Advertisement

The protective effects of Nile tilapia (Oreochromis niloticus) scale collagen hydrolysate against oxidative stress induced by tributyltin in HepG2 cells

  • Jinpeng Ruan
  • Junde Chen
  • Jie Zeng
  • Zhenggang Yang
  • Chonggang Wang
  • Zhuan Hong
  • Zhenghong Zuo
Research Article
  • 23 Downloads

Abstract

Oxidative stress is regarded as one of the most important factors associated with many diseases, such as atherosclerosis, cancer, and diabetes. Various chemicals are released into the environment, causing environmental pollution. Importantly, many of them may cause damage to organisms through oxidative stress. In this work, we investigated the possible protective effects of Nile tilapia (Oreochromis niloticus) scale collagen hydrolysate (TSCH) (molecular weight approximately 4 kDa) against tributyltin (TBT)-induced oxidative stress in vitro. The results showed that pretreatment with TSCH protected against decreases in cell viability and changes in cell morphology in HepG2 cells exposed to TBT. Treatment with TSCH reduced the TBT-induced elevation in malondialdehyde (MDA) levels in HepG2 cells in a dose-dependent manner. Pretreatment with TSCH increased glutathione reductase (GR) and superoxide dismutase (SOD) activity. Moreover, TSCH decreased the expression of the proapoptotic protein Bax, reducing apoptosis. These results suggest that the protective mechanism of TSCH may be associated with its ability to scavenge MDA, increase antioxidant enzyme activity and downregulate the expression of Bax.

Keywords

Scale collagen hydrolysate Protective effect Tributyltin Oxidative stress 

Notes

Funding

This work was supported by the Ocean Public Welfare Scientific Research Special Appropriation Project (201405017), the Major State Basic Research Development Program of China (Grant Nos. 2017YFA0205201), and the Natural Science Foundation of Fujian Province of China (No. 2018 J01067).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11356_2018_3729_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 14 kb)

References

  1. Ahn CB, Je JY, Cho YS (2012) Antioxidant and anti-inflammatory peptide fraction from salmon byproduct protein hydrolysates by peptic hydrolysis. Food Res Int 49:92–98CrossRefGoogle Scholar
  2. Ahn CB, Kim JG, Je JY (2014) Purification and antioxidant properties of octapeptide from salmon byproduct protein hydrolysate by gastrointestinal digestion. Food Chem 147:78–83CrossRefGoogle Scholar
  3. Al-Gubory KH (2014) Environmental pollutants and lifestyle factors induce oxidative stress and poor prenatal development. Reprod BioMed Online 29:17–31CrossRefGoogle Scholar
  4. Antizar-Ladislao B (2008) Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review Environ Int 34:292–308CrossRefGoogle Scholar
  5. Barange M, Merino G, Blanchard JL, Scholtens J, Harle J, Allison EH, Allen JI, Holt J, Jennings S (2014) Impacts of climate change on marine ecosystem production in societies dependent on fisheries. Nat Clim Chang 4:211–216CrossRefGoogle Scholar
  6. Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE (2014) Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev 94:329–354CrossRefGoogle Scholar
  7. Blanco M, Vázquez JA, Pérez-Martín RI, Sotelo CG (2017) Hydrolysates of fish skin collagen: an opportunity for valorizing fish industry byproducts. Mar Drugs 15:131CrossRefGoogle Scholar
  8. Celep E, Aydın A, Kırmızıbekmez H, Yesilada E (2013) Appraisal of in vitro and in vivo antioxidant activity potential of cornelian cherry leaves. Food Chem Toxicol 62:448–455CrossRefGoogle Scholar
  9. Chen YW, Lan KC, Tsai JR, Weng TI, Yang CY, Liu SH (2017) Tributyltin exposure at noncytotoxic doses dysregulates pancreatic β-cell function in vitro and in vivo. Arch Toxicol 91:1–10CrossRefGoogle Scholar
  10. Czabotar PE, Lessene G, Strasser A, Adams JM (2014) Control of apoptosis by the Bcl-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 15:49–63CrossRefGoogle Scholar
  11. Duan X, Ocen D, Wu F, Li M, Yang N, Xu J, Chen H, Huang L, Jin Z, Xu X (2014) Purification and characterization of a natural antioxidant peptide from fertilized eggs. Food Res Int 56:18–24CrossRefGoogle Scholar
  12. Farvin KS, Andersen LL, Nielsen HH, Jacobsen C, Jakobsen G, Johansson I, Jessen F (2014) Antioxidant activity of cod (Gadus morhua) protein hydrolysates: in vitro assays and evaluation in 5% fish oil-in-water emulsion. Food Chem 149:326–334CrossRefGoogle Scholar
  13. García-Nebot MJ, Recio I, Hernández-Ledesma B (2014) Antioxidant activity and protective effects of peptide lunasin against oxidative stress in intestinal Caco-2 cells. Food Chem Toxicol 65:155–161CrossRefGoogle Scholar
  14. Gennari A, Viviani B, Galli CL, Marinovich M, Pieters R, Corsini E (2000) Organotins induce apoptosis by disturbance of [Ca2+]i and mitochondrial activity, causing oxidative stress and activation of caspases in rat thymocytes. Toxicol Appl Pharm 169:185–190CrossRefGoogle Scholar
  15. Ghassem M, Arihara K, Mohammadi S, Sani NA, Babji AS (2017) Identification of two novel antioxidant peptides from edible bird's nest (Aerodramus fuciphagus) protein hydrolysates. Food Funct 8:2046–2052CrossRefGoogle Scholar
  16. Girgih AT, He R, Hasan FM, Udenigwe CC, Gill TA, Aluko RE (2015) Evaluation of the in vitro antioxidant properties of a cod (Gadus morhua) protein hydrolysate and peptide fractions. Food Chem 173:652–659CrossRefGoogle Scholar
  17. Graceli JB, Sena GC, Lopes PF, Zamprogno GC, Da CM, Godoi AF, Dos Santos DM, de Marchi MR, Ma DSF (2013) Organotins: a review of their reproductive toxicity, biochemistry, and environmental fate. Reprod Toxicol 36:40–52CrossRefGoogle Scholar
  18. Huang CF, Yang CY, Tsai JR, Wu CT, Liu SH, Lan KC (2018) Low-dose tributyltin exposure induces an oxidative stress-triggered JNK-related pancreatic β-cell apoptosis and a reversible hypoinsulinemic hyperglycemia in mice. Sci Rep 8:5734CrossRefGoogle Scholar
  19. Ishihara Y, Fujitani N, Kawami T, Adachi C, Ishida A, Yamazaki T (2014) Suppressive effects of 17beta-estradiol on tributyltin-induced neuronal injury via Akt activation and subsequent attenuation of oxidative stress. Life Sci 99:24–30CrossRefGoogle Scholar
  20. Liang R, Zhang Z, Lin S (2017) Effects of pulsed electric field on intracellular antioxidant activity and antioxidant enzyme regulating capacities of pine nut (Pinus koraiensis) peptide QDHCH in HepG2 cells. Food Chem 237:793–802CrossRefGoogle Scholar
  21. Lima CF, Fernandesferreira M, Pereirawilson C (2006) Phenolic compounds protect HepG2 cells from oxidative damage: relevance of glutathione levels. Life Sci 79:2056–2068CrossRefGoogle Scholar
  22. Lin S, Liang R, Li X, Xing J, Yuan Y (2016) Effect of pulsed electric field (PEF) on structures and antioxidant activity of soybean source peptides-SHCMN. Food Chem 213:588–594CrossRefGoogle Scholar
  23. Liu J, Chen Z, He J, Zhang Y, Zhang T, Jiang Y (2014) Anti-oxidative and anti-apoptosis effects of egg white peptide, Trp-Asn-Trp-Ala-Asp, against H2O2-induced oxidative stress in human embryonic kidney 293 cells. Food Funct 5:3179–3188CrossRefGoogle Scholar
  24. Malomo SA, Onuh JO, Girgih AT, Aluko RE (2015) Structural and antihypertensive properties of enzymatic hemp seed protein hydrolysates. Nutrients 7:7616–7632CrossRefGoogle Scholar
  25. Maqbool F, Mostafalou S, Bahadar H, Abdollahi M (2016) Review of endocrine disorders associated with environmental toxicants and possible involved mechanisms. Life Sci 145:265–273CrossRefGoogle Scholar
  26. Meng D, Zhang P, Zhang L, Wang H, Ho CT, Li S, Shahidi F, Zhao H (2017) Detection of cellular redox reactions and antioxidant activity assays. J Funct Foods 37:467–479CrossRefGoogle Scholar
  27. Mitra S, Gera R, Siddiqui WA, Khandelwal S (2013b) Tributyltin induces oxidative damage, inflammation and apoptosis via disturbance in blood-brain barrier and metal homeostasis in cerebral cortex of rat brain: an in vivo and in vitro study. Toxicology 310:39–52CrossRefGoogle Scholar
  28. Mitra S, Srivastava A, Khandelwal S (2013a) Tributyltin chloride induced testicular toxicity by JNK and p38 activation, redox imbalance and cell death in sertoli-germ cell co-culture. Toxicology 314:39–50CrossRefGoogle Scholar
  29. Nazeer RA, Kumar NS, Ganesh RJ (2012) In vitro and in vivo studies on the antioxidant activity of fish peptide isolated from the croaker (Otolithes ruber) muscle protein hydrolysate. Peptides 35:261–268CrossRefGoogle Scholar
  30. Nordberg J, Arner ES (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radical Bio Med 31:1287–1312CrossRefGoogle Scholar
  31. Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74CrossRefGoogle Scholar
  32. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990CrossRefGoogle Scholar
  33. Saidi S, Deratani A, Belleville M-P, Amar RB (2014) Antioxidant properties of peptide fractions from tuna dark muscle protein by-product hydrolysate produced by membrane fractionation process. Food Res Int 65:329–336CrossRefGoogle Scholar
  34. Soboń A, Szewczyk R, Długoński J (2016) Tributyltin (TBT) biodegradation induces oxidative stress of Cunninghamella echinulata. Int Biodeter Biodegr 107:92–101CrossRefGoogle Scholar
  35. Sudhakar S, Nazeer RA (2015) Structural characterization of an Indian squid antioxidant peptide and its protective effect against cellular reactive oxygen species. J Funct Foods 14:502–512CrossRefGoogle Scholar
  36. Tang CH, Chihsin H, Wang WH (2010) Butyltin accumulation in marine bivalves under field conditions in Taiwan. Mar Environ Res 70:125–132CrossRefGoogle Scholar
  37. Théolier J, Hammami R, Labelle P, Fliss I, Jean J (2013) Isolation and identification of antimicrobial peptides derived by peptic cleavage of whey protein isolate. J Funct Foods 5:706–714CrossRefGoogle Scholar
  38. Torres-Fuentes C, Contreras MDM, Recio I, Alaiz M, Vioque J (2015) Identification and characterization of antioxidant peptides from chickpea protein hydrolysates. Food Chem 180:194–202CrossRefGoogle Scholar
  39. Volk APD, Moreland JG (2014) ROS-containing endosomal compartments: implications for signaling. Method Enzymol 535:201–224CrossRefGoogle Scholar
  40. Wang L, Ding L, Yu Z, Zhang T, Ma S, Liu J (2016) Intracellular ROS scavenging and antioxidant enzyme regulating capacities of corn gluten meal-derived antioxidant peptides in HepG2 cells. Food Res Int 90:33–41CrossRefGoogle Scholar
  41. Wattanasiritham L, Theerakulkait C, Wickramasekara S, Maier CS, Stevens JF (2016) Isolation and identification of antioxidant peptides from enzymatically hydrolyzed rice bran protein. Food Chem 192:156–162CrossRefGoogle Scholar
  42. Whalen MM, Loganathan BG, Kannan K (1999) Immunotoxicity of environmentally relevant concentrations of butyltins on human natural killer cells in vitro. Environ Res 81:108–116CrossRefGoogle Scholar
  43. Winterbourn CC (2014) The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Bba-Gen Subjects 1840:730–738CrossRefGoogle Scholar
  44. Yarnpakdee S, Benjakul S, Kristinsson HG, Bakken HE (2015) Preventive effect of Nile tilapia hydrolysate against oxidative damage of HepG2 cells and DNA mediated by H2O2 and AAPH. J Food Sci Technol 52:6194–6205CrossRefGoogle Scholar
  45. Zeng J, Zhang Y, Ruan J, Yang Z, Wang C, Hong Z, Zuo Z (2018) Protective effects of fucoxanthin and fucoxanthinol against tributyltin-induced oxidative stress in HepG2 cells. Environ Sci Pollut Res 25:5582–5589CrossRefGoogle Scholar
  46. Zeng WC, Sun Q, Zhang WH, Liao X-P, Shi B (2017) Antioxidant activity in vivo and biological safety evaluation of a novel antioxidant peptide from bovine hair hydrolysates. Process Biochem 56:193–198CrossRefGoogle Scholar
  47. Zhang Y, Chen Y, Sun L, Liang J, Guo Z, Xu L (2014) Protein phosphatases 2A as well as reactive oxygen species involved in tributyltin-induced apoptosis in mouse livers. Environ Toxicol 29:234–242CrossRefGoogle Scholar
  48. Zhou M, Feng M, Fu LL, Ji LD, Zhao JS, Xu J (2016) Toxicogenomic analysis identifies the apoptotic pathway as the main cause of hepatotoxicity induced by tributyltin. Food Chem Toxicol 97:316–326CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, School of Life SciencesXiamen UniversityXiamenChina
  2. 2.Engineering Research Center of Marine Biological Resource Comprehensive UtilizationThird Institute of Oceanography, State Oceanic AdministrationXiamenChina
  3. 3.Fujian Collaborative Innovation Center for Exploitation and Utilization of Marine Biological ResourcesXiamenChina

Personalised recommendations