Journal of Applied Biological Chemistry

The Korean Society for Applied Biological Chemistry (한국응용생명화학회)
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Effects of sea horse (Hippocampus abdominalis)-derived protein hydrolysate on skeletal muscle development

  • Muthuramalingam, Karthika (Department of Medicine, School of Medicine, Jeju National University) ;
  • Kim, Jun Ho (Department of Medicine, School of Medicine, Jeju National University) ;
  • Jeon, You Jin (Department of Marine Life Science, Jeju National University) ;
  • Rho, Sum (Haechunma Company Ltd) ;
  • Kim, Young Mee (Department of Medicine, School of Medicine, Jeju National University) ;
  • Cho, Moonjae (Department of Medicine, School of Medicine, Jeju National University)
  • Received : 2017.10.12
  • Accepted : 2017.11.07
  • Published : 2017.12.01
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Abstract

Hippocampus abdominalis, the big belly sea horse, is widely known for its medicinal value in Chinese folk medicine. In this study, extract obtained by proteolytic degradation of this species was investigated for its effects on skeletal muscle development, both in vitro and in vivo. Muscle cell lines ($C_2C_{12}$ and $L_6$) treated with the bioactive peptide did not have any detrimental effects on the cell viability, which was above 80%. Optical microscopy analysis on the morphology of the sea horse extract (SHE)-treated cells showed enhanced differentiating ability with myotube formation. Moreover, cells incubated with the hydrolysate displayed decreased proliferation rate, as recorded by the electric cell substrate impedance sensing system, thereby supporting enhanced differentiation. For a period of 12 weeks, mice models were fed with SHE and simultaneously subjected to treadmill exercise, which increased the expression of Myogenin, a key myogenic regulatory factor. In addition, there was an increase in the expression of AMPK- and Cytochrome C, both of which are important in mitochondrial biogenesis. Thus, the SHE from Hippocampus abdominalis can be a promising candidate as protein supplement aiding muscle development.

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References

  1. Bordbar S, Anwar F, Saari N (2011) High-Value Components and Bioactives from Sea Cucumbers for Functional Foods. Marine Drugs 9(10): 1761-1805 https://doi.org/10.3390/md9101761
  2. Borselli C, Storrie H, Benesch-Lee F, Shvartsman D, Cezar C, Lichtman JH, Vandenburgh H, J Mooney D (2010) Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. PNAS 107(8): 3287-3292 https://doi.org/10.1073/pnas.0903875106
  3. Busiello RA, Savarese S, Lombardi A (2015) Mitochondrial uncoupling proteins and energy metabolism. Front Physiol 6: 36
  4. Collu-Marchese M, Shuen M, Pauly M, Saleem A, Hood DA (2015) The regulation of mitochondrial transcription factor A (Tfam) expression during skeletal muscle cell differentiation. Bioscience Rep 35(3): 221
  5. Eva Blomstrand, Jorgen Eliasson, Hakan KR, Karlsson, Rickard Kohnke (2006) Branched-Chain Amino Acids Activate Key Enzymes in Protein Synthesis after Physical Exercise. J Nutr 36(1): 269-273
  6. Feixia Hou, Longlian Wen, Cheng Peng, Jinlin Guo (2016) Identification of marine traditional Chinese medicine dried sea horses in the traditional Chinese medicine market using DNA barcoding. Mitochondr DNA Part A. doi: 10.1080/24701394.2016.1248430
  7. Fernandes T, Soci UPR, Melo SFS, Alves CR, Oliveira EM (2012) Skeletal Muscle-From Myogenesis to Clinical Relations. Dr.Julianna Cseri (Ed.) Signaling Pathways that medicate Skeletal Muscle Hypertrophy: Effects of Exercise Training, InTech. doi:10.5772/51087
  8. Gao AW, Carles C, Houtkooper RH (2014) Mitochondrial Response to Nutrient Availability and Its Role in Metabolic Disease. EMBO Mol Med 6(5): 580-589
  9. Giaever I, Keese CR (1984) Monitoring fibroblast behavior in tissue culture with an applied electric field. Proc Natl Acad Sci U S A 81:3761-3764 https://doi.org/10.1073/pnas.81.12.3761
  10. Guadalupe-Grau A, Fernandez-Elas VE, Ortega JF, Dela F, Helge JW, Mora Rodrguez R (2017) Effects of 6-month aerobic interval training on skeletal muscle metabolism in middle-aged metabolic syndrome patients. Scand J Med Sci Sports. doi: 10.1111/sms.12881
  11. Holloszy JO (1967) Biochemical Adaptations in Muscle: Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 242(9): 2278-2282
  12. Hou Y, Wu Z, Dai Z, Wang G, Wu G (2017) Protein hydrolysates in animal nutrition: Industrial production, bioactive peptides and functional significance. J Anim Sci Biotechno 8: 24 https://doi.org/10.1186/s40104-017-0153-9
  13. Imen Hamed, Fatih Ozogul, Yesim Ozogul, Joe MR (2015) Marine Bioactive Compounds and Their Health Benefits: A Review. Compr Rev Food Sci Food Saf 14: 446-465 https://doi.org/10.1111/1541-4337.12136
  14. Keller Karsten, Engelhardt Martin (2013) Strength and Muscle Mass Loss with Aging Process. Age and Strength Loss. Muscles, Ligaments Tendons J 3(4): 346-350
  15. Kim YM, Jeon YJ, Huh JS, Kim SD, Park KK, Cho MJ (2016) Effects of enzymatic hydrolysate from sea horse Hippocampus abdominalis on testosterone secretion from TM3 Leydig cells and in male mice. Appl Biol Chem 59(6): 869-879 https://doi.org/10.1007/s13765-016-0237-9
  16. Lene Meinert, Eva Honnens de Lichtenberg Broge, Camilla Bejerholm, Kirsten Jensen (2016) Application of hydrolyzed proteins of animal origin in processed meat. Food Sci Nutr 4(2): 290-297 https://doi.org/10.1002/fsn3.289
  17. Manninen AH (2009) Protein hydrolysates in sports nutrition. Nutr Metab 6:38 https://doi.org/10.1186/1743-7075-6-38
  18. McCarthy AL, O'Callaghan YC, O'Brien NM (2013) Protein Hydrolysates from Agricultural Crops-Bioactivity and Potential for Functional Food Development. 112-130
  19. Miranda Nabben, Joris Hoeks (2008) Mitochondrial uncoupling protein 3 and its role in cardiac- and skeletal muscle metabolism. Physiol Behav 94(2): 259-269 https://doi.org/10.1016/j.physbeh.2007.11.039
  20. Nalae Kang, Seo-Young Kim, Sum Rho, Ju-Young Ko, You-Jin Jeon (2017) Anti-fatigue activity of a mixture of sea horse (Hippocampus abdominalis) hydrolysate and red ginseng. Korean J Fish Aquat Sci 20: 3 https://doi.org/10.1186/s41240-017-0048-x
  21. Pacagnelli FL, Aguiar AF, Campos DH, Castan EP, de Souza RW, de Almeida FL, Carani F, Carvalho RF, Cicogna AC, Silva MD (2016) Training improves the oxidative phenotype of muscle during the transition from cardiac hypertrophy to heart failure without altering MyoD and Myogenin. 101(8): 1075-1085 https://doi.org/10.1113/EP085552
  22. Patrick Schrauwen, Joris Hoeks, Matthijs K.C Hesselink (2006) Lipidinduced cell stress and insulin resistance. Scand J Med Sci Sports 50(2):62-67
  23. Paul D. Thompson, Gregory Panza, Amanda Zaleski, Beth Taylor (2016) Statin-Associated Side Effects. J Am Coll Cordiol 67(20): 2395-2410 https://doi.org/10.1016/j.jacc.2016.02.071
  24. Perera N, Godahewa G, Lee J (2016) Copper-zinc-superoxide dismutase (CuZnSOD), an antioxidant gene from sea horse (Hippocampus abdominalis); molecular cloning, sequence characterization, antioxidant activity and potential peroxidation function of its recombinant protein. Fish Shellfish Immunol 57: 386-399 https://doi.org/10.1016/j.fsi.2016.08.052
  25. Philips S (2011) The science of muscle hypertrophy: Making dietary protein count. P Nutr Soc 70(1): 100-103 https://doi.org/10.1017/S002966511000399X
  26. Raja Ganesan, Nina Judith Hos, Saray Gutierrez, Julia Fische, Joanna Magdalena Stepek, Evmorphia Daglid, Martin Kronke, Nirmal Robinson (2017) Salmonella Typhimurium disrupts Sirt1/AMPK checkpoint control of mTOR to impair autophagy. PLoS Pathog 13(2)
  27. Richter EA, Ruderman NB (2009) AMPK and the biochemistry of exercise: Implications for human health and disease. Biochem J 418(2): 261-275 https://doi.org/10.1042/BJ20082055
  28. Schoenfeld BJ, Aragon AA, Krieger JW (2013) The Effect of Protein Timing on Muscle Strength and Hypertrophy: A Meta-Analysis. J Int Soc Sports Nut 10(53)
  29. Sculcek R, Bogaard HJ, van Nieuw Amerongen GP (2014) Electric cellsubstrate impedance sensing for the quantification of endothelial proliferation, barrier function and motility. J Vis Exp 85:e51300
  30. Teng S, Stegner D, Chen Q, Hongu T, Hasegawa H, Chen L, Kanaho Y, Nieswandt B, Frohman MA, Huang P (2015) Phospholipase D1 facilitates second-phase myoblast fusion and skeletal muscle regeneration. Mol Biol Cell 26(3): 506-517 https://doi.org/10.1091/mbc.e14-03-0802
  31. Terjung RL, Winder WW, Baldwin KM, Holloszy JO (1973) Effect of Exercise on the Turnover of Cytochrome c in Skeletal Muscle. J Biol Chem 248(21): 7404-7406
  32. Valente LMP, Moutou KA, Conceicao LEC, Engrola S, Fernandes JMO, Johnston IA (2013) What determines growth potential and juvenile quality of farmed fish species?. Rev Aquacult 5: S168-S193 https://doi.org/10.1111/raq.12020
  33. Vijaykrishnaraj M, Prabhasankar P (2015) Marine protein hydrolysates: their present and future perspectives in food chemistry. 34864-34877 https://doi.org/10.1039/C4RA17205A
  34. Vincenzo Nobile, Elisa Duclos, Angela Michelotti, Gioia Bizzaro, Massimo Negro, Florian Soisson (2016) Supplementation with a fish protein hydrolysate (Micromesistius poutassou): effects on body weight, body composition, and CCK/GLP-1 secretion. Food Nutr Res 60: 29857 https://doi.org/10.3402/fnr.v60.29857
  35. Wengong Wand, Xialing Yang, Isabel Lopez de Silanes, David Carling, Myriam Gorospe (2003) Increased AMP: ATP Ratio and AMP-activated Protein Kinase Activity during Cellular Senescence Linked to Reduced HuR Function. J Biol Chem 278: 27016 https://doi.org/10.1074/jbc.M300318200

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