Oxidative stress contributes to outcome severity in a Drosophila melanogaster model of classic galactosemia

DMM Disease Models and Mechanisms

Volumn 6, Issue 1, 2013, Pages 84-94

  Jumbo Lucioni, Patricia P ^a   Hopson, Marquise L ^a   Hang, Darwin ^b   Liang, Yongliang ^a   Jones, Dean P ^a   Fridovich Keil, Judith L ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; CYSTEINE; DIMETHYL SULFOXIDE; GALACTOSE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE D6; GLUTATHIONE TRANSFERASE E7; GSTD6 PROTEIN; GSTE7 PROTEIN; PARAQUAT; PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DROSOPHILA MELANOGASTER; GALACTOSEMIA; GENETIC MODEL; GENOTYPE; LARVA; MUTANT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL;

ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; CYSTEINE; DIMETHYL SULFOXIDE; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GALACTOSE; GALACTOSEMIAS; GALACTOSEPHOSPHATES; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; GENES, INSECT; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HUMANS; MUTATION; OXIDATIVE STRESS; PARAQUAT; REACTIVE OXYGEN SPECIES; UDPGLUCOSE-HEXOSE-1-PHOSPHATE URIDYLYLTRANSFERASE; XANTHONES;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 84872080381     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.010207     Document Type: Article

References (73)

1. Aguer, C., Gambarotta, D., Mailloux, R. J., Moffat, C., Dent, R., McPherson, R. and Harper, M. E. (2011). Galactose enhances oxidative metabolism and reveals mitochondrial dysfunction in human primary muscle cells. PLoS ONE 6, e28536.
2. Alias, Z. and Clark, A. G. (2007). Studies on the glutathione S-transferase proteome of adult Drosophila melanogaster: responsiveness to chemical challenge. Proteomics 7, 3618-3628.
3. Bahadorani, S., Bahadorani, P., Phillips, J. P. and Hilliker, A. J. (2008). The effects of vitamin supplementation on Drosophila life span under normoxia and under oxidative stress. J. Gerontol. A Biol. Sci. Med. Sci. 63, 35-42.
4. Bennett, M. (2010). Galactosemia diagnosis gets an upgrade. Clin. Chem. 56, 690-692.
5. Berg, J. M., Tymoczko, J. L. and Stryer, L. (2002). Biochemistry. New York: W H Freeman.
6. Berry, G. T., Nissim, I., Lin, Z., Mazur, A. T., Gibson, J. B. and Segal, S. (1995). Endogenous synthesis of galactose in normal men and patients with hereditary galactosemia. Lancet 346, 1073-1074.
7. Bhat, P. J. (2003). Galactose-1-phosphate is a regulator of inositol monophosphatase: a fact or a fiction? Med. Hypotheses 60, 123-128.
8. Bonilla, E., Medina-Leendertz, S., Villalobos, V., Molero, L. and Bohórquez, A. (2006). Paraquat-induced oxidative stress in Drosophila melanogaster: effects of melatonin, glutathione, serotonin, minocycline, lipoic acid and ascorbic acid. Neurochem. Res. 31, 1425-1432.
9. Bosch, A. M. (2006). Classical galactosaemia revisited. J. Inherit. Metab. Dis. 29, 516-525.
10. Bosch, A. M. (2011). Classic galactosemia: dietary dilemmas. J. Inherit. Metab. Dis. 34, 257-260.
11. Boxer, M., Shen, M., Tanega, C., Tang, M., Lai, K. and Auld, D. (2010). Toward improved therapy for classic galactosemia. In Probe Reports from the NIH Molecular Libraries Program [Internet]. Bethesda (MD): National Center for Biotechnology Information (US).
12. Bumrungpert, A., Kalpravidh, R. W., Chuang, C.-C., Overman, A., Martinez, K., Kennedy, A. and McIntosh, M. (2010). Xanthones from mangosteen inhibit inflammation in human macrophages and in human adipocytes exposed to macrophage-conditioned media. J. Nutr. 140, 842-847.
13. Cui, X., Wang, L., Zuo, P., Han, Z., Fang, Z., Li, W. and Liu, J. (2004). D-Galactose-caused life shortening in Drosophila melanogaster and Musca domestica is associated with oxidative stress. Biogerontology 5, 317-325.
14. Cui, X., Zuo, P., Zhang, Q., Li, X., Hu, Y., Long, J., Packer, L. and Liu, J. (2006). Chronic systemic D-galactose exposure induces memory loss, neurodegeneration, and oxidative damage in mice: protective effects of R-alpha-lipoic acid. J. Neurosci. Res. 84, 647-654.
15. De Deken, R. (1966). The Crabtree effect: a regulatory system in yeast. J. Gen. Microbiol. 44, 149-156.
16. Douglas, H. C. and Hawthorne, D. C. (1964). Enzymatic expression and genetic linkage of genes controlling galactose utilization in Saccharomyces. Genetics 49, 837-844.
17. Duarte, T. L. and Lunec, J. (2005). Review part of the series: From dietary antioxidants to regulators in cellular signalling and gene expression review: When is an antioxidant not an antioxidant? A review of novel actions and reactions of vitamin C. Free Radic. Res. 39, 671-686.
18. Engerman, R. L. and Kern, T. S. (1984). Experimental galactosemia produces diabetic-like retinopathy. Diabetes 33, 97-100.
19. Frey, P. A. (1996). The Leloir pathway: a mechanistic imperative for three enzymes to change the sterochemical configuration of a single carbon in galactose. FASEB J. 10, 461-470.
20. Fridovich-Keil, J. (2006). Galactosemia: the good, the bad, and the unknown. J. Cell Physiol. 209, 701-705.
21. Fridovich-Keil, J. L. and Walter, J. H. (2008). Galactosemia. In The Online Metabolic & Molecular Bases of Inherited Disease, Part 7, Chapter 72 (eds D. Valle, A. Beaudet, B. Vogelstein, K. Kinzler, S. Antonarakis and A. Ballabio). New York: McGraw Hill. http://www.ommbid.com/OMMBID/a/c.html/ carbohydrates/galactosemia.
22. Gitzelmann, R. (1995). Galactose-1-phosphate in the pathophysiology of galactosemia. Eur. J. Pediatrics 154 Suppl. 2, S45-S49.
23. Gitzelmann, R. and Steinmann, B. (1984). Galactosemia: how does long-term treatment change the outcome? Enzyme 32, 37-46.
24. Guenin, L., Raharijaona, M., Houlgatte, R. and Baba-Aissa, F. (2010). Expression profiling of prospero in the Drosophila larval chemosensory organ: Between growth and outgrowth. BMC Genomics 11, 47.
25. Ho, S. C., Liu, J. H. and Wu, R. Y. (2003). Establishment of the mimetic aging effect in mice caused by D-galactose. Biogerontology 4, 15-18.
26. Holden, H. M., Rayment, I. and Thoden, J. B. (2003). Structure and function of enzymes of the Leloir pathway for galactose metabolism. J. Biol. Chem. 278, 43885-43888.
27. Hughes, J., Ryan, S., Lambert, D., Geoghegan, O., Clark, A., Rogers, Y., Hendroff, U., Monavari, A., Twomey, E. and Treacy, E. (2009). Outcomes of siblings with classical galactosemia. J. Pediatr. 154, 721-726.
28. - and dimethyl sulfoxide. Biochem. Biophys. Res. Commun. 102, 531-537.
29. Jones, D. P., Carlson, J. L., Samiec, P. S., Sternberg, P., Jr, Mody, V. C., Jr, Reed, R. L. and Brown, L. A. (1998). Glutathione measurement in human plasma. Evaluation of sample collection, storage and derivatization conditions for analysis of dansyl derivatives by HPLC. Clin. Chim. Acta 275, 175-184.
30. Jones, D. P., Carlson, J. L., Mody, V. C., Cai, J., Lynn, M. J. and Sternberg, P. (2000). Redox state of glutathione in human plasma. Free Radic. Biol. Med. 28, 625-635.
31. Jordens, R. G., Berry, M. D., Gillott, C. and Boulton, A. A. (1999). Prolongation of life in an experimental model of aging in Drosophila melanogaster. Neurochem. Res. 24, 227-233.
32. Jumbo-Lucioni, P., Garber, K., Kiel, J., Baric, I., Berry, G., Bosch, A., Burlina, A., Chiesa, A., Pico, M., Estrada, S. et al. (2012). Diversity of approaches to classic galactosemia around the world: a comparison of diagnosis, intervention, and outcomes. J. Inherit. Metab. Dis. [Epub ahead of print] doi:10.1007/s10545-012-9477-y.
33. Jung, H. A., Su, B. N., Keller, W. J., Mehta, R. G. and Kinghorn, A. D. (2006). Antioxidant xanthones from the pericarp of Garcinia mangostana (Mangosteen). J. Agric. Food Chem. 54, 2077-2082.
34. Kabir, M. A., Khanday, F. A., Mehta, D. V. and Bhat, P. J. (2000). Multiple copies of MRG19 suppress transcription of the GAL1 promoter in a GAL80-dependent manner in Saccharomyces cerevisiae. Mol. Gen. Genet. 262, 1113-1122.
35. Kirlin, W. G., Cai, J., Thompson, S. A., Diaz, D., Kavanagh, T. J. and Jones, D. P. (1999). Glutathione redox potential in response to differentiation and enzyme inducers. Free Radic. Biol. Med. 27, 1208-1218.
36. Kowluru, R. A., Kern, T. S. and Engerman, R. L. (1997). Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system. Free Radic. Biol. Med. 22, 587-592.
37. Kushner, R., Ryan, E., Sefton, J., Sanders, R., Lucioni, P., Moberg, K. and Fridovich-Keil, J. (2010). A Drosophila melanogaster model of classic galactosemia. Dis. Model. Mech. 3, 618-627.
38. Lai, K. and Elsas, L. (2000). Overexpression of human UDP-glucose pyrophosphorylase rescues galactose-1-phosphate uridyltransferase-deficient yeast. Biochem. Biophys. Res. Commun. 271, 392-400.
39. Larson, R. T., Lorch, J. M., Pridgeon, J. W., Becnel, J. J., Clark, G. G. and Lan, Q. (2010). The biological activity of alpha-mangostin, a larvicidal botanic mosquito sterol carrier protein-2 inhibitor. J. Med. Entomol. 47, 249-257.
40. Lebea, P. and Pretorius, P. (2005). The molecular relationship between deficient UDP-galactose uridyl transferase (GALT) and ceramide galactosyltransferase (CGT) enzyme function: a possible cause for poor long-term prognosis in classic galactosemia. Med. Hypotheses 65, 1051-1057.
41. Leslie, N. D. (2003). Insights into the pathogenesis of galactosemia. Annu. Rev. Nutr. 23, 59-80.
42. Li, H. M., Buczkowski, G., Mittapalli, O., Xie, J., Wu, J., Westerman, R., Schemerhorn, B. J., Murdock, L. L. and Pittendrigh, B. R. (2008). Transcriptomic profiles of Drosophila melanogaster third instar larval midgut and responses to oxidative stress. Insect Mol. Biol. 17, 325-339.
43. Long, J., Wang, X., Gao, H., Liu, Z., Liu, C., Miao, M., Cui, X., Packer, L. and Liu, J. (2007). D-Galactose toxicity in mice is associated with mitochondrial dysfunction: protecting effects of mitochondrial nutrient R-alpha-lipoic acid. Biogerontology 8, 373-381.
44. Martinez, A., Galano, A. and Vargas, R. (2011). Free radical scavenger properties of alpha-mangostin: thermodynamics and kinetics of HAT and RAF mechanisms. J. Phys. Chem. B 115, 12591-12598.
45. Mayes, J. S. and Miller, L. R. (1973). The metabolism of galactose by galactosemia fibroblasts. Biochim. Biophys. Acta 313, 9-16.
46. Mehta, D. V., Kabir, A. and Bhat, P. J. (1999). Expression of human inositol monophosphatase suppresses galactose toxicity in Saccharomyces cerevisiae: possible implications for galactosemia. Biochim. Biophys. Acta 1454, 217-226.
47. Miller, L. T., Watson, W. H., Kirlin, W. G., Ziegler, T. R. and Jones, D. P. (2002). Oxidation of the glutathione/glutathione disulfide redox state is induced by cysteine deficiency in human colon carcinoma HT29 cells. J. Nutr. 132, 2303-2306.
48. Naidu, K. (2003). Vitamin C in human health and disease is still a mystery? An overview. Nutr. J. 2, 7.
49. Obrosova, I., Faller, A., Burgan, J., Ostrow, E. and Williamson, J. R. (1997). Glycolytic pathway, redox state of NAD(P)-couples and energy metabolism in lens in galactosefed rats: effect of an aldose reductase inhibitor. Curr. Eye Res. 16, 34-43.
50. Openo, K., Schulz, J., Vargas, C., Orton, C., Epstein, M., Schnur, R., Scaglia, F., Berry, G., Gottesman, G., Ficicioglu, C. et al. (2006). Epimerase-deficiency galactosemia is not a binary condition. Am. J. Hum. Genet. 78, 89-102.
51. Parthasarathy, R., Parthasarathy, L. and Vadnal, R. (1997). Brain inositol monophosphatase identified as a galactose-1-phosphatase. Brain Res. 778, 99-106.
52. Pedraza-Chaverri, J., Reyes-Fermin, L. M., Nolasco-Amaya, E. G., Orozco-Ibarra, M., Medina-Campos, O. N., Gonzalez-Cuahutencos, O., Rivero-Cruz, I. and Mata, R. (2009). ROS scavenging capacity and neuroprotective effect of alpha-mangostin against 3-nitropropionic acid in cerebellar granule neurons. Exp. Toxicol. Pathol. 61, 491-501.
53. Pesce, M. and Bodourian, S. (1982). Clinical significance of plasma galactose and erythrocyte galactose-1-phosphate measurements in transferase-deficient galactosemia and in individuals with below-normal transferase activity. Clin. Chem. 28, 301-305.
54. Rose, R. C. and Bode, A. M. (1993). Biology of free radical scavengers: an evaluation of ascorbate. FASEB J. 7, 1135-1142.
55. Ross, K. L., Davis, C. N. and Fridovich-Keil, J. L. (2004). Differential roles of the Leloir pathway enzymes and metabolites in defining galactose sensitivity in yeast. Mol. Gen. Metab. 83, 103-116.
56. Rzezniczak, T. Z., Douglas, L. A., Watterson, J. H. and Merritt, T. J. (2011). Paraquat administration in Drosophila for use in metabolic studies of oxidative stress. Anal. Biochem. 419, 345-347.
57. +-ATPase activities in patients with classical galactosaemia. Clinical Nutr. 24, 151-157.
58. Schulpis, K. H., Papassotiriou, I. and Tsakiris, S. (2006). 8-Hydroxy-2-desoxyguanosine serum concentrations as a marker of DNA damage in patients with classical galactosaemia. Acta Paediatr. 95, 164-169.
59. Schweitzer-Krantz, S. (2003). Early diagnosis of inherited metabolic disorders towards improving outcome: the controversial issue of galactosaemia. Eur. J. Pediatr. 162, S50-S53.
60. Segal, S. (1995). Galactosemia unsolved. Eur. J. Pediatr. 154, S97-S102.
61. Shang, Y. Z., Gong, M. Y., Zhou, X. X., Li, S. T. and Wang, B. Y. (2001). Improving effects of SSF on memory deficits and pathological changes of neural and immunological systems in senescent mice. Acta Pharmacol. Sin. 22, 1078-1083.
62. Shen, Y., Xu, S., Wei, W., Sun, X., Yang, J., Liu, L. and Dong, C. (2002). Melatonin reduces memory changes and neural oxidative damage in mice treated with D-galactose. J. Pineal. Res. 32, 173-178.
63. Song, X., Bao, M., Li, D. and Li, Y. M. (1999). Advanced glycation in D-galactose induced mouse aging model. Mech. Ageing Dev. 108, 239-251.
64. Tang, M., Odejinmi, S., Vankayalapati, H., Wierenga, K. and Lai, K. (2011). Innovative therapy for classic galactosemia - tale of two HTS. Mol. Genet. Metab. 105, 44-55.
65. +-ATPase activities in galactosemia in vitro. Metab. Brain Dis. 20, 87-95.
66. Tyfield, L. and Walter, J. (2002). Galactosemia. In The Metabolic and Molecular Bases of Inherited Disease (ed. C. Scriver, A. Beaudet, W. Sly, D. Valle, B. Childs, K. Kinzler and B. Vogelstein). New York: McGraw-Hill.
67. Udani, J. K., Singh, B. B., Barrett, M. L. and Singh, V. J. (2009). Evaluation of mangosteen juice blend on biomarkers of inflammation in obese subjects: a pilot, dose finding study. Nutr. J. 8, 48.
68. Waggoner, D. D., Buist, N. R. and Donnell, G. N. (1990). Long-term prognosis in galactosaemia: results of a survey of 350 cases. J. Inherit. Metab. Dis. 13, 802-818.
69. Wei, H., Li, L., Song, Q., Ai, H., Chu, J. and Li, W. (2005). Behavioural study of the D-galactose induced aging model in C57BL/6J mice. Behav. Brain Res. 157, 245-251.
70. Wells, W. W., McIntyre, J. P., Schlichter, D. J., Wacholtz, M. C. and Spieker, S. E. (1969). Studies of myo-inositol metabolism in galactosemia. Ann. N. Y. Acad. Sci. 165, 599-608.
71. Wierenga, K., Lai, K., Buchwald, P. and Tang, M. (2008). High-throughput screening for human galactokinase inhibitors. J. Biomol. Screen 13, 415-423.
72. Williams, P., Ongsakul, M., Proudfoot, J., Croft, K. and Beilin, L. (1995). Mangostin inhibits the oxidative modification of human low density lipoprotein. Free Radic. Res. 23, 175-184.
73. Yelinova, V., Glazachev, Y., Khramtsov, V., Kudryashova, L., Rykova, V. and Salganik, R. (1996). Studies of human and rat blood under oxidative stress: changes in plasma thiol level, antioxidant enzyme activity, protein carbonyl content, and fluidity of erythrocyte membrane. Biochem. Biophys. Res. Commun. 221, 300-303.