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Cascading Mechanism Triggering the Activation of Polyphenol Oxidase Zymogen in Shrimp Litopenaeus vannamei After Postmortem and the Correlation with Melanosis Development

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Abstract

Melanization is the major deterioration in organoleptic quality of shrimp Litopenaeus vannamei during cold storage and leads to dramatical reduction of commercial value. So far, the biochemical cascade mechanism triggering and accelerating melanosis progression remains unclear. Herein, this investigation aimed to monitor the melanosis development in L. vannamei during 5 days’ cold storage at 4 °C and to explore the role of serine protease (SP) in zymogen activation of polyphenol oxidase (PPO) by application of low field nuclear magnetic resonance (LF-NMR), transmission electron microscopy (TEM), and immunohistochemistry (IHC). The results showed that melanosis development was positively associated with the increase of PPO and SP activities, and the utmost melanization was observed at cephalothorax segment, following with the telson and abdomen. Besides, LF-NMR relaxometry revealed both a dramatical reduction in trapped water component T22 and a significant increase in free water component T23. Meanwhile, the histopathological findings of hepatopancreas tissue demonstrated the progressive disruption in cytoarchitecture. Along with the increase of T23 and cytoarchitecture disruption, SP and Ca2+ were arbitrarily disseminated in hepatopancreas tissue. In addition, a heat map analysis revealed that there was a highly positive relationship between melanosis development and the aberrant elevation of PPO and SP activities, ratio of T22 components, cytoarchitecture disruption level, and dissemination status of SP and Ca2+. Altogether, the biochemical cascade events for melanosis development of L. vannamei during cold storage could be sketched out; i.e., the cytoarchitecture disruption, in combination with the driving force of free water molecule migration, was greatly favorable for aggregation of SP, Ca2+, and PPO zymogen, following with aberrant activation of PPO zymogen and initiation of melanization. These data provide new insights into the biochemical cascade mechanism of melanosis development in L. vannamei during cold storage and pave new ways for target controlling of melanization at initial stage.

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References

  • Ahn, C. W., Lee, M. J., & Jeung, E. B. (2017). Expression and localization of equine tissue-specific divalent ion-transporting channel proteins. Journal of Equine Veterinary Science, 59, 14–25.

    Article  Google Scholar 

  • Alparslan, Y., & Baygar, T. (2017). Effect of chitosan film coating combined with orange peel essential oil on the shelf life of deepwater pink shrimp. Food Bioprocess Technology, 10, 842–853.

    Article  CAS  Google Scholar 

  • Amparyup, P., Jitvaropas, R., Pulsook, N., & Tassanakajon, A. (2007). Molecular cloning, characterization and expression of a masquerade-like serine proteinase homologue from black tiger shrimp Penaeus monodon. Fish & Shellfish Immunology, 22, 535–546.

    Article  CAS  Google Scholar 

  • Arancibia, M. Y., Lopez-Caballero, M. E., Gomez-Guill, M. C., & Montero, P. (2015). Chitosan coatings enriched with active shrimp waste for shrimp preservation. Food Control, 54, 259–266.

    Article  CAS  Google Scholar 

  • Benjakul, S., Visessanguan, W., & Tanaka, M. (2005). Properties of phenoloxidase isolated from the cephalothorex of kuruma prawn (Penaeus japonicus). Journal of Food Biochemistry, 29, 470–485.

    Article  CAS  Google Scholar 

  • Bradford, M. (1976). A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

  • Buda, S., Elizabeth, S., & Thomas, H. (2005). Expression of a serine proteinase homolog prophenoloxidase-activating factor from the blue crab, Callinectes sapidus. Comparative Biochemistry and Physiology. part: B, 140, 521–531.

    Article  CAS  Google Scholar 

  • Chiu, C. H., Gu, Y. K., Liu, C. H., Pan, T. M., & Cheng, W. (2007). Immune responses and gene expression in Pacific white shrimps, Litopenaeus vannamei, induced by Lactobacillus plantarum. Fish & Shellfish Immunology, 23, 364–377.

    Article  CAS  Google Scholar 

  • Dai, X. Y., Zhang, M. X., Wei, X. Y., Hider, R. C., & Zhou, T. (2016). Novel multifunctional hydroxypyridinone derivatives as potential shrimp preservatives. Food Bioprocess Technology, 9, 1079–1088.

    Article  CAS  Google Scholar 

  • Encarnacion, A. B., Orapint, F. F., Wanchai, J., Ikuo, W., & Toshiaki, H. O. (2012). Application of ergothioneine-rich extract from an edible mushroom Flammulina velutipes for melanosis prevention in shrimp, Penaeus monodon and Litopenaeus vannamei. Food Research International, 45, 232–237.

    Article  CAS  Google Scholar 

  • Erikson, U., Veliyulin, E., Singstad, T. E., & Aursand, M. (2004). Salting and desalting of fresh and frozen-thawed cod (Gadus morhua) fillets: a comparative study using 23 Na NMR, 23Na MRI, low-field 1H NMR, and physicochemical analytical methods. Journal of Food Science, 69, 107–114.

    Article  Google Scholar 

  • Geng, S., Wang, H., Wang, X., Ma, X., Xiao, S., Wang, & Tan, J. M. (2015). A non-invasive NMR and MRI method to analyze the rehydration of dried sea cucumber. Analytical Methods, 7, 2413–2419.

    Article  CAS  Google Scholar 

  • Gokoglu, N., & Yerlikaya, P. (2008). Inhibition effects of grape seed extracts on melanosis formation in shrimp (Parapenaeus longirostris). International Journal of Food Science & Technology, 43, 1004–1008.

    Article  CAS  Google Scholar 

  • Han, M. Y., Wang, P., Xu, X. L., & Zhou, G. H. (2014). Low-field NMR study of heat-induced gelation of pork myofibrillar proteins and its relationship with microstructural characteristics. Food Research International, 62, 1175–1182.

    Article  CAS  Google Scholar 

  • Hu, Y., Ji, R., Jiang, H., Zhang, J., Chen, J., & Ye, X. (2012). Participation of cathepsin L in modori phenomenon in carp (Cyprinus carpio) surimi gel. Food Chemistry, 134, 2014–2020.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, H. B., Wang, Y., Yu, X. Q., Zhu, Y. F., & Kanost, M. (2003). Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochemistry and Molecular Biology, 33, 1049–1060.

    Article  CAS  PubMed  Google Scholar 

  • José-Pablo, Z., Martínez-Álvarez, O., Montero, P., & del Gómez-Guillén, C. M. (2009). Characterisation and tissue distribution of polyphenol oxidase of deepwater pink shrimp (Parapenaeus longirostris). Food Chemistry, 112, 104–111.

    Article  CAS  Google Scholar 

  • Kaur, B. P., Kaushik, N., Rao, P. S., & Chauhan, O. P. (2013). Effect of high-pressure processing on physical, biochemical, and microbiological characteristics of black tiger shrimp (Penaeus monodon). Food Bioprocess Technology, 6, 1390–1400.

    Article  Google Scholar 

  • Li, E. C., Chen, L. Q., Zeng, C. N., Yu, Z. Q., Xiong, Chen, X. F., & Qin, J. G. (2008). Comparison of digestive and antioxidant enzymes activities, haemolymph oxyhemocyanin contents and hepatopancreas histology of white shrimp, Litopenaeus vannamei, at various salinities. Aquaculture, 274, 80–86.

    Article  CAS  Google Scholar 

  • Li, C. B., Liu, D. Y., Zhou, G. H., Xu, X. L., Qi, J., Shi, P. L., & Xia, T. L. (2012). Meat quality and cooking attributes of thawed pork with different low field NMR T21. Meat Science, 92, 79–83.

    Article  PubMed  Google Scholar 

  • Li, M., Li, B., & Zhang, W. J. (2018). Rapid and non-invasive detection and imaging of the hydrocolloid-injected prawns with low-field NMR and MRI. Food Chemistry, 242, 16–21.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y. J., Hou, F. J., Wang, X. Z., & Liu, X. L. (2015a). Recombinant expression and characterization of a serine protease inhibitor (Lvserpin 7) from the Pacific white shrimp, Litopenaeus vannamei. Fish & Shellfish Immunology, 42, 256–263.

    Article  CAS  Google Scholar 

  • Liu, P. F., Liu, Q. H., Wu, Y., & Jie, H. (2015b). A pilot metabolic profiling study in hepatopancreas of Litopenaeus vannamei with white spot syndrome virus based on 1H- NMR spectroscopy. Journal of Invertebrate Pathology, 124, 51–56.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y. J., Liu, T., Hou, F. J., Wang, X. Z., & Liu, X. L. (2016). Lvserpin 3 is involved in shrimp innate immunity via the inhibition of bacterial proteases and proteases involved in prophenoloxidase system. Fish & Shellfish Immunology, 48, 128–135.

    Article  CAS  Google Scholar 

  • Liu, Y. J., Sun, Y. H., Wang, Q., Hou, F. J., & Liu, X. L. (2017). Identification and functional characterizations of serpin 8, a potential prophenoloxidase-activating protease inhibitor in Pacific white shrimp, Litopenaeus vannamei. Fish & Shellfish Immunology, 60, 492–501.

    Article  CAS  Google Scholar 

  • Lopez-Caballero, M., Martínez-Alvarez, O., Gomez-Guillen, M., & Montero, P. (2007). Quality of thawed deepwater pink shrimp (Parapenaeus longirostris) treated with melanosis-inhibiting formulations during chilled storage. International Journal of Food Science & Technology, 42, 1029–1038.

    Article  CAS  Google Scholar 

  • Luna-Acosta, A., Thomas-Guyon, H., Amari, M., Rosenfeld, E., Bustamante, P., & Fruitier-Arnaudin, I. (2011). Differential tissue distribution and specificity of phenoloxidases from the Pacific oyster Crassostrea gigas. Comparative Biochemistry and Physiology Part: B, 159, 220–226.

    Article  CAS  Google Scholar 

  • Manheem, K., Benjakul, S., Kijroongrojana, K., & Visessanguan, W. (2012). The effect of heating conditions on polyphenol oxidase, proteases and melanosis in pre-cooked Pacific white shrimp during refrigerated storage. Food Chemistry, 131, 1370–1375.

    Article  CAS  Google Scholar 

  • Montero, P., Lopez-Caballero, M. E., & Perez-Mateos, M. (2001). The effect of inhibitors and high-pressure treatment to prevent melanosis and microbial growth on chilled prawns (Penaeus japonicus). Journal of Food Science, 66, 1201–1206.

    Article  CAS  Google Scholar 

  • Nirmal, N. P., & Benjaku, S. (2009). Effect of ferulic acid on inhibition of polyphenoloxidase and quality changes of Pacific white shrimp (Litopenaeus vannamei) during iced storage. Food Chemistry, 116, 323–331.

    Article  CAS  Google Scholar 

  • Nunes, E. T., Braga, A. A., & Camargo-Mathias, M. I. (2014). Histochemical study of the hepatopancreas in adult females of the pink-shrimp Farfantepenaeus brasiliensis Latreille, 1817. Acta Histochemistry, 116, 243–251.

    Article  CAS  Google Scholar 

  • Perazzolo, M. L., & Barracco, A. M. (1997). The prophenoloxidase activating system of the shrimp Penaeus paulensi and associated factors. Developmental and Comparative Immunology, 21, 385–395.

    Article  CAS  PubMed  Google Scholar 

  • Reis, C. V., Kelen, E. M. A., Farsky, S. H. P., Portaro, F. C. V., Sampaio, C. A. M., Fernandes, B. L. A. C., Camargo, M., & Chudzinski-Tavassi, A. M. A. (1999). Ca2+ activated serine protease (LOPAP) could be responsible for the hemorrhagic syndrome caused by the caterpillar Lonomia oblique. Lancet, 353, 1942.

    Article  CAS  PubMed  Google Scholar 

  • Romano, N., Koh, C. B., & Ng, W. K. (2015). Dietary microencapsulated organic acids blend enhances growth, phosphorus utilization, immune response, hepatopancreatic integrity and resistance against Vibrio harveyi in white shrimp, Litopenaeus vannamei. Aquaculture, 435, 228–236.

    Article  CAS  Google Scholar 

  • Sánchez-Alonso, I., Martinez, I., Sánchez-Valencia, J., & Careche, M. (2012). Estimation of freezing storage time and quality changes in hake (Merluccius merluccius, L.) by low field NMR. Food Chemistry, 135, 1626–1634.

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Alonso, I., Moreno, P., & Careche, M. (2014). Low field nuclear magnetic resonance (LF-NMR) relaxometry in hake (Merluccius merluccius, L.) muscle after different freezing and storage conditions. Food Chemistry, 153, 250–257.

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Valencia, J., Sánchez-Alonso, I., Martínez, I., & Careche, M. (2014). Estimation of frozen storage time or temperature by kinetic modeling of the Kramer shear resistance and water holding capacity (WHC) of hake (Merluccius merluccius, L.) muscle. Journal of Food Engineering, 120, 37–43.

    Article  Google Scholar 

  • Shao, J. H., Deng, Y. M., Song, L., Batur, A., Jia, N., & Liu, D. Y. (2016). Investigation the effects of protein hydration states on the mobility water and fat in meat batters by LF-NMR technique. LWT-Food Science Technology, 66, 1–6.

    Article  CAS  Google Scholar 

  • Singh, A., & Benjakul, S. (2018). Proteolysis and its control using protease inhibitors in fish and fish products: a review. Comprehensive Review in Food Science and Food Safety, 17, 496–509.

    Article  CAS  Google Scholar 

  • Somprasong, N., Rimphanitchayakit, V., & Tassanakajon, A. (2006). A five-domain Kazal-type serine proteinase inhibitor from black tiger shrimp Penaeus monodon and its inhibitory activities. Developmental & Comparative Immunology, 30, 998–1008.

    Article  CAS  Google Scholar 

  • Visetnan, S., Donpudsa, S., & Supungul, P. A. (2009). Tassanakajon, V. Rimphanitchayakit, Kazal-type serine proteinase inhibitors from the black tiger shrimp Penaeus monodon and the inhibitory activities of SPIPm4 and 5. Fish & Shellfish Immunology, 27, 266–274.

    Article  CAS  Google Scholar 

  • Wang, Y. B., Liu, L., Zhou, J. R., Ruan, X. M., Lin, J. D., & Fu, L. L. (2015a). Effect of chitosan nanoparticle coatings on the quality changes of postharvest white leg shrimp, Litopenaeus vannamei, during storage at 4 °C. Food Bioprocess Technology, 8, 907–915.

    Article  CAS  Google Scholar 

  • Wang, M., Wang, J. J., Sun, X. H., Pan, Y. J., & Zhao, Y. (2015b). Preliminary mechanism of acidic electrolyzed water ice on improving the quality and safety of shrimp. Food Chemistry, 176, 333–341.

    Article  CAS  PubMed  Google Scholar 

  • Wu, J. P., Chen, H. C., & Huang, D. J. (2008). Histopathological and biochemical evidence of hepatopancreatic toxicity caused by cadmium and zinc in the white shrimp, Litopenaeus vannamei. Chemosphere, 73, 1019–1026.

    Article  CAS  PubMed  Google Scholar 

  • Xu, Z. H., Regenstein, J. M., Xie, D. D., Lu, W. J., Ren, X. C., Yuan, J. J., & Mao, L. C. (2018a). The oxidative stress and antioxidant responses of Litopenaeus vannamei to low temperature and air exposure. Fish & Shellfish Immunology, 72, 564–571.

    Article  CAS  Google Scholar 

  • Xu, D. F., Sun, L. J., Li, C. H., Wang, Y. L., & Ye, R. Y. (2018b). Inhibitory effect of glucose oxidase from Bacillus sp. CAMT22370 on the quality deterioration of Pacific white shrimp during cold storage. LWT-Food Science and Technology, 92, 339–346.

    Article  CAS  Google Scholar 

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Funding

The authors received financial support from the National Natural Science Foundation (No. 31201309, 31772048 and 31371777) and the Key Laboratory of Aquatic Products Processing, Ministry of Agriculture, South China Sea Fisheries Research Institute Key Laboratory of Fishery Products Processing, Ministry of Agriculture, People’s Republic of China (No. NYJG201404) and the Natural Science Foundation of Guangdong Ocean University (No. C16396).

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Authors and Affiliations

  1. College of Food Science and Technology, Guangdong Provincial Key Laboratory of Aquatic Product Processing and Safety, Guangdong Provincial Engineering Technology Research Center of Marine Food, Key Laboratory of Advanced Processing of Aquatic Products of Guangdong Higher Education Institution, Guangdong Ocean University, Zhanjiang, 524088, China

    Defeng Xu, Yaling Wang & Lijun Sun

  2. Key Laboratory of Aquatic Products Processing, Ministry of Agriculture and Rural Affairs, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, 510300, China

    Xianqing Yang

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  1. Defeng Xu
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Correspondence to Xianqing Yang or Yaling Wang.

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Research Highlights

1. Biochemical cascade mechanism underlying melanosis development of L. vannamei during storage was investigated.

2. Melanosis development was highly associated with the elevation of PPO and SP activity in hepatopancreas tissue.

3. Gradual disintegration of cytoarchitecture in hepatopancreas tissue was observed using HC and TEM.

4. Both the significant decrease in T22 and increase in T23 components were determined by LF-NMR.

5. Cytoarchitecture disruption and free water molecule migration droved dissemination of sarcoplasmic reticulum SP and Ca2+.

6. Heat map analysis demonstrated the significant correlation between melanosis development and biochemical indicators.

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Xu, D., Yang, X., Wang, Y. et al. Cascading Mechanism Triggering the Activation of Polyphenol Oxidase Zymogen in Shrimp Litopenaeus vannamei After Postmortem and the Correlation with Melanosis Development. Food Bioprocess Technol 13, 1131–1145 (2020). https://doi.org/10.1007/s11947-020-02435-8

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