Differential susceptibility of Plasmodium falciparum versus yeast and mammalian enolases to dissociation into active monomers

FEBS Journal

Volumn 274, Issue 8, 2007, Pages 1932-1945

  Pal Bhowmick, Ipsita ^a   Krishnan, Sadagopan ^a   Jarori, Gotam K ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Enolase; Monomers; Plasmodium falciparum; Rabbit muscle; Yeast

Indexed keywords

ENOLASE; IMIDAZOLE; MAGNESIUM ION; MONOMER;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; GEL FILTRATION CHROMATOGRAPHY; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; THERMOSTABILITY; YEAST;

ANIMALS; CIRCULAR DICHROISM; DIMERIZATION; IMIDAZOLES; KINETICS; PHOSPHOPYRUVATE HYDRATASE; PLASMODIUM FALCIPARUM; PROTEIN CONFORMATION; RABBITS; SACCHAROMYCES CEREVISIAE; SPECIES SPECIFICITY; SPECTROMETRY, FLUORESCENCE;

MAMMALIA; ORYCTOLAGUS CUNICULUS; PLASMODIUM FALCIPARUM;

EID: 34247159617     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05738.x     Document Type: Article

References (60)

1. Wold F (1971) Enolase. In The Enzymes (Boyer PD, eds), Vol. 5, pp. 499-538. Academic Press, New York, NY.
2. Barnes LD & Stellwagen E (1973) Enolase from the thermophile Thermus X-1. Biochemistry 12, 1559-1565.
3. Brown CK, Kuhlman PL, Mattingly S, Slates K, Calie PJ & Farrar WW (1998) A model of the quaternary structure of enolases, based on structural and evolutionary analysis of the octameric enolase from Bacillus subtilis. J Protein Chem 17, 855-866.
4. Kitamura M, Takayama Y, Kojima S, Kohno K, Ogata H, Higuchi Y & Inoue H (2004) Cloning and expression of the enolase gene from Desulfovibrio vulgaris (Miyazaki F). Biochim Biophys Acta 1676, 172-181.
5. Chai G, Brewer JM, Lovelace LL, Aoki T, Minor W & Lebioda L (2004) Expression, purification and the 1.8 angstroms resolution crystal structure of human neuron specific enolase. J Mol Biol 341, 1015-1021.
6. Stec B & Lebioda L (1990) Refined structure of yeast apo-enolase at 2.25 A resolution. J Mol Biol 211, 235-248.
7. Kornblatt MJ, Zheng SX, Lamande N & Lazar M (2002) Cloning, expression and mutagenesis of a subunit contact of rabbit muscle-specific (betabeta) enolase. Biochim Biophys Acta 1597, 311-319.
8. Trepanier D, Wong C & Kornblatt MJ (1990) The salt-induced dissociation and inactivation of a mammalian enolase: evidence for the formation of active monomers. Arch Biochem Biophys 283, 271-277.
9. Gawronski TH & Westhead EW (1969) Equilibrium and kinetic studies on the reversible dissociation of yeast enolase by neutral salts. Biochemistry 8, 4261-4270.
10. Brewer JM & Weber G (1968) The reversible dissociation of yeast enolase. Proc Natl Acad Sci USA 59, 216-223.
11. Kornblatt MJ, Al-Ghanim A & Kornblatt JA (1996) The effects of sodium perchlorate on rabbit muscle enolase - spectral characterization of the monomer. Eur J Biochem 236, 78-84.
12. Holleman WH (1973) The use of absorption optics to measure dissociation of yeast enolase into enzymatically active monomers. Biochim Biophys Acta 327, 176-185.
13. Keresztes-Nagy S & Orman R (1971) Dissociation of yeast enolase into active monomers. Biochemistry 10, 2506-2508.
14. Kornblatt MJ & Hui Bon Hoa G (1987) The pressure-induced inactivation of mammalian enolases is accompanied by dissociation of the dimeric enzyme. Arch Biochem Biophys 252, 277-283.
15. Kornblatt MJ, Lange R & Balny C (1998) Can monomers of yeast enolase have enzymatic activity? Eur J Biochem 251, 775-780.
16. Kornblatt JA, Kornblatt MJ & Hoa GH (1995) Second derivative spectroscopy of enolase at high hydrostatic pressure: an approach to the study of macromolecular interactions. Biochemistry 34, 1218-1223.
17. Kornblatt MJ, Lange R & Balny C (2004) Use of hydrostatic pressure to produce 'native' monomers of yeast enolase. Eur J Biochem 271, 3897-3904.
18. Pancholi V (2001) Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci 58, 902-920.
19. Oelshlegel FJ Jr, Sander BJ & Brewer GJ (1975) Pyruvate kinase in malaria host-parasite interaction. Nature 255, 345-347.
20. Lang-Unnasch N & Murphy AD (1998) Metabolic changes of the malaria parasite during the transition from the human to the mosquito host. Annu Rev Microbiol 52, 561-590.
21. Roth EF Jr, Raventos-Suarez C, Perkins M & Nagel RL (1982) Glutathione stability and oxidative stress in P. falciparum infection in vitro: responses of normal and G6PD deficient cells. Biochem Biophys Res Commun 109, 355-362.
22. Roth E Jr, Joulin V, Miwa S, Yoshida A, Akatsuka J, Cohen-Solal M & Rosa R (1988) The use of enzymopathic human red cells in the study of malarial parasite glucose metabolism. Blood 71, 1408-1413.
23. Mehta M, Sonawat HM & Sharma S (2005) Malaria parasite-infected erythrocytes inhibit glucose utilization in uninfected red cells. FEBS Lett 579, 6151-6158.
24. Pal-Bhowmick I, Sadagopan K, Vora HK, Sehgal A, Sharma S & Jarori GK (2004) Cloning, over-expression, purification and characterization of Plasmodium falciparum enolase. Eur J Biochem 271, 4845-4854.
25. Pal-Bhowmick I, Vora HK, Roy J, Sharma S & Jarori GK (2006) Generation and characterization of monoclonal antibodies specific to Plasmodium falciparum enolase. J Vect Borne Dis 43, 43-52.
26. Schwikowski B, Uetz P & Fields S (2000) A network of protein-protein interactions in yeast. Nat Biotechnol 18, 1257-1261.
27. LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, Hesselberth JR, Schoenfeld LW, Ota I, Sahasrabudhe S, Kurschner C et al. (2005) A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438, 103-107.
28. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M & Sakaki Y (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 98, 4569-4574.
29. Goodsell DS & Olson AJ (2000) Structural symmetry and protein function. Annu Rev Biophys Biomol Struct 29, 105-153.
30. Glaser F, Steinberg DM, Vakser IA & Ben-Tal N (2001) Residue frequencies and pairing preferences at protein-protein interfaces. Proteins 43, 89-102.
31. Perez-Montfort R, Gomez-Puyou MT & Gomez-Puyou A (2002) The interfaces of oligomeric proteins as targets for drug design against enzymes from parasites. Curr Top Med Chem 2, 457-470.
32. Digard P, Williams KP, Hensley P, Brooks IS, Dahl CE & Coen DM (1995) Specific inhibition of herpes simplex virus DNA polymerase by helical peptides corresponding to the subunit interface. Proc Natl Acad Sci USA 92, 1456-1460.
33. Singh SK, Maithal K, Balaram H & Balaram P (2001) Synthetic peptides as inactivators of multimeric enzymes: inhibition of Plasmodium falciparum triosephosphate isomerase by interface peptides. FEBS Lett 501, 19-23.
34. Bowman MJ & Chmielewski J (2002) Novel strategies for targeting the dimerization interface of HIV protease with cross-linked interfacial peptides. Biopolymers 66, 126-133.
35. Liuzzi M, Deziel R, Moss N, Beaulieu P, Bonneau AM, Bousquet C, Chafouleas JG, Garneau M, Jaramillo J, Krogsrud RL et al. (1994) A potent peptidomimetic inhibitor of HSV ribonucleotide reductase with antiviral activity in vivo. Nature 372, 695-698.
36. Cochran AG (2000) Antagonists of protein-protein interactions. Chem Biol 7, R85-R94.
37. McMillan K, Adler M, Auld DS, Baldwin JJ, Blasko E, Browne LJ, Chelsky D, Davey D, Dolle RE, Eagen KA et al. (2000) Allosteric inhibitors of inducible nitric oxide synthase dimerization discovered via combinatorial chemistry. Proc Natl Acad Sci USA 97, 1506-1511.
38. Young K, Lin S, Sun L, Lee E, Modi M, Hellings S, Husbands M, Ozenberger B & Franco R (1998) Identification of a calcium channel modulator using a high throughput yeast two-hybrid screen. Nat Biotechnol 16, 946-950.
39. Poyner RR, Cleland WW & Reed GH (2001) Role of metal ions in catalysis by enolase: an ordered kinetic mechanism for a single substrate enzyme. Biochemistry 40, 8009-8017.
40. Faller LD, Baroudy BM, Johnson AM & Ewall RX (1977) Magnesium ion requirements for yeast enolase activity. Biochemistry 16, 3864-3869.
41. da Silva Giotto MT, Hannaert V, de Vertommen DASNMV, Rider MH, Michels PA, Garratt RC & Rigden DJ (2003) The crystal structure of Trypanosoma brucei enolase: visualisation of the inhibitory metal binding site III and potential as target for selective, irreversible inhibition. J Mol Biol 331, 653-665.
42. Lee BH & Nowak T (1992) Influence of pH on the Mn2+ activation of and binding to yeast enolase: a functional study. Biochemistry 31, 2165-2171.
43. Kornblatt MJ & Klugerman A (1989) Characterization of the enolase isozymes of rabbit brain: kinetic differences between mammalian and yeast enolases. Biochem Cell Biol 67, 103-107.
44. Bohm G, Muhr R & Jaenicke R (1992) Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng 5, 191-195.
45. Duquerroy S, Camus C & Janin J (1995) X-ray structure and catalytic mechanism of lobster enolase. Biochemistry 34, 12513-12523.
46. Wedekind JE, Poyner RR, Reed GH & Rayment I (1994) Chelation of serine 39 to Mg2+ latches a gate at the active site of enolase: structure of the bis(Mg2+) complex of yeast enolase and the intermediate analog phosphonoacetohydroxamate at 2.1-A resolution. Biochemistry 33, 9333-9342.
47. Zhang E, Brewer JM, Minor W, Carreira LA & Lebioda L (1997) Mechanism of enolase: the crystal structure of asymmetric dimer enolase-2-phospho-D- glycerate?enolase-phosphoenolpyruvate at 2.0 A resolution. Biochemistry 36, 12526-12534.
48. Chin CC (1990) The primary structure of rabbit muscle enolase. J Protein Chem 9, 427-432.
49. Kuhnel K & Luisi BF (2001) Crystal structure of the Escherichia coli RNA degradosome component enolase. J Mol Biol 313, 583-592.
50. Janin J, Miller S & Chothia C (1988) Surface, subunit interfaces and interior of oligomeric proteins. J Mol Biol 204, 155-164.
51. Westhead EW (1966) Enolase from yeast and rabbit muscle. Methods Enzymol 9, 670-679.
52. Crowley PB & Golovin A (2005) Cation-pi interactions in protein-protein interfaces. Proteins 59, 231-239.
53. Gallivan JP & Dougherty DA (1999) Cation-pi interactions in structural biology. Proc Natl Acad Sci USA 96, 9459-9464.
54. Wu Y & Voth GA (2005) A computational study of the closed and open states of the influenza A M2 proton channel. Biophys J 89, 2402-2411.
55. Loewenthal R, Sancho J & Fersht AR (1992) Histidine-aromatic interactions in barnase: elevation of histidine pKa and contribution to protein stability. J Mol Biol 224, 759-770.
56. Vivas L, Easton A, Kendrick H, Cameron A, Lavandera JL, Barros D, de las Heras FG, Brady RL & Croft SL (2005) Plasmodium falciparum: stage specific effects of a selective inhibitor of lactate dehydrogenase. Exp Parasitol 111, 105-114.
57. Sriram G, Martinez JA, McCabe ER, Liao JC & Dipple KM (2005) Single-gene disorders: what role could moonlighting enzymes play? Am J Hum Genet 76, 911-924.
58. Stapel SO & de Jong WW (1983) Lamprey 48-kDa lens protein represents a novel class of crystallins. FEBS Lett 162, 305-309.
59. Wistow GJ, Lietman T, Williams LA, Stapel SO, de Jong WW, Horwitz J & Piatigorsky J (1988) Tau-crystallin?alpha-enolase: one gene encodes both an enzyme and a lens structural protein. J Cell Biol 107, 2729-2736.
60. Wold F & Ballou CE (1957) Studies on the enzyme enolase. I. Equilibrium studies. J Biol Chem 227, 301-312.