FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Anal Biochem / Purification of sarcoplasmic reticulum vesicles from horse g...
Analytical biochemistry2020; 610; 113965; doi: 10.1016/j.ab.2020.113965

Purification of sarcoplasmic reticulum vesicles from horse gluteal muscle.

Abstract: We have analyzed protein expression and enzyme activity of the sarcoplasmic reticulum Ca2+-transporting ATPase (SERCA) in horse gluteal muscle. Horses exhibit a high incidence of recurrent exertional rhabdomyolysis, with myosolic Ca2+ proposed, but yet to be established, as the underlying cause. To better assess Ca2+ regulatory mechanisms, we developed an improved protocol for isolating sarcoplasmic reticulum (SR) vesicles from horse skeletal muscle, based on mechanical homogenization and optimized parameters for differential centrifugation. Immunoblotting identified the peak subcellular fraction containing the SERCA1 protein (fast-twitch isoform). Gel analysis using the Stains-all dye demonstrated that calsequestrin (CASQ) and phospholipids are highly enriched in the SERCA-containing subcellular fraction isolated from horse gluteus. Immunoblotting also demonstrated that these horse SR vesicles show low content of glycogen phosphorylase (GP), which is likely an abundant contaminating protein of traditional horse SR preps. The maximal Ca2+-activated ATPase activity (Vmax) of SERCA in horse SR vesicles isolated using this protocol is 5‒25-fold greater than previously-reported SERCA activity in SR preps from horse skeletal muscle. We propose that this new protocol for isolating SR vesicles will be useful for determining enzymatic parameters of horse SERCA with high fidelity, plus assessing regulatory effect of SERCA peptide subunit(s) expressed in horse muscle.
Copyright © 2020 Elsevier Inc. All rights reserved.
Get Full Text
Publication Date: 2020-09-19 PubMed ID: 32956693PubMed Central: PMC7745508DOI: 10.1016/j.ab.2020.113965Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article describes a new method for isolating sarcoplasmic reticulum vesicles from horse muscle tissues. The improved protocol has allowed researchers to better understand the activity and protein expression of a specific enzyme found in horse muscles.

Research Background

  • The sarcoplasmic reticulum Ca-transporting ATPase (SERCA) enzyme in horse muscles was examined in this study, given the high incidence of exertional rhabdomyolysis in horses–a condition suggested to be related to modifications in calcium regulation.
  • The research aimed to generate an improved method for isolating the sarcoplasmic reticulum (SR) vesicles–structures that participate in calcium regulation in muscles–from the gluteal muscle of a horse. Previously, the determination of enzymatic parameters related to SERCA activity in horse muscles had been challenging due to lack of optimized protocols.

Methodology

  • The researchers used a protocol based on mechanical homogenization and optimized parameters for differential centrifugation to isolate the SR vesicles from the horse skeletal muscle.
  • Immunoblotting techniques were used to indicate the presence of SERCA1 protein (the fast-twitch isoform) in the SR subcellular fractions.
  • Gel analysis was performed using the Stains-all dye, a procedure that showed that calsequestrin (CASQ) and phospholipids are significantly enriched in the SERCA-containing fractions.
  • The contamination of the horse SR formations from glycogen phosphorylase (GP), a common contaminating protein, was checked by immunoblotting. The researchers noted that these formations showed a low content of GP.

Key Findings

  • The isolated SR vesicles showed SERCA’s maximal Ca-activated ATPase activity (V) to be 5-25 times higher than previously reported values in similar preparations from horse skeletal muscle, thereby suggesting the effectiveness of the new isolation protocol.
  • From these findings, the researchers propositioned that their new protocol can help in accurately determining the enzymatic parameters of horse SERCA and in assessing the impact of SERCA peptide subunit(s) that are expressed in horse muscles.

Cite This Article

APA
Autry JM, Karim CB, Cocco M, Carlson SF, Thomas DD, Valberg SJ. (2020). Purification of sarcoplasmic reticulum vesicles from horse gluteal muscle. Anal Biochem, 610, 113965. https://doi.org/10.1016/j.ab.2020.113965

Publication

Analytical biochemistry
ISSN: 1096-0309
NlmUniqueID: 0370535
Country: United States
Language: English
Volume: 610
Pages: 113965

Researcher Affiliations

Autry, Joseph M
  • Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA. Electronic address: autry001@umn.edu.
Karim, Christine B
  • Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA.
Cocco, Mariana
  • Department of Veterinary Population Medicine, University of Minnesota, St. Paul, MN, 55108, USA.
Carlson, Samuel F
  • Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA.
Thomas, David D
  • Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA.
Valberg, Stephanie J
  • Department of Large Animal Clinical Sciences, McPhail Equine Performance Center, Michigan State University, East Lansing, MI, 48823, USA. Electronic address: valbergs@msu.edu.

MeSH Terms

  • Animals
  • Calcium / metabolism
  • Centrifugation
  • Electrophoresis, Agar Gel
  • Extracellular Vesicles / chemistry
  • Extracellular Vesicles / metabolism
  • Glycogen Phosphorylase / metabolism
  • Horses
  • Muscle, Skeletal / metabolism
  • Protein Isoforms / metabolism
  • Sarcoplasmic Reticulum / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism

Grant Funding

  • R01 AG026160 / NIA NIH HHS
  • R01 GM027906 / NIGMS NIH HHS
  • R01 HL139065 / NHLBI NIH HHS
  • R37 AG026160 / NIA NIH HHS

Conflict of Interest Statement

Competing Interests Statement. The authors declare that they have no competing interests with the contents of this article.

References

This article includes 77 references
  1. Guhathakurta P, Prochniewicz E, Thomas DD. Actin-myosin interaction: structure, function and drug discovery. Int J Mol Sci 19 (2018).
    pmc: PMC6163256pubmed: 30189615
  2. MacLennan DH. Purification and properties of an adenosine triphosphatase from sarcoplasmic reticulum. J Biol Chem 245 (1970) 4508–18.
    pubmed: 4250726
  3. Rardon DP, Cefali DC, Mitchell RD, Seiler SM, Jones LR. High molecular weight proteins purified from cardiac junctional sarcoplasmic reticulum vesicles are ryanodine-sensitive calcium channels. Circ Res 64 (1989) 779–89.
    pubmed: 2539270
  4. Tupling AR. The decay phase of Ca2+ transients in skeletal muscle: regulation and physiology. Appl Physiol Nutr Metab 34 (2009) 373–6.
    pubmed: 19448701
  5. Kong H, Wang R, Chen W, Zhang L, Chen K, Shimoni Y, Duff HJ, Chen SR. Skeletal and cardiac ryanodine receptors exhibit different responses to Ca2+ overload and luminal ca2+. Biophys J 92 (2007) 2757–70.
    pmc: PMC1831700pubmed: 17259277
  6. Bovo E, Nikolaienko R, Bhayani S, Kahn D, Cao Q, Martin JL, Kuo IY, Robia SL, Zima AV. Novel approach for quantification of endoplasmic reticulum Ca(2+) transport. Am J Physiol Heart Circ Physiol 316 (2019) H1323–H1331.
    pmc: PMC6620677pubmed: 30901276
  7. Sanchez EJ, Lewis KM, Danna BR, Kang C. High-capacity Ca2+ binding of human skeletal calsequestrin. J Biol Chem 287 (2012) 11592–601.
    pmc: PMC3322862pubmed: 22337878
  8. Cala SE, Jones LR. Rapid purification of calsequestrin from cardiac and skeletal muscle sarcoplasmic reticulum vesicles by Ca2+-dependent elution from phenyl-sepharose. J Biol Chem 258 (1983) 11932–6.
    pubmed: 6619149
  9. Murphy RM, Larkins NT, Mollica JP, Beard NA, Lamb GD. Calsequestrin content and SERCA determine normal and maximal Ca2+ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. J Physiol 587 (2009) 443–60.
    pmc: PMC2670055pubmed: 19029185
  10. Manno C, Figueroa LC, Gillespie D, Fitts R, Kang C, Franzini-Armstrong C, Rios E. Calsequestrin depolymerizes when calcium is depleted in the sarcoplasmic reticulum of working muscle. Proc Natl Acad Sci U S A 114 (2017) E638–E647.
    pmc: PMC5278470pubmed: 28069951
  11. Wanson JC, Drochmans P. Role of the sarcoplasmic reticulum in glycogen metabolism. Binding of phosphorylase, phosphorylase kinase, and primer complexes to the sarcovesicles of rabbit skeletal muscle. J Cell Biol 54 (1972) 206–24.
    pmc: PMC2108881pubmed: 5040859
  12. Eletr S, Inesi G. Phospholipid orientation in sarcoplasmic membranes: spin-label ESR and proton NMR studies. Biochim Biophys Acta 282 (1972) 174-&.
    pubmed: 4341786
  13. Fernandez JL, Rosemblatt M, Hidalgo C. Highly purified sarcoplasmic reticulum vesicles are devoid of Ca2+-independent (‘basal’) ATPase activity. Biochim Biophys Acta 599 (1980) 552–68.
    pubmed: 6105877
  14. Ikemoto N, Sreter FA, Gergely J. Structural features of the surface of the vesicles of FSR--lack of functional role in Ca 2+ uptake and ATPase activity. Arch Biochem Biophys 147 (1971) 571–82.
    pubmed: 4257599
  15. Sacchetto R, Bovo E, Salviati L, Damiani E, Margreth A. Glycogen synthase binds to sarcoplasmic reticulum and is phosphorylated by CaMKII in fast-twitch skeletal muscle. Arch Biochem Biophys 459 (2007) 115–21.
    pubmed: 17178096
  16. Volpe P, Mrak RE, Costello B, Fleischer S. Calcium release from sarcoplasmic reticulum of normal and dystrophic mice. Biochim Biophys Acta 769 (1984) 67–78.
    pubmed: 6229283
  17. Shutova AN, Storey KB, Lopina OD, Rubtsov AM. Comparative characteristics of sarcoplasmic reticulum preparations from skeletal muscles of the ground squirrel Spermophilus undulatus, rats, and rabbits. Biochemistry (Mosc) 64 (1999) 1250–7.
    pubmed: 10611529
  18. Scales D, Sabbadini R, Inesi G. The involvement of sarcotubular membranes in genetic muscular dystrophy. Biochim Biophys Acta 465 (1977) 535–49.
    pubmed: 138444
  19. Ohlendieck K, Briggs FN, Lee KF, Wechsler AW, Campbell KP. Analysis of excitation-contraction-coupling components in chronically stimulated canine skeletal muscle. Eur J Biochem 202 (1991) 739–47.
    pubmed: 1662614
  20. McIntosh DB, Berman MC, Kench JE. Characteristics of sarcoplasmic reticulum from slowly glycolysing and from rapidly glycolysing pig skeletal muscle post mortem. Biochem J 166 (1977) 387–98.
    pmc: PMC1165021pubmed: 145857
  21. Sacchetto R, Bertipaglia I, Giannetti S, Cendron L, Mascarello F, Damiani E, Carafoli E, Zanotti G. Crystal structure of sarcoplasmic reticulum Ca2+-ATPase (SERCA) from bovine muscle. J Struct Biol 178 (2012) 38–44.
    pubmed: 22387132
  22. Møller JV, Olesen C, Winther AM, Nissen P. The sarcoplasmic Ca2+-ATPase: design of a perfect chemi-osmotic pump. Q Rev Biophys 43 (2010) 501–66.
    pubmed: 20809990
  23. Bigelow DJ, Inesi G. Contributions of chemical derivatization and spectroscopic studies to the characterization of the Ca2+ transport ATPase of sarcoplasmic reticulum. Biochim Biophys Acta 1113 (1992) 323–38.
    pubmed: 1450205
  24. de Meis L, Vianna AL. Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 48 (1979) 275–92.
    pubmed: 157714
  25. Byrd SK, McCutcheon LJ, Hodgson DR, Gollnick PD. Altered sarcoplasmic reticulum function after high-intensity exercise. J Appl Physiol 67 (1989) 2072–7.
    pubmed: 2532196
  26. Beech J, Lindborg S, Fletcher JE, Lizzo F, Tripolitis L, Braund K. Caffeine contractures, twitch characteristics and the threshold for Ca(2+)-induced Ca2+ release in skeletal muscle from horses with chronic intermittent rhabdomyolysis. Res Vet Sci 54 (1993) 110–7.
    pubmed: 8434138
  27. Wilson JA, Kronfeld DS, Gay L, Wilson TM. Isolating equine sarcoplasmic reticulum: its function during high intensity repeated springs. Equine Vet J Suppl 18 (1995) 252–255.
  28. Wilson JA, Kronfeld DS, Gay LS, Williams JH, Wilson TM, Lindinger MI. Sarcoplasmic reticulum responses to repeated sprints are affected by conditioning of horses. J Anim Sci 76 (1998) 3065–71.
    pubmed: 9928611
  29. Ward TL, Valberg SJ, Gallant EM, Mickelson JR. Calcium regulation by skeletal muscle membranes of horses with recurrent exertional rhabdomyolysis. Am J Vet Res 61 (2000) 242–7.
    pubmed: 10714513
  30. Sacchetto R, Sharova E, Patruno M, Maccatrozzo L, Damiani E, Mascarello F. Overexpression of histidine-rich calcium binding protein in equine ventricular myocardium. Vet J 193 (2012) 157–61.
    pubmed: 22040806
  31. Valberg SJ. Muscle conditions affecting sport horses. Vet Clin North Am Equine Pract 34 (2018) 253–276.
    pubmed: 29853158
  32. Isgren CM, Upjohn MM, Fernandez-Fuente M, Massey C, Pollott G, Verheyen KL, Piercy RJ. Epidemiology of exertional rhabdomyolysis susceptibility in standardbred horses reveals associated risk factors and underlying enhanced performance. PLoS One 5 (2010) e11594.
    pmc: PMC2904368pubmed: 20644724
  33. MacLeay JM, Sorum SA, Valberg SJ, Marsh WE, Sorum MD. Epidemiologic analysis of factors influencing exertional rhabdomyolysis in Thoroughbreds. Am J Vet Res 60 (1999) 1562–6.
    pubmed: 10622169
  34. Mlekoday JA, Mickelson JR, Valberg SJ, Horton JH, Gallant EM, Thompson LV. Calcium sensitivity of force production and myofibrillar ATPase activity in muscles from Thoroughbreds with recurrent exertional rhabdomyolysis. Am J Vet Res 62 (2001) 1647–52.
    pubmed: 11592334
  35. Lentz LR, Valberg SJ, Mickelson JR, Gallant EM. In vitro contractile responses and contracture testing of skeletal muscle from Quarter Horses with exertional rhabdomyolysis. Am J Vet Res 60 (1999) 684–8.
    pubmed: 10376892
  36. Cala SE, Miles K. Phosphorylation of the cardiac isoform of calsequestrin in cultured rat myotubes and rat skeletal muscle. Biochim Biophys Acta 1118 (1992) 277–87.
    pubmed: 1737050
  37. Ohlendieck K, Fromming GR, Murray BE, Maguire PB, Leisner E, Traub I, Pette D. Effects of chronic low-frequency stimulation on Ca2+-regulatory membrane proteins in rabbit fast muscle. Pflugers Arch 438 (1999) 700–8.
    pubmed: 10555569
  38. Valberg SJ, Soave K, Williams ZJ, Perumbakkam S, Schott M, Finno CJ, Petersen JL, Fenger C, Autry JM, Thomas DD. Coding sequences of sarcoplasmic reticulum calcium ATPase regulatory peptides and expression of calcium regulatory genes in recurrent exertional rhabdomyolysis. J Vet Intern Med 33 (2019) 933–941.
    pmc: PMC6430904pubmed: 30720217
  39. Valberg SJ, Perumbakkam S, McKenzie EC, Finno CJ. Proteome and transcriptome profiling of equine myofibrillar myopathy identifies diminished peroxiredoxin 6 and altered cysteine metabolic pathways. Physiol Genomics 50 (2018) 1036–1050.
    pmc: PMC6337024pubmed: 30289745
  40. Leberer E, Pette D. Immunochemical quantification of sarcoplasmic reticulum Ca-ATPase, of calsequestrin and of parvalbumin in rabbit skeletal muscles of defined fiber composition. Eur J Biochem 156 (1986) 489–96.
    pubmed: 2938950
  41. Valberg SJ. Muscle Anatomy: Adaptations to Exercise and Training. in (Hodgson DR, McKeever KH, McGowan CM, Eds.), The Athletic Horse: Principles and Practice of Equine Sports Medicine, Saunders, New York, 2014, pp. 174–201.
  42. Valberg SJ. Genetics of Equine Muscle Disease. Vet Clin North Am Equine Pract 36 (2020) 353–378.
    pubmed: 32654785
  43. Yamaguchi H, Kanda Y, Iwata K. Macromolecular structure and morphology of native glycogen particles isolated from Candida albicans. J Bacteriol 120 (1974) 441–9.
    pmc: PMC245781pubmed: 4608780
  44. Autry JM, Rubin JE, Svensson B, Li J, Thomas DD. Nucleotide activation of the Ca-ATPase. J Biol Chem 287 (2012) 39070–82.
    pmc: PMC3493948pubmed: 22977248
  45. de Meis L, Oliveira GM, Arruda AP, Santos R, Costa RM, Benchimol M. The thermogenic activity of rat brown adipose tissue and rabbit white muscle Ca2+-ATPase. IUBMB Life 57 (2005) 337–45.
    pubmed: 16036618
  46. Molnar E, Seidler NW, Jona I, Martonosi AN. The binding of monoclonal and polyclonal antibodies to the Ca2(+)-ATPase of sarcoplasmic reticulum: effects on interactions between ATPase molecules. Biochim Biophys Acta 1023 (1990) 147–67.
    pubmed: 1691656
  47. Campbell KP, MacLennan DH, Jorgensen AO. Staining of the Ca2+-binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanine dye “Stains-all”. J Biol Chem 258 (1983) 11267–73.
    pubmed: 6193121
  48. Jones LR, Cala SE. Biochemical evidence for functional heterogeneity of cardiac sarcoplasmic reticulum vesicles. J Biol Chem 256 (1981) 11809–18.
    pubmed: 6271762
  49. Kumar S, Li C, Montigny C, le Maire M, Barth A. Conformational changes of recombinant Ca2+-ATPase studied by reaction-induced infrared difference spectroscopy. FEBS J 280 (2013) 5398–407.
    pubmed: 23331704
  50. Butler J, Smyth N, Broadbridge R, Council CE, Lee AG, Stocker CJ, Hislop DC, Arch JR, Cawthorne MA, Malcolm East J. The effects of sarcolipin over-expression in mouse skeletal muscle on metabolic activity. Arch Biochem Biophys 569 (2015) 26–31.
    pmc: PMC4362768pubmed: 25660043
  51. Jones LR, Besch HR Jr., Watanabe AM. Monovalent cation stimulation of Ca2+ uptake by cardiac membrane vesicles. J Biol Chem 252 (1977) 3315–23.
    pubmed: 140870
  52. Jones LR, Besch HR Jr., Fleming JW, McConnaughey MM, Watanabe AM. Separation of vesicles of cardiac sarcolemma from vesicles of cardiac sarcoplasmic reticulum. Comparative biochemical analysis of component activities. J Biol Chem 254 (1979) 530–9.
    pubmed: 216677
  53. Toyoshima C, Iwasawa S, Ogawa H, Hirata A, Tsueda J, Inesi G. Crystal structures of the calcium pump and sarcolipin in the Mg2+-bound E1 state. Nature 495 (2013) 260–4.
    pubmed: 23455422
  54. Toyoshima C, Mizutani T. Crystal structure of the calcium pump with a bound ATP analogue. Nature 430 (2004) 529–35.
    pubmed: 15229613
  55. MacLennan DH, Rice WJ, Green NM. The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases. J Biol Chem 272 (1997) 28815–8.
    pubmed: 9360942
  56. Espinoza-Fonseca LM, Autry JM, Thomas DD. Sarcolipin and phospholamban inhibit the calcium pump by populating a similar metal ion-free intermediate state. Biochem Biophys Res Commun 463 (2015) 37–41.
    pmc: PMC4465059pubmed: 25983321
  57. Autry JM, Thomas DD, Espinoza-Fonseca LM. Sarcolipin promotes uncoupling of the SERCA Ca2+ pump by inducing a structural rearrangement in the energy-transduction domain. Biochemistry 55 (2016) 6083–6086.
    pmc: PMC5506494pubmed: 27731980
  58. Ablorh NA, Dong X, James ZM, Xiong Q, Zhang J, Thomas DD, Karim CB. Synthetic phosphopeptides enable quantitation of the content and function of the four phosphorylation states of phospholamban in cardiac muscle. J Biol Chem 289 (2014) 29397–405.
    pmc: PMC4200288pubmed: 25190804
  59. Ablorh NA, Miller T, Nitu F, Gruber SJ, Karim C, Thomas DD. Accurate quantitation of phospholamban phosphorylation by immunoblot. Anal Biochem 425 (2012) 68–75.
    pmc: PMC3338889pubmed: 22369895
  60. Kang C, Trumble WR, Dunker AK. Crystallization and structure-function of calsequestrin. Methods Mol Biol 172 (2002) 281–94.
    pubmed: 11833354
  61. Aguayo-Ortiz R, Espinoza-Fonseca LM. Linking Biochemical and Structural States of SERCA: Achievements, Challenges, and New Opportunities. Int J Mol Sci 21 (2020).
    pmc: PMC7313052pubmed: 32532023
  62. Jones LR, Besch HR Jr., Watanabe AM. Regulation of the calcium pump of cardiac sarcoplasmic reticulum. Interactive roles of potassium and ATP on the phosphoprotein intermediate of the (K+,Ca2+)-ATPase. J Biol Chem 253 (1978) 1643–53.
    pubmed: 146716
  63. Autry JM, Jones LR. Functional co-expression of the canine cardiac Ca2+ pump and phospholamban in Spodoptera frugiperda (Sf21) cells reveals new insights on ATPase regulation. J Biol Chem 272 (1997) 15872–80.
    pubmed: 9188486
  64. Mahaney JE, Autry JM, Jones LR. Kinetics studies of the cardiac Ca-ATPase expressed in Sf21 cells: new insights on Ca-ATPase regulation by phospholamban. Biophys J 78 (2000) 1306–23.
    pmc: PMC1300731pubmed: 10692318
  65. Autry JM, Rubin JE, Pietrini SD, Winters DL, Robia SL, Thomas DD. Oligomeric interactions of sarcolipin and the Ca-ATPase. J Biol Chem 286 (2011) 31697–706.
    pmc: PMC3173058pubmed: 21737843
  66. Brandl CJ, deLeon S, Martin DR, MacLennan DH. Adult forms of the Ca2+ATPase of sarcoplasmic reticulum. Expression in developing skeletal muscle. J Biol Chem 262 (1987) 3768–74.
    pubmed: 3029125
  67. Paran CW, Verkerke AR, Heden TD, Park S, Zou K, Lawson HA, Song H, Turk J, Houmard JA, Funai K. Reduced efficiency of sarcolipin-dependent respiration in myocytes from humans with severe obesity. Obesity (Silver Spring) 23 (2015) 1440–9.
    pmc: PMC4483165pubmed: 25970801
  68. Nguyen T, Rubinstein NA, Vijayasarathy C, Rome LC, Kaiser LR, Shrager JB, Levine S. Effect of chronic obstructive pulmonary disease on calcium pump ATPase expression in human diaphragm. J Appl Physiol 98 (2005) 2004–10.
    pubmed: 15718407
  69. de Oliveira BM, Matsumura CY, Fontes-Oliveira CC, Gawlik KI, Acosta H, Wernhoff P, Durbeej M. Quantitative proteomic analysis reveals metabolic alterations, calcium dysregulation, and increased expression of extracellular matrix proteins in laminin alpha2 chain-deficient muscle. Mol Cell Proteomics 13 (2014) 3001–13.
    pmc: PMC4223487pubmed: 24994560
  70. Santacatterina F, Sanchez-Arago M, Catalan-Garcia M, Garrabou G, de Arenas CN, Grau JM, Cardellach F, Cuezva JM. Pyruvate kinase M2 and the mitochondrial ATPase Inhibitory Factor 1 provide novel biomarkers of dermatomyositis: a metabolic link to oncogenesis. J Transl Med 15 (2017) 29.
    pmc: PMC5301421pubmed: 28183315
  71. Xirouchaki CE, Mangiafico SP, Bate K, Ruan Z, Huang AM, Tedjosiswoyo BW, Lamont B, Pong W, Favaloro J, Blair AR, Zajac JD, Proietto J, Andrikopoulos S. Impaired glucose metabolism and exercise capacity with muscle-specific glycogen synthase 1 (gys1) deletion in adult mice. Mol Metab 5 (2016) 221–232.
    pmc: PMC4770268pubmed: 26977394
  72. Zhao Y, Zhang Q, Shao X, Ouyang L, Wang X, Zhu K, Chen L. Decreased glycogen content might contribute to chronic stress-induced atrophy of hippocampal astrocyte volume and depression-like behavior in rats. Sci Rep 7 (2017) 43192.
    pmc: PMC5324119pubmed: 28233800
  73. Garvey SM, Russ DW, Skelding MB, Dugle JE, Edens NK. Molecular and metabolomic effects of voluntary running wheel activity on skeletal muscle in late middle-aged rats. Physiol Rep 3 (2015).
    pmc: PMC4393218pubmed: 25716928
  74. Cornea RL, Autry JM, Chen Z, Jones LR. Reexamination of the role of the leucine/isoleucine zipper residues of phospholamban in inhibition of the Ca2+ pump of cardiac sarcoplasmic reticulum. J Biol Chem 275 (2000) 41487–94.
    pubmed: 11016944
  75. Winters DL, Autry JM, Svensson B, Thomas DD. Interdomain fluorescence resonance energy transfer in SERCA probed by cyan-fluorescent protein fused to the actuator domain. Biochemistry 47 (2008) 4246–56.
    pmc: PMC6537896pubmed: 18338856
  76. Strausberg RL, Feingold EA, Grouse LH, Derge JG, Klausner RD, Collins FS, Wagner L, Shenmen CM, Schuler GD, Altschul SF, Zeeberg B, Buetow KH, Schaefer CF, Bhat NK, Hopkins RF, Jordan H, Moore T, Max SI, Wang J, Hsieh F, Diatchenko L, Marusina K, Farmer AA, Rubin GM, Hong L, Stapleton M, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Brownstein MJ, Usdin TB, Toshiyuki S, Carninci P, Prange C, Raha SS, Loquellano NA, Peters GJ, Abramson RD, Mullahy SJ, Bosak SA, McEwan PJ, McKernan KJ, Malek JA, Gunaratne PH, Richards S, Worley KC, Hale S, Garcia AM, Gay LJ, Hulyk SW, Villalon DK, Muzny DM, Sodergren EJ, Lu X, Gibbs RA, Fahey J, Helton E, Ketteman M, Madan A, Rodrigues S, Sanchez A, Whiting M, Madan A, Young AC, Shevchenko Y, Bouffard GG, Blakesley RW, Touchman JW, Green ED, Dickson MC, Rodriguez AC, Grimwood J, Schmutz J, Myers RM, Butterfield YS, Krzywinski MI, Skalska U, Smailus DE, Schnerch A, Schein JE, Jones SJ, Marra MA, Mammalian T Gene Collection Program. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci U S A 99 (2002) 16899–903.
    pmc: PMC139241pubmed: 12477932
  77. Zhang Y, Fujii J, Phillips MS, Chen HS, Karpati G, Yee WC, Schrank B, Cornblath DR, Boylan KB, MacLennan DH. Characterization of cDNA and genomic DNA encoding SERCA1, the Ca(2+)-ATPase of human fast-twitch skeletal muscle sarcoplasmic reticulum, and its elimination as a candidate gene for Brody disease. Genomics 30 (1995) 415–24.
    pubmed: 8825625

Citations

This article has been cited 3 times.
  1. Rivera-Morán MA, Sampedro JG. Isolation of the Sarcoplasmic Reticulum Ca(2+)-ATPase from Rabbit Fast-Twitch Muscle. Methods Protoc 2023 Oct 19;6(5).
    doi: 10.3390/mps6050102pubmed: 37888034google scholar: lookup
  2. Autry JM, Svensson B, Carlson SF, Chen Z, Cornea RL, Thomas DD, Valberg SJ. Sarcoplasmic Reticulum from Horse Gluteal Muscle Is Poised for Enhanced Calcium Transport. Vet Sci 2021 Nov 23;8(12).
    doi: 10.3390/vetsci8120289pubmed: 34941816google scholar: lookup
  3. Autry JM, Karim CB, Perumbakkam S, Finno CJ, McKenzie EC, Thomas DD, Valberg SJ. Sarcolipin Exhibits Abundant RNA Transcription and Minimal Protein Expression in Horse Gluteal Muscle. Vet Sci 2020 Nov 13;7(4).
    doi: 10.3390/vetsci7040178pubmed: 33202832google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.