Effect of Nutrient Restriction and Re-Feeding on Calpain Family Genes in Skeletal Muscle of Channel Catfish (Ictalurus punctatus)

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Preziosa, Elena ^a,b,c   Liu, Shikai ^a   Terova, Genciana ^b,c   Gao, Xiaoyu ^a   Liu, Hong ^a   Kucuktas, Huseyin ^a   Terhune, Jeffery ^a   Liu, Zhanjiang ^a  

^a AUBURN UNIVERSITY   (United States)

^b UNIVERSITY OF INSUBRIA   (Italy)

^c POLITECNICO DI MILANO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN 1; CALPAIN 2; CALPAIN 3; CONNECTIN; MESSENGER RNA;

ARTICLE; BODY WEIGHT; CALPAIN 1 GENE; CALPAIN 2 GENE; CALPAIN 3 GENE; CHANNEL CATFISH; CONTROLLED STUDY; DIET RESTRICTION; DNA SEQUENCE; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; MOLECULAR PHYLOGENY; NONHUMAN; QUANTITATIVE ANALYSIS; REFEEDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; TITIN GENE;

ANALYSIS OF VARIANCE; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BASE SEQUENCE; BODY WEIGHT; CALPAIN; CLUSTER ANALYSIS; DNA PRIMERS; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION; ICTALURIDAE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUSCLE, SKELETAL; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SPECTROPHOTOMETRY; STARVATION;

EID: 84875110634     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059404     Document Type: Article

References (61)

1. Sorimachi H, Hata S, Ono Y, (2011) Calpain chronicle-an enzyme family under multidisciplinary characterization. Proc Jpn Acad B-Phys Biol Sci 87: 287-327.
2. Branca D, Gugliucci A, Bano D, Brini M, Carafoli E, (1999) Expression, partial purification and functional properties of the muscle-specific calpain isoform p94. Eur J of Biochem 265: 839-846.
3. Elce JS, Hegadorn C, Arthur JS, (1997) Autolysis, Ca2+ requirement, and heterodimer stability in m-calpain. J Biol Chem 272: 11268-11275.
4. Sorimachi H, Imajoh-Ohmi S, Emori Y, Kawasaki H, Ohno S, et al. (1989) Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types. Specific expression of the mRNA in skeletal muscle. J Biol Chem 264: 20106-20111.
5. Nemova NN, Lysenko LA, Kantserova NP, (2010) Proteases of the calpain family: Structure and functions. Russ J Develop Biol 41: 318-325.
6. Suzuki K, Hata S, Kawabata Y, Sorimachi H, (2004) Structure, activation, and biology of calpain. Diabetes 53: S12-S18.
7. Goll DE, Thompson VF, Li H, Wei W, Cong J, (2003) The calpain system. Physiol Rev 83: 731-801.
8. Moldoveanu T, Campbell RL, Cuerrier D, Davies PL, (2004) Crystal structures of calpain-E64 and-leupeptin inhibitor complexes reveal mobile loops gating the active site. J Mol Biol 343: 1313-1326.
9. Sorimachi H, Suzuki K, (2001) The structure of calpain. J Biochem 129: 653-664.
10. Cygler M, Grochulski P, Blanchard H, (2002) Crystallization and structural details of Ca(2+)-induced conformational changes in the EF-hand domain VI of calpain. Method Mol Cell Biol 172: 243-260.
11. Pal GP, Elce JS, Jia Z, (2001) Dissociation and aggregation of calpain in the presence of calcium. J Biol Chem 276: 47233-47238.
12. Saido TC, Sorimachi H, Suzuki K, (1994) Calpain: new perspectives in molecular diversity and physiological-pathological involvement. FASEB J 8: 814-822.
13. Sorimachi H, Ishiura S, Suzuki K, (1997) Structure and physiological function of calpains. Biochem J 328: 721-732.
14. Sorimachi H, Kinbara K, Kimura S, Takahashi M, Ishiura S, et al. (1995) Muscle-specific calpain, p94, responsible for limb girdle muscular dystrophy type 2A, associates with connectin through IS2, a p94-specific sequence. J Biol Chem 270: 31158-31162.
15. Richard I, Broux O, Allamand V, Fougerousse F, Chiannilkulchai N, et al. (1995) Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81: 27-40.
16. Costelli P, Baccino FM, (2000) Cancer cachexia: from experimental models to patient management. Current Opinion in Clinical Nutrition and Metabolic Care 3: 177-181.
17. Du J, Hu Z, Mitch WE, (2005) Cellular signals activating muscle proteolysis in chronic kidney disease: a two-stage process. J Biochem Cell Biol 37: 2147-2155.
18. Dudgeon WD, Phillips KD, Carson JA, Brewer RB, Durstine JL, et al. (2006) Counteracting muscle wasting in HIV-infected individuals. HIV Medicine 7: 299-310.
19. Pereira C, Murphy K, Jeschke M, Herndon DN, (2005) Post burn muscle wasting and the effects of treatments. J Biochem Cell Biol 37: 1948-1961.
20. Goll DE, Neti G, Mares SW, Thompson VF, (2008) Myofibrillar protein turnover: the proteasome and the calpains. J Anim Sci 86: E19-35.
21. Kumamoto T, Ueyama H, Watanabe S, Yoshioka K, Miike T, et al. (1995) Immunohistochemical study of calpain and its endogenous inhibitor in the skeletal muscle of muscular dystrophy. ACTA Neuropathol 89: 399-403.
22. 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.
23. Ilian MA, Forsberg NE, (1992) Gene expression of calpains and their specific endogenous inhibitor, calpastatin, in skeletal muscle of fed and fasted rabbits. Biochem J 287 (Pt 1): 163-171.
24. Lepage SE, Bruce AE, (2008) Characterization and comparative expression of zebrafish calpain system genes during early development. Dev dynam 237: 819-829.
25. Macqueen DJ, Meischke L, Manthri S, Anwar A, Solberg C, et al. (2010) Characterisation of capn1, capn2-like, capn3 and capn11 genes in Atlantic halibut (Hippoglossus hippoglossus L.): Transcriptional regulation across tissues and in skeletal muscle at distinct nutritional states. Gene 453: 45-58.
26. USDA (2006) Catfish Processing Report, National Agriculture Statistics Service, USDA Washington, D.C.
27. Liu S, Zhang Y, Zhou Z, Waldbieser G, Sun F, et al. (2012) Efficient assembly and annotation of the transcriptome of catfish by RNA-Seq analysis of a doubled haploid homozygote. BMC Genomics, in press.
28. Liu S, Zhou Z, Lu J, Sun F, Wang S, et al. (2011) Generation of genome-scale gene-associated SNPs in catfish for the construction of a high-density SNP array. BMC Genomics 12.
29. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
30. Tripathi G, Verma P, (2003) Starvation-induced impairment of metabolism in a freshwater catfish. Z Naturforsch C 58: 446-451.
31. Small BC, Murdock CA, Bilodeau-Bourgeois AL, Peterson BC, Waldbieser GC, (2008) Stability of reference genes for real-time PCR analyses in channel catfish (Ictalurus punctatus) tissues under varying physiological conditions. Comp Biochem Physiol B Biochem Mol Biol 151: 296-304.
32. Baoprasertkul P, Peatman E, Somridhivej B, Liu ZJ, (2006) Toll-like receptor 3 and TICAM genes in catfish: species-specific expression profiles following infection with Edwardsiella ictaluri. Immunogenetics 58: 817-830.
33. Jiang Y, Abernathy J, Peatman E, Liu H, Wang S, Xu D-H, Kucuktas H, Klesius P, Liu ZJ, (2010) Identification and characterization of matrix metalloproteinase-13 sequence structure and expression during embryogenesis and infection in channel catfish (Ictalurus punctatus). Dev Comp Immunol 34: 590-597.
34. Sha Z, Abernathy JW, Wang S, Li P, Kucuktas H, Liu H, Peatman E, Liu ZJ, (2009) NOD-like subfamily of the nucleotide-binding domain and leucine rich repeat containing family receptors and their expression in channel catfish. Dev Comp Immunol 31: 991-999.
35. Takano T, Sha Z, Peatman E, Terhune J, Liu H, Kucuktas H, Li P, Edholm E-S, Wilson M, Liu ZJ, (2008) The two channel catfish intelectin genes exhibit highly differential patterns of tissue expression and regulation after infection with Edwardsiella ictaluri. Dev Comp Immunol 32: 693-705.
36. Pfaffl MW, Horgan GW, Dempfle L, (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
37. Vermaelen M, Sirvent P, Raynaud F, Astier C, Mercier J, et al. (2007) Differential localization of autolyzed calpains 1 and 2 in slow and fast skeletal muscles in the early phase of atrophy. Am J Physiol Cell Ph 292: C1723-C1731.
38. Furuno K, Goodman MN, Goldberg AL, (1990) Role of different proteolitic system in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265: 8550-8557.
39. Stockholm D, Herasse M, Marchand S, Praud C, (2001) Calpain3 mRNA expression in vivo after degeneration and during muscle regeneration. Am J Physiol Cell Ph 280: C1561-C1569.
40. Jekely G, Friedrich P, (1999) The evolution of the calpain family as reflected in paralogous chromosome regions. J Mol Evol 49: 272-281.
41. Alderton JM, Steinhardt RA, (2000) Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J Biol Chem 275: 9452-9460.
42. Jackman RW, Kandarian SC, (2004) The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Ph 287: C834-843.
43. Du M, Zhu MJ, Means WJ, Hess BW, Ford SP, (2004) Effect of nutrient restriction on calpain and calpastatin content of skeletal muscle from cows and fetuses. J Anim Sci 82: 2541-2547.
44. Bartoli M, Richard I, (2005) Calpains in muscle wasting. Int J Biochem Cell B 37: 2115-2133.
45. Wang L, Luo GJ, Wang JJ, Hasselgren PO, (1998) Dexamethasone stimulates proteasome and calcium- dependent proteolysis in cultured L6 myotubes. Shock 10: 298-306.
46. Sultan KR, Dittrich BT, Leisner E, Paul N, Pette D, (2001) Fiber type-specific expression of major proteolytic systems in fast- to slow-transforming rabbit muscle. Am J Physiol Cell Physiol 280: C239-C247.
47. Taillandier D, Aurousseau E, Meynial-Denis D, (1996) Coordinate activation of lysosomal, Ca2- activated and ATP-ubiquitindependent proteinases in the unweighted rat soleus muscle. Biochem J 316: 65-72.
48. Tidball JG, Spencer MJ, (2002) Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J Physiol 545: 819-828.
49. Koohmaraie M, Shackelford SD, (1991) Effect of calcium chloride infusion on the tenderness of lambs fed a beta-adrenergic agonist. J Ani Sci 69: 2463-2471.
50. Kretchmar DH, Hathaway MR, Epley RJ, Dayton WR, (1990) Alterations in postmortem degradation of myofibrillar proteins in muscle of lambs fed a beta-adrenergic agonist. J Ani Sci 68: 1760-1772.
51. Melloni E, Michetti M, Salamino F, Minafra R, et al. (1996) Modulation of the calpain autoproteolysis by calpastatin and phospholipids. Biochem Biophys Res Commun 229: 193-197.
52. Arthur GD, Booker TS, Belcastro AN, (1999) Exercise promotes a subcellular redistribution of calcium- stimulated protease activity in striated muscle. Can J Physiol Pharm 77: 42-47.
53. Kuboki M, Ishii H, Kazama M, (1990) Characterization of calpain I-binding proteins in human erythrocyte plasma membrane. J Biochem 107: 776-780.
54. Murphy RM, Verburg E, Lamb GD, (2006) Ca2+ activation of diffusible and bound pools of mu-calpain in rat skeletal muscle. J Physiol 576: 595-612.
55. Huang J, Forsberg NE, (1998) Role of calpain in skeletal-muscle protein degradation. Proc Natl Acad Sci USA 95: 12100-12105.
56. Tsujinaka T, Fujita J, Ebisui C, Yano M, Kominami E, et al. (1996) Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. J Clin Invest 97: 244-249.
57. Gregorio CC, Trombitas K, Centner T, Kolmerer B, Stier G, et al. (1998) The NH2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity. J Cell Biol 143: 1013-1027.
58. Kramerova I, Kudryashova E, Venkatraman G, Spencer MJ, (2005) Calpain 3 participates in sarcomere remodeling by acting upstream of the ubiquitin-proteasome pathway. Hum Mol Genet 14: 2125-2134.
59. Jagoe RT, Lecker SH, Gomes M, Goldberg AL, (2002) Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. The FASEB J 16: 1697-1712.
60. Sarparanta J, Blandin G, Charton K, Vihola A, Marchand S, et al. (2010) Interactions with M-band titin and calpain 3 link myospryn (CMYA5) to tibial and limb-girdle muscular dystrophies. J Biol Chem 285: 30304-30315.
61. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: 2002-2007.