1qk1 Citations

Crystal structure of human ubiquitous mitochondrial creatine kinase.

Abstract

Creatine kinase (CK), catalyzing the reversible trans-phosphorylation between ATP and creatine, plays a key role in the energy metabolism of cells with high and fluctuating energy requirements. We have solved the X-ray structure of octameric human ubiquitous mitochondrial CK (uMtCK) at 2.7 A resolution, representing the first human CK structure. The structure is very similar to the previously determined structure of sarcomeric mitochondrial CK (sMtCK). The cuboidal octamer has 422 point group symmetry with four dimers arranged along the fourfold axis and a central channel of approximately 20 A diameter, which extends through the whole octamer. Structural differences with respect to sMtCK are found in isoform-specific regions important for octamer formation and membrane binding. Octameric uMtCK is stabilized by numerous additional polar interactions between the N-termini of neighboring dimers, which extend into the central channel and form clamp-like structures, and by a pair of salt bridges in the hydrophobic interaction patch. The five C-terminal residues of uMtCK, carrying positive charges likely to be involved in phospholipid-binding, are poorly defined by electron density, indicating a more flexible region than the corresponding one in sMtCK. The structural differences between uMtCK and sMtCK are consistent with biochemical studies on octamer stability and membrane binding of the two isoforms.

Reviews - 1qk1 mentioned but not cited (2)

  1. Metabolic Basis of Creatine in Health and Disease: A Bioinformatics-Assisted Review. Bonilla DA, Kreider RB, Stout JR, Forero DA, Kerksick CM, Roberts MD, Rawson ES. Nutrients 13 1238 (2021)
  2. Dynamic Interplay between Copper Toxicity and Mitochondrial Dysfunction in Alzheimer's Disease. Tassone G, Kola A, Valensin D, Pozzi C. Life (Basel) 11 386 (2021)

Articles - 1qk1 mentioned but not cited (13)

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Reviews citing this publication (6)

  1. The creatine kinase system and pleiotropic effects of creatine. Wallimann T, Tokarska-Schlattner M, Schlattner U. Amino Acids 40 1271-1296 (2011)
  2. Mitochondrial creatine kinase in human health and disease. Schlattner U, Tokarska-Schlattner M, Wallimann T. Biochim Biophys Acta 1762 164-180 (2006)
  3. Metabolism and function of mitochondrial cardiolipin. Ren M, Phoon CK, Schlame M. Prog Lipid Res 55 1-16 (2014)
  4. Relating structure to mechanism in creatine kinase. McLeish MJ, Kenyon GL. Crit Rev Biochem Mol Biol 40 1-20 (2005)
  5. Mitochondrial cardiolipin/phospholipid trafficking: the role of membrane contact site complexes and lipid transfer proteins. Schlattner U, Tokarska-Schlattner M, Rousseau D, Boissan M, Mannella C, Epand R, Lacombe ML. Chem Phys Lipids 179 32-41 (2014)
  6. The advantage of channeling nucleotides for very processive functions. Zala D, Schlattner U, Desvignes T, Bobe J, Roux A, Chavrier P, Boissan M. F1000Res 6 724 (2017)

Articles citing this publication (33)

  1. Development of EGFR-targeted polymer blend nanocarriers for combination paclitaxel/lonidamine delivery to treat multi-drug resistance in human breast and ovarian tumor cells. Milane L, Duan Z, Amiji M. Mol Pharm 8 185-203 (2011)
  2. Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. Epand RF, Tokarska-Schlattner M, Schlattner U, Wallimann T, Epand RM. J Mol Biol 365 968-980 (2007)
  3. Induced fit in guanidino kinases--comparison of substrate-free and transition state analog structures of arginine kinase. Yousef MS, Clark SA, Pruett PK, Somasundaram T, Ellington WR, Chapman MS. Protein Sci 12 103-111 (2003)
  4. Octameric mitochondrial creatine kinase induces and stabilizes contact sites between the inner and outer membrane. Speer O, Bäck N, Buerklen T, Brdiczka D, Koretsky A, Wallimann T, Eriksson O. Biochem J 385 445-450 (2005)
  5. Structural studies of human brain-type creatine kinase complexed with the ADP-Mg2+-NO3- -creatine transition-state analogue complex. Bong SM, Moon JH, Nam KH, Lee KS, Chi YM, Hwang KY. FEBS Lett 582 3959-3965 (2008)
  6. Multiple interference of anthracyclines with mitochondrial creatine kinases: preferential damage of the cardiac isoenzyme and its implications for drug cardiotoxicity. Tokarska-Schlattner M, Wallimann T, Schlattner U. Mol Pharmacol 61 516-523 (2002)
  7. Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes. Epand RF, Schlattner U, Wallimann T, Lacombe ML, Epand RM. Biophys J 92 126-137 (2007)
  8. C-terminal lysines determine phospholipid interaction of sarcomeric mitochondrial creatine kinase. Schlattner U, Gehring F, Vernoux N, Tokarska-Schlattner M, Neumann D, Marcillat O, Vial C, Wallimann T. J Biol Chem 279 24334-24342 (2004)
  9. Differential effects of peroxynitrite on human mitochondrial creatine kinase isoenzymes. Inactivation, octamer destabilization, and identification of involved residues. Wendt S, Schlattner U, Wallimann T. J Biol Chem 278 1125-1130 (2003)
  10. Divergent enzyme kinetics and structural properties of the two human mitochondrial creatine kinase isoenzymes. Schlattner U, Eder M, Dolder M, Khuchua ZA, Strauss AW, Wallimann T. Biol Chem 381 1063-1070 (2000)
  11. Cloning and expression of mitochondrial and protoflagellar creatine kinases from a marine sponge: implications for the origin of intracellular energy transport systems. Sona S, Suzuki T, Ellington WR. Biochem Biophys Res Commun 317 1207-1214 (2004)
  12. Unassisted refolding of urea-denatured arginine kinase from shrimp Feneropenaeus chinensis: evidence for two equilibrium intermediates in the refolding pathway. Pan JC, Yu Z, Su XY, Sun YQ, Rao XM, Zhou HM. Protein Sci 13 1892-1901 (2004)
  13. Mitochondrial creatine kinase adsorption to biomimetic membranes: a Langmuir monolayer study. Vernoux N, Maniti O, Besson F, Granjon T, Marcillat O, Vial C. J Colloid Interface Sci 310 436-445 (2007)
  14. The tryptophane residues of dimeric arginine kinase: roles of Trp-208 and Trp-218 in active site and conformation stability. Guo Q, Zhao F, Guo SY, Wang X. Biochimie 86 379-386 (2004)
  15. Regulation of brain-type creatine kinase by AMP-activated protein kinase: interaction, phosphorylation and ER localization. Ramírez Ríos S, Lamarche F, Cottet-Rousselle C, Klaus A, Tuerk R, Thali R, Auchli Y, Brunisholz R, Neumann D, Barret L, Tokarska-Schlattner M, Schlattner U. Biochim Biophys Acta 1837 1271-1283 (2014)
  16. Interfacial behavior of cytoplasmic and mitochondrial creatine kinase oligomeric states. Vernoux N, Granjon T, Marcillat O, Besson F, Vial C. Biopolymers 81 270-281 (2006)
  17. Consequences of a six residual deletion from the N-terminal of rabbit muscle creatine kinase. Guo SY, Wang Z, Ni SW, Wang XC. Biochimie 85 999-1005 (2003)
  18. Evidence that the amino acid residue P272 of arginine kinase is involved in its activity, structure and stability. Wu QY, Li F, Wang XY. Int J Biol Macromol 43 367-372 (2008)
  19. Cloning and expression of a lombricine kinase from an echiuroid worm: insights into structural correlates of substrate specificity. Ellington WR, Bush J. Biochem Biophys Res Commun 291 939-944 (2002)
  20. Organization of the gene for an invertebrate mitochondrial creatine kinase: comparisons with genes of higher forms and correlation of exon boundaries with functional domains. Pineda AO, Ellington WR. Gene 265 115-121 (2001)
  21. Letter Creatine kinases: a cornerstone for structural research in the phosphagen kinase family. Wallimann T, Schlattner U. FASEB J 24 7 (2010)
  22. Crystallization and X-ray analysis of the Schistosoma mansoni guanidino kinase. Awama AM, Paracuellos P, Laurent S, Dissous C, Marcillat O, Gouet P. Acta Crystallogr Sect F Struct Biol Cryst Commun 64 854-857 (2008)
  23. Expression of Torpedo californica creatine kinase in Escherichia coli and purification from inclusion bodies. Wang PF, Novak WR, Cantwell JS, Babbitt PC, McLeish MJ, Kenyon GL. Protein Expr Purif 26 89-95 (2002)
  24. Asparagine 285 plays a key role in transition state stabilization in rabbit muscle creatine kinase. Borders CL, MacGregor KM, Edmiston PL, Gbeddy ER, Thomenius MJ, Mulligan GB, Snider MJ. Protein Sci 12 532-537 (2003)
  25. Cooperativity and evolution of Tetrahymena two-domain arginine kinase. Okazaki N, Motomura S, Okazoe N, Yano D, Suzuki T. Int J Biol Macromol 79 696-703 (2015)
  26. Loop movement and catalysis in creatine kinase. Wang PF, Flynn AJ, McLeish MJ, Kenyon GL. IUBMB Life 57 355-362 (2005)
  27. The substrate-free and -bound crystal structures of the duplicated taurocyamine kinase from the human parasite Schistosoma mansoni. Merceron R, Awama AM, Montserret R, Marcillat O, Gouet P. J Biol Chem 290 12951-12963 (2015)
  28. Mitochondrial creatine kinase interaction with heterogeneous monolayers: Effect on lipid lateral organization. Vernoux N, Maniti O, Marcillat O, Vial C, Granjon T. Biochimie 91 752-764 (2009)
  29. The effects of creatine supplementation on striatal neural progenitor cells depend on developmental stage. Andres RH, Ducray AD, Andereggen L, Hohl T, Schlattner U, Wallimann T, Widmer HR. Amino Acids 48 1913-1927 (2016)
  30. Mitochondrial creatine kinase with atypical pI values detected in serum of a patient with ovarian hepatoid yolk sac tumor. Kanemitsu F, Kageoka T, Kira S. J Chromatogr B Analyt Technol Biomed Life Sci 783 191-197 (2003)
  31. Alkylation of rabbit muscle creatine kinase surface methionine residues inhibits enzyme activity in vitro. Steinritz D, Lüling R, Siegert M, Mückter H, Popp T, Reinemer P, Gudermann T, Thiermann H, John H. Arch Toxicol 95 3253-3261 (2021)
  32. Depletion of creatine phosphagen energetics with a covalent creatine kinase inhibitor. Darabedian N, Ji W, Fan M, Lin S, Seo HS, Vinogradova EV, Yaron TM, Mills EL, Xiao H, Senkane K, Huntsman EM, Johnson JL, Che J, Cantley LC, Cravatt BF, Dhe-Paganon S, Stegmaier K, Zhang T, Gray NS, Chouchani ET. Nat Chem Biol 19 815-824 (2023)
  33. Tongue sole creatine kinases function as DAMP and activate antimicrobial immunity via TLR2. Li X, Jiang S, Sun L. Front Immunol 14 1142488 (2023)


Related citations provided by authors (1)

  1. Structure of mitochondrial creatine kinase.. Fritz-Wolf K, Schnyder T, Wallimann T, Kabsch W Nature 381 341-5 (1996)