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Expressions and characterization of MuRFs, Atrogin-1, F-box25 genes in tilapia, Oreochromis niloticus, in response to starvation

  • Walaa M. Shaalan
  • Nassr Allah Abd El-Hameid
  • Sabry S. El-Serafy
  • Mohamed SalemEmail author
Article

Abstract

Muscle accretion is affected by the difference between protein synthesis and its degradation. Studies on different species revealed that muscle proteolysis is mediated by different pathways including the ubiquitin-proteasome pathway in which the ubiquitin protein ligases play an important role. These muscle atrophy associated ligases were not well studied in tilapia. In this study, we characterized the ubiquitin protein ligases MuRF1/2/3, Atrogin-1 and F-box25, members of the ubiquitin-proteasome pathway in tilapia, Oreochromis niloticus, and their expressions in the muscle of starved, fed, refed, and control fish. Sequences of these genes revealed presence of Ring finger, B-box, and Cos domains in all MuRF genes, as well as F-box domain in Atrogin-1 and F-box25 genes. Real-time qPCR data analysis showed that expression of MuRF1/2/3, Atrogin-1, F-box25, and proteasome complex genes was significantly upregulated in starved fish compared to fed fish. Concurrently, the proteasome activity was 1.7-folds elevated in the starved fish compared to fed fish. These results confirm the important role of these genes in muscle degradation and suggest potential usage as markers of muscle accretion in tilapia.

Keywords

Tilapia MuRFs Atrogin-1 F-box25 Proteolysis Proteasome 

Notes

Funding

This project was funded by the Ministry of higher education, Egyptian government.

References

  1. Aanyu M, Ganda E, Richard D, Musimbi Constantine F, Ondhoro C (2017) Feeding chart for semi-intensive pond production of Nile Tilapia (Oreochromis niloticus) fed on a plant-based diet and economic performanceGoogle Scholar
  2. Ali A, Al-Tobasei R, Kenney B, Leeds TD, Salem M (2018) Integrated analysis of lncRNA and mRNA expression in rainbow trout families showing variation in muscle growth and fillet quality traits. Sci Rep-Uk 8:12111.  https://doi.org/10.1038/s41598-018-30655-8 CrossRefGoogle Scholar
  3. Bodine SC, Baehr LM (2014) Skeletal muscle atrophy and the E3 ubiquitin ligases MuRF1 and MAFbx/atrogin-1. Am J Physiol Endocrinol Metab 307:E469–E484.  https://doi.org/10.1152/ajpendo.00204.2014 CrossRefGoogle Scholar
  4. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, Dechiara TM, Stitt TN, Yancopoulos GD, Glass DJ (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704–1708.  https://doi.org/10.1126/science.1065874 CrossRefGoogle Scholar
  5. Bonaldo P, Sandri M (2013) Cellular and molecular mechanisms of muscle atrophy. Dis Model Mech 6:25–39.  https://doi.org/10.1242/dmm.010389 CrossRefGoogle Scholar
  6. Borden KL (1998) RING fingers and B-boxes: zinc-binding protein-protein interaction domains. Biochem Cell Biol 76:351–358CrossRefGoogle Scholar
  7. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ (2007) The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6:376–385.  https://doi.org/10.1016/j.cmet.2007.09.009 CrossRefGoogle Scholar
  8. Cleveland BM, Evenhuis JP (2010) Molecular characterization of atrogin-1/F-box protein-32 (FBXO32) and F-box protein-25 (FBXO25) in rainbow trout (Oncorhynchus mykiss): expression across tissues in response to feed deprivation. Comp Biochem Physiol B Biochem Mol Biol 157:248–257.  https://doi.org/10.1016/j.cbpb.2010.06.010 CrossRefGoogle Scholar
  9. De Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, Maganaris CN, Maffulli N, Movin T, Narici MV, Rennie MJ (2007) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585:241–251.  https://doi.org/10.1113/jphysiol.2007.142828 CrossRefGoogle Scholar
  10. Dehoux M, Van Beneden R, Pasko N, Lause P, Verniers J, Underwood L, Ketelslegers JM, Thissen JP (2004) Role of the insulin-like growth factor I decline in the induction of atrogin-1/MAFbx during fasting and diabetes. Endocrinology 145:4806–4812.  https://doi.org/10.1210/en.2004-0406 CrossRefGoogle Scholar
  11. Fareed MU, Evenson AR, Wei W, Menconi M, Poylin V, Petkova V, Pignol B, Hasselgren PO (2006) Treatment of rats with calpain inhibitors prevents sepsis-induced muscle proteolysis independent of atrogin-1/MAFbx and MuRF1 expression. Am J Physiol Regul Integr Comp Physiol 290:R1589–R1597.  https://doi.org/10.1152/ajpregu.00668.2005 CrossRefGoogle Scholar
  12. Fielitz J, Van Rooij E, Spencer JA, Shelton JM, Latif S, Van Der Nagel R, Bezprozvannaya S, De Windt L, Richardson JA, Bassel-Duby R, Olson EN (2007) Loss of muscle-specific RING-finger 3 predisposes the heart to cardiac rupture after myocardial infarction. Proc Natl Acad Sci U S A 104:4377–4382.  https://doi.org/10.1073/pnas.0611726104 CrossRefGoogle Scholar
  13. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98:14440–14445.  https://doi.org/10.1073/pnas.251541198 CrossRefGoogle Scholar
  14. Jagoe RT, Lecker SH, Gomes M, Goldberg AL (2002) Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J 16:1697–1712.  https://doi.org/10.1096/fj.02-0312com CrossRefGoogle Scholar
  15. Kõressaar T, Lepamets M, Kaplinski L, Raime K, Andreson R, Remm M (2018) Primer3_masker: integrating masking of template sequence with primer design software. Bioinformatics. 34:1937–1938.  https://doi.org/10.1093/bioinformatics/bty036 CrossRefGoogle Scholar
  16. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18:39–51.  https://doi.org/10.1096/fj.03-0610com CrossRefGoogle Scholar
  17. Macqueen DJ, Fuentes EN, Valdés JA, Molina A, Martin SaM (2014) The vertebrate muscle-specific RING finger protein family includes MuRF4 – a novel, conserved E3-ubiquitin ligase. FEBS Lett 588:4390–4397.  https://doi.org/10.1016/j.febslet.2014.10.008 CrossRefGoogle Scholar
  18. Meng L, Mohan R, Kwok BH, Elofsson M, Sin N, Crews CM (1999) Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc Natl Acad Sci U S A 96:10403–10408CrossRefGoogle Scholar
  19. Mzengereza K (2016) Apparent Nutrient Digestibility of Plant Based Diets by Tilapia rendalli(Boulenger, 1896)Google Scholar
  20. Nebo C, Overturf K, Brezas A, Dal-Pai-Silva M, Portella MC (2017) Alteration in expression of atrogenes and IGF-1 induced by fasting in Nile tilapia Oreochromis niloticus juveniles. Int Aquat Res 9:361–372.  https://doi.org/10.1007/s40071-017-0182-1 CrossRefGoogle Scholar
  21. Okamoto T, Torii S, Machida S (2011) Differential gene expression of muscle-specific ubiquitin ligase MAFbx/Atrogin-1 and MuRF1 in response to immobilization-induced atrophy of slow-twitch and fast-twitch muscles. J Physiol Sci 61:537–546.  https://doi.org/10.1007/s12576-011-0175-6 CrossRefGoogle Scholar
  22. Paneru B, Ali A, Al-Tobasei R, Kenney B, Salem M (2018) Crosstalk among lncRNAs, microRNAs and mRNAs in the muscle 'degradome' of rainbow trout. Sci Rep-Uk 8:8416.  https://doi.org/10.1038/s41598-018-26753-2 CrossRefGoogle Scholar
  23. Perera S, Mankoo B, Gautel M (2012) Developmental regulation of MURF E3 ubiquitin ligases in skeletal muscle. J Muscle Res Cell Motil 33:107–122.  https://doi.org/10.1007/s10974-012-9288-7 CrossRefGoogle Scholar
  24. Salem M, Nath J, Rexroad CE, Killefer J, Yao J (2005) Identification and molecular characterization of the rainbow trout calpains (Capn1 and Capn2): their expression in muscle wasting during starvation. Comp Biochem Physiol B Biochem Mol Biol 140:63–71.  https://doi.org/10.1016/j.cbpc.2004.09.007 CrossRefGoogle Scholar
  25. Salem M, Kenney PB, Rexroad CE 3rd, Yao J (2006) Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol Genomics 28:33–45.  https://doi.org/10.1152/physiolgenomics.00114.2006 CrossRefGoogle Scholar
  26. Salem M, Silverstein J, Rexroad CE, Yao J (2007) Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 8:328.  https://doi.org/10.1186/1471-2164-8-328 CrossRefGoogle Scholar
  27. Seiliez I, Panserat S, Skiba-Cassy S, Fricot A, Vachot C, Kaushik S, Tesseraud S (2008) Feeding status regulates the polyubiquitination step of the ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss) muscle. J Nutr 138:487–491.  https://doi.org/10.1093/jn/138.3.487 CrossRefGoogle Scholar
  28. Seiliez I, Dias K, Cleveland BM (2014) Contribution of the autophagy-lysosomal and ubiquitin-proteasomal proteolytic systems to total proteolysis in rainbow trout (Oncorhynchus mykiss) myotubes. Am J Physiol Regul Integr Comp Physiol 307:R1330–R1337.  https://doi.org/10.1152/ajpregu.00370.2014 CrossRefGoogle Scholar
  29. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, Mcwilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal omega. Mol Syst Biol 7:539.  https://doi.org/10.1038/msb.2011.75 CrossRefGoogle Scholar
  30. Spencer JA, Eliazer S, Ilaria RL Jr, Richardson JA, Olson EN (2000) Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J Cell Biol 150:771–784CrossRefGoogle Scholar
  31. Tacchi L, Bickerdike R, Secombes CJ, Pooley NJ, Urquhart KL, Collet B, Martin SA (2010) Ubiquitin E3 ligase atrogin-1 (Fbox-32) in Atlantic salmon (Salmo salar): sequence analysis, genomic structure and modulation of expression. Comp Biochem Physiol B Biochem Mol Biol 157:364–373.  https://doi.org/10.1016/j.cbpb.2010.08.004 CrossRefGoogle Scholar
  32. Wang J, Salem M, Qi N, Kenney PB, Rexroad CE, Yao J (2011) Molecular characterization of the MuRF genes in rainbow trout: potential role in muscle degradation. Comp Biochem Physiol B Biochem Mol Biol 158:208–215.  https://doi.org/10.1016/j.cbpb.2010.11.010 CrossRefGoogle Scholar
  33. Witt SH, Granzier H, Witt CC, Labeit S (2005) MURF-1 and MURF-2 target a specific subset of Myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J Mol Biol 350:713–722.  https://doi.org/10.1016/j.jmb.2005.05.021 CrossRefGoogle Scholar
  34. Yang CG, Wang XL, Tian J, Liu W, Wu F, Jiang M, Wen H (2013) Evaluation of reference genes for quantitative real-time RT-PCR analysis of gene expression in Nile tilapia (Oreochromis niloticus). Gene 527:183–192.  https://doi.org/10.1016/j.gene.2013.06.013 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of BiologyMiddle Tennessee State UniversityMurfreesboroUSA
  2. 2.Department of Zoology, Faculty of ScienceBenha UniversityBenhaEgypt

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