One-step purification and regulation of fructose 1,6-bisphosphatase from the liver of the freeze-tolerant wood frog, Rana sylvatica.
Rana sylvatica
enzyme regulation
freeze tolerance
fructose-1,6-bisphosphatase
gluconeogenesis
metabolic rate depression
posttranslational modification
Journal
Cell biochemistry and function
ISSN: 1099-0844
Titre abrégé: Cell Biochem Funct
Pays: England
ID NLM: 8305874
Informations de publication
Date de publication:
Jul 2022
Jul 2022
Historique:
revised:
13
04
2022
received:
09
02
2022
accepted:
08
05
2022
pubmed:
24
5
2022
medline:
28
7
2022
entrez:
23
5
2022
Statut:
ppublish
Résumé
The wood frog (Rana sylvatica) undergoes numerous changes to its physiology and metabolic processes to survive the winter months, including adaptations that let them endure whole-body freezing. The regulation of key enzymes of central carbohydrate metabolism in the liver plays a crucial role in mediating the synthesis and maintenance of high concentrations of glucose as a cryoprotectant during freezing as well as glucose reconversion to glycogen after thawing. The present study characterized the regulation of fructose-1,6-bisphosphatase (FBPase; EC 3.1.3.11) from wood frog liver during freezing, FBPase being a crucial enzyme regulating gluconeogenesis. Liver FBPase was purified to homogeneity from control and frozen wood frogs by a one-step chromatographic process. Kinetic and regulatory parameters of the enzyme were investigated and demonstrated a significant decrease in sensitivity to its substrate fructose-1,6-bisphosphate in the liver of frozen frogs, as compared with controls. Immunoblotting also revealed freeze-responsive changes in posttranslational modifications with a significant decrease in serine phosphorylation (by 53%) for FBPase from frozen frogs. Taken together, these results suggest that FBPase is suppressed, and gluconeogenesis is inhibited during freezing. This response acts as an important component of the metabolic survival strategy of the wood frog.
Substances chimiques
Fructose
30237-26-4
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
491-500Subventions
Organisme : Natural Sciences and Engineering Research Council of Canada
Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Storey KB, Storey JM. Natural freezing survival in animals. Annu Rev Ecol Syst. 1996;27:365-385. doi:10.1146/annurev.ecolsys.27.1.365
Storey KB, Storey JM. Molecular physiology of freeze tolerance in vertebrates. Physiol Rev. 2017;97(2):623-665. doi:10.1152/physrev.00016.2016
Storey KB, Storey JM. Freeze tolerance and intolerance as strategies of winter survival in terrestrially-hibernating amphibians. Comp Biochem Physiol A Comp Physiol. 1986;83(4):613-617. doi:10.1016/0300-9629(86)90699-7
Costanzo JP, do Amaral MCF, Rosendale AJ, Lee RE. Hibernation physiology, freezing adaptation and extreme freeze tolerance in a northern population of the wood frog. J Exp Biol. 2013;216(pt 18):3461-3473. doi:10.1242/jeb.089342
Dieni CA, Storey KB. Regulation of hexokinase by reversible phosphorylation in skeletal muscle of a freeze-tolerant frog. Comp Biochem Physiol B Biochem Mol Biol. 2011;159(4):236-243. doi:10.1016/j.cbpb.2011.05.003
Feder ME, Burggren WW. Environmental Physiology of the Amphibians. University of Chicago Press; 1992.
Storey KB. Biochemistry of natural freeze tolerance in animals: Molecular adaptations and applications to cryopreservation. Biochem Cell Biol. 1990;68(4):687-698. doi:10.1139/o90-100
Storey KB. Life in a frozen state: adaptive strategies for natural freeze tolerance in amphibians and reptiles. Am J Physiol. 1990;258(3 pt 2):R559-R568. doi:10.1152/ajpregu.1990.258.3.R559
do Amaral MCF, Lee RE, Costanzo JP. Enzymatic regulation of seasonal glycogen cycling in the freeze-tolerant wood frog, Rana sylvatica. J Comparat Physiol B: Biochem, Syst, and Environ Physiol. 2016;186(8):1045-1058. doi:10.1007/s00360-016-1012-2
Storey KB. Glycolysis and the regulation of cryoprotectant synthesis in liver of the freeze tolerant wood frog. J Comp Physiol B. 1987;157(3):373-380. doi:10.1007/BF00693364
Smolinski MB, Mattice JJL, Storey KB. Regulation of pyruvate kinase in skeletal muscle of the freeze tolerant wood frog, Rana sylvatica. Cryobiology. 2017;77:25-33. doi:10.1016/j.cryobiol.2017.06.002
Underwood A, Newsholme E. Some properties of fructose 1,6-diphosphatase of rat liver and their relation to the control of gluconeogenesis. Biochem J. 1965;95(3):767-774. doi:10.1042/bj0950767
Rakus D, Mamczur P, Gizak A, Dus D, Dzugaj A. Colocalization of muscle FBPase and muscle aldolase on both sides of the Z-line. Biochem Biophys Res Commun. 2003;311(2):294-299. doi:10.1016/j.bbrc.2003.09.209
Rosa JL, Ventura F, Carreras J, Bartrons R. Fructose 2,6-bisphosphate and 6-phosphofructo-2-kinase during liver regeneration. Biochem J. 1990;270:645-649.
Stone SR, Fromm HJ. Studies on the mechanism of adenosine 5ʹ-monophosphate inhibition of bovine liver fructose 1, 6-bisphosphatase. Biochemistry. 1980. doi:10.1021/bi00545a003
Van Schaftingen E, Hers HG. Inhibition of fructose-1,6-bisphosphatase by fructose 2,6-biphosphate. Proc Natl Acad Sci USA. 1981. doi:10.1073/pnas.78.5.2861
Ayna A, Moody PCE. Activity of fructose-1,6-bisphosphatase from Campylobacter jejuni. Biochem Cell Biol. 2020;98(4):518-524. doi:10.1139/bcb-2020-0021
Zhang Ye, Xie Z, Zhou G, Zhang H, Lu J, Zhang WJ. Fructose-1,6-bisphosphatase regulates glucose-stimulated insulin secretion of mouse pancreatic β-cells. Endocrinology. 2010;151(10):4688-4695. doi:10.1210/en.2009-1185
Layne JR, Lee RE, Heil TL. Freezing-induced changes in the heart rate of wood frogs (Rana sylvatica). Am J Physiol. 1989;257(5 pt 2):R1046-R1049. doi:10.1152/ajpregu.1989.257.5.R1046
Layne JackR, Lee RE. Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool. 1987;65(8):2062-2065. doi:10.1139/z87-315
Gromova I, Celis JE. Protein detection in gels by silver staining: a procedure compatible with mass spectrometry. In: Celis JE, Carter N, Hunter T, Shotton D, Simons K, Small JV, eds. Cell Biology. A Laboratory Handbook. Vol 4. Academic Press; 2006. CAA Laboratory Handbook. In: Celis JE, Carter N, Hunter T, Shotton D, Simons K, eds. Vol 4.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1-2):248-254. doi:10.1016/0003-2697(76)90527-3
Smolinski MB, Varma A, Green SR, Storey KB. Purification and regulation of pyruvate kinase from the foot muscle of the anoxia and freeze tolerant marine snail, Littorina littorea. Protein J. 2020;39(5):531-541. doi:10.1007/s10930-020-09934-9
Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 2004;4(6):1633-1649. doi:10.1002/pmic.200300771
Sievers F, Wilm A, Dineen D, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7(1):539. doi:10.1038/msb.2011.75
Marchler-Bauer A, Bo Y, Han L, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45(D1):D200-D203. doi:10.1093/nar/gkw1129
Marchler-Bauer A, Derbyshire MK, Gonzales NR, et al. CDD: NCBI's conserved domain database. Nucleic Acids Res. 2015;43:D222-D226. doi:10.1093/nar/gku1221
Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc. 2010;5(4):725-738. doi:10.1038/nprot.2010.5
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. The I-TASSER suite: protein structure and function prediction. Nat Methods. 2015;12(1):7-8. doi:10.1038/nmeth.3213
Zhang Yang. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008;9(1):40. doi:10.1186/1471-2105-9-40
Brooks SPJ. A program for analyzing enzyme rate data obtained from a microplate reader. Biotechniques. 1994;17(6):1154-1161.
Brooks SPJ. A simple computer program with statistical tests for the analysis of enzyme kinetics. Biotechniques. 1992;13(6):906-911.
Zhang J, Storey KB. RBioplot: an easy-to-use R pipeline for automated statistical analysis and data visualization in molecular biology and biochemistry. PeerJ. 2016;4:e2436. doi:10.7717/peerj.2436
Ke H, Thorpe CM, Seaton BA, Marcus F, Lipscomb WN. Molecular structure of fructose-1,6-bisphosphatase at 2.8-A resolution. Proc Natl Acad Sci USA. 1989;86(5):1475-1479. doi:10.1073/pnas.86.5.1475
Barciszewski J, Szpotkowski K, Wisniewski J, et al. Structural studies of human muscle FBPase. Acta Biochim Pol. 2021;68(1):5-14. doi:10.18388/abp.2020_5554
Storey KB. Organic solutes in freezing tolerance. Comp Biochem Physiol - A Physiol. 1997;117(3):319-326. doi:10.1016/S0300-9629(96)00270-8
Bell RAV, Storey KB. Stable suppression of skeletal muscle fructose-1,6-bisphosphatase during ground squirrel hibernation: potential implications of reversible acetylation as a regulatory mechanism. Cryobiology. 2021;102:97-103. doi:10.1016/j.cryobiol.2021.07.006
Gupta A, Varma A, Storey KB. New insights to regulation of fructose-1,6-bisphosphatase during anoxia in red-eared slider, Trachemys scripta elegans. Biomolecules. 2021;11(10):1548. doi:10.3390/biom11101548
Pilkis SJ, El-Maghrabi MR, McGrane M, Pilkis J, Fox E, Claus TH. Fructose 2,6-bisphosphate: a mediator of hormone action at the fructose 6-phosphate/fructose 1,6-bisphosphate substrate cycle. Mol Cell Endocrinol. 1982;25(3):245-266. doi:10.1016/0303-7207(82)90082-X
Rider MH. Regulation of fructose-2,6-bisphosphate synthesis and breakdown in heart and skeletal muscle. Biochem Soc Trans. 1987;15(5):988-991. doi:10.1042/bst0150988
Vidal H, Roux B, Riou JP. Phosphorylation- and ligand-induced conformational changes of rat liver fructose-1,6-bisphosphatase. Arch Biochem Biophys. 1986;248(2):604-611. doi:10.1016/0003-9861(86)90514-X
Ekdahl KN. Further studies on the phosphorylation and kinetics of rat liver fructose-1,6-bisphosphatase: Importance of the three-dimensional structure of a substrate to protein kinase A1. J Biochem. 1992;112(5):719-723. doi:10.1093/oxfordjournals.jbchem.a123964
Meek DW, Nimmo HG. Effects of phosphorylation on the kinetic properties of rat liver fructose-1,6-bisphosphatase. Biochem J. 1984;222(1):125-130. doi:10.1042/bj2220125
Storey KB, Storey JM. Natural freeze tolerance in ectothermic vertebrates. Annu Rev Physiol. 1992;54:619-637. doi:10.1146/annurev.ph.54.030192.003155
Holden CP, Storey KB. Fructose-1,6-bisphosphatase from a cold-hardy insect: control of cryoprotectant glycerol catabolism. Arch Insect Biochem Physiol. 1995;28(3):225-235. doi:10.1002/arch.940280304
Muise AM, Storey KB. Reversible phosphorylation of fructose 1,6-bisphosphatase mediates enzyme role in glycerol metabolism in the freeze-avoiding gall moth Epiblema scudderiana. Insect Biochem Mol Biol. 1997;27(7):617-623. doi:10.1016/S0965-1748(97)00037-4
Dieni CA, Storey KB. Creatine kinase regulation by reversible phosphorylation in frog muscle. Comp Biochem Physiol B Biochem Mol Biol. 2009;152(4):405-412. doi:10.1016/j.cbpb.2009.01.012
Abnous K, Dieni CA, Storey KB. Suppression of MAPKAPK2 during mammalian hibernation. Cryobiology. 2012;65(3):235-241. doi:10.1016/j.cryobiol.2012.06.009
Struvay C, Feller G. Optimization to low temperature activity in psychrophilic enzymes. Int J Mol Sci. 2012;13(9):11643-11665. doi:10.3390/ijms130911643
Siddiqui KS, Cavicchioli R. Cold-adapted enzymes. Annu Rev Biochem. 2006;75:403-433. doi:10.1146/annurev.biochem.75.103004.142723
Bell RAV, Smith JC, Storey KB. Purification and properties of glyceraldehyde-3-phosphate dehydrogenase fromthe skeletal muscle of the hibernating ground squirrel, Ictidomys tridecemlineatus. PeerJ. 2014;2:e634. doi:10.7717/peerj.634
Abboud J, Storey KB. Novel control of lactate dehydrogenase from the freeze tolerant wood frog: role of posttranslational modifications. PeerJ. 2013;1:e12. doi:10.7717/peerj.12
MacDonald JA, Storey KB. Protein phosphatase responses during freezing and thawing in wood frogs: Control of liver cryoprotectant metabolism. Cryo-Letters. 1999;20(5):297-306.
Dieni CA, Storey KB. Regulation of glucose-6-phosphate dehydrogenase by reversible phosphorylation in liver of a freeze tolerant frog. J Comp Physiol B. 2010;180(8):1133-1142. doi:10.1007/s00360-010-0487-5