A new insight on copper: Promotion of collagen synthesis and myofiber growth and development in juvenile grass carp (Ctenopharyngodon idella)

Rui Ma; Lin Feng; Pei Wu; Yang Liu; Hong-Mei Ren; Shu-Wei Li; Ling Tang; Cheng-Bo Zhong; Dong Han; Wen-Bing Zhang; Jia-Yong Tang; Xiao-Qiu Zhou; Wei-Dan Jiang

doi:10.1016/j.aninu.2023.06.009

A new insight on copper: Promotion of collagen synthesis and myofiber growth and development in juvenile grass carp (Ctenopharyngodon idella)

Anim Nutr. 2023 Jul 8:15:22-33. doi: 10.1016/j.aninu.2023.06.009. eCollection 2023 Dec.

Authors

Rui Ma¹, Lin Feng^{1

2

3}, Pei Wu^{1

2

3}, Yang Liu^{1

2

3}, Hong-Mei Ren¹, Shu-Wei Li⁴, Ling Tang⁴, Cheng-Bo Zhong⁴, Dong Han⁵, Wen-Bing Zhang⁶, Jia-Yong Tang¹, Xiao-Qiu Zhou^{1

2

3}, Wei-Dan Jiang^{1

2

3}

Affiliations

¹ Animal Nutrition Institute, Sichuan Agricultural University, Chengdu, 611130, China.
² Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, 611130, China.
³ Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education, Ministry of Agriculture and Rural Affairs, Key Laboratory of Sichuan Province, Sichuan, 611130, China.
⁴ Animal Nutrition Institute, Sichuan Academy of Animal Science, Sichuan Animtech Feed Co. Ltd, Chengdu, 610066, Sichuan, China.
⁵ State Key Laboratory of Fresh Water Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China.
⁶ The Key Laboratory of Mariculture, Ministry of Education, The Key Laboratory of Aquaculture Nutrition and Feeds, Ministry of Agriculture, Ocean University of China, Qingdao, 266003, China.

Abstract

Copper (Cu) is a trace element, essential for fish growth. In the current study, in addition to growth performance, we first explored the effects of Cu on collagen synthesis and myofiber growth and development in juvenile grass carp (Ctenopharyngodon idella). A total of 1080 fish (11.16 ± 0.01 g) were randomly divided into 6 treatments (3 replicates per treatment) to receive five doses of organic Cu, which were Cu citrate (CuCit) at 0.99 (basal diet), 2.19, 4.06, 6.15, and 8.07 mg/kg, and one dose of inorganic Cu (CuSO₄·5H₂O at 3.15 mg/kg), for 9 weeks. The results showed appropriate Cu level (4.06 mg/kg) enhanced growth performance, improved nutritional Cu status, and downregulated Cu-transporting ATPase 1 mRNA levels in the hepatopancreas, intestine, and muscle of juvenile grass carp. Meanwhile, collagen content in fish muscle was increased after Cu intake, which was probably due to the following pathways: (1) activating CTGF/TGF-β1/Smads signaling pathway to regulate collagen transcription; (2) upregulating of La ribonucleoprotein domain family 6 (LARP6) mRNA levels to regulate translation initiation; (3) increasing proline hydroxylase, lysine hydroxylase, and lysine oxidase activities to regulate posttranslational modifications. In addition, optimal Cu group increased myofiber diameters and the frequency of myofibers with diameter >50 μm, which might be associated with upregulation of cyclin B, cyclin D, cyclin E, proliferating cell nuclear antigen, myogenic determining factor (MyoD), myogenic factor 5, myogenin (MyoG), myogenic regulatory factor 4 and myosin heavy chain (MyHC) and downregulation of myostatin mRNA levels, increasing protein levels of MyoD, MyoG and MyHC in fish muscle. Finally, based on percentage weight gain (PWG), serum ceruloplasmin (Cp) activity and collagen content in fish muscle, Cu requirements were determined as 4.74, 4.37 and 4.62 mg/kg diet (CuCit as Cu source) of juvenile grass carp, respectively. Based on PWG and Cp activity, compared to CuSO₄·5H₂O, the efficacy of CuCit were 131.80% and 115.38%, respectively. Our findings provide new insights into Cu supplementation to promote muscle growth in fish, and help improve the overall productivity of aquaculture.

Keywords: Collagen synthesis; Copper; Grass carp (Ctenopharyngodon idella); Myofiber.