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Lipid metabolic disorders and physiological stress caused by a high-fat diet have lipid source-dependent effects in juvenile black seabream Acanthopagrus schlegelii

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Abstract

This study was conducted to evaluate the effects of different dietary lipid sources on growth performance, lipid metabolism, and physiological stress responses including oxidative stress (OS) and endoplasmic reticulum stress (ERS) of juvenile Acanthopagrus schlegelii (initial weight 0.88 ± 0.01 g) fed a high-fat diet (HFD). Four isonitrogenous and isolipidic experimental diets containing different lipid sources were formulated: fish oil (FO), palm oil (PO), linseed oil (LO), and soybean oil (SO), respectively. Results indicated that fish fed HFD supplemented with FO significantly improved growth than SO treatment. The high concentrations of aspartate aminotransferase and alanine transaminase were found in HFD supplemented with SO. Fish fed dietary LO supplementation showed significantly lower serum cholesterol, triglyceride, low-density lipoprotein, and high-density lipoprotein contents than those in SO group. Likewise, hepatic paraffin section analysis indicated that HFD with PO or SO supplementation increased fat drop. The expression levels of peroxisome proliferators-activated receptor alpha (pparα) and silent regulator 1 (sirt1) were significantly elevated by HFD with FO or LO supplementation. Additionally, the key marker of OS malonaldehyde was significantly increased in FO and SO groups. ERS-related genes were activated in dietary PO or SO supplementation and, hence, triggering inflammation and apoptosis by promoting the expression levels of nuclear factor kappa B (nf-κb) and c-Jun N-terminal kinase (jnk). Overall, the present study reveals that lipid metabolic disorders and physiological stress caused by a HFD have significant lipid source-dependent effects, which have important guiding significance for the use of HFD in marine fish.

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Data availability

All data generated or analyzed during this study are included in this published article.

Abbreviations

ALT:

Alanine transaminase

AST:

Aspartate aminotransferase

atf6 :

Activating transcription factor 6

bax :

Bcl2-associated X

bcl-2 :

B cell leukemia 2

Cu/Zn-sod :

Cu-Zn superoxide dismutase

DHA:

Docosahexaenoic

EPA:

Eicosapentaenoic acid

ERS:

Endoplasmic reticulum stress

FO:

Fish oil

FW:

Final weight

gpx:

Glutathione peroxidase

grp78 :

Glucose regulated protein 78

GSH-px:

Glutathione peroxidase

HDL-C:

High-density lipoprotein cholesterol

HFD:

High-fat diet

il-10 :

Interleukin-10

il-1β :

Interleukin-1β

ire1α :

Inositol requiring enzyme-1 ɑ;

IW:

Initial weight

jnk :

C-Jun N-terminal kinase

LC-PUFA:

Long-chain polyunsaturated fatty acid

LDL-C:

Low-density lipoprotein cholesterol

LO:

Linseed oil

MDA:

Malonaldehyde

Mn-sod :

Mn superoxide dismutase

n-3 PUFA:

Omega-3 polyunsaturated fatty acid

n-6 PUFA:

Omega-6 polyunsaturated fatty acid

nf-κb :

Nuclear factor kappa B

OS:

Oxidative stress

PO:

Palm oil

pparα :

Perixisome proliferation-activated receptor alpha

SGR:

Specific growth ratio

sirt1 :

Silent regulator 1

SO:

Soybean oil

SOD:

Superoxide dismutase

SR:

Survival rate;

srebp-1 :

Sterol regulatory element-binding protein-1

TC:

Total cholesterol

TG:

Triglyceride

tgfβ :

Transforming growth factor β

tnfα :

Tumor necrosis factor α

UPR:

Unfolded protein response

Vos:

Vegetable oils

WG:

Weight gain

xbp-1 :

X-box binding protein 1

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Funding

This research was supported by the National Natural Science Foundation of China (31802303), National Key R & D Program of China (2018YFD0900400), Scientific Research Foundation of Ningbo University (XYL20007), Fundamental Research Funds for the Provincial Universities of Zhejiang (SJLY2021007), the Open Fund of Zhejiang Provincial Top Key Discipline of Aquaculture in Ningbo University, and K. C. Wong Magna Fund in Ningbo University.

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Authors and Affiliations

  1. Laboratory of Fish and Shellfish Nutrition, School of Marine Sciences, Ningbo University, Ningbo, 315211, China

    Yuedong Shen, Xuejiao Li, Yangguang Bao, Tingting Zhu, Zhaoxun Wu, Bingqian Yang, Lefei Jiao, Qicun Zhou & Min Jin

  2. Key Laboratory of Aquacultural Biotechnology Ministry of Education, Ningbo University, Ningbo, 315211, China

    Yuedong Shen, Xuejiao Li, Yangguang Bao, Tingting Zhu, Zhaoxun Wu, Bingqian Yang, Lefei Jiao, Qicun Zhou & Min Jin

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  1. Yuedong Shen
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  9. Min Jin
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Contributions

Qicun Zhou and Min Jin: conceptualization, methodology, validation and supervision; Yuedong Shen, Xuejiao Li, Yangguang Bao, and Tingting Zhu: formal analysis, software, validation; Zhaoxun Wu, Bingqian Yang, and Lefei Jiao: resources; Yuedong Shen: writing—original draft; Qicun Zhou and Min Jin: writing—reviewing and editing. All authors read and approved the final manuscript.

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Correspondence to Qicun Zhou or Min Jin.

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Animal experimentation within the present study was conducted in accordance with the Animal Research Institute Committee guidelines of Ningbo University, China, and approved by the Committee of Animal Research Institute, Ningbo University, China.

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Shen, Y., Li, X., Bao, Y. et al. Lipid metabolic disorders and physiological stress caused by a high-fat diet have lipid source-dependent effects in juvenile black seabream Acanthopagrus schlegelii. Fish Physiol Biochem 48, 955–971 (2022). https://doi.org/10.1007/s10695-022-01095-z

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