X-ray analysis of phosphoglycerate kinase 2, a sperm-specific isoform from Mus musculus

Proteins: Structure, Function and Genetics

Volumn 71, Issue 3, 2008, Pages 1134-1144

  Sawyer, Gregory M ^a   Monzingo, Arthur F ^a   Poteet, Ethan C ^a   O'Brien, Deborah A ^b   Robertus, Jon D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Catalytic conformation; Glycolysis; Membrane localization; Open conformation; Sequence comparison; X ray crystallography

Indexed keywords

ADENOSINE TRIPHOSPHATE; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE KINASE 1; PHOSPHOGLYCERATE KINASE2; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ANALYSIS; FLAGELLUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; SPERM; X RAY;

AMINO ACID SEQUENCE; ANIMALS; APOENZYMES; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; GLYCERIC ACIDS; ISOENZYMES; MALE; MICE; MICE, INBRED C3H; MOLECULAR SEQUENCE DATA; PHOSPHOGLYCERATE KINASE; PROTEIN STRUCTURE, TERTIARY; SPERMATOZOA; SUBSTRATE SPECIFICITY;

MAMMALIA; MUS MUSCULUS;

EID: 42449098514     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21801     Document Type: Article

References (61)

1. Eddy EM. Male germ cell gene expression. Recent Prog Horm Res 2002;57:103-128.
2. Welch JE, Brown PL, O'Brien DA, Magyar PL, Bunch DO, Mori C, Eddy EM. Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J Androl 2000;21:328-338.
3. Mori C, Nakamura N, Welch JE, Gotoh H, Goulding EH, Fujioka M, Eddy EM. Mouse spermatogenic cell-specific type 1 hexokinase (mHk1-s) transcripts are expressed by alternative splicing from the mHk1 gene and the HK1-S protein is localized mainly in the sperm tail. Mol Reprod Dev 1998;49:374-385.
4. Millan JL, Driscoll CE, LeVan KM, Goldberg E. Epitopes of human testis-specific lactate dehydrogenase deduced from a cDNA sequence. Proc Natl Acad Sci USA 1987;84:5311-5315.
5. McCarrey JR, Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 1987;326:501-505.
6. Boer PH, Adra CN, Lau YF, McBurney MW. The testis-specific phosphoglycerate kinase gene pgk-2 is a recruited retroposon. Mol Cell Biol 1987;7:3107-3112.
7. Eddy EM, Toshimori K, O'Brien DA. Fibrous sheath of mammalian spermatozoa. Microsc Res Tech 2003;61:103-115.
8. Travis AJ, Jorgez CJ, Merdiushev T, Jones BH, Dess DM, Diaz-Cueto L, Storey BT, Kopf GS, Moss SB. Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J Biol Chem 2001;276:7630-7636.
9. Bradley MP, Geelan A, Leitch V, Goldberg E. Cloning, sequencing, and characterization of LDH-C4 from a fox testis cDNA library. Mol Reprod Dev 1996;44:452-459.
10. Westhoff D, Kamp G. Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J Cell Sci 1997;110 (Part 15):1821-1829.
11. Bunch DO, Welch JE, Magyar PL, Eddy EM, O'Brien DA. Glyceraldehyde 3-phosphate dehydrogenase-S protein distribution during mouse spermatogenesis. Biol Reprod 1998;58:834-841.
12. Krisfalusi M, Miki K, Magyar PL, O'Brien DA. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod 2006;75:270-278.
13. Beyler SA, Wheat TE, Goldberg E. Binding of antibodies against antigenic domains of murine lactate dehydrogenase-C4 to human and mouse spermatozoa. Biol Reprod 1985;32:1201-1210.
14. Gillis BA, Tamblyn TM. Association of bovine sperm aldolase with sperm subcellular components. Biol Reprod 1984;31:25-35.
15. Jones AR, Cooper TG. A re-appraisal of the post-testicular action and toxicity of chlorinated antifertility compounds. Int J Androl 1999;22:130-138.
16. Goldberg E. Isozymes in testes and spermatozoa. Curr Top Biol Med Res 1977;1:79-124.
17. Williams AC, Ford WC. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl 2001;22:680-695.
18. Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, Strader LF, Perreault SD, Eddy EM, O'Brien DA. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci USA 2004;101:16501-16506.
19. Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod 2004;71:540-547.
20. Curi SM, Ariagno JI, Chenlo PH, Mendeluk GR, Pugliese MN, Sardi Segovia LM, Repetto HE, Blanco AM. Asthenozoospermia: analysis of a large population. Arch Androl 2003;49:343-349.
21. Watson HC, Walker NP, Shaw PJ, Bryant TN, Wendell PL, Fothergill LA, Perkins RE, Conroy SC, Dobson MJ, Tuite MF, Kingsman AJ, Kingsman SM. Sequence and structure of yeast phosphoglycerate kinase. EMBO J 1982;1:1635-1640.
22. Blake CC, Evans PR. Structure of horse muscle phosphoglycerate kinase. Some results on the chain conformation, substrate binding and evolution of the molecule from a 3 angstrom Fourier map. J Mol Biol 1974;84:585-601.
23. Flachner B, Kovari Z, Varga A, Gugolya Z, Vonderviszt F, Naray-Szabo G, Vas M. Role of phosphate chain mobility of MgATP in completing the 3-phosphoglycerate kinase catalytic site: binding, kinetic, and crystallographic studies with ATP and MgATP. Biochemistry 2004;43:3436-3449.
24. Bernstein BE, Williams DM, Bressi JC, Kuhn P, Gelb MH, Blackburn GM, Hol WG. A bisubstrate analog induces unexpected conformational changes in phosphoglycerate kinase from Trypanosoma brucei. J Mol Biol 1998;279:1137-1148.
25. Lee JH, Im YJ, Bae J, Kim D, Kim MK, Kang GB, Lee DS, Eom SH. Crystal structure of Thermus caldophilus phosphoglycerate kinase in the open conformation. Biochem Biophys Res Commun 2006;350:1044-1049.
26. Harlos K, Vas M, Blake CF. Crystal structure of the binary complex of pig muscle phosphoglycerate kinase and its substrate 3-phospho-D- glycerate. Proteins 1992;12:133-144.
27. Davies GJ, Gamblin SJ, Littlechild JA, Dauter Z, Wilson KS, Watson HC. Structure of the ADP complex of the 3-phosphoglycerate kinase from Bacillus stearothermophilus at 1.65 Å. Acta Crystallogr D Biol Crystallogr 1994;50 (Part 2):202-209.
28. Szilagyi AN, Ghosh M, Garman E, Vas M. A 1.8 Å resolution structure of pig muscle 3-phosphoglycerate kinase with bound MgADP and 3-phosphoglycerate in open conformation: new insight into the role of the nucleotide in domain closure. J Mol Biol 2001;306:499-511.
29. Kovari Z, Flachner B, Naray-Szabo G, Vas M. Crystallographic and thiol-reactivity studies on the complex of pig muscle phosphoglycerate kinase with ATP analogues: correlation between nucleotide binding mode and helix flexibility. Biochemistry 2002;41:8796-8806.
30. Bernstein BE, Michels PA, Hol WG. Synergistic effects of substrate-induced conformational changes in phosphoglycerate kinase activation. Nature 1997;385:275-278.
31. Auerbach G, Huber R, Grattinger M, Zaiss K, Schurig H, Jaenicke R, Jacob U. Closed structure of phosphoglycerate kinase from Thermotoga maritima reveals the catalytic mechanism and determinants of thermal stability. Structure 1997;5:1475-1483.
32. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol 1983;166:557-580.
33. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;27:307-326.
34. Kissinger CR, Gehlhaar DK, Smith BA, Bouzida D. Molecular replacement by evolutionary search. Acta Crystallogr D Biol Crystallogr 2001;57 (Part 10):1474-1479.
35. Vagin A, Teplyakov A. MOLREP: an automated program for molecular replacement. J Appl Crystallogr 1997;30:1022-1025.
36. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 1994;5:760-763.
37. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 1991;47 (Part 2):110-119.
38. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, GrosseKunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54 (Part 5):905-921.
39. Read RJ. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr Sect A 1986;42:140-149.
40. Brunger AT. Assessment of phase accuracy by cross validation: the free R value. Methods and applications. Acta Crystallogr D Biol Crystallogr 1993;49 (Part 1):24-36.
41. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
42. Esnouf RM. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr D Biol Crystallogr 1999;55 (Part 4):938-940.
43. Kraulis PJ. MOLSCRIPT. A program to produce both detailed and schematic plots of protein structure. J Appl Crystallogr 1991;2:946-950.
44. Merritt EA, Bacon DJ. Raster3D photorealistic molecular graphics. Methods Enzymol 1997;277:505-524.
45. Matthews BW. Solvent content of protein crystals. J Mol Biol 1968;33:491-497.
46. Flachner B, Varga A, Szabo J, Barna L, Hajdu I, Gyimesi G, Zavodszky P, Vas M. Substrate-assisted movement of the catalytic Lys 215 during domain closure: site-directed mutagenesis studies of human 3-phosphoglycerate kinase. Biochemistry 2005;44:16853-16865.
47. Banks RD, Blake CC, Evans PR, Haser R, Rice DW, Hardy GW, Merrett M, Phillips AW. Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. Nature 1979;279:773-777.
48. Sherman MA, Szpikowska BK, Dean SA, Mathiowetz AM, McQueen NL, Mas MT. Probing the role of arginines and histidines in the catalytic function and activation of yeast 3-phosphoglycerate kinase by site-directed mutagenesis. J Biol Chem 1990;265:10659-10665.
49. Sherman MA, Fairbrother WJ, Mas MT. Characterization of the structure and properties of the His 62->Ala and Arg 38->Ala mutants of yeast phosphoglycerate kinase: an investigation of the catalytic and activatory sites by site-directed mutagenesis and NMR. Protein Sci 1992;1:752-760.
50. Mori N, Singer-Sam J, Lee CY, Riggs AD. The nucleotide sequence of a cDNA clone containing the entire coding region for mouse X-chromosome-linked phosphoglycerate kinase. Gene 1986;45:275-280.
51. Chen K, Knorr C, Moser G, Gatphayak K, Brenig B. Molecular characterization of the porcine testis-specific phosphoglycerate kinase 2 (PGK2) gene and its association with male fertility. Mamm Genome 2004;15:996-1006.
52. Xu DQ, Zhang YB, Xiong YZ, Gui JF, Jiang SW, Su YH. Construction of forward and reverse subtracted cDNA libraries between muscle tissue of Meishan and Landrace pigs. Yi Chuan Xue Bao 2003;30:668-672.
53. Michelson AM, Markham AF, Orkin SH. Isolation and DNA sequence of a full-length cDNA clone for human X chromosome-encoded phosphoglycerate kinase. Proc Natl Acad Sci USA 1983;80:472-476.
54. Barton GJ. ALSCRIPT. A tool to format multiple sequence alignments. Protein Eng 1993;6:37-40.
55. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet 2000;16:276-277.
56. Pegoraro B, Lee CY. Purification and characterization of two isozymes of 3-phosphoglycerate kinase from the mouse. Biochim Biophys Acta 1978;522:423-433.
57. Lee CY, Niesel D, Pegoraro B, Erickson RP. Immunological and structural relatedness of isozymes and genetic variants of 3-phosphoglycerate kinase from the mouse. J Biol Chem 1980;255:2590-2595.
58. McCarrey JR, Kumari M, Aivaliotis MJ, Wang Z, Zhang P, Marshall F, Vandeberg JL. Analysis of the cDNA and encoded protein of the human testis-specific PGK-2 gene. Dev Genet 1996;19:321-332.
59. Shoichet BK. Virtual screening of chemical libraries. Nature 2004;432:862-865.
60. Jorgensen WL. The many roles of computation in drug discovery. Science 2004;303:1813-1818.
61. Warren GL, Andrews CW, Capelli AM, Clarke B, Lalonde J, Lambert MH, Lindvall M, Nevins N, Semus SF, Senger S, Tedesco G, Wall ID, Woolven JM, Peishoff CE, Head MS. A critical assessment of docking programs and scoring functions. J Med Chem 2006;49:5912-5931.