The function and the role of the mitochondrial glycerol-3-phosphate dehydrogenase in mammalian tissues

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1827, Issue 3, 2013, Pages 401-410

  Mráček, Tomáš ^a   Drahota, Zdeněk ^a   Houštěk, Josef ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

Glycerophosphate shuttle; GPD2 gene; Mitochondrial glycerol 3 phosphate dehydrogenase; Pathophysiology; ROS production

Indexed keywords

BACTERIAL ENZYME; FATTY ACID; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHATE; MITOCHONDRIAL ENZYME; MITOCHONDRIAL GLYCEROL 3 PHOSPHATE DEHYDROGENASE; OXIDOREDUCTASE; PHOSPHATE; REACTIVE OXYGEN METABOLITE; THYROID HORMONE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ACROSOME REACTION; ALLOSTERISM; BINDING SITE; BROWN ADIPOSE TISSUE; CALCIUM BINDING; CALCIUM TRANSPORT; CHROMOSOME 2; CHROMOSOME 3; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME STRUCTURE; FATTY ACID METABOLISM; FATTY ACID OXIDATION; GLYCOLYSIS; HORMONE RESPONSIVE ELEMENT; INSULIN RELEASE; LIPOGENESIS; MAMMAL; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PANCREAS ISLET; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR OCCUPANCY; RESPIRATORY CHAIN; REVIEW; SPERMATOZOON CAPACITATION;

ALLOSTERIC REGULATION; ANIMALS; FATTY ACIDS; GLYCEROLPHOSPHATE DEHYDROGENASE; GLYCOLYSIS; HUMANS; MITOCHONDRIA; ORGAN SPECIFICITY; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SUCCINATE DEHYDROGENASE;

MAMMALIA;

EID: 84872102687     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.11.014     Document Type: Review

References (135)

1. D.E. Green alpha-Glycerophosphate dehydrogenase Biochem. J. 30 1936 629 644
2. A. Garrib, and W.C. McMurray Purification and characterization of glycerol-3-phosphate dehydrogenase (flavin-linked) from rat liver mitochondria J. Biol. Chem. 261 1986 8042 8048
3. A. Garrib, and W.C. McMurray Cell-free synthesis of a putative precursor to the rat liver mitochondrial glycerol-3-phosphate dehydrogenase J. Biol. Chem. 263 1988 19821 19826
4. S. Muller, and H.J. Seitz Cloning of a cDNA for the FAD-linked glycerol-3-phosphate dehydrogenase from rat liver and its regulation by thyroid hormones Proc. Natl. Acad. Sci. U. S. A. 91 1994 10581 10585
5. R.L. Ringler, and T.P. Singer Solubilization and assay of the insoluble alpha-glycero-phosphate dehydrogenase of animal tissues Biochim. Biophys. Acta 29 1958 661 662
6. A.P. Dawson, and C.J. Thorne Preparation and some properties of L-3-glycerophosphate dehydrogenase from pig brain mitochondria Biochem. J. 111 1969 27 34
7. E.S. Cole, C.A. Lepp, P.D. Holohan, and T.P. Fondy Isolation and characterization of flavin-linked glycerol-3-phosphate dehydrogenase from rabbit skeletal muscle mitochondria and comparison with the enzyme from rabbit brain J. Biol. Chem. 253 1978 7952 7959
8. J. Swierczynski, P. Scislowski, and Z. Aleksandrowicz High activity of alpha-glycerophosphate oxidation by human placental mitochondria Biochim. Biophys. Acta 429 1976 46 54
9. 2 + stimulation of rat liver mitochondrial glycerophosphate dehydrogenase J. Biol. Chem. 256 1981 12767 12771
10. I.R. Cottingham, and C.I. Ragan Purification and properties of L-3-glycerophosphate dehydrogenase from pig brain mitochondria Biochem. J. 192 1980 9 18
11. C.M. Gomes, G. Silva, S. Oliveira, J. LeGall, M.Y. Liu, A.V. Xavier, C. Rodrigues-Pousada, and M. Teixeira Studies on the redox centers of the terminal oxidase from Desulfovibrio gigas and evidence for its interaction with rubredoxin J. Biol. Chem. 272 1997 22502 22508
12. L. Chen, M.Y. Liu, J. Legall, P. Fareleira, H. Santos, and A.V. Xavier Purification and characterization of an NADH-rubredoxin oxidoreductase involved in the utilization of oxygen by Desulfovibrio gigas Eur. J. Biochem. 216 1993 443 448
13. J.I. Yeh, U. Chinte, and S. Du Structure of glycerol-3-phosphate dehydrogenase, an essential monotopic membrane enzyme involved in respiration and metabolism Proc. Natl. Acad. Sci. U. S. A. 105 2008 3280 3285
14. T. Colussi, D. Parsonage, W. Boles, T. Matsuoka, T.C. Mallett, P.A. Karplus, and A. Claiborne Structure of alpha-glycerophosphate oxidase from Streptococcus sp.: a template for the mitochondrial alpha-glycerophosphate dehydrogenase Biochemistry 47 2008 965 977
15. N.J. Watmough, and F.E. Frerman The electron transfer flavoprotein: ubiquinone oxidoreductases Biochim. Biophys. Acta 1797 2010 1910 1916
16. J. Zhang, F.E. Frerman, and J.J. Kim Structure of electron transfer flavoprotein-ubiquinone oxidoreductase and electron transfer to the mitochondrial ubiquinone pool Proc. Natl. Acad. Sci. U. S. A. 103 2006 16212 16217
17. M.H. Bracey, B.F. Cravatt, and R.C. Stevens Structural commonalities among integral membrane enzymes FEBS Lett. 567 2004 159 165
18. M.J. Janssen, F. van Voorst, G.E. Ploeger, P.M. Larsen, M.R. Larsen, A.I. de Kroon, and B. de Kruijff Photolabeling identifies an interaction between phosphatidylcholine and glycerol-3-phosphate dehydrogenase (Gut2p) in yeast mitochondria Biochemistry 41 2002 5702 5711
19. M.J. MacDonald, and L.J. Brown Calcium activation of mitochondrial glycerol phosphate dehydrogenase restudied Arch. Biochem. Biophys. 326 1996 79 84
20. G. von Heijne Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule J. Mol. Biol. 225 1992 487 494
21. 2 + as modulators of mitochondrial L-glycerol-3-phosphate dehydrogenase Eur. J. Biochem. 170 1988 631 636
22. G. Benard, B. Faustin, E. Passerieux, A. Galinier, C. Rocher, N. Bellance, J.P. Delage, L. Casteilla, T. Letellier, and R. Rossignol Physiological diversity of mitochondrial oxidative phosphorylation Am. J. Physiol. Cell Physiol. 291 2006 C1172 C1182
23. C. van Waveren, and C.T. Moraes Transcriptional co-expression and co-regulation of genes coding for components of the oxidative phosphorylation system BMC Genomics 9 2008 18
24. J. Houstek, B. Cannon, and O. Lindberg Gylcerol-3-phosphate shuttle and its function in intermediary metabolism of hamster brown-adipose tissue Eur. J. Biochem. 54 1975 11 18
25. P.L. Ratner, M. Fisher, D. Burkart, J.R. Cook, and L.P. Kozak The role of mRNA levels and cellular localization in controlling sn-glycerol-3-phosphate dehydrogenase expression in tissues of the mouse J. Biol. Chem. 256 1981 3576 3579
26. R.A. Koza, U.C. Kozak, L.J. Brown, E.H. Leiter, M.J. MacDonald, and L.P. Kozak Sequence and tissue-dependent RNA expression of mouse FAD-linked glycerol-3-phosphate dehydrogenase Arch. Biochem. Biophys. 336 1996 97 104
27. T. Mracek, A. Pecinova, M. Vrbacky, Z. Drahota, and J. Houstek High efficiency of ROS production by glycerophosphate dehydrogenase in mammalian mitochondria Arch. Biochem. Biophys. 481 2009 30 36
28. M.J. MacDonald High content of mitochondrial glycerol-3-phosphate dehydrogenase in pancreatic islets and its inhibition by diazoxide J. Biol. Chem. 256 1981 8287 8290
29. M.J. MacDonald, T.F. Warner, and J.R. Pellett Increased mitochondrial glycerol phosphate dehydrogenase activity in insulinomas of two hypoglycemic infants J. Clin. Endocrinol. Metab. 57 1983 662 664
30. J.M. Weitzel, N.B. Shiryaeva, R. Middendorff, M. Balvers, C. Radtke, R. Ivell, and H.J. Seitz Testis-specific expression of rat mitochondrial glycerol-3-phosphate dehydrogenase in haploid male germ cells Biol. Reprod. 68 2003 699 707
31. J. Swierczynski, P. Scislowski, and Z. Aleksandrowicz Regulation of alpha-glycerophosphate dehydrogenase activity in human term placental mitochondria Biochim. Biophys. Acta 452 1976 310 319
32. D. Chretien, P. Rustin, T. Bourgeron, A. Rotig, J.M. Saudubray, and A. Munnich Reference charts for respiratory chain activities in human tissues Clin. Chim. Acta 228 1994 53 70
33. D.W. Gong, S. Bi, B.D. Weintraub, and M. Reitman Rat mitochondrial glycerol-3-phosphate dehydrogenase gene: multiple promoters, high levels in brown adipose tissue, and tissue-specific regulation by thyroid hormone DNA Cell Biol. 17 1998 301 309
34. J.M. Weitzel, S. Grott, C. Radtke, S. Kutz, and H.J. Seitz Multiple promoters direct the tissue-specific expression of rat mitochondrial glycerol-3-phosphate dehydrogenase Biol. Chem. 381 2000 611 614
35. J.M. Weitzel, S. Kutz, C. Radtke, S. Grott, and H.J. Seitz Hormonal regulation of multiple promoters of the rat mitochondrial glycerol-3-phosphate dehydrogenase gene: identification of a complex hormone-response element in the ubiquitous promoter B Eur. J. Biochem. 268 2001 4095 4103
36. Y.P. Lee, A.E. Takemori, and H. Lardy Enhanced oxidation of alpha-glycerophosphate by mitochondria of thyroid-fed rats J. Biol. Chem. 234 1959 3051 3054
37. J.H. Oppenheimer, E. Silva, H.L. Schwartz, and M.I. Surks Stimulation of hepatic mitochondrial alpha-glycerophosphate dehydrogenase and malic enzyme by L-triiodothyronine. Characteristics of the response with specific nuclear thyroid hormone binding sites fully saturated J. Clin. Investig. 59 1977 517 527
38. K. Dummler, S. Muller, and H.J. Seitz Regulation of adenine nucleotide translocase and glycerol 3-phosphate dehydrogenase expression by thyroid hormones in different rat tissues Biochem. J. 317 Pt 3 1996 913 918
39. T. Mracek, P. Jesina, P. Krivakova, R. Bolehovska, Z. Cervinkova, Z. Drahota, and J. Houstek Time-course of hormonal induction of mitochondrial glycerophosphate dehydrogenase biogenesis in rat liver Biochim. Biophys. Acta 1726 2005 217 223
40. J.G. Dewan, and D.E. Green Coenzyme-linked reactions between dehydrogenase systems Biochem. J. 31 1937 1074 1085
41. D.E. Green, D.M. Needham, and J.G. Dewan Dismutations and oxidoreductions Biochem. J. 31 1937 2327 2352
42. K.I. Ohkawa, M.T. Vogt, and E. Farber Unusually high mitochondrial alpha glycerophosphate dehydrogenase activity in rat brown adipose tissue J. Cell Biol. 41 1969 441 449
43. B. Sacktor, and D.G. Cochran The respiratory metabolism of insect flight muscle. I. Manometric studies of oxidation and concomitant phosphorylation with sarcosomes Arch. Biochem. Biophys. 74 1958 266 276
44. R.W. Lennie, and L.M. Birt Aspects of the development of flight-muscle sarcosomes in the sheep blowfly, Lucilia cuprina, in relation to changes in the distribution of protein and some respiratory enzymes during metamorphosis Biochem. J. 102 1967 338 350
45. E.C. Zebe, and W.H. McShan Lactic and alpha-glycerophosphate dehydrogenases in insects J. Gen. Physiol. 40 1957 779 790
46. V. Kubista Accumulation of a stable phosphorus compound in glycolysing insect muscle Nature 180 1957 549
47. T. Bucher, and M. Klingenberg Wege des Wasserstoffs in der lebendigen Organisation Angew. Chem. 70 1958 552 570
48. E. Zebe, A. Delbruck, and T. Bucher Uber den Glycerin-1-P-Cyclus im Flugmuskel von Locusta migratoria Biochem. Z. 331 1959 254 272
49. R.W. Estabrook, and B. Sacktor alpha-Glycerophosphate oxidase of flight muscle mitochondria J. Biol. Chem. 233 1958 1014 1019
50. B. Cannon, and G. Vogel The mitochondrial ATPase of brown adipose tissue. Purification and comparison with the mitochondrial ATPase from beef heart FEBS Lett. 76 1977 284 289
51. J. Houstek, and Z. Drahota Purification and properties of mitochondrial adenosine triphosphatase of hamster brown adipose tissue Biochim. Biophys. Acta 484 1977 127 139
52. D.G. Nicholls, and R.M. Locke Thermogenic mechanisms in brown fat Physiol. Rev. 64 1984 1 64
53. R.M. Bell, and R.A. Coleman Enzymes of glycerolipid synthesis in eukaryotes Annu. Rev. Biochem. 49 1980 459 487
54. H. Lardy, C.-Y. Su, N. Kneer, and S. Wielgus Dehydroepiandrosterone induces enzymes that permit thermogenesis and decrease metabolic efficiency H. Lardy, F. Stratman, Hormones, Thermogenesis, and Obesity 1989 Elsevier Science Publishing Co, Inc. 415 426
55. N. Taleux, B. Guigas, H. Dubouchaud, M. Moreno, J.M. Weitzel, F. Goglia, R. Favier, and X.M. Leverve High expression of thyroid hormone receptors and mitochondrial glycerol-3-phosphate dehydrogenase in the liver is linked to enhanced fatty acid oxidation in Lou/C, a rat strain resistant to obesity J. Biol. Chem. 284 2009 4308 4316
56. H. Wohlrab The divalent cation requirement of the mitochondrial glycerol-3-phosphate dehydrogenase Biochim. Biophys. Acta 462 1977 102 112
57. A. Carmon, and R. MacIntyre The alpha glycerophosphate cycle in Drosophila melanogaster VI. structure and evolution of enzyme paralogs in the genus Drosophila J. Hered. 101 2010 225 234
58. E. Carafoli, and B. Sacktor The effects of ruthenium red on reactions of blowfly flight muscle mitochondria with calcium Biochem. Biophys. Res. Commun. 49 1972 1498 1503
59. H. Rauchova, P.P. Kaul, and Z. Drahota Activation of mitochondrial glycerol 3-phosphate dehydrogenase by cadmium ions Gen. Physiol. Biophys. 4 1985 29 33
60. A.P. Dawson, and C.J. Thorne L-3-glycerophosphate dehydrogenase from pig brain mitochondria Methods Enzymol. 41 1975 254 259
61. J. Swierczynski, P. Scislowski, and Z. Aleksandrowicz Inhibition of alpha-glycerophosphate dehydrogenase activity in human placental mitochondria by phosphoenolpyruvate FEBS Lett. 64 1976 303 306
62. L.J. Bukowiecki, and O. Lindberg Control of sn-glycerol 3-phosphate oxidation in brown adipose tissue mitochondria by calcium and acyl-CoA Biochim. Biophys. Acta 348 1974 115 125
63. J. Houstek, and Z. Drahota The regulation of glycerol 3-phosphate oxidase of rate brown adipose tissue mitochondria by long-chain free fatty acids Mol. Cell. Biochem. 7 1975 45 50
64. A. Bulychev, R. Kramar, Z. Drahota, and O. Lindberg Role of a specific endogenous fatty acid fraction in the coupling-uncoupling mechanism of oxidative phosphorylation of brown adipose tissue Exp. Cell Res. 72 1972 169 187
65. H. Rauchova, and Z. Drahota Inhibition of the glycerol 3-phosphate oxidation by free fatty acids Int. J. Biochem. 16 1984 243 245
66. E. Amler, H. Rauchova, J. Svobodova, and Z. Drahota Regulation of glycerol 3-phosphate oxidation in mitochondria by changes in membrane microviscosity FEBS Lett. 206 1986 1 3
67. E. Amler, R. Jasinska, Z. Drahota, and J. Zborowski Membrane lateral pressure as a modulator of glycerol-3-phosphate dehydrogenase activity FEBS Lett. 271 1990 165 168
68. M.J. Nalecz, J. Zborowski, K.S. Famulski, and L. Wojtczak Effect of phospholipid composition on the surface potential of liposomes and the activity of enzymes incorporated Eur. J. Biochem. 112 1980 75 80
69. P.J. Rijken, B. De Kruijff, and A.I. De Kroon Phosphatidylcholine is essential for efficient functioning of the mitochondrial glycerol-3-phosphate dehydrogenase Gut2 in Saccharomyces cerevisiae Mol. Membr. Biol. 24 2007 269 281
70. H. Rauchova, Z. Beleznai, and Z. Drahota Effect of chemical modification in situ on L-glycerol-3-phosphate dehydrogenase in brown adipose tissue mitochondria J. Bioenerg. Biomembr. 20 1988 623 632
71. Z. Drahota, P. Saf, H. Rauchova, and M. Kalous Dicarbanonaborates - new inhibitors of mitochondrial L-glycerol-3-phosphate dehydrogenase Biochem. Biophys. Res. Commun. 210 1995 760 765
72. E.B. Tahara, F.D. Navarete, and A.J. Kowaltowski Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation Free Radic. Biol. Med. 46 2009 1283 1297
73. B.S. Sekhar, C.K. Kurup, and T. Ramasarma Generation of hydrogen peroxide by brown adipose tissue mitochondria J. Bioenerg. Biomembr. 19 1987 397 407
74. R.S. Sohal Hydrogen peroxide production by mitochondria may be a biomarker of aging Mech. Ageing Dev. 60 1991 189 198
75. Z. Drahota, S.K. Chowdhury, D. Floryk, T. Mracek, J. Wilhelm, H. Rauchova, G. Lenaz, and J. Houstek Glycerophosphate-dependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide J. Bioenerg. Biomembr. 34 2002 105 113
76. L. Tretter, and V. Adam-Vizi Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase J. Neurosci. 24 2004 7771 7778
77. 2 emission during long-chain fatty acid oxidation J. Biol. Chem. 285 2010 5748 5758
78. C.L. Quinlan, A.L. Orr, I.V. Perevoshchikova, J.R. Treberg, B.A. Ackrell, and M.D. Brand Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions J. Biol. Chem. 287 2012 27255 27264
79. S. Miwa, and M.D. Brand The topology of superoxide production by complex III and glycerol 3-phosphate dehydrogenase in Drosophila mitochondria Biochim. Biophys. Acta 1709 2005 214 219
80. S. Miwa, and M.D. Brand Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling Biochem. Soc. Trans. 31 2003 1300 1301
81. M. Vrbacky, Z. Drahota, T. Mracek, A. Vojtiskova, P. Jesina, P. Stopka, and J. Houstek Respiratory chain components involved in the glycerophosphate dehydrogenase-dependent ROS production by brown adipose tissue mitochondria Biochim. Biophys. Acta 1767 2007 989 997
82. T.V. Votyakova, and I.J. Reynolds DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria J. Neurochem. 79 2001 266 277
83. 2 generation in brain mitochondria J. Neurochem. 100 2007 650 663
84. I.G. Shabalina, and J. Nedergaard Mitochondrial ('mild') uncoupling and ROS production: physiologically relevant or not? Biochem. Soc. Trans. 39 2011 1305 1309
85. A. Dlaskova, K.J. Clarke, and R.K. Porter The role of UCP 1 in production of reactive oxygen species by mitochondria isolated from brown adipose tissue Biochim. Biophys. Acta 1797 2010 1470 1476
86. R. Oelkrug, M. Kutschke, C.W. Meyer, G. Heldmaier, and M. Jastroch Uncoupling protein 1 decreases superoxide production in brown adipose tissue mitochondria J. Biol. Chem. 285 2010 21961 21968
87. P. Schonfeld, and L. Wojtczak Brown adipose tissue mitochondria oxidizing fatty acids generate high levels of reactive oxygen species irrespective of the uncoupling protein-1 activity state Biochim. Biophys. Acta 1817 2012 410 418
88. A.L. Orr, C.L. Quinlan, I.V. Perevoshchikova, M.D. Brand, A refined analysis of superoxide production by mitochondrial sn-glycerol 3-phosphate dehydrogenase, J. Biol. Chem. (in press) First Published on November 2, 2012, http://dx.doi.org/10.1074/jbc.M112.397828.
89. R. Horsefield, V. Yankovskaya, G. Sexton, W. Whittingham, K. Shiomi, S. Omura, B. Byrne, G. Cecchini, and S. Iwata Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase): a mechanism of electron transfer and proton conduction during ubiquinone reduction J. Biol. Chem. 281 2006 7309 7316
90. C.A. Yu, S. Nagaoka, L. Yu, and T.E. King Evidence for the existence of a ubiquinone protein and its radical in the cytochromes b and c1 region in the mitochondrial electron transport chain Biochem. Biophys. Res. Commun. 82 1978 1070 1078
91. -, oxidative stress, and genomic instability Cancer Res. 66 2006 7615 7620
92. T. Mracek, E. Holzerova, N. Kovarova, P. Jesina, Z. Drahota, and J. Houstek Reactive oxygen species production by flavin dehydrogenases of the mitochondrial respiratory chain Biochim. Biophys. Acta 1817 2012 S100 S101 (Supplement)
93. R. Acin-Perez, P. Fernandez-Silva, M.L. Peleato, A. Perez-Martos, and J.A. Enriquez Respiratory active mitochondrial supercomplexes Mol. Cell 32 2008 529 539
94. H. Schagger Respiratory chain supercomplexes of mitochondria and bacteria Biochim. Biophys. Acta 1555 2002 154 159
95. G. Lenaz, and M.L. Genova Supramolecular organisation of the mitochondrial respiratory chain: a new challenge for the mechanism and control of oxidative phosphorylation Adv. Exp. Med. Biol. 748 2012 107 144
96. Y. Wang, A.W. Mohsen, S.J. Mihalik, E.S. Goetzman, and J. Vockley Evidence for physical association of mitochondrial fatty acid oxidation and oxidative phosphorylation complexes J. Biol. Chem. 285 2010 29834 29841
97. X. Grandier-Vazeille, K. Bathany, S. Chaignepain, N. Camougrand, S. Manon, and J.M. Schmitter Yeast mitochondrial dehydrogenases are associated in a supramolecular complex Biochemistry 40 2001 9758 9769
98. P.M. Sousa, S.T. Silva, B.L. Hood, N. Charro, J.N. Carita, F. Vaz, D. Penque, T.P. Conrads, and A.M. Melo Supramolecular organizations in the aerobic respiratory chain of Escherichia coli Biochimie 93 2011 418 425
99. J. Rutter, D.R. Winge, and J.D. Schiffman Succinate dehydrogenase - assembly, regulation and role in human disease Mitochondrion 10 2010 393 401
100. F. Distelmaier, W.J. Koopman, L.P. van den Heuvel, R.J. Rodenburg, E. Mayatepek, P.H. Willems, and J.A. Smeitink Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease Brain 132 2009 833 842
101. S.I. Goodman, R.J. Binard, M.R. Woontner, and F.E. Frerman Glutaric acidemia type II: gene structure and mutations of the electron transfer flavoprotein:ubiquinone oxidoreductase (ETF:QO) gene Mol. Genet. Metab. 77 2002 86 90
102. R.A. DosSantos, A. Alfadda, K. Eto, T. Kadowaki, and J.E. Silva Evidence for a compensated thermogenic defect in transgenic mice lacking the mitochondrial glycerol-3-phosphate dehydrogenase gene Endocrinology 144 2003 5469 5479
103. A. Alfadda, R.A. DosSantos, Z. Stepanyan, H. Marrif, and J.E. Silva Mice with deletion of the mitochondrial glycerol-3-phosphate dehydrogenase gene exhibit a thrifty phenotype: effect of gender Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 2004 R147 R156
104. L.J. Brown, R.A. Koza, C. Everett, M.L. Reitman, L. Marshall, L.A. Fahien, L.P. Kozak, and M.J. MacDonald Normal thyroid thermogenesis but reduced viability and adiposity in mice lacking the mitochondrial glycerol phosphate dehydrogenase J. Biol. Chem. 277 2002 32892 32898
105. L.J. Brown, R.A. Koza, L. Marshall, L.P. Kozak, and M.J. MacDonald Lethal hypoglycemic ketosis and glyceroluria in mice lacking both the mitochondrial and the cytosolic glycerol phosphate dehydrogenases J. Biol. Chem. 277 2002 32899 32904
106. H. Daoud, N. Gruchy, J.M. Constans, E. Moussaoui, S. Saumureau, N. Bayou, M. Amy, S. Vedrine, P.Y. Vu, A. Rotig, F. Laumonnier, P. Vourc'h, C.R. Andres, N. Leporrier, and S. Briault Haploinsufficiency of the GPD2 gene in a patient with nonsyndromic mental retardation Hum. Genet. 124 2009 649 658
107. C.B. Wollheim, and G.W. Sharp Regulation of insulin release by calcium Physiol. Rev. 61 1981 914 973
108. 2 + concentration in an electrically excitable cell, the insulin-secreting pancreatic B-cell J. Biol. Chem. 267 1992 20713 20720
109. S. Misler, D.W. Barnett, K.D. Gillis, and D.M. Pressel Electrophysiology of stimulus-secretion coupling in human beta-cells Diabetes 41 1992 1221 1228
110. + channels in mouse B cells J. Clin. Invest. 89 1992 1288 1295
111. F. Schuit, A. De Vos, S. Farfari, K. Moens, D. Pipeleers, T. Brun, and M. Prentki Metabolic fate of glucose in purified islet cells. Glucose-regulated anaplerosis in beta cells J. Biol. Chem. 272 1997 18572 18579
112. M.D. Meglasson, K.M. Smith, D. Nelson, and M. Erecinska alpha-Glycerophosphate shuttle in a clonal beta-cell line Am. J. Physiol. 256 1989 E173 E178
113. C.G. Ostenson, S.M. Abdel-Halim, J. Rasschaert, F. Malaisse-Lagae, S. Meuris, A. Sener, S. Efendic, and W.J. Malaisse Deficient activity of FAD-linked glycerophosphate dehydrogenase in islets of GK rats Diabetologia 36 1993 722 726
114. A. Sener, L. Herberg, and W.J. Malaisse FAD-linked glycerophosphate dehydrogenase deficiency in pancreatic islets of mice with hereditary diabetes FEBS Lett. 316 1993 224 227
115. J. Rasschaert, F. Malaisse-Lagae, A. Sener, V. Leclercq-Meyer, L. Herberg, and W.J. Malaisse Impaired FAD-glycerophosphate dehydrogenase activity in islet and liver homogenates of fa/fa rats Mol. Cell. Biochem. 135 1994 137 141
116. M.H. Giroix, J. Rasschaert, D. Bailbe, V. Leclercq-Meyer, A. Sener, B. Portha, and W.J. Malaisse Impairment of glycerol phosphate shuttle in islets from rats with diabetes induced by neonatal streptozocin Diabetes 40 1991 227 232
117. J. Fernandez-Alvarez, I. Conget, J. Rasschaert, A. Sener, R. Gomis, and W.J. Malaisse Enzymatic, metabolic and secretory patterns in human islets of type 2 (non-insulin-dependent) diabetic patients Diabetologia 37 1994 177 181
118. M. Gudayol, M.E. Fabregat, J. Rasschaert, A. Sener, W.J. Malaisse, and R. Gomis Site-directed mutations in the FAD-binding domain of glycerophosphate dehydrogenase: catalytic defects with preserved mitochondrial anchoring of the enzyme in transfected COS-7 cells Mol. Genet. Metab. 75 2002 168 173
119. M.E. Fabregat, C. Benito, M. Gudayol, J. Vidal, T. Gallart, W.J. Malaisse, and R. Gomis Enzyme-linked immunosorbent assay of autoantibodies against mitochondrial glycerophosphate dehydrogenase in insulin-dependent and non-insulin-dependent diabetic subjects Biochem. Mol. Med. 62 1997 172 177
120. M.A. Ravier, K. Eto, F.C. Jonkers, M. Nenquin, T. Kadowaki, and J.C. Henquin The oscillatory behavior of pancreatic islets from mice with mitochondrial glycerol-3-phosphate dehydrogenase knockout J. Biol. Chem. 275 2000 1587 1593
121. K. Ueda, Y. Tanizawa, H. Ishihara, N. Kizuki, Y. Ohta, A. Matsutani, and Y. Oka Overexpression of mitochondrial FAD-linked glycerol-3-phosphate dehydrogenase does not correct glucose-stimulated insulin secretion from diabetic GK rat pancreatic islets Diabetologia 41 1998 649 653
122. K. Eto, Y. Tsubamoto, Y. Terauchi, T. Sugiyama, T. Kishimoto, N. Takahashi, N. Yamauchi, N. Kubota, S. Murayama, T. Aizawa, Y. Akanuma, S. Aizawa, H. Kasai, Y. Yazaki, and T. Kadowaki Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion Science 283 1999 981 985
123. T. Saheki, K. Inoue, H. Ono, A. Tushima, N. Katsura, M. Yokogawa, Y. Yoshidumi, T. Kuhara, M. Ohse, K. Eto, T. Kadowaki, D.S. Sinasac, and K. Kobayashi Metabolomic analysis reveals hepatic metabolite perturbations in citrin/mitochondrial glycerol-3-phosphate dehydrogenase double-knockout mice, a model of human citrin deficiency Mol. Genet. Metab. 104 2011 492 500
124. T. Saheki, M. Iijima, M.X. Li, K. Kobayashi, M. Horiuchi, M. Ushikai, F. Okumura, X.J. Meng, I. Inoue, A. Tajima, M. Moriyama, K. Eto, T. Kadowaki, D.S. Sinasac, L.C. Tsui, M. Tsuji, A. Okano, and T. Kobayashi Citrin/mitochondrial glycerol-3-phosphate dehydrogenase double knock-out mice recapitulate features of human citrin deficiency J. Biol. Chem. 282 2007 25041 25052
125. V. Kota, V.M. Dhople, and S. Shivaji Tyrosine phosphoproteome of hamster spermatozoa: role of glycerol-3-phosphate dehydrogenase 2 in sperm capacitation Proteomics 9 2009 1809 1826
126. V. Kota, P. Rai, J.M. Weitzel, R. Middendorff, S.S. Bhande, and S. Shivaji Role of glycerol-3-phosphate dehydrogenase 2 in mouse sperm capacitation Mol. Reprod. Dev. 77 2010 773 783
127. J.B. Schenkman, D.A. Richert, and W.W. Westerfeld Alpha-Glycerophosphate dehydrogenase activity in rat spermatozoa Endocrinology 76 1965 1055 1061
128. L. Myatt, and X. Cui Oxidative stress in the placenta Histochem. Cell Biol. 122 2004 369 382
129. A.A. Olivera, and R.A. Meigs Mitochondria from human term placenta. II. Characterization of respiratory pathways and coupling mechanisms Biochim. Biophys. Acta 376 1975 436 445
130. T. Honzik, Z. Drahota, M. Bohm, P. Jesina, T. Mracek, J. Paul, J. Zeman, and J. Houstek Specific properties of heavy fraction of mitochondria from human-term placenta - glycerophosphate-dependent hydrogen peroxide production Placenta 27 2006 348 356
131. S.M. Hunt, M. Osnos, and R.S. Rivlin Thyroid hormone regulation of mitochondrial alpha-glycerophosphate dehydrogenase in liver and hepatoma Cancer Res. 30 1970 1764 1768
132. O. Dionisi, A. Cittadini, G. Gelmuzzi, T. Galeotti, and T. Terranova The role of the alpha-glycerophosphate shuttle in the reoxidation of cytosolic NADH in Ehrlich ascites tumour cells Biochim. Biophys. Acta 216 1970 71 79
133. U. Karsten, G. Sydow, A. Wollenberger, and A. Graffi Rat liver glycerolphosphate dehydrogenases: activity changes and induction by thyroid hormone of the mitochondrial enzyme in hepatomas and in precancerous and growing liver Acta Biol. Med. Ger. 26 1971 1131 1140
134. S.K. Chowdhury, S. Raha, M.A. Tarnopolsky, and G. Singh Increased expression of mitochondrial glycerophosphate dehydrogenase and antioxidant enzymes in prostate cancer cell lines/cancer Free Radic. Res. 41 2007 1116 1124
135. S.K. Chowdhury, A. Gemin, and G. Singh High activity of mitochondrial glycerophosphate dehydrogenase and glycerophosphate-dependent ROS production in prostate cancer cell lines Biochem. Biophys. Res. Commun. 333 2005 1139 1145