Biochemistry (Moscow)

, Volume 80, Issue 13, pp 1672–1689 | Cite as

Sperm-Specific Glyceraldehyde-3-Phosphate Dehydrogenase–An Evolutionary Acquisition of Mammals

  • V. I. MuronetzEmail author
  • M. L. Kuravsky
  • K. V. Barinova
  • E. V. Schmalhausen


This review is focused on the mammalian sperm-specific glyceraldehyde-3-phosphate dehydrogenase (GAPDS). GAPDS plays the major role in the production of energy required for sperm cell movement and does not perform non-glycolytic functions that are characteristic of the somatic isoenzyme of glyceraldehyde-3-phosphate dehydrogenase. The GAPDS sequence is composed of 408 amino acid residues and includes an additional N-terminal region of 72 a.a. that binds the protein to the sperm tail cytoskeleton. GAPDS is present only in the sperm cells of mammals and lizards, possibly providing them with certain evolutionary advantages in reproduction. In this review, studies concerning the problems of GAPDS isolation, its catalytic properties, and its structural features are described in detail. GAPDS is much more stable compared to the somatic isoenzyme, perhaps due to the necessity of maintaining the enzyme function in the absence of protein expression. The site-directed mutagenesis approach revealed the two GAPDS-specific proline residues, as well as three salt bridges, which seem to be the basis of the increased stability of this protein. As distinct from the somatic isoenzyme, GAPDS exhibits positive cooperativity in binding of the coenzyme NAD+. The key role in transduction of structural changes induced by NAD+ is played by the salt bridge D311–H124. Disruption of this salt bridge cancels GAPDS cooperativity and twofold increases its enzymatic activity instead. The expression of GAPDS was detected in some melanoma cells as well. Its role in the development of certain pathologies, such as cancer and neurodegenerative diseases, is discussed.

Key words

glyceraldehyde-3-phosphate dehydrogenase sperm-specific glyceraldehyde-3-phosphate dehydrogenase GAPDH evolution of GAPDH stability of GAPDH sperm motility glycolysis melanoma cells oncomarker NAD-binding 



somatic glyceraldehyde-3-phosphate dehydrogenase


sperm-specific glyceraldehyde-3-phosphate dehydrogenase


guanidine hydrochloride


Michaelis constant.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Glaser, P. E., and Gross, R. W. (1995) Rapid plas-menylethanolamine-selective fusion of membrane bilayers catalyzed by an isoform of glyceraldehyde-3-phosphate dehydrogenase: discrimination between glycolytic and fusogenic roles of individual isoforms, Biochemistry, 34, 12193–12203.PubMedCrossRefGoogle Scholar
  2. 2.
    Robbins, A. R., Ward, R. D., and Oliver, C. (1995) A muta-tion in glyceraldehyde 3-phosphate dehydrogenase alters endocytosis in CHO cells, J. Cell Biol., 130, 1093–1104.PubMedCrossRefGoogle Scholar
  3. 3.
    Raje, C. I., Kumar, S., Harle, A., Nanda, J. S., and Raje, M. (2007) The macrophage cell surface glyceraldehyde-3-phosphate dehydrogenase is a novel transferrin receptor, J. Biol. Chem., 282, 3252–3261.PubMedCrossRefGoogle Scholar
  4. 4.
    Hessler, R. J., Blackwood, R. A., Brock, T. G., Francis, J. W., Harsh, D. M., and Smolen, J. E. (1998) Identification of glyceraldehyde-3-phosphate dehydrogenase as a Ca2+-dependent fusogen in human neutrophil cytosol, J. Leukoc. Biol., 63, 331–336.PubMedGoogle Scholar
  5. 5.
    Muronetz, V. I., Wang, Z. X., Keith, T. J., Knull, H. R., and Srivastava, D. K. (1994) Binding constants and stoichiome-tries of glyceraldehyde 3-phosphate dehydrogenase–tubu-lin complexes, Arch. Biochem. Biophys., 313, 253–260.PubMedCrossRefGoogle Scholar
  6. 6.
    Volker, K. W., Reinitz, C. A., and Knull, H. R. (1995) Glycolytic enzymes and assembly of microtubule networks, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 112, 503–514.PubMedCrossRefGoogle Scholar
  7. 7.
    Cueille, N., Blanc, C. T., Riederer, I. M., and Riederer, B. M. (2007) Microtubule-associated protein 1B binds glycer-aldehyde-3-phosphate dehydrogenase, J. Proteome Res., 6, 2640–2647.PubMedCrossRefGoogle Scholar
  8. 8.
    Bryksin, A. V., and Laktionov, P. P. (2008) Role of glycer-aldehyde-3-phosphate dehydrogenase in vesicular trans-port from Golgi apparatus to endoplasmic reticulum, Biochemistry (Moscow), 73, 619–625.CrossRefGoogle Scholar
  9. 9.
    Tisdale, E. J., Azizi, F., and Artalejo, C. R. (2009) Rab2 utilizes glyceraldehyde-3-phosphate dehydrogenase and protein kinase Cι to associate with microtubules and to recruit dynein, J. Biol. Chem., 284, 5876–5884.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Engel, M., Seifert, M., Theisinger, B., Seyfert, U., and Welter, C. (1998) Glyceraldehyde-3-phosphate dehydroge-nase and Nm23-H1/nucleoside diphosphate kinase A. Two old enzymes combine for the novel Nm23 protein phos-photransferase function, J. Biol. Chem., 273, 20058–20065.PubMedCrossRefGoogle Scholar
  11. 11.
    Duclos-Vallee, J. C., Capel, F., Mabit, H., and Petit, M. A. (1998) Phosphorylation of the hepatitis B virus core protein by glyceraldehyde-3-phosphate dehydrogenase protein kinase activity, J. Gen. Virol., 79, 1665–1670.PubMedCrossRefGoogle Scholar
  12. 12.
    Dai, R.-P., Yu, F. X., Goh, S. R., Chng, H. W., Tan, Y. L., Fu, J. L., Zheng, L., and Luo, Y. (2008) Histone 2B (H2B) expression is confined to a proper NAD+/NADH redox sta-tus, J. Biol. Chem., 283, 26894–28901.PubMedCrossRefGoogle Scholar
  13. 13.
    Li, Y., Huang, T., Zhang, X., Wan, T., Hu, J., Huang, A., and Tang, H. (2009) Role of glyceraldehyde-3-phosphate dehydrogenase binding to hepatitis B virus posttranscrip-tional regulatory element in regulating expression of HBV surface antigen, Arch. Virol., 154, 519–524.PubMedCrossRefGoogle Scholar
  14. 14.
    Kondo, S., Kubota, S., Mukudai, Y., Nishida, T., Yoshihama, Y., Shirota, T., Shintani, S., and Takigawa, M. (2011) Binding of glyceraldehyde-3-phosphate dehydroge-nase to the cis-acting element of structure-anchored repression in ccn2 mRNA, Biochem. Biophys. Res. Commun., 405, 382–387.PubMedCrossRefGoogle Scholar
  15. 15.
    Sundararaj, K. P., Wood, R. E., Ponnusamy, S., Salas, A. M., Szulc, Z., Bielawska, A., Obeid, L. M., Hannun, Y. A., and Ogretmen, B. (2004) Rapid shortening of telomere length in response to ceramide involves the inhibition of telomere binding activity of nuclear glyceraldehyde-3-phosphate dehydrogenase, J. Biol. Chem., 279, 6152–6162.PubMedCrossRefGoogle Scholar
  16. 16.
    Demarse, N. A., Ponnusamy, S., Spicer, E. K., Apohan, E., Baatz, J. E., Ogretmen, B., and Davies, C. (2009) Direct binding of glyceraldehyde 3-phosphate dehydrogenase to telomeric DNA protects telomeres against chemotherapy-induced rapid degradation, J. Mol. Biol., 394, 789–803.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Nakagawa, T., Hirano, Y., Inomata, A., Yokota, S., Miyachi, K., Kaneda, M., Umeda, M., Furukawa, K., Omata, S., and Horigome, T. (2003) Participation of a fusogenic protein, glyceraldehyde-3-phosphate dehydroge-nase, in nuclear membrane assembly, J. Biol. Chem., 278, 20395–20404.PubMedCrossRefGoogle Scholar
  18. 18.
    Singh, R., and Green, M. R. (1993) Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase, Science, 259, 365–368.PubMedCrossRefGoogle Scholar
  19. 19.
    Meyer-Siegler, K., Mauro, D. J., Seal, G., Wurzer, J., De Riel, J. K., and Sirover, M. A. (1991) A human nuclear uracil DNA glycosylase is the 37-kDa subunit of glycer-aldehyde-3-phosphate dehydrogenase, Proc. Natl. Acad. Sci. USA, 88, 8460–8464.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Azam, S., Jouvet, N., Jilani, A., Vongsamphanh, R., Yang, X., Yang, S., and Ramotar, D. (2008) Human glyceralde-hyde-3-phosphate dehydrogenase plays a direct role in reactivating oxidized forms of the DNA repair enzyme APE1, J. Biol. Chem., 283, 30632–30641.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Arutyunova, E. I., Danshina, P. V., Domnina, L. V., Pleten, A. P., and Muronetz, V. I. (2003) Oxidation of glyceraldehyde-3-phosphate dehydrogenase enhances its binding to nucleic acids, Biochem. Biophys. Res. Commun., 307, 547–552.PubMedCrossRefGoogle Scholar
  22. 22.
    Hara, M. R., Cascio, M. B., and Sawa, A. (2006) GAPDH as a sensor of NO stress, Biochim. Biophys. Acta, 1762, 502–509.PubMedCrossRefGoogle Scholar
  23. 23.
    Hara, M. R., and Snyder, S. H. (2006) Nitric oxide-GAPDH-Siah: a novel cell death cascade, Cell. Mol. Neurobiol., 26, 527–538.PubMedCrossRefGoogle Scholar
  24. 24.
    Sen, N., Hara, M. R., Kornberg, M. D., Cascio, M. B., Bae, B. I., Shahani, N., Thomas, B., Dawson, T. M., Dawson, V. L., Snyder, S. H., and Sawa, A. (2008) Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis, Nat. Cell Biol., 10, 866–873.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Hwang, N. R., Yim, S. H., Kim, Y. M., Jeong, J., Song, E. J., Lee, Y., Lee, J. H., Choi, S., and Lee, K. J. (2009) Oxidative modifications of glyceraldehyde-3-phosphate dehydrogenase play a key role in its multiple cellular func-tions, Biochem. J., 423, 253–264.PubMedCrossRefGoogle Scholar
  26. 26.
    Mazzola, J. L., and Sirover, M. A. (2001) Reduction of glyceraldehyde-3-phosphate dehydrogenase activity in Alzheimer’s disease and in Huntington’s disease fibro-blasts, J. Neurochem., 76, 442–449.PubMedCrossRefGoogle Scholar
  27. 27.
    Naletova, I., Schmalhausen, E., Kharitonov, A., Katrukha, A., Saso, L., Caprioli, A., and Muronetz, V. (2008) Non-native glyceraldehyde-3-phosphate dehydrogenase can be an intrinsic component of amyloid structures, Biochim. Biophys. Acta, 1784, 2052–2058.PubMedCrossRefGoogle Scholar
  28. 28.
    Butterfield, D. A., Hardas, S. S., and Lange, M. L. (2010) Oxidatively modified glyceraldehyde-3-phosphate dehy-drogenase (GAPDH) and Alzheimer’s disease: many path-ways to neurodegeneration, J. Alzheimer’s Dis., 20, 369–393.Google Scholar
  29. 29.
    Mazzola, J. L., and Sirover, M. A. (2002) Alteration of nuclear glyceraldehyde-3-phosphate dehydrogenase struc-ture in Huntington’s disease fibroblasts, Brain Res. Mol. Brain Res., 100, 95–101.PubMedCrossRefGoogle Scholar
  30. 30.
    Bae, B.-I., Hara, M. R., Cascio, M. B., Wellington, C. L., Hayden, M. R., Ross, C. A., Ha, H. C., Li, X. J., Snyder, S. H., and Sawa, A. (2006) Mutant huntingtin: nuclear translocation and cytotoxicity mediated by GAPDH, Proc. Natl. Acad. Sci. USA, 103, 3405–3409.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Warburg, O., Posener, K., and Negelein, E. (1924) Ueber den stoffwechsel der tumoren, Biochem. Z., 152, 319–344.Google Scholar
  32. 32.
    Warburg, O. (1956) On the origin of cancer cells, Science, 123, 309–314.PubMedCrossRefGoogle Scholar
  33. 33.
    Schmalhausen, E. V., and Muronetz, V. I. (1997) An uncoupling of the processes of oxidation and phosphoryla-tion in glycolysis, Biosci. Rep., 17, 521–527.PubMedCrossRefGoogle Scholar
  34. 34.
    Schmalhausen, E. V., Nagradova, N. K., Boschi-Muller, S., Branlant, G., and Muronetz, V. I. (1999) Mildly oxi-dized GAPDH: the coupling of the dehydrogenase and acyl phosphatase activities, FEBS Lett., 452, 219–222.PubMedCrossRefGoogle Scholar
  35. 35.
    Weber, J. P., and Bernhard, S. A. (1982) Transfer of 1,3-diphosphoglycerate between glyceraldehyde-3-phosphate dehydrogenase and 3-phosphoglycerate kinase via an enzyme–substrate–enzyme complex, Biochemistry, 21, 4189–4194.PubMedCrossRefGoogle Scholar
  36. 36.
    Sukhodolets, M. V., Muronetz, V. I., Tsuprun, V. L., Kaftanova, A. S., and Nagradova, N. K. (1988) Association of rabbit muscle glyceraldehyde-3-phosphate dehydroge-nase and 3-phosphoglycerate kinase. The biochemical and electron-microscopic evidence, FEBS Lett., 238, 161–166.PubMedCrossRefGoogle Scholar
  37. 37.
    Tompa, P., and Batke, J. (1990) Fructose-1,6-bisphosphate aldolase preferentially associates to glyceraldehyde-3-phos-phate dehydrogenase in a mixture of cytosolic proteins as revealed by fluorescence energy transfer measurements, Biochem. Int., 20, 487–494.PubMedGoogle Scholar
  38. 38.
    Fokina, K. V., Dainyak, M. B., Nagradova, N. K., and Muronetz, V. I. (1997) A study on the complexes between human erythrocyte enzymes participating in the conver-sions of 1,3-diphosphoglycerate, Arch. Biochem. Biophys., 345, 185–192.PubMedCrossRefGoogle Scholar
  39. 39.
    Clarke, F. M., and Masters, C. J. (1975) On the association of glycolytic enzymes with structural proteins of skeletal muscle, Biochim. Biophys. Acta, 381, 37–46.PubMedCrossRefGoogle Scholar
  40. 40.
    Ryazanov, A. G., Ashmarina, L. I., and Muronetz, V. I. (1988) Association of glyceraldehyde-3-phosphate dehy-drogenase with mono-and polyribosomes of rabbit reticu-locytes, Eur. J. Biochem., 171, 301–305.PubMedCrossRefGoogle Scholar
  41. 41.
    Walsh, J. L., Keith, T. J., and Knull, H. R. (1989) Glycolytic enzyme interactions with tubulin and micro-tubules, Biochim. Biophys. Acta, 999, 64–70.PubMedCrossRefGoogle Scholar
  42. 42.
    Sirover, M. A. (1997) Role of the glycolytic protein, glycer-aldehyde-3-phosphate dehydrogenase, in normal cell func-tion and in cell pathology, J. Cell. Biochem., 66, 133–140.PubMedCrossRefGoogle Scholar
  43. 43.
    Tatton, W. G., Chalmers-Redman, R. M., Elstner, M., Leesch, W., Jagodzinski, F. B., Stupak, D. P., Sugrue, M. M., and Tatton, N. A. (2000) Glyceraldehyde-3-phosphate dehydrogenase in neurodegeneration and apoptosis signal-ing, J. Neural Transm. Suppl., 60, 77–100.PubMedGoogle Scholar
  44. 44.
    Lee, S. Y., Kim, J. H., Jung, H., Chi, S. W., Chung, S. J., Lee, C. K., Park, B. C., Bae, K. H., and Park, S. G. (2012) Glyceraldehyde-3-phosphate, a glycolytic intermediate, prevents cells from apoptosis by lowering S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase, J. Microbiol. Biotechnol., 22, 571–573.PubMedCrossRefGoogle Scholar
  45. 45.
    Arutyunova, E. I., Domnina, L. V., Chudinova, A. A., Makshakova, O. N., Arutyunov, D. Y., and Muronetz, V. I. (2013) Localization of non-native D-glyceraldehyde-3-phosphate dehydrogenase in growing and apoptotic HeLa cells, Biochemistry (Moscow), 78, 91–95.CrossRefGoogle Scholar
  46. 46.
    Sevostyanova, I. A., Kulikova, K. V., Kuravsky, M. L., Schmalhausen, E. V., and Muronetz, V. I. (2012) Sperm-specific glyceraldehyde-3-phosphate dehydrogenase is expressed in melanoma cells, Biochem. Biophys. Res. Commun., 427, 649–653.PubMedCrossRefGoogle Scholar
  47. 47.
    Li, Y., Nowotny, P., Holmans, P., Smemo, S., Kauwe, J. S., Hinrichs, A. L., Tacey, K., Doil, L., Van Luchene, R., Garcia, V., Rowland, C., Schrodi, S., Leong, D., Gogic, G., Chan, J., Cravchik, A., Ross, D., Lau, K., Kwok, S., Chang, S. Y., Catanese, J., Sninsky, J., White, T. J., Hardy, J., Powell, J., Lovestone, S., Morris, J. C., Thal, L., Owen, M., Williams, J., Goate, A, and Grupe, A. (2004) Association of late-onset Alzheimer’s disease with genetic variation in multiple members of the GAPD gene family, Proc. Natl. Acad. Sci. USA, 101, 15688–15693.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Welch, J. E., Schatte, E. C., O’Brien, D. A., and Eddy, E. M. (1992) Expression of a glyceraldehyde 3-phosphate dehydrogenase gene specific to mouse spermatogenic cells, Biol. Reprod., 46, 869–878.PubMedCrossRefGoogle Scholar
  49. 49.
    Welch, J. E., Brown, P. L., O’Brien, D. A., Magyar, P. L., Bunch, D. O., Mori, C., and Eddy, E. M. (2000) Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells, J. Androl., 21, 328–338.PubMedGoogle Scholar
  50. 50.
    Bunch, D. O., Welch, J. E., Magyar, P. L., Eddy, E. M., and O’Brien, D. A. (1998) Glyceraldehyde 3-phosphate dehy-drogenase-S protein distribution during mouse spermato-genesis, Biol. Reprod., 58, 834–841.PubMedCrossRefGoogle Scholar
  51. 51.
    Kuravsky, M. L., and Muronetz, V. I. (2007) Somatic and sperm-specific isoenzymes of glyceraldehyde-3-phosphate dehydrogenase: comparative analysis of primary structures and functional features, Biochemistry (Moscow), 72, 744–749.CrossRefGoogle Scholar
  52. 52.
    Kuravsky, M. L., Aleshin, V. V., Frishman, D., and Muronetz, V. I. (2011) Testis-specific glyceraldehyde-3-phosphate dehydrogenase: origin and evolution, BMC Evol. Biol., 11, 160.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Kamp, G., Busselmann, G., and Lauterwein, J. (1996) Spermatozoa: models for studying regulatory aspects of energy metabolism, Experientia, 52, 487–494.PubMedCrossRefGoogle Scholar
  54. 54.
    Turner, R. M. (2003) Tales from the tail: what do we really know about sperm motility? J. Androl., 24, 790–803.PubMedCrossRefGoogle Scholar
  55. 55.
    Ford, W. C. (2006) Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum. Reprod. Update, 12, 269–274.PubMedCrossRefGoogle Scholar
  56. 56.
    Nevo, A. C., and Rikmenspoel, R. (1970) Diffusion of ATP in sperm flagella, J. Theor. Biol., 26, 11–18.PubMedCrossRefGoogle Scholar
  57. 57.
    Adam, D. E., and Wei, J. (1975) Mass transport of ATP within the motile sperm, J. Theor. Biol., 49, 125–145.PubMedCrossRefGoogle Scholar
  58. 58.
    Gage, M. J. (1998) Mammalian sperm morphometry, Proc. Biol. Sci., 265, 97–103.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Nicholls, D. G., and Ferguson, S. J. (2002) Bioenergetics, 3rd Edn., Academic Press.Google Scholar
  60. 60.
    Tombes, R. M., and Shapiro, B. M. (1985) Metabolite channeling: a phosphorylcreatine shuttle to mediate high energy phosphate transport between sperm mitochondrion and tail, Cell, 41, 325–334.PubMedCrossRefGoogle Scholar
  61. 61.
    Tombes, R. M., and Shapiro, B. M. (1987) Enzyme termi-ni of a phosphocreatine shuttle. Purification and character-ization of two creatine kinase isozymes from sea urchin sperm, J. Biol. Chem., 262, 16011–16019.PubMedGoogle Scholar
  62. 62.
    Steeghs, K., Oerlemans, F., and Wieringa, B. (1995) Mice deficient in ubiquitous mitochondrial creatine kinase are viable and fertile, Biochim. Biophys. Acta, 1230, 130–138.PubMedCrossRefGoogle Scholar
  63. 63.
    Yeung, C. H., Majumder, G. C., Rolf, C., Behre, H. M., and Cooper, T. G. (1996) The role of phosphocreatine kinase in the motility of human spermatozoa supported by different metabolic substrates, Mol. Hum. Reprod., 2, 591–596.PubMedCrossRefGoogle Scholar
  64. 64.
    Smith, M. B., Babcock, D. F., and Lardy, H. A. (1985) A 31P-NMR study of the epididymis and epididymal sperm of the bull and hamster, Biol. Reprod., 33, 1029–1040.PubMedCrossRefGoogle Scholar
  65. 65.
    Robitaille, P. M., Robitaille, P. A., Martin, P. A., and Brown, G. G. (1987) Phosphorus-31 nuclear magnetic res-onance studies of spermatozoa from the boar, ram, goat and bull, Comp. Biochem. Physiol. B, 87, 285–296.PubMedGoogle Scholar
  66. 66.
    Mita, M., and Ueta, N. (1988) Energy metabolism of sea urchin spermatozoa, with phosphatidylcholine as the pre-ferred substrate, Biochim. Biophys. Acta, 959, 361–369.PubMedCrossRefGoogle Scholar
  67. 67.
    Mukai, C., and Okuno, M. (2004) Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement, Biol. Reprod., 71, 540–547.PubMedCrossRefGoogle Scholar
  68. 68.
    Hiipakka, R. A., and Hammerstedt, R. H. (1978) 2-Deoxyglucose transport and phosphorylation by bovine sperm, Biol. Reprod., 19, 368–379.PubMedCrossRefGoogle Scholar
  69. 69.
    Hyne, R. V., and Edwards, K. P. (1985) Influence of 2-deoxy-D-glucose and energy substrates on guinea-pig sperm capacitation and acrosome reaction, J. Reprod. Fertil., 73, 59–69.PubMedCrossRefGoogle Scholar
  70. 70.
    Miki, K., Qu, W., Goulding, E. H., Willis, W. D., Bunch, D. O., Strader, L. F., Perreault, S. D., Eddy, E. M., and O’Brien, D. A. (2004) Glyceraldehyde 3-phosphate dehy-drogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility, Proc. Natl. Acad. Sci. USA, 101, 16501–16506.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Elkina, Y. L., Atroshchenko, M. M., Bragina, E. E., Muronetz, V. I., and Schmalhausen, E. V. (2011) Oxidation of glyceraldehyde-3-phosphate dehydrogenase decreases sperm motility, Biochemistry (Moscow), 76, 268–272.CrossRefGoogle Scholar
  72. 72.
    Westhoff, D., and Kamp, G. (1997) Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa, J. Cell Sci., 110, 1821–1829.PubMedGoogle Scholar
  73. 73.
    Frayne, J., Taylor, A., Cameron, G., and Hadfield, A. T. (2009) Structure of insoluble rat sperm glyceraldehyde-3-phosphate dehydrogenase (GAPDH) via heterotetramer formation with Escherichia coli GAPDH reveals target for contraceptive design, J. Biol. Chem., 284, 22703–22712.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Shchutskaya, Y. Y., Elkina, Y. L., Kuravsky, M. L., Bragina, E. E., and Schmalhausen, E. V. (2008) Investigation of glyceraldehyde-3-phosphate dehydrogenase from human sperms, Biochemistry (Moscow), 73, 185–191.CrossRefGoogle Scholar
  75. 75.
    Conway, A., and Koshland, D. E. (1968) Negative cooper-ativity in enzyme action. The binding of diphosphopyridine nucleotide to glyceraldehyde 3-phosphate dehydrogenase, Biochemistry, 7, 4011–4023.PubMedCrossRefGoogle Scholar
  76. 76.
    De Vijlder, J. J., and Slater, E. C. (1968) The reaction between NAD+ and rabbit-muscle glyceraldehyde phos-phate dehydrogenase, Biochim. Biophys. Acta, 167, 23–34.PubMedCrossRefGoogle Scholar
  77. 77.
    Kuravsky, M. L., Barinova, K. V., Asryants, R. A., Schmalhausen, E. V., and Muronetz, V. I. (2015) Structural basis for the NAD binding cooperativity and catalytic char-acteristics of sperm-specific glyceraldehyde-3-phosphate dehydrogenase, Biochimie, 115, 28–34.PubMedCrossRefGoogle Scholar
  78. 78.
    Elkina, Y. L., Kuravsky, M. L., El’darov, M. A., Stogov, S. V., Muronetz, V. I., and Schmalhausen, E. V. (2010) Recombinant human sperm-specific glyceraldehyde-3-phosphate dehydrogenase: structural basis for enhanced stability, Biochim. Biophys. Acta, 1804, 2207–2212.PubMedCrossRefGoogle Scholar
  79. 79.
    Naletova, I. N., Popova, K. M., Eldarov, M. A., Kuravsky, M. L., Schmalhausen, E. V., Sevostyanova, I. A., and Muronetz, V. I. (2011) Chaperonin TRiC assists the refold-ing of sperm-specific glyceraldehyde-3-phosphate dehy-drogenase, Arch. Biochem. Biophys., 516, 75–83.PubMedCrossRefGoogle Scholar
  80. 80.
    Goldberg, E. (1972) Amino acid composition and proper-ties of crystalline lactate dehydrogenase X from mouse testes, J. Biol. Chem., 247, 2044–2048.PubMedGoogle Scholar
  81. 81.
    Bogin, O., Peretz, M., Hacham, Y., Korkhin, Y., Frolow, F., Kalb(Gilboa), A. J., and Burstein, Y. (1998) Enhanced thermal stability of Clostridium beijerinckii alcohol dehy-drogenase after strategic substitution of amino acid residues with prolines from the homologous thermophilic Thermoanaerobacter brockii alcohol dehydrogenase, Protein Sci., 7, 1156–1163.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Matthews, B. W., Nicholson, H., and Becktel, W. J. (1987) Enhanced protein thermostability from site-directed muta-tions that decrease the entropy of unfolding, Proc. Natl. Acad. Sci. USA, 84, 6663–6667.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Masui, A., Fujiwara, N., and Imanaka, T. (1994) Stabilization and rational design of serine protease AprM under highly alkaline and high-temperature conditions, Appl. Environ. Microbiol., 60, 3579–3584.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Veltman, O. R., Vriend, G., and Middelhoven, P. J. (1996) Analysis of structural determinants of the stability of ther-molysin-like proteases by molecular modelling and site-directed mutagenesis, Protein Eng., 9, 1181–1189.PubMedCrossRefGoogle Scholar
  85. 85.
    Watanabe, K., Masuda, T., Ohashi, H., Mihara, H., and Suzuki, Y. (1994) Multiple proline substitutions cumula-tively thermostabilize Bacillus cereus ATCC7064 oligo-1,6-glucosidase. Irrefragable proof supporting the proline rule, Eur. J. Biochem., 226, 277–283.PubMedCrossRefGoogle Scholar
  86. 86.
    Fan, H., Liu, J., Ren, W., Zheng, Z., Zhang, Y., Yang, X., Li, H., Wang, X., and Zou, G. (2008) pH induces thermal unfolding of UTI: an implication of reversible and irre-versible mechanism based on the analysis of thermal stabil-ity, thermodynamic, conformational characterization, J. Fluoresc., 18, 305–317.PubMedCrossRefGoogle Scholar
  87. 87.
    Kurganov, B. I., Sugrobova, N. P., and Yakovlev, V. A. (1972) Estimation of dissociation constant of enzyme–lig-and complex from fluorometric data by “difference” method, FEBS Lett., 19, 308–310.PubMedCrossRefGoogle Scholar
  88. 88.
    Patra, S., Ghosh, S., Bera, S., Roy, A., Ray, S., and Ray, M. (2009) Molecular characterization of tumor associated glyceraldehyde-3-phosphate dehydrogenase, Biochemistry (Moscow), 74, 717–727.CrossRefGoogle Scholar
  89. 89.
    Kuravsky, M. L., Schmalhausen, E. V., Pozdnyakova, N. V., and Muronetz, V. I. (2012) Isolation of antibodies against different protein conformations using immuno-affinity chromatography, Anal. Biochem., 426, 47–53.PubMedCrossRefGoogle Scholar
  90. 90.
    Mikhailova, I. N., Lukashina, M. I., Baryshnikov, A. Yu., Morozova, L. F., Byrova, O. S., Pankina, T. N., Kozlov, A. M., Golubeva, V. A., Cheremushkin, E. A., Doroshenko, M. B., Demidov, L. V., Kiselev, S. L., Larin, S. S., and Georgiev, G. P. (2005) Melanoma cell lines as the back-ground for creating antitumour vaccines, Vestnik Ross. Akad. Med. Nauk, 7, 37–40.Google Scholar
  91. 91.
    Mikhaylova, I. N., Kovalevsky, D. A., Morozova, L. F., Golubeva, V. A., Cheremushkin, E. A., Lukashina, M. I., Voronina, E. S., Burova, O. S., Utyashev, I. A., Kiselev, S. L., Demidov, L. V., Beabealashvilli, R. Sh., and Baryshnikov, A. Y. (2008) Cancer/testis genes expression in human melanoma cell lines, Melanoma Res., 18, 303–313.PubMedCrossRefGoogle Scholar
  92. 92.
    Lemehov, V. G. (2001) Epidemiology, risk factors, screen-ing of skin melanoma, Prakt. Onkol., 2, 3–11.Google Scholar
  93. 93.
    Ferlay, J., Shin, H. R., Bray, F., Forman, D., Mathers, C., and Parkin, D. M. (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008, Int. J. Cancer, 127, 2893–2917.PubMedCrossRefGoogle Scholar
  94. 94.
    Dvoyrin, V. V., Trapeznikov, N. N., and Mikhailovskii, A. V. (1997) Statistics of skin melanoma in Russia, Vestnik RONTs Blokhina RAMN, 8, 3–12.Google Scholar
  95. 95.
    Evdokimov, V. V., Barinova, K. V., Turovetskii, V. B., Muronetz, V. I., and Schmalhausen, E. V. (2015) Low con-centrations of hydrogen peroxide activate the antioxidant defense system in human sperm cells, Biochemistry (Moscow), 80, 1178–1185.CrossRefGoogle Scholar
  96. 96.
    Margaryan, H., Dorosh, A., Capkova, J., Manaskova-Postlerova, P., Philimonenko, A., Hozak, P., and Peknicova, J. (2015) Characterization and possible func-tion of glyceraldehyde-3-phosphate dehydrogenase-sper-matogenic protein GAPDHS in mammalian sperm, Reprod. Biol. Endocrinol., 13, 15.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Chaikuad, A., Shafqat, N., Al-Mokhtar, R., Cameron, G., Clarke, A. R., Brady, R. L., Oppermann, U., Frayne, J., and Yue, W. W. (2011) Structure and kinetic characteriza-tion of human sperm-specific glyceraldehyde-3-phosphate dehydrogenase, GAPDS, Biochem. J., 435, 401–409.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  • V. I. Muronetz
    • 1
    • 2
    Email author
  • M. L. Kuravsky
    • 1
  • K. V. Barinova
    • 1
    • 2
  • E. V. Schmalhausen
    • 1
  1. 1.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Faculty of Bioengineering and BioinformaticsLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations