Dynamic Oligomeric Properties

  • Norbert W. Seidler
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 985)


This chapter provides a foundation for further research into the relationship between dynamic oligomeric properties and functional diversity. The structural basis that underlies the conformational sub-states of the GAPDH oligomer is discussed. The issue of protein stability is given a thorough analysis, since it is well-established that the primary strategy for protein oligomerization is to stabilize conformation. Several factors that affect oligomerization are described, including chemical modification by synthetic reagents. The effects of native substrates and coenzymes are also discussed. The curious feature of chloride ions having a de-stabilizing effect on native GAPDH structure is described. Additionally, the role of adenine dinucleotides in tetramer-dimer equilibrium dynamics is suggested to be a major part of the physiological regulation of GAPDH structure and function. This chapter also contends that a vast amount of useful information can come from comparative analyses of diverse species, particularly regarding protein stability and subunit-subunit interaction. Lastly, the concept of domain exchange is introduced as a means of understanding the stabilization of dynamic oligomers, suggesting that inter-subunit contacts may also be a way of masking docking sites to other proteins.


Adenine Nucleotide Succinic Anhydride Sedimentation Coefficient Bacillus Stearothermophilus Negative Cooperativity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Hoagland VD Jr, Teller DC (1969) Influence of substrates on the dissociation of rabbit muscle D-glyceraldehyde 3-phosphate dehydrogenase. Biochemistry 8:594–602PubMedGoogle Scholar
  2. 2.
    Liang SJ, Lin YZ, Zhou JM et al (1990) Dissociation and aggregation of D-glyceraldehyde-3-phosphate dehydrogenase during denaturation by guanidine hydrochloride. Biochim Biophys Acta 1038:240–246PubMedGoogle Scholar
  3. 3.
    Harris J, Waters M (1975) Glyceraldehyde-3-phosphate dehydrogenase. In: Boyer PD (ed) The enzymes, vol 13. Academic, OrlandoGoogle Scholar
  4. 4.
    Kirschner K, Gallego E, Schuster I et al (1971) Co-operative binding of nicotinamide-adenine dinucleotide to yeast glyceraldehyde-3-phosphate dehydrogenase. J Mol Biol 58:29–50PubMedGoogle Scholar
  5. 5.
    Kirschner K (1971) Co-operative binding of nicotinamide-adenine dinucleotide to yeast glyceraldehyde-3-phosphate dehydrogenase. J Mol Biol 58:51–68PubMedGoogle Scholar
  6. 6.
    Conway A, Koshland DE Jr (1968) Negative cooperativity in enzyme action. Biochemistry 7:4011–4023PubMedGoogle Scholar
  7. 7.
    de Vijlder JJ, Boers W, Slater EC (1969) Binding and properties of NAD+ in glyceraldehydephosphate dehydrogenase from lobster-tail muscle. Biochim Biophys Acta 191:214–220PubMedGoogle Scholar
  8. 8.
    Moras D, Olsen KW, Sabesan MN et al (1975) Studies of asymmetry in the three-dimensional structure of lobster D-glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 250:9137–9162PubMedGoogle Scholar
  9. 9.
    Shaltiel S, Tauber-Finkelstein M (1971) Introduction of an intramolecular crosslink at the active site of glyceraldehyde 3-phosphate dehydrogenase. Biochem Biophys Res Commun 44:484–490PubMedGoogle Scholar
  10. 10.
    Méjean C, Pons F, Benyamin Y et al (1989) Antigenic probes locate binding sites for the glycolytic enzymes glyceraldehyde-3-phosphate dehydrogenase, aldolase and phosphofructokinase on the actin monomer in microfilaments. Biochem J 264:671–677PubMedGoogle Scholar
  11. 11.
    Tanner JJ, Hecht RM, Krause KL (1996) Determinants of enzyme thermostability observed in the molecular structure of Thermus aquaticus D-glyceraldehyde-3-phosphate dehydrogenase at 25 angstroms resolution. Biochemistry 35:2597–2609PubMedGoogle Scholar
  12. 12.
    Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88–118PubMedGoogle Scholar
  13. 13.
    Koshland DE Jr, Némethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5:365–385PubMedGoogle Scholar
  14. 14.
    Furfine CS, Velick SF (1965) The acyl-enzyme intermediate and the kinetic mechanism of the glyceraldehyde 3-phosphate dehydrogenase reaction. J Biol Chem 240:844–855PubMedGoogle Scholar
  15. 15.
    Boers W, Oosthuizen C, Slater EC (1971) Binding of NAD+ and NADH to rabbit-muscle glyceraldehydephosphate dehydrogenase. Biochim Biophys Acta 250:35–46PubMedGoogle Scholar
  16. 16.
    Kelemen N, Kellershohn N, Seydoux F (1975) Sturgeon glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 57:69–78PubMedGoogle Scholar
  17. 17.
    Seydoux F, Bernhard S, Pfenninger O et al (1973) Preparation and active-site specific properties of sturgeon muscle glyceraldehyde-3-phoshate dehydrogenase. Biochemistry 12:4290–4300PubMedGoogle Scholar
  18. 18.
    Krimsky I, Racker E (1955) Acyl derivatives of glyceraldehyde-3-phosphate dehydrogenase. Science 122:319–321PubMedGoogle Scholar
  19. 19.
    Racker E, Krimsky I (1952) The mechanism of oxidation of aldehydes by glyceralde-hyde-3-phosphate dehydrogenase. J Biol Chem 198:731–743PubMedGoogle Scholar
  20. 20.
    Buehner M, Ford GC, Olsen KW et al (1974) Three-dimensional structure of D-glyceraldehyde-3-phosphate dehydrogenase. J Mol Biol 90:25–49PubMedGoogle Scholar
  21. 21.
    Markossian KA, Khanova HA, Yu S et al (2006) Mechanism of thermal aggregation of rabbit muscle glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 45:13375–13384PubMedGoogle Scholar
  22. 22.
    Durchschlag H et al (1971) X-Ray small-angle scattering of yeast glyceraldehyde-3-phosphate dehydrogenase as a function of saturation with nicotinamide-adenine-dinucleotide. Eur J Biochem 19:9–22PubMedGoogle Scholar
  23. 23.
    Seidler NW, Yeargans GS (2002) Effects of thermal denaturation on protein glycation. Life Sci 70:1789–1799PubMedGoogle Scholar
  24. 24.
    Suzuki K, Imahori K (1973) Glyceraldehyde 3-phosphate dehydrogenase of Bacillus stearothermophilus. Kinetics and physicochemical studies. J Biochem 74:955–970PubMedGoogle Scholar
  25. 25.
    Roitel O, Ivinova O, Muronetz V et al (2002) Thermal unfolding used as a probe to characterize the intra- and intersubunit stabilizing interactions in phosphorylating D-glyceraldehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus. Biochemistry 41:7556–7564PubMedGoogle Scholar
  26. 26.
    Jia B, le Linh T, Lee S et al (2011) Biochemical characterization of glyceraldehyde-3-phosphate dehydrogenase from Thermococcus kodakarensis KOD1. Extremophiles 15:337–346PubMedGoogle Scholar
  27. 27.
    Littlechild JA, Guy JE, Isupov MN (2004) Hyperthermophilic dehydrogenase enzymes. Biochem Soc Trans 32:255–258PubMedGoogle Scholar
  28. 28.
    Isupov MN, Fleming TM, Dalby AR et al (1999) Crystal structure of the glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic archaeon Sulfolobus solfataricus. J Mol Biol 291:651–660PubMedGoogle Scholar
  29. 29.
    Fernandez-Lafuente R (2009) Stabilization of multimeric enzymes: strategies to prevent subunit dissociation. Enzyme Microb Tech 45:405–418Google Scholar
  30. 30.
    Mrabet NT, Van den Broeck A, Van den brande I et al (1992) Arginine residues as stabilizing elements in proteins. Biochemistry 31:2239–2253PubMedGoogle Scholar
  31. 31.
    Fridovich I (1963) Inhibition of acetoacetic decarboxylase by anions. The Hofmeister lyotropic series. J Biol Chem 238:592–598PubMedGoogle Scholar
  32. 32.
    Wang CC, Tsou CL (1993) Protein disulfide isomerase is both an enzyme and a chaperone. FASEB J 7:1515–1517PubMedGoogle Scholar
  33. 33.
    Fu XM, Zhu BT (2010) Human pancreas-specific protein disulfide-isomerase (PDIp) can function as a chaperone independently of its enzymatic activity by forming stable complexes with denatured substrate proteins. Biochem J 429:157–169PubMedGoogle Scholar
  34. 34.
    Ruddock LW, Freedman RB, Klappa P (2000) Specificity in substrate binding by protein folding catalysts: tyrosine and tryptophan residues are the recognition motifs for the binding of peptides to the pancreas-specific protein disulfide isomerase PDIp. Protein Sci 9:758–764PubMedGoogle Scholar
  35. 35.
    Ferns JE, Theisen CS, Fibuch EE et al (2012) Protection against protein aggregation by alpha-crystallin as a mechanism of preconditioning. Neurochem Res 37:244–252PubMedGoogle Scholar
  36. 36.
    Diamant S, Eliahu N, Rosenthal D et al (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591PubMedGoogle Scholar
  37. 37.
    Mehta AD, Seidler NW (2005) β-Alanine suppresses heat inactivation of lactate dehydrogenase. J Enzyme Inhib Med Chem 20:199–203PubMedGoogle Scholar
  38. 38.
    Lin YZ, Liang SJ, Zhou JM et al (1990) Comparison of inactivation and conformational changes of D-glyceraldehyde-3-phosphate dehydrogenase during thermal denaturation. Biochim Biophys Acta 1038:247–252PubMedGoogle Scholar
  39. 39.
    Velasco PT, Lukas TJ, Murthy SN et al (1997) Hierarchy of lens proteins requiring protection against heat-induced precipitation by the alpha crystallin chaperone. Exp Eye Res 65:497–505PubMedGoogle Scholar
  40. 40.
    Khanova HA, Markossian KA, Kleimenov SY et al (2007) Effect of alpha-crystallin on thermal denaturation and aggregation of rabbit muscle glyceraldehyde-3-phosphate dehydrogenase. Biophys Chem 125:521–531PubMedGoogle Scholar
  41. 41.
    Lin Z, Schwartz FP, Eisenstein E (1995) The hydrophobic nature of GroEL-substrate binding. J Biol Chem 270:1011–1014PubMedGoogle Scholar
  42. 42.
    Naletova IN, Muronetz VI, Schmalhausen EV (2006) Unfolded, oxidized, and thermoinactivated forms of glyceraldehyde-3-phosphate dehydrogenase interact with the chaperonin GroEL in different ways. Biochim Biophys Acta 1764:831–838PubMedGoogle Scholar
  43. 43.
    Polyakova OV, Roitel O, Asryants RA et al (2005) Misfolded forms of glyceraldehydes-3-phosphate dehydrogenase interact with GroEL and inhibit chaperonin-assisted folding of the wild-type enzyme. Protein Sci 14:921–928PubMedGoogle Scholar
  44. 44.
    Roitel O, Sergienko E, Branlant G (1999) Dimers generated from tetrameric phosphorylating glyceraldehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus are inactive but exhibit cooperativity in NAD binding. Biochemistry 38:16084–16091PubMedGoogle Scholar
  45. 45.
    Roitel O, Vachette P, Azza S et al (2003) P but not R-axis interface is involved in cooperative binding of NAD on tetrameric phosphorylating glyceraldehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus. J Mol Biol 326:1513–1522PubMedGoogle Scholar
  46. 46.
    Trost P, Fermani S, Marri L et al (2006) Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase: autonomous vs. CP12-dependent mechanisms. Photosynth Res 89:263–275PubMedGoogle Scholar
  47. 47.
    Cerff R, Chambers SE (1979) Subunit structure of higher plant glyceraldehyde-3-phosphate dehydrogenases (EC and EC J Biol Chem 254:6094–6098PubMedGoogle Scholar
  48. 48.
    Pohlmeyer K, Paap BK, Soll J et al (1996) CP12: a small nuclear-encoded chloroplast protein provides novel insights into higher-plant GAPDH evolution. Plant Mol Biol 32:969–978PubMedGoogle Scholar
  49. 49.
    Erales J, Lignon S, Gontero B (2009) CP12 from Chlamydomonas reinhardtii, a permanent specific “chaperone-like” protein of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 284:12735–12744PubMedGoogle Scholar
  50. 50.
    Lin Z, Wang C, Tsou C (2000) High concentrations of D-glyceraldehyde-3-phosphate dehydrogenase stabilize the enzyme against denaturation by low concentrations of GuHCl. Biochim Biophys Acta 1481:283–288PubMedGoogle Scholar
  51. 51.
    Ren G, Lin Z, Tsou CL, Wang CC (2003) Effects of macromolecular crowding on the unfolding and the refolding of D-glyceraldehyde-3-phosophospate dehydrogenase. J Protein Chem 22:431–439PubMedGoogle Scholar
  52. 52.
    Chilson OP, Kitto GB, Pudles J et al (1966) Reversible inactivation of dehydrogenases. J Biol Chem 241:2431–2445PubMedGoogle Scholar
  53. 53.
    Kim JY, Theisen CS, Seidler NW (2011) GAPDH architecture at low guanidine concentrations: first derivative analysis of the descending slope of the UV absorbance peak. In: Arabnia HR, Tran Q-N (eds) Proceedings of the 2011 international conference on bioinformatics and computational biology, vol 2. CSREA Press, Las VegasGoogle Scholar
  54. 54.
    Baldwin RL (2005) Early days of studying the mechanism of protein folding. In: Buchner J, Kiefhaber T (eds) Protein folding handbook, vol 1. Wiley-VCH, WeiheimGoogle Scholar
  55. 55.
    Wetlaufer DB (1973) Nucleation, rapid folding, and globular intrachain regions in proteins. Proc Natl Acad Sci USA 70:697–701PubMedGoogle Scholar
  56. 56.
    Lesk AM, Rose GD (1990) Folding units in globular proteins. Proc Natl Acad Sci USA 78:4304–4308Google Scholar
  57. 57.
    Duzhenkova IV, Asriiants RA, Muronets VI et al (1986) Immobilized active monomers of D-glyceraldehyde-3-phosphate dehydrogenase from rabbit skeletal muscles and their coenzyme-binding properties. Biokhimiia 51:1899–1907PubMedGoogle Scholar
  58. 58.
    Deal WC Jr (1969) Metabolic control and structure of glycolytic enzymes. Biochemistry 8:2795–2805PubMedGoogle Scholar
  59. 59.
    Krebs H, Rudolph R, Jaenicke R (1979) Influence of coenzyme on the refolding and reassociation in vitro of glyceraldehyde-3-phosphate dehydrogenase from yeast. Eur J Biochem 100:359–364PubMedGoogle Scholar
  60. 60.
    Anfinsen CB, Scheraga HA (1975) Experimental and theoretical aspects of protein folding. Adv Protein Chem 29:205–300PubMedGoogle Scholar
  61. 61.
    Jaenicke R (1978) Folding and association of oligomeric enzymes. Naturwissenschaften 65:569–577PubMedGoogle Scholar
  62. 62.
    Rudolph R, Gerschitz J, Jaenicke R (1978) Effect of zinc(II) on the refolding and reactivation of liver alcohol dehydrogenase. Eur J Biochem 87:601–606PubMedGoogle Scholar
  63. 63.
    Mounaji K, Vlassi M, Erraiss NE et al (2003) In vitro effect of metal ions on the activity of two amphibian glyceraldehyde-3-phosphate dehydrogenases: potential metal binding sites. Comp Biochem Physiol B Biochem Mol Biol 135:241–254PubMedGoogle Scholar
  64. 64.
    Krotkiewska B, Banaś T (1992) Interaction of Zn2+ and Cu2+ ions with glyceraldehyde-3-phosphate dehydrogenase from bovine heart and rabbit muscle. Int J Biochem 24:1501–1505PubMedGoogle Scholar
  65. 65.
    Fox JB Jr, Dandliker WB (1956) A study of some of the physical properties of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 218:53–57PubMedGoogle Scholar
  66. 66.
    Taylor JF, Lowry C (1956) The molecular weights of some crystalline enzymes from muscle and yeast. I. Aldolase and D-glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 20:109–114PubMedGoogle Scholar
  67. 67.
    Elias HG, Garbe A, Lamprecht W (1960) The determination of the molecular weight of D-glyceraldehyde-3-phosphate dehydrogenase. Hoppe Seylers Z Physiol Chem 319:22–34PubMedGoogle Scholar
  68. 68.
    Harrington WF, Karr GM (1965) Subunit structure of glyceraldehyde 3-phosphate dehydrogenase. J Mol Biol 13:885–893Google Scholar
  69. 69.
    Harris JI, Perham RN (1965) Glyceraldehyde 3-phosphate dehydrogenases. I. The protein chains in glyceraldehyde 3-phosphate dehydrogenase from pig muscle. J Mol Biol 13:876–884Google Scholar
  70. 70.
    Osborne HH, Hollaway MR (1975) The investigation of substrate-induced changes in subunit interactions in glyceraldehyde 3-phosphate dehydrogenases by measurement of the kinetics and thermodynamics of subunit exchange. Biochem J 151:37–45PubMedGoogle Scholar
  71. 71.
    Pattin AE, Ochs S, Theisen CS et al (2010) Isoflurane’s effect on interfacial dynamics in GAPDH influences methylglyoxal reactivity. Arch Biochem Biophys 498:7–12PubMedGoogle Scholar
  72. 72.
    Elodi P, Jecsai G (1960) Studies on D-glyceraldehyde-3-phosphate dehydrogenase. XV. The effect of urea. Acta Physiol Acad Sci Hung 17:175–182PubMedGoogle Scholar
  73. 73.
    Elodi P, Jecsai G, Mozolovszky A (1960) Studies on D-glyceraldehyde-3-phosphate dehydrogenase. XIV. The effect of pH on the steric properties. Acta Physiol Acad Sci Hung 17:165–173PubMedGoogle Scholar
  74. 74.
    Jaenicke R, Schmid D, Knof S (1968) Monodispersity and quaternary structure of glyceraldehyde 3-phosphate dehydrogenase. Biochemistry 7:919–926PubMedGoogle Scholar
  75. 75.
    Meighen EA, Schachman HK (1970) Hybridization of native and chemically modified enzymes. II. Native and succinylated glyceraldehyde 3-phosphate dehydrogenase. Biochemistry 9:1177–1184PubMedGoogle Scholar
  76. 76.
    Spotorno GM, Hollaway MR (1970) Hybrid molecules of yeast and rabbit GPD containing native and modified subunits. Nature 226:756–757Google Scholar
  77. 77.
    Suzuki K, Harris JI (1975) Hybridization of glyceraldehyde-3-phosphate dehydrogenase. J Biochem 77:587–593PubMedGoogle Scholar
  78. 78.
    Nagradova NK, Guseva MK (1971) Reversible dissociation of glyceraldehyde-3-phosphate dehydrogenase from rat skeletal muscles. Biokhimiia 36:841–847PubMedGoogle Scholar
  79. 79.
    Constantinides SM, Deal WC Jr (1969) Reversible dissociation of tetrameric rabbit muscle glyceraldehyde 3-phosphate dehydrogenase into dimers or monomers by adenosine triphosphate. J Biol Chem 244:5695–5702PubMedGoogle Scholar
  80. 80.
    Yang ST, Deal WC Jr (1969) Metabolic control and structure of glycolytic enzymes. VI. Competitive inhibition of yeast glyceraldehyde 3-phosphate dehydrogenase by cyclic adenosine monophosphate, adenosine triphosphate, and other adenine-containing compounds. Biochemistry 8:2806–2813PubMedGoogle Scholar
  81. 81.
    Bolotina IA, Markovich DS, Volkenstein MV et al (1967) Investigation of the conformation of D-glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 132:260–270PubMedGoogle Scholar
  82. 82.
    Magar ME (1967) Optical rotatory dispersion of aldolase and glyceraldehyde 3-phosphate dehydrogenase. J Biol Chem 242:2517–2521PubMedGoogle Scholar
  83. 83.
    Ovãdi J, Telegdi M, Batke J et al (1971) Functional non-identity of subunits and isolation of active dimers of D-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 22:430–438PubMedGoogle Scholar
  84. 84.
    Agatova AI (1967) The influence of n-propylgallate and cystein upon the quaternary structure of D-glyceraldehyde-3-phosphate dehydrogenase from the rabbit muscles. Biokhimiia 32:1107–1114PubMedGoogle Scholar
  85. 85.
    Nagradova NK (1986) The role of oligomeric structure in the functioning of D-glyceraldehyde-3-phosphate dehydrogenase. Biokhimiia 51:2030–2053PubMedGoogle Scholar
  86. 86.
    Smith GD, Schachman HK (1973) Effect of D2O and nicotinamide adenine dinucleotide on the sedimentation properties and structure of glyceraldehyde phosphate dehydrogenase. Biochemistry 12:3789–3801PubMedGoogle Scholar
  87. 87.
    Fahien LA (1966) A study of the reaction of glyceraldehyde with glyceraldehyde 3-phosphate dehydrogenase. J Biol Chem 241:4115–4123PubMedGoogle Scholar
  88. 88.
    Greene FC, Feeney RE (1970) Properties of muscle glyceraldehyde-3-phosphate dehydrogenase from the cold-adapted antarctic fish Dissostichus mawsoni. Biochim Biophys Acta 220:430–442PubMedGoogle Scholar
  89. 89.
    Molina y Vedia L, McDonald B, Reep B et al (1992) Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation. J Biol Chem 267:24929–24932PubMedGoogle Scholar
  90. 90.
    Butler PJ, Harris JI, Hartley BS et al (1967) Reversible blocking of peptide amino groups by maleic anhydride. Biochem J 103:78P–79PPubMedGoogle Scholar
  91. 91.
    Bruton CJ, Hartley BS (1968) Sub-unit structure and specificity of methionyl-transfer-ribonucleic acid synthetase from Escherichia coli. Biochem J 108:281–288PubMedGoogle Scholar
  92. 92.
    Rapoport G, Davis L, Horecker BL (1969) The subunit structure of the fructose diphosphate aldolase from spinach leaf. Arch Biochem Biophys 132:286–293PubMedGoogle Scholar
  93. 93.
    Sia CL, Traniello S, Pontremoli S et al (1969) Studies on the subunit structure of rabbit liver fructose diphosphatase. Arch Biochem Biophys 132:325–330PubMedGoogle Scholar
  94. 94.
    Buehner M, Ford GC, Moras D et al (1973) D-glyceraldehyde-3-phosphate dehydrogenase: three-dimensional structure and evolutionary significance. Proc Natl Acad Sci USA 70:3052–3054PubMedGoogle Scholar
  95. 95.
    Harris JI, Polgár L (1965) Amino acid sequence around a reactive lysine in glyceraldehyde 3-phosphate dehydrogenase. Mol Biol 14:630–633Google Scholar
  96. 96.
    Polgar L (1964) Specific acetylation of a lysine residue during the hydrolytic action of glyceraldehyde-3-phosphate dehydrogenase. Acta Physiol Acad Sci Hung 25:1–4PubMedGoogle Scholar
  97. 97.
    Polgár L (1966) The effect of coenzyme on the S-N acyl migration in glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 118:276–284PubMedGoogle Scholar
  98. 98.
    Park JH, Shaw DC, Mathew E et al (1970) Enzymatic characterization of the N-acetylation of 3-phosphoglyceraldehyde dehydrogenase by acetyl phosphate. J Biol Chem 245:2946–2953PubMedGoogle Scholar
  99. 99.
    Forcina BG, Ferri G, Zapponi MC et al (1971) Identification of lysines reactive with pyridoxal 5′-phosphate in glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 20:535–540PubMedGoogle Scholar
  100. 100.
    Zapponi MC, Ferri G, Forcina BG et al (1973) Reaction of rabbit muscle apo-glyceraldehyde-3-P-dehydrogenase with pyridoxal-5′-phosphate. FEBS Lett 31:287–291PubMedGoogle Scholar
  101. 101.
    Elodi P (1958) Comparative studies on D-glyceraldehyde-3-phosphate dehydrogenases. II. Physicochemical investigations. Acta Physiol Hung 13:199–206PubMedGoogle Scholar
  102. 102.
    Wang Z, Nicholls SJ, Rodriguez ER et al (2007) Protein carbamylation links inflammation, smoking, uremia and atherogenesis. Nat Med 13:1176–1184PubMedGoogle Scholar
  103. 103.
    Habeeb AF, Cassidy HG, Singer SJ (1958) Molecular structural effects produced in proteins by reaction with succinic anhydride. Biochim Biophys Acta 29:587–593PubMedGoogle Scholar
  104. 104.
    Klotz IM, Keresztes-Nagy S (1963) Hemerythrin: molecular weight and dissociation into subunits. Biochemistry 2:445–452PubMedGoogle Scholar
  105. 105.
    Allen G, Harris JI (1976) Succinylation of glyceraldehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus. A reactive threonine residue in the apoenzyme. Eur J Biochem 62:601–612PubMedGoogle Scholar
  106. 106.
    Bloxham DP, Sharma RP (1979) The development of SS′-polymethylenebis(methanethiosulphonates) as reversible cross-linking reagents for thiol groups and their use to form stable catalytically active cross-linked dimers within glyceraldehyde 3-phosphate dehydrogenase. Biochem J 181:355–366PubMedGoogle Scholar
  107. 107.
    Bottoms CA, Smith PE, Tanner JJ (2002) A structurally conserved water molecule in Rossmann dinucleotide-binding domains. Protein Sci 11:2125–2137PubMedGoogle Scholar
  108. 108.
    Rudolph R, Heider I, Jaenicke R (1977) Mechanism of reactivation and refolding of glyceraldehyde-3-phosphate dehydrogenase from yeast after denaturation and dissociation. Eur J Biochem 81:563–570PubMedGoogle Scholar
  109. 109.
    Lakatos S, Závodsky P (1976) The effect of substrates on the association equilibrium of mammalian D-glyceraldehyde 3-phosphate dehydrogenase. FEBS Lett 63:145–148PubMedGoogle Scholar
  110. 110.
    Osborne HH, Hollaway MR (1976) An investigation of the nicotinamide-adenine dinucleotide-induced ‘tightening’ of the structure of glyceraldehyde 3-phosphate dehydrogenase. Biochem J 157:255–259PubMedGoogle Scholar
  111. 111.
    Nagradova NK, Golovina TO, Mevkh AT (1974) Immobilized dimers of D-glyceraldehyde-3-phosphate dehydrogenase. FEBS Lett 49:242–245PubMedGoogle Scholar
  112. 112.
    Ovádi J, Batke J, Bartha F et al (1979) Effect of association-dissociation on the catalytic properties of glyceraldehyde 3-phosphate dehydrogenase. Arch Biochem Biophys 193:28–33PubMedGoogle Scholar
  113. 113.
    Ovádi J, Keleti T (1978) Kinetic evidence for interaction between aldolase and D-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 85:157–161PubMedGoogle Scholar
  114. 114.
    Cerff R (1979) Quaternary structure of higher plant glyceraldehyde-3-phosphate dehydrogenases. Eur J Biochem 94:243–247PubMedGoogle Scholar
  115. 115.
    Cerff R, Chambers SE (1978) Glyceraldehyde-3-phosphate dehydrogenase (NADP) from Sinapis alba L. Isolation and electrophoretic characterization of isoenzymes. Hoppe Seylers Z Physiol Chem 359:769–772PubMedGoogle Scholar
  116. 116.
    Nagradova NK, Muronetz VI, Grozdova ID et al (1975) Cold inactivation of glyceraldehyde-phosphate dehydrogenase from rat skeletal muscle. Biochim Biophys Acta 377:15–25PubMedGoogle Scholar
  117. 117.
    Chilson OP, Kitto GB, Kaplan NO (1965) Factors affecting the reversible dissociation of dehydrogenases. Proc Natl Acad Sci USA 53:1006–1014PubMedGoogle Scholar
  118. 118.
    Nagy B, Jencks WP (1965) Depolymerization of f-actin by concentrated solutions of salts and denaturing agents. J Am Chem Soc 87:2480–2488PubMedGoogle Scholar
  119. 119.
    Markert CL (1963) Lactate dehydrogenase isozymes: dissociation and recombination of subunits. Science 140:1329–1330PubMedGoogle Scholar
  120. 120.
    Glass TL, Hylemon PB (1980) Characterization of a pyridine nucleotide-nonspecific glutamate dehydrogenase from Bacteroides thetaiotaomicron. J Bacteriol 141:1320–1330PubMedGoogle Scholar
  121. 121.
    Tagaki W, Westheimer FH (1968) Acetoacetate decarboxylase. Reassociation of subunits. Biochemistry 7:891–894PubMedGoogle Scholar
  122. 122.
    Marion JD, Van DN, Bell JE et al (2010) Measuring the effect of ligand binding on the interface stability of multimeric proteins using dynamic light scattering. Anal Biochem 407:278–280PubMedGoogle Scholar
  123. 123.
    Warren JC, Stowring L, Morales MF (1966) The effect of structure-disrupting ions on the activity of myosin and other enzymes. J Biol Chem 241:309–316PubMedGoogle Scholar
  124. 124.
    Beeckmans S, Kanarek L (1982) Subunit interactions in pig heart fumarase–I. Study of tetramer-dimer equilibrium in dilute urea solutions. Int J Biochem 14:965–970PubMedGoogle Scholar
  125. 125.
    Stancel GM, Deal WC Jr (1968) Metabolic control and structure of glycolytic enzymes. V. Dissociation of yeast glyceraldehyde-3-phosphate dehydrogenase into subunits by ATP. Biochem Biophys Res Commun 31:398–403PubMedGoogle Scholar
  126. 126.
    Stancel GM, Deal WC Jr (1969) Reversible dissociation of yeast glyceraldehyde 3-phosphate dehydrogenase by adenosine triphosphate. Biochemistry 8:4005–4011PubMedGoogle Scholar
  127. 127.
    Yang ST, Deal WC Jr (1969) Metabolic control and structure of glycolytic enzymes. VII. Destabilization and inactivation of yeast glyceraldehyde 3-phosphate dehydrogenase by adenosine phosphates and chymotrypsin. Biochemistry 8:2814–2820PubMedGoogle Scholar
  128. 128.
    Kauzmann W (1959) Some factors in the interpretation of protein denaturation. Adv Protein Chem 14:1–63PubMedGoogle Scholar
  129. 129.
    Tisdale EJ (2002) Glyceraldehyde-3-phosphate dehydrogenase is phosphorylated by protein kinase Ciota/lambda and plays a role in microtubule dynamics in the early secretory pathway. J Biol Chem 277:3334–3341PubMedGoogle Scholar
  130. 130.
    Seo J, Jeong J, Kim YM et al (2008) Strategy for comprehensive identification of post-translational modifications in cellular proteins, including low abundant modifications: application to glyceraldehyde-3-phosphate dehydrogenase. J Proteome Res 7:587–602PubMedGoogle Scholar
  131. 131.
    Baalmann E, Scheibe R, Cerff R et al (1996) Functional studies of chloroplast glyceraldehyde-3-phosphate dehydrogenase subunits A and B expressed in Escherichia coli: formation of highly active A4 and B4 homotetramers and evidence that aggregation of the B4 complex is mediated by the B subunit carboxy terminus. Plant Mol Biol 32:505–513PubMedGoogle Scholar
  132. 132.
    Laschet JJ, Minier F, Kurcewicz I et al (2004) Glyceraldehyde-3-phosphate dehydrogenase is a GABAA receptor kinase linking glycolysis to neuronal inhibition. J Neurosci 24:7614–7622PubMedGoogle Scholar
  133. 133.
    Baxi MD, Vishwanatha JK (1995) Uracil DNAglycosylase/glyceraldehyde-3-phosphate dehydrogenase is an Ap4A binding protein. Biochemistry 34:9700–9707PubMedGoogle Scholar
  134. 134.
    Nakagawa T, Nagayama F (1989) Enzymatic properties of glyceraldehyde-3-phosphate dehydrogenase from fish muscle. Comp Biochem Physiol B 93:379–384PubMedGoogle Scholar
  135. 135.
    Marcinkowska A, Danielewicz R, Wolny M (1990) The effect of temperature on catalytic function of glyceraldehyde-3-phosphate dehydrogenase from muscle of pig and carp Cyprinus carpio. Comp Biochem Physiol B 97:49–54PubMedGoogle Scholar
  136. 136.
    Lebherz HG, Savage B, Abacherli E (1973) Adenine nucleotide-mediated subunit exchange between isoenzymes of glyceraldehyde-3-phosphate dehydrogenase. Nat New Biol 245:269–271PubMedGoogle Scholar
  137. 137.
    Kemp BE, Pearson RB (1990) Protein kinase recognition sequence motifs. Trends Biochem Sci 15:342–346PubMedGoogle Scholar
  138. 138.
    Rescigno M, Perham RN (1994) Structure of the NADPH-binding motif of glutathione reductase: efficiency determined by evolution. Biochemistry 33:5721–5727PubMedGoogle Scholar
  139. 139.
    Pancholi V, Fischetti VA (1992) A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med 176:415–426PubMedGoogle Scholar
  140. 140.
    Talfournier F, Colloc’h N, Mornon JP et al (1999) Functional characterization of the phosphorylating D-glyceraldehyde 3-phosphate dehydrogenase from the archaeon Methanothermus fervidus by comparative molecular modelling and site-directed mutagenesis. Eur J Biochem 265:93–104PubMedGoogle Scholar
  141. 141.
    Schlunegger MP, Bennett MJ, Eisenberg D (1997) Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly. Adv Protein Chem 50:61–122PubMedGoogle Scholar
  142. 142.
    Pieters BJ, Fibuch EE, Eklund JD et al (2010) Inhaled anesthetics promote albumin dimerization through reciprocal exchange of subdomains. Biochem Res Int 2010:516704PubMedGoogle Scholar
  143. 143.
    Eklund JD, Seidler NW (2009) Computational analysis of shifts in the fluorescence spectra of human serum albumin. In: Arabnia HR (ed) Proceedings of the 2009 international conference on bioinformatics and computational biology, vol 1. CSREA Press, Las VegasGoogle Scholar
  144. 144.
    Marchetti A, Abril-Marti M, Illi B et al (1995) Analysis of the Myc and Max interaction specificity with λ repressor-HLH domain fusions. J Mol Biol 248:541–550PubMedGoogle Scholar
  145. 145.
    Gotte G, Libonati M (2004) Oligomerization of ribonuclease A: two novel three-dimensional domain-swapped tetramers. J Biol Chem 279:36670–36679PubMedGoogle Scholar
  146. 146.
    Patel S, Balaji PV, Sasidhar YU (2007) The sequence TGAAKAVALVL from glyceraldehyde-3-phosphate dehydrogenase displays structural ambivalence and interconverts between alpha-helical and beta-hairpin conformations mediated by collapsed conformational states. J Pept Sci 13:314–326PubMedGoogle Scholar
  147. 147.
    Kuznetsov IB, Rackovsky S (2003) On the properties and sequence context of structurally ambivalent fragments in proteins. Protein Sci 12:2420–2433PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Norbert W. Seidler
    • 1
  1. 1.Department of BiochemistryKansas City University of Medicine and BiosciencesKansas CityUSA

Personalised recommendations