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Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi

Year 2023, , 93 - 101, 31.08.2023
https://doi.org/10.25048/tudod.1342082

Abstract

Amaç: Uyku, kas metabolizması için önemli faktörlerden biridir. Uyku yoksunluğunun (UY) kas rejenerasyonunu bozduğu gösterilmiştir.
Myostatin iskelet kası hücreleri tarafından eksprese edilir ve kas büyümesini sınırlandırır. Çalışmamızın amacı, sıçanlarda akut uyku
yoksunluğunun iskelet kası myostatin düzeyleri üzerindeki etkilerini değerlendirmektir.
Gereç ve Yöntemler: Yirmi bir erkek Wistar albino sıçan (200-250g) rastgele üç gruba (n=7) ayrılmıştır: Kontrol grubu, Geniş platform
(GP) grubu ve UY grubu. REM UY, 72 saat boyunca modifiye çoklu platform yöntemi kullanılarak indüklenmiştir. Lökomotor aktivite
gruplar arasında açık alan testi (OFT) kullanılarak değerlendirilmiştir. Gastroknemius ve soleus kas dokuları alınmış ve kas dokularında
myostatin, malondialdehit (MDA), glutatyon (GSH) ve glikojen seviyeleri ölçülmüştür.
Bulgular: Bu çalışma, akut UY’nin kontrol grubuna kıyasla soleus kasında myostatin (1161±39,55) ve MDA (115,37±8,47) seviyelerinde
artışa neden olduğunu göstermiştir (sırasıyla p=0,036 ve p=0,01). OFT’de geçilen kare sayısı diğer gruplarla karşılaştırıldığında artmıştır
(56,33±22,02) (p=0,001 ve p=0,044). Gastroknemius kasında GSH (4,86±0,26) ve glikojen seviyeleri (5,13±0,21) UY grubunda azalmıştır
(sırasıyla p=0,007 ve p=0,028).
Sonuç: Bu veriler, REM uyku yoksunluğunun iskelet kasındaki myostatin seviyelerini ve oksidatif stres parametrelerini farklı kas tiplerinde
farklı miktarlarda değiştirerek kas metabolizmasını etkilediğini gösterebilir.

Project Number

1919B012112894

References

  • 1. Parmar S, Tadavarty R, Sastry BR. G-protein coupled receptors and synaptic plasticity in sleep deprivation. World J Psychiatry. 2021 Nov 19;11(11):954-980.
  • 2. Medic G, Wille M, Hemels ME. Short- and long-term health consequences of sleep disruption. Nat Sci Sleep. 2017 May 19;9:151-161.
  • 3. Turan I, Sayan Ozacmak H, Ozacmak VH, Ergenc M, Bayraktaroğlu T. The effects of glucagon-like peptide 1 receptor agonist (exenatide) on memory impairment, and anxiety- and depression-like behavior induced by REM sleep deprivation. Brain Res Bull. 2021 Sep;174:194-202.
  • 4. Wang T, Niu K, Fan A, Bi N, Tao H, Chen XT, Wang HL. Dietary intake of polyunsaturated fatty acids alleviates cognition deficits and depression-like behaviour via cannabinoid system in sleep deprivation rats. Behav Brain Res. 2020;384:112545.
  • 5. Killgore WD. Effects of sleep deprivation on cognition. Prog Brain Res. 2010;185:105-129.
  • 6. Kordestani-Moghadam P, Nasehi M, Khodagholi F, Vaseghi S, Zarrindast MR, Khani M. The fluctuations of metabotropic glutamate receptor subtype 5 (mGluR5) in the amygdala in fear conditioning model of male Wistar rats following sleep deprivation, reverse circadian and napping. Brain Res. 2020;1734:146739.
  • 7. Lamon S, Morabito A, Arentson-Lantz E, Knowles O, Vincent GE, Condo D, Alexander SE, Garnham A, Paddon-Jones D, Aisbett B. The effect of acute sleep deprivation on skeletal muscle protein synthesis and the hormonal environment. Physiol Rep. 2021;9(1):e14660.
  • 8. Meerlo P, Sgoifo A, Suchecki D. Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Med Rev. 2008;12(3):197–210.
  • 9. St-Onge MP, O’Keeffe M, Roberts AL, RoyChoudhury A, Laferrère B. Short sleep duration, glucose dysregulation and hormonal regulation of appetite in men and women. Sleep. 2012;35(11):1503-1510.
  • 10. Dattilo M, Antunes HK, Medeiros A, Mônico-Neto M, Souza Hde S, Lee KS, Tufik S, de Mello MT. Paradoxical sleep deprivation induces muscle atrophy. Muscle Nerve. 2012;45(3):431-433.
  • 11. Mônico-Neto M, Dáttilo M, Ribeiro DA, Lee KS, de Mello MT, Tufik S, Antunes HKM. REM sleep deprivation impairs muscle regeneration in rats. Growth Factors. 2017;35(1):12- 18.
  • 12. Pasquale Esposito, Daniela Picciotto, Yuri Battaglia, Francesca Costigliolo, Francesca Viazzi, Daniela Verzola, Chapter Five - Myostatin: Basic biology to clinical application, Editor(s): Gregory S. Makowski, Advances in Clinical Chemistry, Elsevier, Vol. 106, 2022;181-234.
  • 13. Carlson CJ, Booth FW, Gordon SE: Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading. Am J Physiol 1999;277:R601-R606.
  • 14. Hittel DS, Berggren JR, Shearer J, Boyle K, Houmard JA. Increased secretion and expression of myostatin in skeletal muscle from extremely obese women. Diabetes. 2009;58(1):30- 38.
  • 15. Machado RB, Hipólide DC, Benedito-Silva AA, Tufik S. Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery. Brain Res. 2004;1004(1-2):45-51.
  • 16. Rajizadeh MA, Esmaeilpour K, Haghparast E, Ebrahimi MN, Sheibani V. Voluntary exercise modulates learning & memory and synaptic plasticity impairments in sleep deprived female rats. Brain Res. 2020;1729:146598.
  • 17. Lo S, Russell JC, Taylor AW. Determination of glycogen in small tissue samples. J Appl Physiol. 1970;28(2):234-236.
  • 18. Casini AF, Ferrali M, Pompella A, Maellaro E, Comporti M. Lipid peroxidation and cellular damage in extrahepatic tissues of bromobenzene-intoxicated mice. Am J Pathol. 1986;123(3):520-531.
  • 19. Aykaç G, Uysal M, Yalçin AS, Koçak-Toker N, Sivas A, Oz H. The effect of chronic ethanol ingestion on hepatic lipid peroxide, glutathione, glutathione peroxidase and glutathione transferase in rats. Toxicology. 1985;36(1):71-76.
  • 20. Morrison M, Halson SL, Weakley J, Hawley JA. Sleep, circadian biology and skeletal muscle interactions: Implications for metabolic health. Sleep Med Rev. 2022;66:101700.
  • 21. Mônico-Neto M, Antunes HK, Dattilo M, Medeiros A, Souza HS, Lee KS, de Melo CM, Tufik S, de Mello MT. Resistance exercise: a non-pharmacological strategy to minimize or reverse sleep deprivation-induced muscle atrophy. Med Hypotheses. 2013;80(6):701-705.
  • 22. de Sá Souza H, Antunes HKM, Dáttilo M, Lee KS, Mônico-Neto M, de Campos Giampa SQ, Phillips SM, Tufik S, de Mello MT. Leucine supplementation is anti-atrophic during paradoxical sleep deprivation in rats. Amino Acids. 2016;48(4):949-957.
  • 23. Lloyd EM, Pinniger GJ, Murphy RM, Grounds MD. Slow or fast: Implications of myofibre type and associated differences for manifestation of neuromuscular disorders. Acta Physiol (Oxf). 2023;238(4):e14012.
  • 24. Armstrong RB, Phelps RO. Muscle fiber type composition of the rat hindlimb. Am J Anat. 1984;171(3):259-272.
  • 25. Sugama S, Tachino K, Haida N. Effect of immobilization on solubility of soleus and gastrocnemius muscle collagen: -biochemical studies on collagen from soleus and gastrocnemius muscles of rat. J Jpn Phys Ther Assoc. 1999;2(1):25-29.
  • 26. Gelfi C, Viganò A, De Palma S, Ripamonti M, Begum S, Cerretelli P, Wait R. 2-D protein maps of rat gastrocnemius and soleus muscles: a tool for muscle plasticity assessment. Proteomics. 2006;6(1):321-340.
  • 27. Umek N, Horvat S, Cvetko E. Skeletal muscle and fiber typespecific intramyocellular lipid accumulation in obese mice. Bosn J Basic Med Sci. 2021;21(6):730-738.
  • 28. Jackson MJ. Reactive oxygen species and redox-regulation of skeletal muscle adaptations to exercise. Philos Trans R Soc Lond B Biol Sci. 2005;360(1464):2285-2291.
  • 29. Mishra P, Varuzhanyan G, Pham AH, Chan DC. Mitochondrial Dynamics is a distinguishing feature of skeletal muscle fiber types and regulates organellar compartmentalization. Cell Metab. 2015;22(6):1033-1044.
  • 30. Mônico-Neto M, Lee KS, da Luz MHM, Pino JMV, Ribeiro DA, Cardoso CM, Sueur-Maluf LL, Tufik S, Antunes HKM. Histopathological changes and oxidative damage in type I and type II muscle fibers in rats undergoing paradoxical sleep deprivation. Cell Signal. 2021;81:109939.
  • 31. Liu X, Zhang N, Sun B, Wang B. Time-specific effects of acute eccentric exercise on myostatin, follistatin and decorin in the circulation and skeletal muscle in rats. Physiol Res. 2022;71(6):783-790.
  • 32. Gonzalez-Cadavid NF, Taylor WE, Yarasheski K, Sinha-Hikim I, Ma K, Ezzat S, Shen R, Lalani R, Asa S, Mamita M, Nair G, Arver S, Bhasin S. Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting. Proc Natl Acad Sci U S A. 1998;95(25):14938- 14943.
  • 33. Ju CR, Chen RC. Serum myostatin levels and skeletal muscle wasting in chronic obstructive pulmonary disease. Respir Med. 2012;106(1):102-108.
  • 34. García PS, Cabbabe A, Kambadur R, Nicholas G, Csete M. Brief-reports: elevated myostatin levels in patients with liver disease: a potential contributor to skeletal muscle wasting. Anesth Analg. 2010;111(3):707-709.
  • 35. Wehling M, Cai B, Tidball JG. Modulation of myostatin expression during modified muscle use. FASEB J. 2000;14(1):103-110.
  • 36. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol. 2003;162(6):1135-1147.
  • 37. Kambadur R, Sharma M, Smith TP, Bass JJ. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res. 1997;7(9):910-916.
  • 38. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997;387(6628):83-90.
  • 39. Williams MS. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med. 2004;351(10):1030-1031; author reply 1030-1031.
  • 40. Hadeiy SK, Habtemariam S, Shankayi Z, Shahyad S, Sahraei H, Asghardoust Rezaei M, Bahrami F. Amelioration of pain and anxiety in sleep-deprived rats by intra-amygdala injection of cinnamaldehyde. Sleep Med X. 2023;5:100069.

The Effects of REM Sleep Deprivation on Skeletal Muscle Myostatin Levels in Rats

Year 2023, , 93 - 101, 31.08.2023
https://doi.org/10.25048/tudod.1342082

Abstract

Aim: Sleep is one of the crucial factors for muscle metabolism. It has been shown that sleep deprivation (SD) impairs muscle regeneration.
Myostatin is expressed by skeletal muscle cells and limits muscle growth. The purpose of our study was to evaluate the effects of acute
sleep deprivation on skeletal muscle myostatin levels in rats.
Material and Methods: Twenty one male Wistar albino rats (200-250g) were randomly allocated in to three groups (n=7): Control
group, Wide platform (WP) group and SD group. REM SD was induced by using the modified multiple platform method for 72
hours. The locomotor activity were evaluated among groups using open field test (OFT). Gastrocnemius and soleus muscle tissue were
harvested and the levels of myostatin, malondialdehyde (MDA), glutathione (GSH) and glycogen was measured in the muscle tissues.
Results: This study showed that acute SD caused an increase in myostatin (1161±39.55) and MDA levels (115.37±8.47) in the soleus
muscle compared to the control group (respectively p=0.036 ve p=0.01). Compared with the other groups, the number of crossing square
was increased in OFT (56.33±22.02) (p=0.001 ve p=0.044). GSH (4.86±0.26) and glycogen levels (5.13±0.21) in gastrocnemius muscle
was decresead in SD group (respectively p=0.007 ve p=0.028).
Conclusion: These data may represent that REM sleep deprivation affects muscle metabolism by changing myostatin levels and oxidative
stress parameters in skeletal muscle to different extents in different muscle types.

Supporting Institution

TÜBİTAK 2209-A

Project Number

1919B012112894

References

  • 1. Parmar S, Tadavarty R, Sastry BR. G-protein coupled receptors and synaptic plasticity in sleep deprivation. World J Psychiatry. 2021 Nov 19;11(11):954-980.
  • 2. Medic G, Wille M, Hemels ME. Short- and long-term health consequences of sleep disruption. Nat Sci Sleep. 2017 May 19;9:151-161.
  • 3. Turan I, Sayan Ozacmak H, Ozacmak VH, Ergenc M, Bayraktaroğlu T. The effects of glucagon-like peptide 1 receptor agonist (exenatide) on memory impairment, and anxiety- and depression-like behavior induced by REM sleep deprivation. Brain Res Bull. 2021 Sep;174:194-202.
  • 4. Wang T, Niu K, Fan A, Bi N, Tao H, Chen XT, Wang HL. Dietary intake of polyunsaturated fatty acids alleviates cognition deficits and depression-like behaviour via cannabinoid system in sleep deprivation rats. Behav Brain Res. 2020;384:112545.
  • 5. Killgore WD. Effects of sleep deprivation on cognition. Prog Brain Res. 2010;185:105-129.
  • 6. Kordestani-Moghadam P, Nasehi M, Khodagholi F, Vaseghi S, Zarrindast MR, Khani M. The fluctuations of metabotropic glutamate receptor subtype 5 (mGluR5) in the amygdala in fear conditioning model of male Wistar rats following sleep deprivation, reverse circadian and napping. Brain Res. 2020;1734:146739.
  • 7. Lamon S, Morabito A, Arentson-Lantz E, Knowles O, Vincent GE, Condo D, Alexander SE, Garnham A, Paddon-Jones D, Aisbett B. The effect of acute sleep deprivation on skeletal muscle protein synthesis and the hormonal environment. Physiol Rep. 2021;9(1):e14660.
  • 8. Meerlo P, Sgoifo A, Suchecki D. Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Med Rev. 2008;12(3):197–210.
  • 9. St-Onge MP, O’Keeffe M, Roberts AL, RoyChoudhury A, Laferrère B. Short sleep duration, glucose dysregulation and hormonal regulation of appetite in men and women. Sleep. 2012;35(11):1503-1510.
  • 10. Dattilo M, Antunes HK, Medeiros A, Mônico-Neto M, Souza Hde S, Lee KS, Tufik S, de Mello MT. Paradoxical sleep deprivation induces muscle atrophy. Muscle Nerve. 2012;45(3):431-433.
  • 11. Mônico-Neto M, Dáttilo M, Ribeiro DA, Lee KS, de Mello MT, Tufik S, Antunes HKM. REM sleep deprivation impairs muscle regeneration in rats. Growth Factors. 2017;35(1):12- 18.
  • 12. Pasquale Esposito, Daniela Picciotto, Yuri Battaglia, Francesca Costigliolo, Francesca Viazzi, Daniela Verzola, Chapter Five - Myostatin: Basic biology to clinical application, Editor(s): Gregory S. Makowski, Advances in Clinical Chemistry, Elsevier, Vol. 106, 2022;181-234.
  • 13. Carlson CJ, Booth FW, Gordon SE: Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading. Am J Physiol 1999;277:R601-R606.
  • 14. Hittel DS, Berggren JR, Shearer J, Boyle K, Houmard JA. Increased secretion and expression of myostatin in skeletal muscle from extremely obese women. Diabetes. 2009;58(1):30- 38.
  • 15. Machado RB, Hipólide DC, Benedito-Silva AA, Tufik S. Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery. Brain Res. 2004;1004(1-2):45-51.
  • 16. Rajizadeh MA, Esmaeilpour K, Haghparast E, Ebrahimi MN, Sheibani V. Voluntary exercise modulates learning & memory and synaptic plasticity impairments in sleep deprived female rats. Brain Res. 2020;1729:146598.
  • 17. Lo S, Russell JC, Taylor AW. Determination of glycogen in small tissue samples. J Appl Physiol. 1970;28(2):234-236.
  • 18. Casini AF, Ferrali M, Pompella A, Maellaro E, Comporti M. Lipid peroxidation and cellular damage in extrahepatic tissues of bromobenzene-intoxicated mice. Am J Pathol. 1986;123(3):520-531.
  • 19. Aykaç G, Uysal M, Yalçin AS, Koçak-Toker N, Sivas A, Oz H. The effect of chronic ethanol ingestion on hepatic lipid peroxide, glutathione, glutathione peroxidase and glutathione transferase in rats. Toxicology. 1985;36(1):71-76.
  • 20. Morrison M, Halson SL, Weakley J, Hawley JA. Sleep, circadian biology and skeletal muscle interactions: Implications for metabolic health. Sleep Med Rev. 2022;66:101700.
  • 21. Mônico-Neto M, Antunes HK, Dattilo M, Medeiros A, Souza HS, Lee KS, de Melo CM, Tufik S, de Mello MT. Resistance exercise: a non-pharmacological strategy to minimize or reverse sleep deprivation-induced muscle atrophy. Med Hypotheses. 2013;80(6):701-705.
  • 22. de Sá Souza H, Antunes HKM, Dáttilo M, Lee KS, Mônico-Neto M, de Campos Giampa SQ, Phillips SM, Tufik S, de Mello MT. Leucine supplementation is anti-atrophic during paradoxical sleep deprivation in rats. Amino Acids. 2016;48(4):949-957.
  • 23. Lloyd EM, Pinniger GJ, Murphy RM, Grounds MD. Slow or fast: Implications of myofibre type and associated differences for manifestation of neuromuscular disorders. Acta Physiol (Oxf). 2023;238(4):e14012.
  • 24. Armstrong RB, Phelps RO. Muscle fiber type composition of the rat hindlimb. Am J Anat. 1984;171(3):259-272.
  • 25. Sugama S, Tachino K, Haida N. Effect of immobilization on solubility of soleus and gastrocnemius muscle collagen: -biochemical studies on collagen from soleus and gastrocnemius muscles of rat. J Jpn Phys Ther Assoc. 1999;2(1):25-29.
  • 26. Gelfi C, Viganò A, De Palma S, Ripamonti M, Begum S, Cerretelli P, Wait R. 2-D protein maps of rat gastrocnemius and soleus muscles: a tool for muscle plasticity assessment. Proteomics. 2006;6(1):321-340.
  • 27. Umek N, Horvat S, Cvetko E. Skeletal muscle and fiber typespecific intramyocellular lipid accumulation in obese mice. Bosn J Basic Med Sci. 2021;21(6):730-738.
  • 28. Jackson MJ. Reactive oxygen species and redox-regulation of skeletal muscle adaptations to exercise. Philos Trans R Soc Lond B Biol Sci. 2005;360(1464):2285-2291.
  • 29. Mishra P, Varuzhanyan G, Pham AH, Chan DC. Mitochondrial Dynamics is a distinguishing feature of skeletal muscle fiber types and regulates organellar compartmentalization. Cell Metab. 2015;22(6):1033-1044.
  • 30. Mônico-Neto M, Lee KS, da Luz MHM, Pino JMV, Ribeiro DA, Cardoso CM, Sueur-Maluf LL, Tufik S, Antunes HKM. Histopathological changes and oxidative damage in type I and type II muscle fibers in rats undergoing paradoxical sleep deprivation. Cell Signal. 2021;81:109939.
  • 31. Liu X, Zhang N, Sun B, Wang B. Time-specific effects of acute eccentric exercise on myostatin, follistatin and decorin in the circulation and skeletal muscle in rats. Physiol Res. 2022;71(6):783-790.
  • 32. Gonzalez-Cadavid NF, Taylor WE, Yarasheski K, Sinha-Hikim I, Ma K, Ezzat S, Shen R, Lalani R, Asa S, Mamita M, Nair G, Arver S, Bhasin S. Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting. Proc Natl Acad Sci U S A. 1998;95(25):14938- 14943.
  • 33. Ju CR, Chen RC. Serum myostatin levels and skeletal muscle wasting in chronic obstructive pulmonary disease. Respir Med. 2012;106(1):102-108.
  • 34. García PS, Cabbabe A, Kambadur R, Nicholas G, Csete M. Brief-reports: elevated myostatin levels in patients with liver disease: a potential contributor to skeletal muscle wasting. Anesth Analg. 2010;111(3):707-709.
  • 35. Wehling M, Cai B, Tidball JG. Modulation of myostatin expression during modified muscle use. FASEB J. 2000;14(1):103-110.
  • 36. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol. 2003;162(6):1135-1147.
  • 37. Kambadur R, Sharma M, Smith TP, Bass JJ. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res. 1997;7(9):910-916.
  • 38. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997;387(6628):83-90.
  • 39. Williams MS. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med. 2004;351(10):1030-1031; author reply 1030-1031.
  • 40. Hadeiy SK, Habtemariam S, Shankayi Z, Shahyad S, Sahraei H, Asghardoust Rezaei M, Bahrami F. Amelioration of pain and anxiety in sleep-deprived rats by intra-amygdala injection of cinnamaldehyde. Sleep Med X. 2023;5:100069.
There are 40 citations in total.

Details

Primary Language Turkish
Subjects Medical Physiology (Other)
Journal Section Research Article
Authors

İsmetcan İleri 0009-0002-4712-6017

İnci Turan 0000-0003-2211-3914

Project Number 1919B012112894
Publication Date August 31, 2023
Acceptance Date August 23, 2023
Published in Issue Year 2023

Cite

APA İleri, İ., & Turan, İ. (2023). Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi. Turkish Journal of Diabetes and Obesity, 7(2), 93-101. https://doi.org/10.25048/tudod.1342082
AMA İleri İ, Turan İ. Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi. Turk J Diab Obes. August 2023;7(2):93-101. doi:10.25048/tudod.1342082
Chicago İleri, İsmetcan, and İnci Turan. “Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi”. Turkish Journal of Diabetes and Obesity 7, no. 2 (August 2023): 93-101. https://doi.org/10.25048/tudod.1342082.
EndNote İleri İ, Turan İ (August 1, 2023) Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi. Turkish Journal of Diabetes and Obesity 7 2 93–101.
IEEE İ. İleri and İ. Turan, “Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi”, Turk J Diab Obes, vol. 7, no. 2, pp. 93–101, 2023, doi: 10.25048/tudod.1342082.
ISNAD İleri, İsmetcan - Turan, İnci. “Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi”. Turkish Journal of Diabetes and Obesity 7/2 (August 2023), 93-101. https://doi.org/10.25048/tudod.1342082.
JAMA İleri İ, Turan İ. Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi. Turk J Diab Obes. 2023;7:93–101.
MLA İleri, İsmetcan and İnci Turan. “Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi”. Turkish Journal of Diabetes and Obesity, vol. 7, no. 2, 2023, pp. 93-101, doi:10.25048/tudod.1342082.
Vancouver İleri İ, Turan İ. Sıçanlarda REM Uyku Yoksunluğunun İskelet Kası Myostatin Düzeylerine Etkisi. Turk J Diab Obes. 2023;7(2):93-101.

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