms in rats. Diabetes 1987;36:169-173. https://doi.org/10.2337/diab.36.2.169
  • 29. Bell D. Epigenetic puzzle. Zonal heterogeneity of peroxisomal enzymes in rat liver: differential induction by three divergent hypolipidemic drugs. Hum Exp Toxicol 1994;13:907-908.
  • 30. Pak HH, Haws SA, Green CL, et al. Fasting drives the metabolic, molecular and geroprotective effects of a calorie-restricted diet in mice. Nat Metab 2021;3:1327-1341. https://doi.org/10.1038/s42255-021-00466-9
  • 31. Manoogian ENC, Chow LS, Taub PR, Laferrere B, Panda S. Time-restricted Eating for the Prevention and Management of Metabolic Diseases. Endocr Rev 2022;43:405-436. https://doi.org/10.1210/endrev/bnab027
  • 32. Faulks SC, Turner N, Else PL, Hulbert AJ. Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J Gerontol A Biol Sci Med Sci 2006;61:781-794. https://doi.org/10.1093/gerona/61.8.781
  • 33. Jove M, Naudi A, Ramirez Nunez O, et al. Caloric restriction reveals a metabolomic and lipidomic signature in liver of male mice. Aging Cell 2014;13:828-837. https://doi.org/10.1111/acel.12241
  • 34. Strand E, Lysne V, Grinna ML, et al. Short-term activation of peroxisome proliferator-activated receptors and ınduces tissue-specific effects on lipid metabolism and fatty acid composition in male wistar rats. Ppar Res 2019;2019:8047627(e1-13). https://doi.org/10.1155/2019/8047627
  • 35. Du ZY, Clouet P, Degrace P, et al. Hypolipidaemic effects of fenofibrate and fasting in the herbivorous grass carp (Ctenopharyngodon idella) fed a high-fat diet. Brit J Nutr 2008;100:1200-1212. https://doi.org/10.1017/S0007114508986840
  • 36. Tallima H, El Ridi R. Arachidonic acid: Physiological roles and potential health benefits-A review. J Adv Res 2018;11:33-41. https://doi.org/10.1016/j.jare.2017.11.004

Sıçanlarda sirkadiyen ritim bozuklukları ile ilgili çeşitli koşulların plazma ve eritrosit lipidleri üzerindeki etkileri: peroksizomal bir bakış açısı

Yıl 2024, Cilt: 17 Sayı: 1, 87 - 98, 01.01.2024
https://doi.org/10.31362/patd.1327736

Öz

Amaç: Lipidomik çalışmalar; sirkadiyen ritim bozukluklarıyla ilişkili olduğu bilinen uyku kısıtlamasının karaciğer peroksizomlarında sentezlenen plazmalojenler dahil olmak üzere bazı plazma fosfolipid düzeylerinde değişikliklere neden olduğunu ortaya koymuştur. Bu nedenle bu çalışmada, sirkadiyen ritim bozukluklarına neden olduğu bilinen çeşitli koşulların bazı peroksizomal parametreler üzerindeki etkilerinin araştırılması ve bu etkilerin, bir peroksizom proliferatör reseptör agonisti olan fenofibrat ile karşılaştırılması amaçlandı.
Gereç ve yöntem: Eritrosit lizatlarındaki plazmalojenler ve bazı yağ asitleri GC ile analiz edildi. Plazmadaki çok uzun zincirli yağ asitlerinin yanı sıra fitanik ve pristanik asitleri içeren peroksizomal metabolitler GC-MS ile ölçüldü. Karaciğer kesitlerinde katalaz antikorları ile immünohistolojik analizler gerçekleştirildi.
Bulgular: Test edilen tüm koşullar, kontrollere kıyasla karaciğer kesitlerinde artmış katalaz immünoreaktivitesi gösterdi. Hem kalori kısıtlaması, hem de zaman kısıtlamalı beslenme, ayrıca fenofibrat tedavisi, eritrosit lizatlarında daha düşük C18:0 plazmalojen içeriğini sergiledi. Plazmalogenlerin peroksizomlar tarafından sentezlendiği bilindiğinden, mevcut sonuçlar, eritrosit membranındaki peroksizomal lipit içeriğinin, sirkadiyen ritim bozukluklarından etkilenebileceğini göstermektedir.
Sonuç: Sirkadiyen ritim bozuklukları ve fenofibratın peroksizomal indüksiyonunun eritrosit membran lipidleri üzerindeki ortak etkileri, bunlar arasında bir bağlantı olduğunu göstermektedir.

Kaynakça

  • 1. Weljie AM, Meerlo P, Goel N, et al. Oxalic acid and diacylglycerol 36:3 are cross-species markers of sleep debt. PNAS 2015;112:2569-2574. https://doi.org/10.1073/pnas.1417432112
  • 2. Froy O, Miskin R. The interrelations among feeding, circadian rhythms and ageing. Prog Neurobiol 2007;82:142-150. https://doi.org/10.1016/j.pneurobio.2007.03.002
  • 3. Zvonic S, Ptitsyn AA, Conrad SA, et al. Characterization of peripheral circadian clocks in adipose tissues. Diabetes 2006;55:962-970. https://doi.org/10.2337/diabetes.55.04.06.db05-0873
  • 4. Froy O. The relationship between nutrition and circadian rhythms in mammals. Front Neuroendocrin 2007;28:61-71. https://doi.org/10.1016/j.yfrne.2007.03.001
  • 5. Fonken LK, Nelson RJ. The effects of light at night on circadian clocks and metabolism. Endocr Rev 2014;35:648-670. https://doi.org/10.1210/er.2013-1051
  • 6. Wideman CH, Murphy HM. Constant light induces alterations in melatonin levels, food intake, feed efficiency, visceral adiposity, and circadian rhythms in rats. Nutr Neurosci 2009;12:233-240. https://doi.org/10.1179/147683009x423436
  • 7. Charoensuksai P, Xu W. PPARs in rhythmic metabolic regulation and ımplications in health and disease. Ppar Res 2010;2010;243643(e1-9). https://doi.org/10.1155/2010/243643
  • 8. Çolak C, Parlakpinar H. Hayvan Deneyleri: In Vivo Denemelerin Bildirimi: ARRIVE Kılavuzu-Derleme. İnönü Üniversitesi Tıp Fakültesi Dergisi 2012;19:128-131. https://doi.org/10.7247/jiumf.19.2.14
  • 9. Taslidere E, Dogan Z, Elbe H, Vardi N, Cetin A, Turkoz Y. Quercetin protection against ciprofloxacin induced liver damage in rats. Biotech Histochem 2016;91:116-121. https://doi.org/10.3109/10520295.2015.1085093
  • 10. Parlakpinar H, Ozhan O, Ermis N, et al. Acute and subacute effects of low versus high doses of standardized panax ginseng extract on the heart: an experimental study. Cardiovasc Toxicol 2019;19:306-320. https://doi.org/10.1007/s12012-019-09512-1
  • 11. Duran M, Wanders RJA. Plasmalogens and polyunsaturated fatty acids. In: Duran M, Wanders RJA eds. Laboratory guide to the methods in biochemical genetics. 1st ed. Berlin: Springer, 2008:207-220. Available at: https://link.springer.com/chapter/10.1007/978-3-540-76698-8_11. Accessed March 13, 2019
  • 12. Horta Remedios M, Liang W, Gonzalez LN, Li V, Da Ros VG, Cohen DJ, et al. Ether lipids and a peroxisomal riddle in sperm. Front Cell Dev Biol 2023;11:1166232. https://doi.org/10.3389/fcell.2023.1166232
  • 13. Astudillo AM, Balboa MA, Balsinde J. Compartmentalized regulation of lipid signaling in oxidative stress and inflammation: Plasmalogens, oxidized lipids and ferroptosis as new paradigms of bioactive lipid research. Prog Lipid Res 2023;89:101207. https://doi.org/10.1016/j.plipres.2022.101207
  • 14. Collet TH, Sonoyama T, Henning E, et al. A metabolomic signature of acute caloric restriction. J Clin Endocr Metab 2017;102:4486-4495. https://doi.org/10.1210/jc.2017-01020
  • 15. Morand OH, Zoeller RA, Raetz CRH. Disappearance of plasmalogens from membranes of animal-cells subjected to photosensitized oxidation. J Biol Chem 1988;263:11597-11606.
  • 16. Braverman NE, Moser AB. Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta 2012;1822:1442-1452. https://doi.org/10.1016/j.bbadis.2012.05.008
  • 17. Adam M, Gajdova S, Kolarova H, et al. Red blood cells serve as intravascular carriers of myeloperoxidase. J Mol Cell Cardiol 2014;74:353-363. https://doi.org/10.1016/j.yjmcc.2014.06.009
  • 18. van Veldhoven PP, Baes M. Peroxisome deficient invertebrate and vertebrate animal models. Front Physiol 2013;4:335(e1-19). https://doi.org/10.3389/fphys.2013.00335
  • 19. Kleiboeker B, Lodhi IJ. Peroxisomal regulation of energy homeostasis: effect on obesity and related metabolic disorders. Mol Metab 2022;65:101577. https://doi.org/10.1016/j.molmet.2022.101577
  • 20. Malhi H, Barreyro FJ, Isomoto H, Bronk SF, Gores GJ. Free fatty acids sensitise hepatocytes to TRAIL mediated cytotoxicity. Gut 2007;56:1124-1131. https://doi.org/10.1136/gut.2006.118059
  • 21. Malhi H, Bronk SF, Werneburg NW, Gores GJ. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 2006;281:12093-12101. https://doi.org/10.1074/jbc.M510660200
  • 22. Moravcova A, Cervinkova Z, Kucera O, Mezera V, Rychtrmoc D, Lotkova H. The effect of oleic and palmitic acid on ınduction of steatosis and cytotoxicity on rat hepatocytes in primary culture. Physiol Res 2015;64:627-636. https://doi.org/10.33549/physiolres.933224
  • 23. Burri L, Thoresen GH, Berge RK. The Role of PPAR alpha activation in liver and muscle. Ppar Res 2010;2010:542359. https://doi.org/10.1155/2010/542359
  • 24. Sanchez Aguilar M, Ibarra Lara L, Cano Martinez A, et al. PPAR alpha activation by clofibrate alleviates ıschemia/reperfusion ınjury in metabolic syndrome rats by decreasing cardiac ınflammation and remodeling and by regulating the atrial natriuretic peptide compensatory response. Int J Mol Sci 2023;24:5321. https://doi.org/10.3390/ijms24065321
  • 25. Di Cara F, Savary S, Kovacs WJ, Kim P, Rachubinski RA. The peroxisome: an up-and-coming organelle in immunometabolism. Trends Cell Biol 2023;33:70-86. https://doi.org/10.1016/j.tcb.2022.06.001
  • 26. Halliwell B, Gutteridge J. Oxygen: boon yet bane—introducing oxygen toxicity and reactive species. In: Halliwell B, Gutteridge J eds. Free radicals in biology and medicine. 5th ed. New York: Oxford University Press, 2015;29-35. Available at: https://books.google.com/books?id=HABlCgAAQBAJ&printsec=frontcover&hl=tr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false. Accessed November 20, 2019
  • 27. Pascual P, Pedrajas JR, Toribio F, Lopez Barea J, Peinado J. Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem-Biol Interact 2003;145:191-199. https://doi.org/10.1016/S0009-2797(03)00002-4
  • 28. Wohaieb SA, Godin DV. Starvation-related alterations in free-radical tissue defense-mechanisms in rats. Diabetes 1987;36:169-173. https://doi.org/10.2337/diab.36.2.169
  • 29. Bell D. Epigenetic puzzle. Zonal heterogeneity of peroxisomal enzymes in rat liver: differential induction by three divergent hypolipidemic drugs. Hum Exp Toxicol 1994;13:907-908.
  • 30. Pak HH, Haws SA, Green CL, et al. Fasting drives the metabolic, molecular and geroprotective effects of a calorie-restricted diet in mice. Nat Metab 2021;3:1327-1341. https://doi.org/10.1038/s42255-021-00466-9
  • 31. Manoogian ENC, Chow LS, Taub PR, Laferrere B, Panda S. Time-restricted Eating for the Prevention and Management of Metabolic Diseases. Endocr Rev 2022;43:405-436. https://doi.org/10.1210/endrev/bnab027
  • 32. Faulks SC, Turner N, Else PL, Hulbert AJ. Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J Gerontol A Biol Sci Med Sci 2006;61:781-794. https://doi.org/10.1093/gerona/61.8.781
  • 33. Jove M, Naudi A, Ramirez Nunez O, et al. Caloric restriction reveals a metabolomic and lipidomic signature in liver of male mice. Aging Cell 2014;13:828-837. https://doi.org/10.1111/acel.12241
  • 34. Strand E, Lysne V, Grinna ML, et al. Short-term activation of peroxisome proliferator-activated receptors and ınduces tissue-specific effects on lipid metabolism and fatty acid composition in male wistar rats. Ppar Res 2019;2019:8047627(e1-13). https://doi.org/10.1155/2019/8047627
  • 35. Du ZY, Clouet P, Degrace P, et al. Hypolipidaemic effects of fenofibrate and fasting in the herbivorous grass carp (Ctenopharyngodon idella) fed a high-fat diet. Brit J Nutr 2008;100:1200-1212. https://doi.org/10.1017/S0007114508986840
  • 36. Tallima H, El Ridi R. Arachidonic acid: Physiological roles and potential health benefits-A review. J Adv Res 2018;11:33-41. https://doi.org/10.1016/j.jare.2017.11.004

Ayrıntılar

Birincil Dil İngilizce
Konular Biyokimya ve Hücre Biyolojisi (Diğer)
Bölüm Araştırma Makalesi
Yazarlar

Hüsniye Gül OTLU 0000-0001-5815-000X

Yılmaz UĞUR 0000-0002-9040-4249

Azibe YILDIZ 0000-0001-5686-7867

Selim ERDOĞAN 0000-0002-9169-9771

Saim YOLOĞLU 0000-0002-9619-3462

Nigar VARDI 0000-0003-0576-1696

Tayfun GÜLDÜR 0000-0002-1623-2880

Proje Numarası Contract TDK-2017-601
Erken Görünüm Tarihi 28 Kasım 2023
Yayımlanma Tarihi 1 Ocak 2024
Gönderilme Tarihi 26 Temmuz 2023
Kabul Tarihi 28 Kasım 2023
Yayımlandığı Sayı Yıl 2024 Cilt: 17 Sayı: 1

Kaynak Göster

APA OTLU, H. G., UĞUR, Y., YILDIZ, A., ERDOĞAN, S., vd. (2024). Effects of various conditions related to circadian rhythm disturbances on plasma and erythrocyte lipids in rats: a peroxisomal perspective. Pamukkale Medical Journal, 17(1), 87-98. https://doi.org/10.31362/patd.1327736
AMA OTLU HG, UĞUR Y, YILDIZ A, ERDOĞAN S, YOLOĞLU S, VARDI N, GÜLDÜR T. Effects of various conditions related to circadian rhythm disturbances on plasma and erythrocyte lipids in rats: a peroxisomal perspective. Pam Tıp Derg. Ocak 2024;17(1):87-98. doi:10.31362/patd.1327736
Chicago OTLU, Hüsniye Gül, Yılmaz UĞUR, Azibe YILDIZ, Selim ERDOĞAN, Saim YOLOĞLU, Nigar VARDI, ve Tayfun GÜLDÜR. “Effects of Various Conditions Related to Circadian Rhythm Disturbances on Plasma and Erythrocyte Lipids in Rats: A Peroxisomal Perspective”. Pamukkale Medical Journal 17, sy. 1 (Ocak 2024): 87-98. https://doi.org/10.31362/patd.1327736.
EndNote OTLU HG, UĞUR Y, YILDIZ A, ERDOĞAN S, YOLOĞLU S, VARDI N, GÜLDÜR T (01 Ocak 2024) Effects of various conditions related to circadian rhythm disturbances on plasma and erythrocyte lipids in rats: a peroxisomal perspective. Pamukkale Medical Journal 17 1 87–98.
IEEE H. G. OTLU, “Effects of various conditions related to circadian rhythm disturbances on plasma and erythrocyte lipids in rats: a peroxisomal perspective”, Pam Tıp Derg, c. 17, sy. 1, ss. 87–98, 2024, doi: 10.31362/patd.1327736.
ISNAD OTLU, Hüsniye Gül vd. “Effects of Various Conditions Related to Circadian Rhythm Disturbances on Plasma and Erythrocyte Lipids in Rats: A Peroxisomal Perspective”. Pamukkale Medical Journal 17/1 (Ocak 2024), 87-98. https://doi.org/10.31362/patd.1327736.
JAMA OTLU HG, UĞUR Y, YILDIZ A, ERDOĞAN S, YOLOĞLU S, VARDI N, GÜLDÜR T. Effects of various conditions related to circadian rhythm disturbances on plasma and erythrocyte lipids in rats: a peroxisomal perspective. Pam Tıp Derg. 2024;17:87–98.
MLA OTLU, Hüsniye Gül vd. “Effects of Various Conditions Related to Circadian Rhythm Disturbances on Plasma and Erythrocyte Lipids in Rats: A Peroxisomal Perspective”. Pamukkale Medical Journal, c. 17, sy. 1, 2024, ss. 87-98, doi:10.31362/patd.1327736.
Vancouver OTLU HG, UĞUR Y, YILDIZ A, ERDOĞAN S, YOLOĞLU S, VARDI N, GÜLDÜR T. Effects of various conditions related to circadian rhythm disturbances on plasma and erythrocyte lipids in rats: a peroxisomal perspective. Pam Tıp Derg. 2024;17(1):87-98.
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