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Enzymes

  • Natalya Kurochkina
Chapter

Abstract

Enzymes increase rate of chemical reactions. Structure of the enzyme reveals how functional groups and the entire molecule work together to optimize this process. Structural data combined with kinetic data allow propose and refine catalytic mechanisms, understand relationships between structure and function of the enzyme, and apply this knowledge to design new enzymes, inhibitors, modulators, and activators for industrial and biomedical applications. From first steps to modern approaches, studies of enzymes bring new isoforms that work more efficiently and selectively than native molecules.

Keywords

Enzyme Catalysis Specificity Stereoselectivity Active site 

References

  1. Achilonu I, Gildenhuys S, Fisher L, Burke J, Fanucchi S, Sewell BT, Fernandes M, Dirr HW (2010) The role of a topologically conserved isoleucine in glutathione transferase structure, stability and function. Acta Crystallogr Sect F Struct Biol Cryst Commun 66(Pt 7):776–780.  https://doi.org/10.1107/S1744309110019135. Epub 2010 Jun 23. PubMed PMID: 20606271; PubMed Central PMCID: PMC2898459CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arif A (2012) Extraneuronal activities and regulatory mechanisms of the atypical cyclin-dependent kinase Cdk5. Biochem Pharmacol 84:985–993CrossRefGoogle Scholar
  3. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25:25–29. http://www.ncbi.nlm.nih.gov/pubmed/10802651?ordinalpos=3&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVDocSum CrossRefGoogle Scholar
  4. Azzi L, Meijer L, Ostvold A-C, Lew J, Wang JH (1994) Purification of a 15-kDa cdk4- and cdk5-binding Protein. J Biol Chem 269:13279–13288PubMedGoogle Scholar
  5. Ayala R, Shu T, Tsai LH (2007) Trecking across the brain: the journey of neuronal migration. Cell 128:29–43CrossRefGoogle Scholar
  6. Balchin D, Fanucchi S, Achilonu I, Adamson RJ, Burke J, Fernandes M, Gildenhuys S, Dirr HW (2010) Stability of the domain interface contributes towards the catalytic function at the H-site of class alpha glutathione transferase A1-1. Biochim Biophys Acta 1804(12):2228–2233.  https://doi.org/10.1016/j.bbapap.2010.09.003. Epub 2010 Sep 15. PubMed PMID: 20833278CrossRefPubMedGoogle Scholar
  7. Bernstein FC, Koetzle TF, Williams GJB, Meyer EF Jr, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) The protein data bank: a computer-based archival file for macromolecular structures. J Mol Biol 112:535CrossRefGoogle Scholar
  8. Board PG, Coggan M, Watson S, Gage PW, Dulhunty AF (2004) CLIC-2 modulates cardiac ryanodine receptor Ca2+ release channels. Int J Biochem Cell Biol 36(8):1599–1612. PubMed PMID: 15147738CrossRefGoogle Scholar
  9. Bodra N, Young D, Astolfi Rosado L, Pallo A, Wahni K, De Proft F, Huang J, Van Breusegem F, Messens J (2017) Arabidopsis thaliana dehydroascorbate reductase 2: Conformational flexibility during catalysis. Sci Rep 7:42494. doi: 10.1038/srep42494. Erratum in: Sci Rep 7:46896. PubMed PMID: 28195196; PubMed Central PMCID: PMC5307357Google Scholar
  10. Brinkkoetter PT, Olivier P, Wu JS, Henderson S, Krofft RD, Pippin JW, Hockenbery D, Roberts JM, Shankland SJ (2009) J Clin Invest 119:3089CrossRefGoogle Scholar
  11. Brock J, Board PG, Oakley AJ (2013) Structural insights into omega-class glutathione transferases: a snapshot of enzyme reduction and identification of a non-catalytic ligandin site. PLoS One 8(4):e60324.  https://doi.org/10.1371/journal.pone.0060324. Print 2013. PubMed PMID: 23593192; PubMed Central PMCID: PMC3621891CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brown NR, Noble MEM, Endicott JE, Johnson LN (1999) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Cell biology 1:438–443PubMedGoogle Scholar
  13. Bryda EC, Ling H, Rathbun DE, Burmeister M, Flaherty L (1996) Fine genetic map of mouse chromosome 10 around the polycystic kidney disease gene, jcpk, and ankyrin 3. Genomics 35(3):425–430. PubMed PMID: 8812475CrossRefGoogle Scholar
  14. Caing-Carlsson R, Goyal P, Sharma A, Ghosh S, Setty TG, North RA et al (2017) Crystal structure of N-acetylmannosamine kinase from Fusobacterium nucleatum. Acta Crystallogr Sect F Struct Biol Cryst Commun 73(Pt 6):356–362.  https://doi.org/10.1107/S2053230X17007439 CrossRefGoogle Scholar
  15. Chan W, Sit ST, Manser E (2011a) The Cdc42-associated kinase ACK1 is not autoinhibited but requires Src for Activation. Biochem J. (2011) 435:355–364CrossRefGoogle Scholar
  16. Chan PW, Yakunin AF, Edwards EA, Pai EF (2011b) Mapping the reaction coordinates of enzymatic defluorination. J Am Chem Soc 133(19):7461–7468.  https://doi.org/10.1021/ja200277d. Epub 2011 Apr 21. PubMed PMID: 21510690; PubMed Central PMCID: PMC3101105CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chin L, Gray JW (2008) Translating insights from the cancer genome into clinical practice. Nature 452:553–563CrossRefGoogle Scholar
  18. Cho HY, Maeng SJ, Cho HJ, Choi YS, Chung JM, Lee S, Kim HK, Kim JH, Eom CY, Kim YG, Guo M, Jung HS, Kang BS, Kim S (2015) Assembly of multi-tRNA Synthetase complex via heterotetrameric glutathione transferase-homology domains. J Biol Chem 290(49):29313–29328.  https://doi.org/10.1074/jbc.M115.690867. Epub 2015 Oct 15. PubMed PMID: 26472928; PubMed Central PMCID: PMC4705937CrossRefPubMedPubMedCentralGoogle Scholar
  19. Comba FN, Romero MR, Garay FS, Baruzzi AM (2018) Mucin and carbon nanotube-based biosensor for detection of glucose in human plasma. Anal Biochem 550:34–40. doi: 10.1016/j.ab.2018.04.006. [Epub ahead of print] PubMed PMID: 29649474CrossRefGoogle Scholar
  20. Contreras-Vallejos E, Utreras E, Gonzalez-Billault C (2012) Going out of the brain: Non-nervous system physiological and pathological functions of Cdk5. Cellular Signalling 24(2012):44–52CrossRefGoogle Scholar
  21. Demelash A, Rudrabhatla P, Pant HC, Wang X, Amin ND, McWhite CD, Xu N, Ilona Linnoila R (2012) Achaete-scute homologue-1 (ASH1) stimulates migration of lung cancer cells through Cdk5/p35 pathway. Mol Biol Cell 23:2856–2866CrossRefGoogle Scholar
  22. Effertz K, Hinderlich S, Reutter W (1999) Selective Loss of either the Epimerase or Kinase Activity of UDP-N-acetylglucosamine 2-Epimerase/N-Acetylmannosamine Kinase due to Site-directed Mutagenesis Based on Sequence Alignments. J Biol Chem 274:28771CrossRefGoogle Scholar
  23. Eisenberg I, Avidan N, Potikha T, Hochner H, Chen M, Olender T, Barash M, Shemesh M, Sadeh M, Grabov-Nardini G, Shmilevich I, Friedmann A, Karpati G, Bradley WG, Baumbach L, Lancet D, Asher EB, Beckmann JS, Argov Z, Mitrani-Rosenbaum S (2001) The UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy. Nat Genet 29:83CrossRefGoogle Scholar
  24. Ferofontov A, Strulovich R, Marom M, Giladi M, Haitin Y (2018) Inherent flexibility of CLIC6 revealed by crystallographic and solution studies. Sci Rep 8(1):6882.  https://doi.org/10.1038/s41598-018-25231-z. PubMed PMID: 29720717; PubMed Central PMCID: PMC5931990CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fredslund F, Borchert MS, Poulsen JN, Mortensen SB, Perner M, Streit WR, Lo LL (2018) Structure of a hyperthermostable carbonic anhydrase identified from an active hydrothermal vent chimney. Enzyme Microb Technol 114:48–54.  https://doi.org/10.1016/j.enzmictec.2018.03.009. Epub 2018 Mar 30. PubMed PMID: 29685353CrossRefPubMedGoogle Scholar
  26. Fritz-Wolf K, Becker K, Rahlfs S, Harwaldt P, Schirmer RH, Kabsch W, Becker K (2003) X-ray structure of glutathione S-transferase from the malarial parasite Plasmodium falciparum. 100(24):13821–13826Google Scholar
  27. Ghaderi D, Strauss HM, Reinke S, Cirak S, Reutter W, Lucka L, Hinderlich S (2007) Evidence for dynamic interplay of different oligomeric states of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase by biophysical methods. J Mol Biol 369:746–758CrossRefGoogle Scholar
  28. Goto M, Miyahara I, Hayashi H, Kagamiyama H, Hirotsu K (2003) Crystal structures of branched-chain amino acid aminotransferase complexed with glutamate and glutarate: true reaction intermediate and double substrate recognition of the enzyme. Biochemistry 42(13):3725–3733. PubMed PMID: 12667063CrossRefGoogle Scholar
  29. Haa BH, Matthew J, Davisa B, Chena C, Loua HJ, Jia Gaoa C, Zhanga R, Krauthammerd M, Halabane R, Schlessingera J, Turka BE, Boggon TJ (2012) Type II p21-activated kinases (PAKs) are regulated by an autoinhibitory pseudosubstrate. Proc Natl Acad Sci 109:16107–16112CrossRefGoogle Scholar
  30. Hall BE, Prochazkova M, Sapio MR, Minetos P, Kurochkina N, Binukumar BK, Amin ND, Terse A, Joseph J, Raithel SJ, Mannes AJ, Pant HC, Chung MK, Iadarola MJ, Kulkarni AB (2018) Phosphorylation of the Transient Receptor Potential Ankyrin 1 by Cyclin-dependent Kinase 5 affects Chemo-nociception. Sci Rep 8(1):1177.  https://doi.org/10.1038/s41598-018-19532-6. PubMed PMID: 29352128; PubMed Central PMCID: PMC5775258CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hinderlich S, Stasche R, Zeitler R, Reitter W (1997) A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis of rat liver. Purification and characterization of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase. J Biol Chem 272:24313–24318CrossRefGoogle Scholar
  32. Huizing M (2005) Disease mechanisms associated with mutations of the GNE gene. Drug discovery today: Disease mechanisms 2:519–527CrossRefGoogle Scholar
  33. Huizing M, Krasnewich DM (2009) Hereditary inclusion body myopathy: a decade of progress. Biochim Biophys Acta 1792:881CrossRefGoogle Scholar
  34. Huizing M, Rakocevic G, Sparks SE, Mamali I, Shatunov A, Goldfarb L, Krasnewich D, Gahl WA, Dalakas MC (2004) Hypoglycosylation of alpha-dystroglycan in patients with hereditary IBM due to GNE mutations. Mol Genet Metab 81:196CrossRefGoogle Scholar
  35. Jeffrey PD, Russo AA, Polyak K, Gibbs E, Hurwltz J, Massague J, Pavletich NP (1995) Mechanism of CDK activationrevealed by the structure of a cyclinA-CDK2 complex. Nature 376:313–320CrossRefGoogle Scholar
  36. Jeppesen MG, Ortiz P, Shepard W et al (2003) The Crystal Structure of the Glutathione S-Transferase-like Domain of Elongation Factor 1B from Saccharomyces cerevisiae. J Biol Chem 278:47190–47198CrossRefGoogle Scholar
  37. Kamei H, Saito T, Ozawa M, Fujita‡ Y, Asada‡ A, Bibb§ JA, Takaomi C, Saido HS, Hisanaga S-i (2007) Cleavage of the CDK5 activator p35 to p25 by site-specific phosphorylation. J Biol Chem 282:1687–1694CrossRefGoogle Scholar
  38. Karpusas M, Axarli I, Chiniadis L, Papakyriakou A, Bethanis K, Scopelitou K, Clonis YD, Labrou NE (2013) The interaction of the chemotherapeutic drug chlorambucil with human glutathione transferase A1-1: kinetic and structural analysis. PLoS One 8(2):e56337.  https://doi.org/10.1371/journal.pone.0056337. Epub 2013 Feb 27. PubMed PMID: 23460799; PubMed Central PMCID: PMC3584069CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kendrew JC, Bodo G, Dintzis HM, Parrish RG, Wyckoff H, Phillips DC (1958) A three-dimensional model of the myoglobin molecule obtained by x-ray analysis. Nature 181(4610):662–666CrossRefGoogle Scholar
  40. Kim KJ, Park MC, Choi SJ, Oh YS, Choi EC, Cho HJ, Kim MH, Kim SH, Kim DW, Kim S, Kang BS (2008) Determination of three-dimensional structure and residues of the novel tumor suppressor AIMP3/p18 required for the interaction with ATM. J Biol Chem 283(20):14032–14040.  https://doi.org/10.1074/jbc.M800859200. Epub 2008 Mar 14. PubMed PMID: 18343821CrossRefPubMedGoogle Scholar
  41. Kim TH, Mehrabi P, Ren Z, Sljoka A, Ing C, Bezginov A, Ye L, Pomès R, Prosser RS, Pai EF (2017) The role of dimer asymmetry and protomer dynamics in enzyme catalysis. Science 355(6322). pii: eaag2355. doi:10.1126/science.aag2355. PubMed PMID: 28104837CrossRefGoogle Scholar
  42. Ko TP, Lai SJ, Hsieh TJ, Yang CS, Chen Y (2018) The tetrameric structure of sialic acid-synthesizing UDP-GlcNAc 2-epimerase from Acinetobacter baumannii: A comparative study with human GNE. J Biol Chem. 293(26):10119–10127. doi:  https://doi.org/10.1074/jbc.RA118.001971. Epub 2018 May 15. PubMed PMID: 29764940; PubMed Central PMCID: PMC6028959CrossRefGoogle Scholar
  43. Kontur WS, Bingman CA, Olmsted CN, Wassarman DR, Ulbrich A, Gall DL, Smith RW, Yusko LM, Fox BG, Noguera DR, Coon JJ, Donohue TJ (2018) Novosphingobium aromaticivorans uses a Nu-class glutathione S-transferase as a glutathione lyase in breaking the ß-aryl ether bond of lignin. J Biol Chem 293(14):4955–4968. doi:  https://doi.org/10.1074/jbc.RA117.001268. Epub 2018 Feb 15. PubMed PMID: 29449375; PubMed Central PMCID: PMC5892560.CrossRefGoogle Scholar
  44. Kurochkina N, Bhaskar M, Yadav SP, Pant HC (2018) Phosphorylation, Dephosphorylation, and multiprotein assemblies regulate dynamic behavior of neuronal cytoskeleton: a mini-review. Front Mol Neurosci 11:373.  https://doi.org/10.3389/fnmol.2018.00373. eCollection 2018. PubMed PMID: 30349458; PubMed Central PMCID: PMC6186834CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kurochkina N (2007) J Theor Biol 247:110–121CrossRefGoogle Scholar
  46. Kurochkina N (2008) J Theor Biol 255:188–198CrossRefGoogle Scholar
  47. Kurochkina N, Choekyi T (2011) Helix-helix interfaces and ligand binding. J Theor Biol 283:92–102CrossRefGoogle Scholar
  48. Kurochkina N, Guha U (2013) SH3 domains: modules of protein-protein interactions. Biol Rev 5:29–39Google Scholar
  49. Lapouge K, Smith SJM, Walker PA, Gamblin SJ, Smerdon SJ, Rittinger K (2000) Structure of the TPR Domain of p67phox in Complex with Rac·GTP. Molecula Cell 6:899–907CrossRefGoogle Scholar
  50. Lim LH, Pervaiz S (2007) Annexin 1: the new face of an old molecule. Faseb J 21:968–975CrossRefGoogle Scholar
  51. Mapelli M, Massimiliano L, Crovace C, Seeliger MA, Tsai L-H, Meijer L, Musacchio A (2005) Mechanism of CDK5/p25 binding by CDK inhibitors. J Med Chem 2005(48):671–679CrossRefGoogle Scholar
  52. Martinez J, Nguyen LD, Hinderlich S, Zimmer R, Tauberger E, Reutter W et al (2012) Crystal structures of N-Acetylmannosamine Kinase provide insights into enzyme activity and inhibition. J Biol Chem 287(17):13656–13665.  https://doi.org/10.1074/jbc.M111.318170 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Mott HR, Owen D, Nietlispach D, Lowe PN, Manser E, Limk L, Laue ED (1999) Structure of the small G protein Cdc42 bound to the GTPase-binding domain of ACK. Nature 399:384–388CrossRefGoogle Scholar
  54. Noble ME, Endicott JA, Brown NR, Johnson LN (1997) The cyclin box fold: protein recognition in cell-cycle and transcription control. Trends Biochem Sci 22:482–487CrossRefGoogle Scholar
  55. Ohshima T, Ward JM, Huh CG, Longenecker G, Veeranna Pant HC, Brady RO, Martin LJ, Kulkarni AB (1996) Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc Natl Acad Sci USA 93:11173–11178CrossRefGoogle Scholar
  56. Pareek TK, Keller J, Kesavapany S, Agarwal N, Kuner R, Pant H, Iadarola MJ, Brady RO, Kulkarni AB (2006) Cyclin-dependent kinase 5 modulates nociceptive signaling through direct phosphorylation of transient receptor potential vanilloid 1. Proc Natl Acad Sci 104:660–665CrossRefGoogle Scholar
  57. Perutz MF, Rossmann MG, Cullis AF, Muirhead H, Will G, North AC (1960) Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5-A. resolution, obtained by X-ray analysis. Nature 185(4711):416–422. PubMed PMID: 18990801 CrossRefGoogle Scholar
  58. Ramkumar K, Samanta S, Kyani A, Yang S, Tamura S, Ziemke E, Stuckey JA, Li S, Chinnaswamy K, Otake H, Debnath B, Yarovenko V, Sebolt-Leopold JS, Ljungman M, Neamati N (2016) Mechanistic evaluation and transcriptional signature of a glutathione S-transferase omega 1 inhibitor. Nat Commun 7:13084.  https://doi.org/10.1038/ncomms13084. PubMed PMID: 27703239; PubMed Central PMCID: PMC5059489
  59. Reinke SO, Eidenschink C, Jay CM, Hinderlich S (2009) Biochemical characterization of human and murine isoforms of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase (GNE). Glycoconj J 26:415CrossRefGoogle Scholar
  60. Romney DK, Murciano-Calles J, Wehrmüller JE, Arnold FH (2017) Unlocking reactivity of TrpB: a general biocatalytic platform for synthesis of tryptophan analogues. J Am Chem Soc 139(31):10769–10776.  https://doi.org/10.1021/jacs.7b05007. Epub 2017 Jul 28. PubMed PMID: 28708383; PubMed Central PMCID: PMC5589443CrossRefGoogle Scholar
  61. Rubin DL, Lewis SE, Mungall CJ, Misra S, Westerfield M, Ashburner M, Sim I, Chute CG, Solbrig H, Storey MA, Smith B, Richter JD, Noy NF, Musen MA (2006) The national center for biomedical ontology: advancing biomedicine through structured organization of scientific knowledge. OMICS 10:185–198CrossRefGoogle Scholar
  62. Saleh T, Kalodimos CG (2017) Enzymes at work are enzymes in motion. Science 355(6322):247–248.  https://doi.org/10.1126/science.aal4632. PubMed PMID: 28104853CrossRefGoogle Scholar
  63. Sayer C, Martinez-Torres RJ, Richter N, Isupov MN, Hailes HC, Littlechild JA, Ward JM (2014) The substrate specificity, enantioselectivity and structure of the (R)-selective amine: pyruvate transaminase from Nectria haematococca. FEBS J 281(9):2240–2253.  https://doi.org/10.1111/febs.12778. Epub 2014 Apr 7. PubMed PMID: 24618038; PubMed Central PMCID: PMC4255305CrossRefGoogle Scholar
  64. Schulze-Gahmen U, Kim S-H (2002) Structural basis for CDK6 activation by a virus-encoded cyclin. Nature Str Biol 9:177–181Google Scholar
  65. Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16CrossRefGoogle Scholar
  66. Chen S-C, Huang C-H, Lai S-J, Yang CS, Hsiao T-H, Lin C-H, Fu P-K, Ko T-P, Chen Y (2016) Mechanism and inhibition of human UDP-GlcNAc 2-epimerase, the key enzyme in sialic acid biosynthesis. Sci Rep 6:23274.  https://doi.org/10.1038/srep23274 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13(12):1501–1512. Review. PubMed PMID: 10385618CrossRefGoogle Scholar
  68. Sicheri F, Moarefi I, Kuriyan J (1997) Crystal structure of the Src family tyrosine kinase Hck. Nature 385:602–609CrossRefGoogle Scholar
  69. Sparks SE, Ciccone C, Lalor M, Orvisky E, Klootwijk R, Savelkoul PJ, Dalakas MC, Krasnewich DM, Gahl WA, Huizing M (2005) Use of a cell-free system to determine UDP-N-acetylglucosamine 2-epimerase and N-acetylmannoseamine kinase activities in human hereditary inclusion body myopathy. Glycobiology 15:1102CrossRefGoogle Scholar
  70. Sundaram JR, Poore CP, Sulaimee NHB, Pareek T, Asad ABMA, Rajkumar R, Cheong WF, Wenk MR, Dawe GS, Chuang K-H, Pant HC, Kesavapan S (2013) Specific inhibition of p25/Cdk5 activity by the Cdk5 inhibitory peptide reduces neurodegeneration in vivo. J Neurosci 33(1):334–343CrossRefGoogle Scholar
  71. Tajima Y, Uyama E, Go S, Sato C, Tao N, Kotani M, Hino H, Suzuki A, Sanai Y, Kitajima K, Sakuraba H (2005) Distal myopathy with rimmed vacuoles: impaired O-glycan formation in muscular glycoproteins. Am J Pathol 166:1121CrossRefGoogle Scholar
  72. Tarricone C, Dhavan R, Peng J, Areces LB, Tsai L-H, Musacchio A (2001) Structure and regulation of the CDK5-p25nck5a complex. Mol Cell 8:657–669CrossRefGoogle Scholar
  73. Valenzuela-Chavira I, Contreras-Vergara CA, Arvizu-Flores AA, Serrano-Posada H, Lopez-Zavala AA, García-Orozco KD, Hernandez-Paredes J, Rudiño-Piñera E, Stojanoff V, Sotelo-Mundo RR, Islas-Osuna MA (2017) Insights into ligand binding to a glutathione S-transferase from mango: Structure, thermodynamics and kinetics. Biochimie 135:35–45.  https://doi.org/10.1016/j.biochi.2017.01.005. Epub 2017 Jan 17. PubMed PMID: 28104507; PubMed Central PMCID: PMC5346462.CrossRefGoogle Scholar
  74. Vuilleumier S (1997) Minireview. Bacterial glutathione S-transferases: What are they good for? J Bact 179:1431–1441CrossRefGoogle Scholar
  75. Wang C, Shang Y, Yu J, Zhang M (2012) Substrate recognition mechanism of atypical protein Kinase Cs revealed by the structure of PKCi in complex with a substrate peptide from Par-3. Structure 20:791–801CrossRefGoogle Scholar
  76. Yang J, Cron P, Good VM, Thompson V, Hemmings BA, Barford D (2002) Crystal structure of an activated Akt/protein kinase B ternary complex with GSK3-peptide and AMP-PNP. Nat Struct Biol 9(12):940–944. PubMed PMID: 12434148CrossRefGoogle Scholar
  77. Yuan C, Li J, Selby TL (1999) Byeon I-J L and Tsai M-D (1999) tumor suppressor INK4: comparisons of conformational properties between p16INK4A and p18INK4C J. Mol Biol 294:201–211CrossRefGoogle Scholar
  78. Zheng Y-L, Li B-S, Rudrabhatla P, Shukla V, Amin ND, Maric D, Kesavapany S, Kanungo J, Pareek TK, Takahashi S, Grant P, Kulkarni AB, Pant HC (2010a) Phosphorylation of p27Kip1 at Thr187 by Cyclin-dependent Kinase 5 modulates neural stem cell differentiation. Mol Biol Cell 21:3601–3614CrossRefGoogle Scholar
  79. Zheng Y-L, Amin ND, Hu Y-F, Rudrabhatla P, Shukla V, Kanungo J, Kesavapany S, Grant P, Albers W, Pant HC (2010b) A 24-residue Peptide (p5), derived from p35, the Cdk5 neuronal activator, specifically inhibits Cdk5-p25 hyperactivity and tau hyperphosphorylation. J Biol Chem 285(44):34202–34212CrossRefGoogle Scholar
  80. Zukerberg LR, Patrick GN, Nikolic M, Humbert S, Wu CL, Lanier LM, Gertler FB, Vidal M, Van Etten RA, Tsai LH (2000) Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 26(3):633–646. PubMed PMID: 10896159CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Natalya Kurochkina
    • 1
  1. 1.Department of BiophysicsSchool of Theoretical ModelingWashington, DCUSA

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