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In vivo anti-lipidemic and antioxidant potential of collagen peptides obtained from great hammerhead shark skin waste

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Abstract

The aim of the present study was to evaluate the ability of fish collagen peptides (FCP) derived from the skin of great hammerhead shark (Sphyrna mokarran) in attenuating the high fat diet-alcohol induced hyperlipidemia. The oral supplementation of FCP in high fat diet-alcohol fed experimental rats confirmed the regulation of body weight to normal level. The FCP treated group revealed the efficient lipid lowering ability by enhancing the cholesterol metabolism. Western blot analysis of the lipid metabolic enzymes revealed that the oral-intake of FCP has down-regulated the expression levels of fatty acid synthase and 3-Hydroxy-3-methylglutaryl-CoA reductase (HMGCR). Simultaneously, the expression levels of Lecithin–cholesterol acyltransferase (LCAT) in liver was up-regulated. Histopathology analysis of liver tissues demonstrated that the FCP treated group maintained normal liver parenchyma with moderate inflammatory infiltration, whereas the statin treated group developed centrilobular fibrosis, atrophy of hepatocytes and moderate inflammatory infiltration. Oral dietary supplementation of FCP enhanced the activity levels of both superoxide dismutase and catalase enzymes and, lowered the levels of lipid peroxidation in liver tissues.

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Abbreviations

ABTS:

2,2′Azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt

ASC:

Acid soluble collagen

BHT:

Butylated hydroxytoluene

CPCSEA:

Committee for the Purpose of Control and Supervision of Experiments on Animals

ELISA:

Enzyme linked immunosorbent assay

FAS:

Fatty acid synthase

FCP:

Fish collagen peptides

FCH:

Fish collagen hydrolysate

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

H&E:

Haematoxylin and eosin

HDL-C:

High density lipoprotein- cholesterol

HMG CoA:

3-Hydroxy-3-methylglutaryl-CoA

HMGCR:

3-Hydroxy-3-methylglutaryl-CoA reductase

LCAT:

Lecithin–cholesterol acyltransferase

LDL-C:

Low density lipoprotein-cholesterol

NADPH:

Nicotinamide adenine dinucleotide phosphate

NC:

Normal control

PBS:

Phosphate buffered saline

PC:

Positive control

PUFA:

Poly unsaturated fatty acid

ROS:

Reactive oxygen species

SDS-PAGE:

Sodium dodecyl sulphate–polyacrylamide gel electrophoresis

SOD:

Superoxide dismutase

Stat:

Statin

TBARS:

Thiobarbituric acid reactive substances

TC:

Total cholesterol

TG:

Triglyceride

VLDL-C:

Very low-density lipoprotein- cholesterol

References

  • Anandan R, Ganesan B, Obulesu T, Mathew S, Asha KK, Lakshmanan PT, Zynudheen AA (2013) Antiaging effect of dietary chitosan supplementation on glutathione-dependent antioxidant system in young and aged rats. Cell Stress Chaperon 18:121–125

    Article  CAS  Google Scholar 

  • AOAC (2000) Official methods of analysis of AOAC International, 17th edn. AOAC, Gaithersburg, MD, USA

  • Argo CK, Loria P, Caldwell SH, Lonardo A (2008) Statins in liver disease: a molehill, an iceberg, or neither? Hepatology 48:662–669

    Article  CAS  PubMed  Google Scholar 

  • Bao L, Hu L, Zhang Y, Wang Y (2016) Hypolipidemic effects of flavonoids extracted from Lomatogonium rotatum. Exp The Med 11:1417–1424

    Article  CAS  Google Scholar 

  • Bruha R, Dvorak K, Petrtyl J (2012) Alcoholic liver disease. World J Hepatol 4(3):81–90

    Article  PubMed  PubMed Central  Google Scholar 

  • Buege JA, Aust SD, Fleischer S, Packer L (1978) Microsomal lipid peroxidation. Biological oxidations, Academic press, Biomembranes-Part C, pp 302–310

    Google Scholar 

  • Carroll KK, Kurowska EM (1995) Soy consumption and cholesterol reduction: review of animal and human studies. J Nutr 12:594–597

    Google Scholar 

  • Chakravarty B, Gu Z, Chirala SS, Wakil SJ, Quiocho FA (2004) Human fatty acid synthase: Structure and substrate selectivity of the thioesterase domain. PNAS 101(44):15567–15572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dara PK, Raghavankutty M, Sebastian N, Chatterjee NS, Mathew S, Ravishankar CN, Anandan R (2020a) Rheological, physico-chemical, and surface-active properties of gelatin extracted from bigeye tuna (Thunnus obesus) skin waste. J Aq Food Product Tech 29(5):428–444

    Article  CAS  Google Scholar 

  • Dara PK, Elavarasan K, Shamasunadar BA (2020b) Characterization of antioxidant and surface-active properties of gelatin protein hydrolysates obtained from croaker fish skin. Int Aq Res 12:116–126

    Google Scholar 

  • Dara PK, Elavarasan K, Shamasundar BA (2020c) Improved utilization of croaker skin waste and freshwater carps visceral waste: conversion of waste to health benefitting peptides. Int J Peptide Res Therap 26:2641–2651

    Article  CAS  Google Scholar 

  • Divya KV, Sreerekha PR, Elavarasan K, Mathew S, Ravi Shankar CN, Anandan R (2018a) Determination of electrophoretic subunit pattern and peptide mapping of collagen and collagen peptides extracted from skin of hammerhead shark (Sphyrnae mokkaran). SF J Anal Biochem 1:1–8

    Google Scholar 

  • Divya KV, Sreerekha PR, Tejpal CS, Asha KK, Mathew S, Ravishankar CN, Anandan R (2018b) Extraction and characterization of acid soluble collagen (ASC) from airbladder of striped cat fish (Pangasius hypophthalmus). Int J Fish Aquat Stud 6(4):310–318

    Google Scholar 

  • Duly AMP, Alani B, Huang EW, Yee C, Haber PS, McLennan SV, Seth D (2015) Effect of multiple binge alcohol on diet-induced liver injury ina mouse model of obesity. Nutr Diabetes 5:154

    Article  Google Scholar 

  • El-Tantawy WH (2015) Biochemical effects, hypolipidemic and antiinflammatory activities of Artemisia vulgaris extract in hypercholesterolemic rats. J Clin Biochem Nutr 57(1):33–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedwald WT, Levy RJ, Fredricken DS (1972) Estimation of VLDLcholesterol in the plasma without the use of preparative ultracentrifuge. Clin Chem 18:449

    Google Scholar 

  • Glomset JA, Janssen ET, Kennedy R, Dobbins J (1966) Role of plasma lecithin:cholesterolacyltransferase in the metabolism of high density lipoproteins. J Lipid Res 7:638–648

    Article  CAS  PubMed  Google Scholar 

  • Gu J, Zhang Y, Xu D, Zhao Z, Zhang Y, Pan Y, Cao P, Wang Z, Chen Y (2015) Ethanol-induced hepatic steatosis is modulated by glycogen level in the liver. J Lipid Res 56(7):1329–1339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Sun J, He H, Yu GC, Du J (2009) Antihepatotoxic effect of corn peptides against Bacillus Calmette-Guerin/lipopolysaccharide- induced liver injury in mice. Food Chem Toxicol 47:2431–2435

    Article  CAS  PubMed  Google Scholar 

  • Handel VE, Zilversmit DB (1957) Micro method for the direct determination of serum triglycerides. J Lab Clin Med 50(1):152–157

    Google Scholar 

  • Hema GS, Shyni K, Ganesan B, Joshy CG, Manu Prasad M, Suseela M (2016) In vivo and in vitro studies on joint regenerative potential of fish skin derived collagen peptides. World J Pharm Res 5(7):916–930

    Google Scholar 

  • Ishida Y, Fugita T, Asai K (1981) New detection and separation method for amino acids by high performance liquid chromatography. J Chroma 204:143–148

    Article  CAS  Google Scholar 

  • Ji G, Zhao X, Leng L, Liu P, Jiang Z (2011) Comparison of dietary control and atorvastatin on high fat diet induced hepatic steatosis and hyperlipidemia in rats. Lipids Health Dis 10:23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirpich IA, McClain CJ, Vatsalya V, Schwandt M, Phillips M, Falkner KC, Zhang L, Harwell C, George DT, Umhau JC (2017) Liver injury and endotoxemia in male and female alcohol-dependent individuals admitted to an alcohol treatment program. Alcohol Clin Exp Res 41(4):747–757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koyama Y, Kusubata M (2013) Effects of collagen peptide ingestion on blood lipids in rats fed a high-lipid and high-sucrose diet. Food SciTech Res 19(6):1149–1153

    CAS  Google Scholar 

  • Kumar DP, Chandra MV, Elavarasan K, Shamasundar BA (2017) Structural properties of gelatin extracted from croaker fish (Johniussp) skin waste. Int J of Food Prop 20:S2612–S2625

    Article  CAS  Google Scholar 

  • Lee KJ, Song NY, Oh YC, Cho WK, Ma JY (2014) Isolation and bioactivity analysis of ethyl acetate extract from Acer tegmentosum using in vitro assay and on-line screening HPLC-ABTS+ system. J Anal Met Chem 150509:1–15

    Google Scholar 

  • Liang K, Vaziri ND (2003) HMG-CoA reductase, cholesterol 7 alpha-hydroxylase, LCAT, ACAT, LDL receptor, and SRB-1 in hereditary analbuminemia. Kidney Int 64:192–198

    Article  CAS  PubMed  Google Scholar 

  • Lim SY (2013) Role of statins in coronary artery disease. Chonnam Med J 49:1–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin B, Zhang F, Yu Y, Jiang Q, Zhang Z, Wang J, Li Y (2012) Marine collagen peptides protect against early alcoholic liver injury in rats. Br J Nutr 107:1160–1166

    Article  CAS  PubMed  Google Scholar 

  • Miasoedov NF, Shubina TA, OberganTIu GME, Andreeva LA, Liapina LA (2013) Cholesterol-lowering effect of the regulatory peptide Pro-Gly-Pro-Leu. VoprPitan 82(5):41–45

    CAS  Google Scholar 

  • Misra HP, Fridovich T (1972) The role of superoxide ion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175

    Article  CAS  PubMed  Google Scholar 

  • Mizushige T, Komiya M, Onda M, Uchida K, Hayamizu K, Kabuyama Y (2017) Fish protein hydrolysate exhibits anti-obesity activity and reduces hypothalamic neuropeptide Y and agouti-related protein mRNA expressions in rats. Biomed Res 38(6):351–357

    Article  CAS  PubMed  Google Scholar 

  • Nawar WW (1998) Volatile components of the frying process. Grasasy Aceites 49(3–4):271–274

    Article  CAS  Google Scholar 

  • Ngatchic JTM, Njintang NY, Bernard C, Oben J, Mbofung CM (2016) Lipid-lowering properties of protein-rich mucuna product. Nutrire 41:2

    Article  Google Scholar 

  • Rao AV, Ramakrishnan S (1975) Indirect assessment of hydroxymethylglutaryl Co-A reductase (NADPH) activity in liver tissue. Clin Chem 21(10):1523–1525

    Article  CAS  PubMed  Google Scholar 

  • Ruiz JR, Ancona DB, Campos MS (2014) Bioactive vegetable proteins and peptides in lipid-lowering; nutraceutical potential. Nutr Hosp 29(4):776–784

    CAS  Google Scholar 

  • Siperstein MD, Guest MJ (1960) Studies on the site of the feedback control of cholesterol synthesis. J Clin Invest 39:642–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sreerekha PR, Dara PK, Vijayan DK, Chatterjee NS, Raghavankutty M, Mathew S, Ravishankar CN, Anandan R (2021) Dietary supplementation of encapsulated anthocyanin loaded-chitosan nanoparticles attenuates hyperlipidemic aberrations in male wistar rats. Carb Poly Tech App 2:100051

    Google Scholar 

  • Takahara S, Hamilton BH, Nell JV, Kobra TY, Ogawa Y, Nishimura ET (1960) Hypocatalasemia: a new genetic carried state. J Clin Invest 39(4):610–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taskiran D, TaskiranE YH, Kutay F (1999) Quantification of total collagen in rabbit tendonby the sirius red method. Tr J Med Sci 29:7–9

    CAS  Google Scholar 

  • Varma PS, Aruna K, Rukkumani R, Menon VP (2004) Alcohol and thermally oxidized pufa induced oxidative stress: role of N-acetyl cysteine. Ital J Biochem 53(1):10–15

    CAS  PubMed  Google Scholar 

  • WHO (2014) Global status report on alcohol and health. World Health Organization

  • Woo M, Song YO, Kang K, Noh JS (2018) Anti-Obesity effects of collagen peptide derived from skate (Raja kenojei) Skin through regulation of lipid metabolism. Mar Drugs 16:306

    Article  PubMed Central  Google Scholar 

  • Zlatkis A, Zak B, Boyle AJ (1953) A new method for the direct determination of serum cholesterol. J Lab Clin Med 41(3):486–492

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Director, ICAR-Central Institute of Fisheries Technology (ICAR-CIFT), Cochin, Kerala, India for providing the facilities to carry out this work and also for granting permission to publish the data acquired from the study. The authors would like to express their sincere gratitude to ICAR for providing funds to carry out the research work under ICAR-National Fellow Scheme. The authors are grateful to Dr. Rohit and Dr. Reghu Nandan, Clinical Pathologists, MedHelix Laboratory for doing histopathology analysis and interpretation of the data. The authors are grateful to the Dr. B. Ganesan (Chief Technical Officer, Animal lab facility), Mrs. P. A. Jaya (Technical Officer), Mr. P. Suresh (Senior Technician), Mrs. N. Lekha (Technical Officer) ICAR-Central Institute of Fisheries Technology (CIFT), Cochin, Kerala for providing technical support to carry out the analyses.

Funding

ICAR-National Fellow Scheme.

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Authors and Affiliations

Authors

Contributions

Research concept- Dr. DKV, Dr. RA, Research design- Dr. DKV, Dr. RA, Dr SM, Supervision- Dr RA and Dr SM and Dr CNR, Experiments- Dr. DKV, Dr. PRS, Data analysis and Interpretation- Dr. DKV, Dr. PKD, Ms. MRJ, Dr. RA, Dr SM, Writing article- Dr. DKV, Dr. PKD, Ms. MRJ, Critical review- Dr SM, Dr CNR, Article editing- Dr. PKD, Ms. MRJ, Final approval- Dr SM, Dr CNR.

Corresponding author

Correspondence to Anandan Rangasamy.

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The authors declare that they have no conflict of interest.

Ethics approval

The experimental rats were maintained and performed as per the guidelines on the regulation of scientific experiments on animals of Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA), Govt. of India and approved by the Institutional Animal Ethics Committee of ICAR-Central Institute of Fisheries Technology.

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Vijayan, D.K., Perumcherry Raman, S., Dara, P.K. et al. In vivo anti-lipidemic and antioxidant potential of collagen peptides obtained from great hammerhead shark skin waste. J Food Sci Technol 59, 1140–1151 (2022). https://doi.org/10.1007/s13197-021-05118-0

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