CHANGES IN SECONDARY STRUCTURE OF PROTEIN IN SKELETAL MUSCLE DUE TO HIGH-CARBOHYDRATE OR HIGH-FAT DIETS
Year 2024,
Volume: 25 Issue: 3, 233 - 243, 30.09.2024
Nazlı Ezer Özer
,
Ayça Doğan Mollaoğlu
Abstract
Objective: Obesity, which arises from changes in lifestyle and feeding habits, is a threat to human health. One essential contributor to the increase in obesity rates is the popularity of high-calorie diets. This study aims to investigate high-fat (HFD) and high-carbohydrate (HCD) diet-induced molecular changes in protein secondary structure in longissimus dorsi skeletal muscle tissues of female inbred C57BL/6J mice by utilizing Attenuated Total Reflectance-Fourier Transform Infrared (ATR-FTIR) spectroscopy.
Materials and Methods: Mice were fed a control diet, HCD, or HFD for 24 weeks. Their skeletal muscle tissues were collected, and their spectra were recorded using a Bruker Invenio S ATR-FTIR spectrometer in the 4000-400 cm-1 region.
Results: The protein secondary structure profiles of the HCD group demonstrated a significant rise in antiparallel β-sheet and β-turn and a decline in parallel β-sheets together with the insignificant increase in aggregated β-sheets and a decrease in α-helix. The impact of an HFD on protein conformation is less pronounced than HCD. The HFD diet led to an increase in antiparallel β-sheets and a decrease in parallel β-sheets. Although it was not significant, an increase was observed in β-turn and α-helix.
Conclusion: These results propose the appearance of protein aggregation and/or formation of protein-protein intermolecular interaction in skeletal muscle tissues of female inbred C57BL/6J mice. Collectively, these data suggest that both high-calorie diets impair secondary structures of protein in skeletal muscle that may affect its metabolic function.
Ethical Statement
The experimental protocol of this study was approved by the Uskudar University Animal Research Local Ethics Committee (Approval No: 2017/02).
Supporting Institution
The Scientific and Technological Research Institution of Turkiye (TUBITAK)
Project Number
TUBITAK-3501-118S484
Thanks
We would like to thank The Scientific and Technological Research Institution of Turkiye (TUBITAK) for their support in conducting this study.
References
- 1. Sartori R, Romanello V, Sandri M. Mechanisms of muscle atrophy and hypertrophy: implications in health and disease. Nat Commun 2021; 12(1): 330.
- 2. Bergman BC, Goodpaster BH. Exercise and Muscle Lipid Content, Composition, and Localization: Influence on Muscle Insulin Sensitivity. Diabetes 2020; 69(5): 848-58.
- 3. Sen I, Bozkurt O, Aras E, Heise S, Brockmann GA, Severcan F. Lipid Profiles of Adipose and Muscle Tissues in
Mouse Models of Juvenile Onset of Obesity without High Fat Diet Induction: A Fourier Transform Infrared (FT-IR)Spectroscopic Study. Appl Spectrosc 2015; 69(6): 679-88.
- 4. Beals JW, Burd NA, Moore DR, Van Vliet S. Obesity alters the muscle protein synthetic response to nutrition and exercise. Front Nutr 2019; 6: 87.
- 5. Dideriksen K, Reitelseder S, Holm L. Influence of amino acids, dietary protein, and physical activity on muscle mass development in humans. Nutrients 2013; 5(3): 852-76.
- 6. Marinko JT, Huang H, Penn WD, Capra JA, Schlebach JP, Sanders CR. Folding and Misfolding of Human
Membrane Proteins in Health and Disease: From Single Molecules to Cellular Proteostasis. Chem Rev 2019; 119(9): 5537-606.
- 7. Anfinsen CB. Principles that govern the folding of protein chains. Science 1973; 181(4096): 223-30.
- 8. Stollar EJ, Smith DP. Uncovering protein structure. Essays Biochem 2020; 64(4): 649-80. Erratum in: Essays
Biochem 2021; 65(2): 407.
- 9. Severcan F, Haris PI. Fourier transform infrared spectroscopy suggests unfolding of loop structures precedes complete unfolding of pig citrate synthase. Biopolymers 2003; 69(4): 440-47.
- 10. Bozkurt O, Severcan M, Severcan F. Diabetes induces compositional, structural and functional alterations on rat skeletal soleus muscle revealed by FTIR spectroscopy: a comparative study with EDL muscle. The Analyst 2010; 135(12): 3110.
- 11. Garip S, Gozen AC, Severcan F. Use of Fourier transform infrared spectroscopy for rapid comparative analysis of Bacillus and Micrococcus isolates. Food Chem 2009; 113(4):1301-07.
- 12. Cakmak G, Togan I, Severcan F. 17β-Estradiol induced compositional, structural and functional changes in
rainbow trout liver, revealed by FT-IR spectroscopy: A comparative study with nonylphenol. Aquat Toxicol 2006; 77(1): 53-63.
- 13. Ezer N, Sahin I, Kazanci N. Alliin interacts with DMPC model membranes to modify the membrane dynamics: FTIR and DSC Studies. Vib Spectrosc 2017; 89: 1-8.
- 14. Mollaoğlu AD, Gurbanov R, Severcan M, Severcan F. CoronaVac (Sinovac) COVID-19 vaccine-induced
molecular changes in healthy human serum by infrared spectroscopy coupled with chemometrics. Turk J Biol 2021; 45(7): 569-77.
- 15. Miller LM, Bourassa MW, Smith RJ. FTIR spectroscopic imaging of protein aggregation in living cells. Biochim Biophys Acta 2013; 1828(10): 2339-46.
- 16. Barth A. Infrared spectroscopy of proteins. Biochim Biophys Acta 2007; 1767(9): 1073-101.
- 17. Krimm S, Bandekar J. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv Protein Chem 1986; 38: 181-364.
- 18. Toyran N, Zorlu F, Severcan F. Effect of stereotactic radiosurgery on lipids and proteins of normal and
hypoperfused rat brain homogenates: a Fourier transform infrared spectroscopy study. Int J Radiat Biol 2005; 81(12): 911- 18.
19. Mithal A, Bonjour J-P, Boonen S, Burckhardt P, Degens H, El Hajj Fuleihan G, et al. Impact of nutrition on muscle mass, strength, and performance in older adults [published correction appears in Osteoporos Int 2013; 24(4): 1527- 8]. Osteoporos Int 2013; 24(5): 1555-66.
- 20. Deldicque L, Cani PD, Philp A, Raymackers J-M, Meakin PJ, Ashford MLJ, et al. The unfolded protein response is activated in skeletal muscle by high-fat feeding: potential role in the downregulation of protein synthesis. Am J PhysiolEndocrinol Metab 2010; 299(5): 695-705.
- 21. Anderson SR, Gilge DA, Steiber AL, Previs SF. Diet-induced obesity alters protein synthesis: tissue-specific
effects in fasted versus fed mice. Metabolism 2008; 57(3): 347-54.
- 22. Masgrau A, Mishellany-Dutour A, Murakami H, Beaufrère A-M, Walrand S, Giraudet C, et al. Time-course
changes of muscle protein synthesis associated with obesity-induced lipotoxicity. J Physiol 2012; 590(20): 5199-210.
- 23. Vihinen, M. Functional effects of protein variants. Biochimie 2021; 180: 104-20.
- 24. Collin F, Cerlati O, Couderc F, Lonetti B, Marty J-D, Mingotaud A-F. Multidisciplinary analysis of protein-lipid interactions and implications in neurodegenerative disorders. Trends Anal Chem 2020; 132: 116059.
- 25. Shea D, Hsu CC, Bi TM, Paranjapye N, Childers MC, Cochran J, et al. α-Sheet secondary structure in amyloid β-peptide drives aggregation and toxicity in Alzheimer’s disease. Proc Natl Acad Sci USA 2019; 116(18): 8895-900.
- 26. Bozkurt O, Haman Bayari S, Severcan M, Krafft C, Popp J, Severcan F. Structural alterations in rat liver proteins due to streptozotocin-induced diabetes and the recovery effect of selenium: Fourier transform infrared microspectroscopy and neural network study. J Biomed Opt 2012; 17(7): 0760231.
- 27. Siddique MAB, Maresca P, Pataro G, Ferrari G. Effect of pulsed light treatment on structural and functional properties of whey protein isolate. Food Res Int 2016; 87:189-96.
- 28. Harnkarnsujarit N, Kawai K, Suzuki T. Effects of Freezing Temperature and Water Activity on Microstructure, Color, and Protein Conformation of Freeze-Dried Bluefin Tuna (Thunnus orientalis). Food Bioprocess Technol. 2015; 8: 916- 25.
- 29. Wachirattanapongmetee K, Katekaew S, Weerapreeyakul N, Thawornchinsombut S. Differentiation of protein types extracted from tilapia byproducts by FTIR spectroscopy combined with chemometric analysis and their antioxidant protein hydrolysates. Food Chem 2024; 437(2): 137862.
- 30. Xiong YL. Structure function relationships of muscle proteins. In: Damodaran S, Paraf A, editors. Food Proteins and Their Applications. Marcel Dekker Inc, 1997: 341-92.
- 31. Rayment I, Rypniewski WR, Schmidt-Bäse K, Smith R, Tomchick D, Benning M, et al. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 1993; 261(5117): 50-8.
- 32. Mahon AB, Arora PS. End-Capped α-Helices as Modulators of Protein Function. Drug Discov Today Technol 2012; 9(1):57-62.
- 33. Gurbanov R, Bilgin M, Severcan F. Restoring effect of selenium on the molecular content, structure and fluidity of diabetic rat kidney brush border cell membrane. Biochim Biophys Acta-Biomembr 2016; 1858(4): 845-54.
- 34. Petibois C, Gouspillou G, Wehbe K, Delage J-P, Déléris G. Analysis of type I and IV collagens by FT-IR spectroscopy and imaging for a molecular investigation of skeletal muscle connective tissue. Anal Bioanal Chem 2006; 386: 1961-66.
- 35. Sitnick M, Bodine SC, Rutledge JC. Chronic high fat feeding attenuates load-induced hypertrophy in mice. J Physiol 2009; 587(23): 5753-65.
- 36. Antunes MM, Godoy G, de Almeida-Souza CB, da Rocha BA, da Silva-Santi LG, Masi LN, et al. A highcarbohydrate diet induces greater inflammation than a high-fat diet in mouse skeletal muscle. Braz J Med Biol Res 2020; 53(3): 9039.
- 37. Simsek Ozek N, Sara Y, Onur R, Severcan F. Low dose simvastatin induces compositional, structural and dynamic changes in rat skeletal extensor digitorum longus muscle tissue. Biosci Rep 2009; 30(1): 41-50.
- 38. Garip S, Bayari SH, Severcan M, Abbas S, Lednev IK, Severcan F. Structural effects of simvastatin on rat liver tissue: Fourier transform infrared and Raman microspectroscopic studies. J Biomed Opt 2016; 21(2): 025008.
YÜKSEK KARBONHİDRATLI VEYA YÜKSEK YAĞLI DİYETLERE BAĞLI OLARAK İSKELET KASINDAKİ PROTEİNİN SEKONDER YAPISINDA MEYDANA GELEN DEĞİŞİKLİKLER
Year 2024,
Volume: 25 Issue: 3, 233 - 243, 30.09.2024
Nazlı Ezer Özer
,
Ayça Doğan Mollaoğlu
Abstract
Amaç: Yaşam tarzı ve beslenme alışkanlıklarındaki değişikliklerden kaynaklanan obezite, insan sağlığı için bir tehdit oluşturmaktadır. Obezite artışına katkıda bulunan temel etkenlerden biri yüksek kalorili diyet tüketiminin popülerliğidir. Bu çalışmada, Zayıflatılmış Toplam Yansıma-Fourier Dönüşüm Kızılötesi (ATR-FTIR) spektroskopisi kullanılarak dişi C57BL/6J farelerinin longissimus dorsi iskelet kas dokularında yüksek yağlı (HFD) ve yüksek karbonhidratlı (HCD) diyetin neden olduğu protein sekonder yapısındaki moleküler değişikliklerin araştırılması amaçlanmıştır.
Gereç ve Yöntemler: Farelere 24 hafta boyunca kontrol, HCD veya HFD diyetleri uygulandı. İskelet kas dokuları toplandı ve spektrumları Bruker Invenio S ATR-FTIR spektrometresi kullanılarak 4000-400 cm-1 bölgesinde kaydedildi.
Bulgular: HCD grubunun protein sekonder yapı profilleri, antiparalel β-tabaka ve β-dönüşte önemli bir artış ve paralel β-tabakalarda bir düşüş ile birlikte kümelenmiş β-tabakalarda önemsiz bir artış ve α-helikste bir azalma gösterdi. HFD'nin protein konformasyonu üzerindeki etkisi HCD'den daha az belirgindi. HFD diyeti, antiparalel β-tabakalarda bir artışa ve paralel β-tabakalarda bir azalmaya yol açtı. Önemli olmasa da β-dönüşte ve α-helikste bir artış gözlendi.
Sonuç: Bu sonuçlar, dişi inbred C57BL/6J farelerinin iskelet kas dokularında protein agregasyonunun ve/veya protein-protein moleküller arası etkileşimlerinin ortaya çıktığını ileri sürmektedir. Bu veriler her iki yüksek kalorili diyetin de iskelet kasının sekonder protein yapılarını bozarak metabolik işlevini etkileyebileceğini göstermektedir.
Project Number
TUBITAK-3501-118S484
References
- 1. Sartori R, Romanello V, Sandri M. Mechanisms of muscle atrophy and hypertrophy: implications in health and disease. Nat Commun 2021; 12(1): 330.
- 2. Bergman BC, Goodpaster BH. Exercise and Muscle Lipid Content, Composition, and Localization: Influence on Muscle Insulin Sensitivity. Diabetes 2020; 69(5): 848-58.
- 3. Sen I, Bozkurt O, Aras E, Heise S, Brockmann GA, Severcan F. Lipid Profiles of Adipose and Muscle Tissues in
Mouse Models of Juvenile Onset of Obesity without High Fat Diet Induction: A Fourier Transform Infrared (FT-IR)Spectroscopic Study. Appl Spectrosc 2015; 69(6): 679-88.
- 4. Beals JW, Burd NA, Moore DR, Van Vliet S. Obesity alters the muscle protein synthetic response to nutrition and exercise. Front Nutr 2019; 6: 87.
- 5. Dideriksen K, Reitelseder S, Holm L. Influence of amino acids, dietary protein, and physical activity on muscle mass development in humans. Nutrients 2013; 5(3): 852-76.
- 6. Marinko JT, Huang H, Penn WD, Capra JA, Schlebach JP, Sanders CR. Folding and Misfolding of Human
Membrane Proteins in Health and Disease: From Single Molecules to Cellular Proteostasis. Chem Rev 2019; 119(9): 5537-606.
- 7. Anfinsen CB. Principles that govern the folding of protein chains. Science 1973; 181(4096): 223-30.
- 8. Stollar EJ, Smith DP. Uncovering protein structure. Essays Biochem 2020; 64(4): 649-80. Erratum in: Essays
Biochem 2021; 65(2): 407.
- 9. Severcan F, Haris PI. Fourier transform infrared spectroscopy suggests unfolding of loop structures precedes complete unfolding of pig citrate synthase. Biopolymers 2003; 69(4): 440-47.
- 10. Bozkurt O, Severcan M, Severcan F. Diabetes induces compositional, structural and functional alterations on rat skeletal soleus muscle revealed by FTIR spectroscopy: a comparative study with EDL muscle. The Analyst 2010; 135(12): 3110.
- 11. Garip S, Gozen AC, Severcan F. Use of Fourier transform infrared spectroscopy for rapid comparative analysis of Bacillus and Micrococcus isolates. Food Chem 2009; 113(4):1301-07.
- 12. Cakmak G, Togan I, Severcan F. 17β-Estradiol induced compositional, structural and functional changes in
rainbow trout liver, revealed by FT-IR spectroscopy: A comparative study with nonylphenol. Aquat Toxicol 2006; 77(1): 53-63.
- 13. Ezer N, Sahin I, Kazanci N. Alliin interacts with DMPC model membranes to modify the membrane dynamics: FTIR and DSC Studies. Vib Spectrosc 2017; 89: 1-8.
- 14. Mollaoğlu AD, Gurbanov R, Severcan M, Severcan F. CoronaVac (Sinovac) COVID-19 vaccine-induced
molecular changes in healthy human serum by infrared spectroscopy coupled with chemometrics. Turk J Biol 2021; 45(7): 569-77.
- 15. Miller LM, Bourassa MW, Smith RJ. FTIR spectroscopic imaging of protein aggregation in living cells. Biochim Biophys Acta 2013; 1828(10): 2339-46.
- 16. Barth A. Infrared spectroscopy of proteins. Biochim Biophys Acta 2007; 1767(9): 1073-101.
- 17. Krimm S, Bandekar J. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv Protein Chem 1986; 38: 181-364.
- 18. Toyran N, Zorlu F, Severcan F. Effect of stereotactic radiosurgery on lipids and proteins of normal and
hypoperfused rat brain homogenates: a Fourier transform infrared spectroscopy study. Int J Radiat Biol 2005; 81(12): 911- 18.
19. Mithal A, Bonjour J-P, Boonen S, Burckhardt P, Degens H, El Hajj Fuleihan G, et al. Impact of nutrition on muscle mass, strength, and performance in older adults [published correction appears in Osteoporos Int 2013; 24(4): 1527- 8]. Osteoporos Int 2013; 24(5): 1555-66.
- 20. Deldicque L, Cani PD, Philp A, Raymackers J-M, Meakin PJ, Ashford MLJ, et al. The unfolded protein response is activated in skeletal muscle by high-fat feeding: potential role in the downregulation of protein synthesis. Am J PhysiolEndocrinol Metab 2010; 299(5): 695-705.
- 21. Anderson SR, Gilge DA, Steiber AL, Previs SF. Diet-induced obesity alters protein synthesis: tissue-specific
effects in fasted versus fed mice. Metabolism 2008; 57(3): 347-54.
- 22. Masgrau A, Mishellany-Dutour A, Murakami H, Beaufrère A-M, Walrand S, Giraudet C, et al. Time-course
changes of muscle protein synthesis associated with obesity-induced lipotoxicity. J Physiol 2012; 590(20): 5199-210.
- 23. Vihinen, M. Functional effects of protein variants. Biochimie 2021; 180: 104-20.
- 24. Collin F, Cerlati O, Couderc F, Lonetti B, Marty J-D, Mingotaud A-F. Multidisciplinary analysis of protein-lipid interactions and implications in neurodegenerative disorders. Trends Anal Chem 2020; 132: 116059.
- 25. Shea D, Hsu CC, Bi TM, Paranjapye N, Childers MC, Cochran J, et al. α-Sheet secondary structure in amyloid β-peptide drives aggregation and toxicity in Alzheimer’s disease. Proc Natl Acad Sci USA 2019; 116(18): 8895-900.
- 26. Bozkurt O, Haman Bayari S, Severcan M, Krafft C, Popp J, Severcan F. Structural alterations in rat liver proteins due to streptozotocin-induced diabetes and the recovery effect of selenium: Fourier transform infrared microspectroscopy and neural network study. J Biomed Opt 2012; 17(7): 0760231.
- 27. Siddique MAB, Maresca P, Pataro G, Ferrari G. Effect of pulsed light treatment on structural and functional properties of whey protein isolate. Food Res Int 2016; 87:189-96.
- 28. Harnkarnsujarit N, Kawai K, Suzuki T. Effects of Freezing Temperature and Water Activity on Microstructure, Color, and Protein Conformation of Freeze-Dried Bluefin Tuna (Thunnus orientalis). Food Bioprocess Technol. 2015; 8: 916- 25.
- 29. Wachirattanapongmetee K, Katekaew S, Weerapreeyakul N, Thawornchinsombut S. Differentiation of protein types extracted from tilapia byproducts by FTIR spectroscopy combined with chemometric analysis and their antioxidant protein hydrolysates. Food Chem 2024; 437(2): 137862.
- 30. Xiong YL. Structure function relationships of muscle proteins. In: Damodaran S, Paraf A, editors. Food Proteins and Their Applications. Marcel Dekker Inc, 1997: 341-92.
- 31. Rayment I, Rypniewski WR, Schmidt-Bäse K, Smith R, Tomchick D, Benning M, et al. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 1993; 261(5117): 50-8.
- 32. Mahon AB, Arora PS. End-Capped α-Helices as Modulators of Protein Function. Drug Discov Today Technol 2012; 9(1):57-62.
- 33. Gurbanov R, Bilgin M, Severcan F. Restoring effect of selenium on the molecular content, structure and fluidity of diabetic rat kidney brush border cell membrane. Biochim Biophys Acta-Biomembr 2016; 1858(4): 845-54.
- 34. Petibois C, Gouspillou G, Wehbe K, Delage J-P, Déléris G. Analysis of type I and IV collagens by FT-IR spectroscopy and imaging for a molecular investigation of skeletal muscle connective tissue. Anal Bioanal Chem 2006; 386: 1961-66.
- 35. Sitnick M, Bodine SC, Rutledge JC. Chronic high fat feeding attenuates load-induced hypertrophy in mice. J Physiol 2009; 587(23): 5753-65.
- 36. Antunes MM, Godoy G, de Almeida-Souza CB, da Rocha BA, da Silva-Santi LG, Masi LN, et al. A highcarbohydrate diet induces greater inflammation than a high-fat diet in mouse skeletal muscle. Braz J Med Biol Res 2020; 53(3): 9039.
- 37. Simsek Ozek N, Sara Y, Onur R, Severcan F. Low dose simvastatin induces compositional, structural and dynamic changes in rat skeletal extensor digitorum longus muscle tissue. Biosci Rep 2009; 30(1): 41-50.
- 38. Garip S, Bayari SH, Severcan M, Abbas S, Lednev IK, Severcan F. Structural effects of simvastatin on rat liver tissue: Fourier transform infrared and Raman microspectroscopic studies. J Biomed Opt 2016; 21(2): 025008.