Oxidative stress and adrenocortical insufficiency

Journal of Endocrinology

Volumn 221, Issue 3, 2014, Pages

  Prasad, R ^a   Kowalczyk, J C ^a   Meimaridou, E ^a   Storr, H L ^a   Metherell, L A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Adrenal insufficiency; Oxidative stress; Reactive oxygen species; Steroidogenesis

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CORTICOTROPIN; CORTICOTROPIN RECEPTOR; CYTOCHROME P450; FERREDOXIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; ISOCITRATE DEHYDROGENASE; MELANOCORTIN 2 RECEPTOR; MINICHROMOSOME MAINTENANCE PROTEIN 4; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; NITRIC OXIDE SYNTHASE; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RETINOL; SELENOCYSTEINE; SUPEROXIDE DISMUTASE; UBIQUINOL CYTOCHROME C REDUCTASE; XANTHINE OXIDASE;

ADRENAL CORTEX FUNCTION; ADRENAL CORTEX INSUFFICIENCY; ADRENAL INSUFFICIENCY; ADRENOLEUKODYSTROPHY; ALLGROVE SYNDROME; ANTIOXIDANT ACTIVITY; CELL FUNCTION; CIRCADIAN RHYTHM; CONGESTIVE CARDIOMYOPATHY; DEGENERATIVE DISEASE; ELECTRON TRANSPORT; GENOTYPE PHENOTYPE CORRELATION; HUMAN; MITOCHONDRIAL RESPIRATION; NEUROLOGIC DISEASE; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RESPIRATORY CHAIN; RETINOL DEFICIENCY; REVIEW; STEROIDOGENESIS;

ADRENAL INSUFFICIENCY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; STEROIDOGENESIS;

ADRENAL INSUFFICIENCY; ANTIOXIDANTS; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84901638216     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0346     Document Type: Review

References (87)

1. Allgrove J, Clayden GS, Grant DB & Macaulay JC 1978 Familial glucocorticoid deficiency with achalasia of the cardia and deficient tear production. Lancet 1 1284-1286. (doi:10.1016/S0140-6736(78) 91268-0)
2. Azhar S, Cao L & Reaven E 1995 Alteration of the adrenal antioxidant defense system during aging in rats. Journal of Clinical Investigation 96 1414-1424. (doi:10.1172/JCI118177)
3. Baker BY, Lin L, Kim CJ, Raza J, Smith CP, Miller WL & Achermann JC 2006 Nonclassic congenital lipoid adrenal hyperplasia: a new disorder of the steroidogenic acute regulatory protein with very late presentation and normal male genitalia. Journal of Clinical Endocrinology and Metabolism 91 4781-4785. (doi:10.1210/jc.2006-1565)
4. Basel-Vanagaite L, Muncher L, Straussberg R, Pasmanik-Chor M, Yahav M, Rainshtein L, Walsh CA, Magal N, Taub E, Drasinover V et al. 2006 Mutated nup62 causes autosomal recessive infantile bilateral striatal necrosis. Annals of Neurology 60 214-222. (doi:10.1002/ana.20902)
5. Behne D & Hofer-Bosse T 1984 Effects of a low selenium status on the distribution and retention of selenium in the rat. Journal of Nutrition 114 1289-1296.
6. Brites P, Mooyer PA, El Mrabet L, Waterham HR & Wanders RJ 2009 Plasmalogens participate in very-long-chain fatty acid-induced pathology. Brain 132 482-492. (doi:10.1093/brain/awn295)
7. Chanoine JP, Compagnone NA, Wong AC & Mellon SH 2001 Modulation of steroidogenesis by selenium in a novel adrenal cell line developed using targeted tumorigenesis. Bio Factors 14 229-238. (doi:10.1002/biof. 5520140129)
8. Cho AR, Yang KJ, Bae Y, Bahk YY, Kim E, Lee H, Kim JK, Park W, Rhim H, Choi SY et al. 2009 Tissue-specific expression and subcellular localization of ALADIN, the absence of which causes human triple A syndrome. Experimental &Molecular Medicine 41 381-386. (doi:10.3858/emm.2009.41.6.043)
9. Clark AJ, Mc Loughlin L & Grossman A 1993 Familial glucocorticoid deficiency associated with point mutation in the adrenocorticotropin receptor. Lancet 341 461-462. (doi:10.1016/0140-6736(93)90208-X)
10. Cox AG, Winterbourn CC & Hampton MB 2010 Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochemical Journal 425 313-325. (doi:10.1042/BJ20091541)
11. Diemer T, Allen JA, Hales KH & Hales DB 2003 Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (St AR) protein and steroidogenesis. Endocrinology 144 2882-2891. (doi:10.1210/en.2002-0090)
12. Dixit A, Chow G & Sarkar A 2011 Neurologic presentation of triple A syndrome. Pediatric Neurology 45 347-349. (doi:10.1016/j.pediatrneurol.2011.07.003)
13. Ferrari E, Cravello L, Muzzoni B, Casarotti D, Paltro M, Solerte SB, Fioravanti M, Cuzzoni G, Pontiggia B & Magri F 2001 Age-related changes of the hypothalamic-pituitary-adrenal axis: pathophysiological correlates. European Journal of Endocrinology 144 319-329. (doi:10.1530/eje.0.1440319)
14. Forss-Petter S, Werner H, Berger J, Lassmann H, Molzer B, Schwab MH, Bernheimer H, Zimmermann F & Nave KA 1997 Targeted inactivation of the X-linked adrenoleukodystrophy gene in mice. Journal of Neuroscience Research 50 829-843. (doi:10.1002/(SICI)1097-4547 (19971201)50:5%3C;829::AID-JNR19%3E;3.0.CO;2-W)
15. Fourcade S, Lopez-Erauskin J, Galino J, Duval C, Naudi A, Jove M, Kemp S, Villarroya F, Ferrer I, Pamplona R et al. 2008 Early oxidative damage underlying neurodegeneration in X-adrenoleukodystrophy. Human Molecular Genetics 17 1762-1773. (doi:10.1093/hmg/ddn085)
16. Galea E, Launay N, Portero-Otin M, Ruiz M, Pamplona R, Aubourg P, Ferrer I & Pujol A 2012 Oxidative stress underlying axonal degeneration in adrenoleukodystrophy: a paradigm for multifactorial neurodegenerative diseases? Biochimica et Biophysica Acta 1822 1475-1488. (doi:10.1016/j.bbadis.2012.02.005)
17. Galino J, Ruiz M, Fourcade S, Schluter A, Lopez-Erauskin J, Guilera C, Jove M, Naudi A, Garcia-Arumi E, Andreu AL et al. 2011 Oxidative damage compromises energy metabolism in the axonal degeneration mouse model of X-adrenoleukodystrophy. Antioxidants and Redox Signaling 15 2095-2107. (doi:10.1089/ars.2010.3877)
18. Gigliotti S, Callaini G, Andone S, Riparbelli MG, Pernas-Alonso R, Hoffmann G, Graziani F & Malva C 1998 Nup154, a new Drosophila gene essential for male and female gametogenesis is related to the Nup155 vertebrate nucleoporin gene. Journal of Cell Biology 142 1195-1207. (doi:10.1083/jcb.142.5.1195)
19. Goncharova ND & Lapin BA 2004 Age-related endocrine dysfunction in nonhuman primates. Annals of the New York Academy of Sciences 1019 321-325. (doi:10.1196/annals.1297.054)
20. Goncharova ND, Marenin VY & Bogatyrenko TN 2008a Stress, aging and reliability of antioxidant enzyme defense. Current Aging Science 1 22-29. (doi:10.2174/1874609810801010022)
21. Goncharova ND, Shmaliy AV,Marenin VY, Smelkova SA & Lapin BA 2008b Circadian and age-related changes in stress responsiveness of the adrenal cortex and erythrocyte antioxidant enzymes in female rhesus monkeys. Journal of Medical Primatology 37 229-238. (doi:10.1111/j.1600-0684.2007.00278.x)
22. Goncharova ND, Marenin VY & Vengerin AA 2013 Age-related changes in the reliability of antioxidant enzyme defense in monkeys with different types of adaptive behavior. Current Aging Science 6 163-169. (doi:10.2174/18746098112059990004)
23. Grimaldi MR, Cozzolino L, Malva C, Graziani F & Gigliotti S 2007 nup154 genetically interacts with cup and plays a cell-type-specific function during Drosophila melanogaster egg-chamber development. Genetics 175 1751-1759. (doi:10.1534/genetics.106.062844)
24. Grinberg AV, Hannemann F, Schiffler B, Muller J, Heinemann U&Bernhardt R 2000 Adrenodoxin: structure, stability, and electron transfer properties. Proteins 40 590-612. (doi:10.1002/1097-0134(20000901)40:4%3C;590::AID-PROT50%3E;3.0.CO;2-P)
25. Gruber KA, O'Brien LV & Gerstner R 1976 Vitamin A: not required for adrenal steroidogenesis in rats. Science 191 472-475. (doi:10.1126/science.1246630)
26. Hamre K, Tharp R, Poon K, Xiong X & Smeyne RJ 1999 Differential strain susceptibility following 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) administration acts in an autosomal dominant fashion:quantitative analysis in seven strains of Mus musculus. Brain Research 828 91-103. (doi:10.1016/S0006-8993(99)01273-1)
27. Handschug K, Sperling S, Yoon SJ, Hennig S, Clark AJ & Huebner A 2001 Triple A syndrome is caused by mutations in AAAS, a new WD-repeat protein gene. Human Molecular Genetics 10 283-290. (doi:10.1093/hmg/10.3.283)
28. Hanschmann EM, Lonn ME, Schutte LD, Funke M, Godoy JR, Eitner S, Hudemann C & Lillig CH 2010 Both thioredoxin 2 and glutaredoxin 2 contribute to the reduction of the mitochondrial 2-Cys peroxiredoxin Prx3. Journal of Biological Chemistry 285 40699-40705. (doi:10.1074/jbc.M110.185827)
29. Hanukoglu I 2006 Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metabolism Reviews 38 171-196. (doi:10.1080/03602530600570040)
30. Hanukoglu I & Hanukoglu Z 1986 Stoichiometry of mitochondrial cytochromes P-450, adrenodoxin and adrenodoxin reductase in adrenal cortex and corpus luteum. Implications for membrane organization and gene regulation. European Journal of Biochemistry 157 27-31. (doi:10.1111/j.1432-1033.1986.tb09633.x)
31. Hayashi H & Oohashi M 1995 Incorporation of acetyl-Co A generated from peroxisomal b-oxidation into ethanolamine plasmalogen of rat liver. Biochimica et Biophysica Acta 1254 319-325. (doi:10.1016/0005-2760 (94)00194-4)
32. Hirano M, Furiya Y, Asai H, Yasui A & Ueno S 2006 ALADINI482S causes selective failure of nuclear protein import and hypersensitivity to oxidative stress in triple A syndrome. PNAS 103 2298-2303. (doi:10.1073/pnas.0505598103)
33. Hoftberger R, Kunze M, Weinhofer I, Aboul-Enein F, Voigtlander T,Oezen I, Amann G, Bernheimer H, Budka H & Berger J 2007 Distribution and cellular localization of adrenoleukodystrophy protein in human tissues:implications for X-linked adrenoleukodystrophy. Neurobiology of Disease 28 165-174. (doi:10.1016/j.nbd.2007.07.007)
34. Hornig D 1975 Distribution of ascorbic acid, metabolites and analogues in man and animals. Annals of the New York Academy of Sciences 258 103-118. (doi:10.1111/j.1749-6632.1975.tb29271.x)
35. Hornsby PJ 1980 Regulation of cytochrome P-450-supported 11b-hydroxylation of deoxycortisol by steroids, oxygen, and antioxidants in adrenocortical cell cultures. Journal of Biological Chemistry 255 4020-4027.
36. Houlden H, Smith S, De Carvalho M, Blake J,Mathias C, Wood NW& Reilly MM 2002 Clinical and genetic characterization of families with triple A (Allgrove) syndrome. Brain 125 2681-2690. (doi:10.1093/brain/awf270)
37. Huang TT, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, Carlson EJ & Epstein CJ 2006 Genetic modifiers of the phenotype ofmice deficient in mitochondrial superoxide dismutase. Human Molecular Genetics 15 1187-1194. (doi:10.1093/hmg/ddl034)
38. Huebner A, Kaindl AM, Braun R & Handschug K 2002 New insights into the molecular basis of the triple A syndrome. Endocrine Research 28 733-739. (doi:10.1081/ERC-120016998)
39. Huebner A, Mann P, Rohde E, Kaindl AM, Witt M, Verkade P, Jakubiczka S, Menschikowski M, Stoltenburg-Didinger G & Koehler K 2006 Mice lacking the nuclear pore complex protein ALADIN show female infertility but fail to develop a phenotype resembling human triple A syndrome. Molecular and Cellular Biology 26 1879-1887. (doi:10.1128/MCB.26.5.1879-1887.2006)
40. Hughes CR, Guasti L, Meimaridou E, Chuang CH, Schimenti JC, King PJ, Costigan C, Clark AJ & Metherell LA 2012 MCM4 mutation causes adrenal failure, short stature, and natural killer cell deficiency in humans. Journal of Clinical Investigation 122 814-820. (doi:10.1172/JCI60224)
41. Imai H, Hakkaku N, Iwamoto R, Suzuki J, Suzuki T, Tajima Y, Konishi K, Minami S, Ichinose S, Ishizaka K et al. 2009 Depletion of selenoprotein GPx4 in spermatocytes causes male infertility in mice. Journal of Biological Chemistry 284 32522-32532. (doi:10.1074/jbc.M109.016139)
42. Ivashchenko O, Van Veldhoven PP, Brees C, Ho YS, Terlecky SR & Fransen M 2011 Intraperoxisomal redox balance in mammalian cells:oxidative stress and interorganellar cross-talk. Molecular Biology of the Cell 22 1440-1451. (doi:10.1091/mbc.E10-11-0919)
43. Kemp S, Berger J & Aubourg P 2012 X-linked adrenoleukodystrophy:clinical, metabolic, genetic and pathophysiological aspects. Biochimica et Biophysica Acta 1822 1465-1474. (doi:10.1016/j.bbadis.2012.03.012)
44. Khan M, Singh J & Singh I 2008 Plasmalogen deficiency in cerebral adrenoleukodystrophy and its modulation by lovastatin. Journal of Neurochemistry 106 1766-1779. (doi:10.1111/j.1471-4159.2008.05513.x)
45. Kil IS, Lee SK, Ryu KW, Woo HA, Hu MC, Bae SH & Rhee SG 2012 Feedback control of adrenal steroidogenesis via H2O2-dependent, reversible inactivation of peroxiredoxin III in mitochondria. Molecular Cell 46 584-594. (doi:10.1016/j.molcel.2012.05.030)
46. Kim A, Chen CH, Ursell P & Huang TT 2010 Genetic modifier of mitochondrial superoxide dismutase-deficientmice delays heart failure and prolongs survival. Mammalian Genome 21 534-542. (doi:10.1007/s00335-010-9299-x)
47. Kind B, Koehler K, Krumbholz M, Landgraf D & Huebner A 2010 Intracellular ROS level is increased in fibroblasts of triple A syndrome patients. Journal of Molecular Medicine 88 1233-1242. (doi:10.1007/s00109-010-0661-y)
48. Kiriyama T, Hirano M, Asai H, Ikeda M, Furiya Y & Ueno S 2008 Restoration of nuclear-import failure caused by triple A syndrome and oxidative stress. Biochemical and Biophysical Research Communications 374 631-634. (doi:10.1016/j.bbrc.2008.07.088)
49. Korytowski W, Pilat A, Schmitt JC & Girotti AW 2013 Deleterious cholesterol hydroperoxide trafficking in steroidogenic acute regulatory (St AR) protein-expressing MA-10 Leydig cells: implications for oxidative stress-impaired steroidogenesis. Journal of Biological Chemistry 288 11509-11519. (doi:10.1074/jbc.M113.452151)
50. Krumbholz M, Koehler K & Huebner A 2006 Cellular localization of 17 natural mutant variants of ALADIN protein in triple A syndrome -shedding light on an unexpected splice mutation. Biochemistry and Cell Biology 84 243-249. (doi:10.1139/o05-198)
51. Kulkarni RN, Almind K, Goren HJ,Winnay JN, Ueki K, Okada T & Kahn CR 2003 Impact of genetic background on development of hyperinsulinemia and diabetes in insulin receptor/insulin receptor substrate-1 double heterozygous mice. Diabetes 52 1528-1534. (doi:10.2337/diabetes.52.6.1528)
52. Lu JF, Barron-Casella E, Deering R, Heinzer AK, Moser AB, de Mesy Bentley KL, Wand GS, C McGuinness M, Pei Z, Watkins PA et al. 2007 The role of peroxisomal ABC transporters in the mouse adrenal gland: the loss of Abcd2 (ALDR), not Abcd1 (ALD), causes oxidative damage. Laboratory Investigation 87 261-272. (doi:10.1038/labinvest. 3700512)
53. Meimaridou E, Kowalczyk J, Guasti L, Hughes CR, Wagner F, Frommolt P, Nurnberg P, Mann NP, Banerjee R, Saka HN et al. 2012 Mutations in NNT encoding nicotinamide nucleotide transhydrogenase cause familial glucocorticoid deficiency. Nature Genetics 44 740-742. (doi:10.1038/ng.2299)
54. Meimaridou E, Hughes CR, Kowalczyk J, Chan LF, Clark AJ & Metherell LA 2013 ACTH resistance: genes and mechanisms. Endocrine Development 24 57-66. (doi:10.1159/000342504)
55. Metherell LA, Chapple JP, Cooray S, David A, Becker C, Ruschendorf F, Naville D, Begeot M, Khoo B, Nurnberg P et al. 2005 Mutations in MRAP, encoding a new interacting partner of the ACTH receptor, cause familial glucocorticoid deficiency type 2. Nature Genetics 37 166-170. (doi:10.1038/ng1501)
56. Metherell LA, Naville D, Halaby G, Begeot M, Huebner A, Nurnberg G, Nurnberg P, Green J, Tomlinson JW, Krone NP et al. 2009 Nonclassic lipoid congenital adrenal hyperplasia masquerading as familial glucocorticoid deficiency. Journal of Clinical Endocrinology and Metabolism 94 3865-3871. (doi:10.1210/jc.2009-0467)
57. Milenkovic T, Zdravkovic D, Savic N, Todorovic S, Mitrovic K, Koehler K & Huebner A 2010 Triple A syndrome: 32 years experience of a single centre (1977-2008). European Journal of Pediatrics 169 1323-1328. (doi:10.1007/s00431-010-1222-7)
58. Miller WL 2005 Minireview: Regulation of steroidogenesis by electron transfer. Endocrinology 146 2544-2550. (doi:10.1210/en.2005-0096)
59. Miller WL 2011 Role of mitochondria in steroidogenesis. Endocrine Development 20 1-19. (doi:10.1016/j.beem.2012.05.002)
60. Neilson DE 2010 The interplay of infection and genetics in acute necrotizing encephalopathy. Current Opinion in Pediatrics 22 751-757. (doi:10.1097/MOP.0b013e3283402bfe)
61. Neilson DE, Adams MD, Orr CM, Schelling DK, Eiben RM, Kerr DS, Anderson J, Bassuk AG, Bye AM, Childs AM et al. 2009 Infectiontriggered familial or recurrent cases of acute necrotizing encephalopathy caused by mutations in a component of the nuclear pore, RANBP2. American Journal of Human Genetics 84 44-51. (doi:10.1016/j.ajhg.2008.12.009)
62. Palmieri F 1994 Mitochondrial carrier proteins. FEBS Letters 346 48-54. (doi:10.1016/0014-5793(94)00329-7)
63. Papadopoulos V & Miller WL 2012 Role of mitochondria in steroidogenesis. Best Practice & Research. Clinical Endocrinology & Metabolism 26 771-790. (doi:10.1016/j.beem.2012.05.002)
64. Powers JM, Pei Z, Heinzer AK, Deering R, Moser AB, Moser HW, Watkins PA & Smith KD 2005 Adreno-leukodystrophy: oxidative stress of mice and men. Journal of Neuropathology and Experimental Neurology 64 1067-1079. (doi:10.1097/01.jnen.0000190064.28559.a4)
65. Prasad R, Metherell LA, Clark AJ & Storr HL 2013 Deficiency of ALADIN impairs redox homeostasis in human adrenal cells and inhibits steroidogenesis. Endocrinology 154 3209-3218. (doi:10.1210/en.2013-1241)
66. Pujol A, Hindelang C, Callizot N, Bartsch U, Schachner M & Mandel JL 2002 Late onset neurological phenotype of the X-ALD gene inactivation in mice: a mouse model for adrenomyeloneuropathy. Human Molecular Genetics 11 499-505. (doi:10.1093/hmg/11.5.499)
67. Pujol A, Ferrer I, Camps C, Metzger E, Hindelang C, Callizot N, Ruiz M, Pampols T, Giros M & Mandel JL 2004 Functional overlap between ABCD1 (ALD) and ABCD2 (ALDR) transporters: a therapeutic target for X-adrenoleukodystrophy. Human Molecular Genetics 13 2997-3006. (doi:10.1093/hmg/ddh323)
68. Rapoport R, Sklan D & Hanukoglu I 1995 Electron leakage from the adrenal cortex mitochondrial P450scc and P450c11 systems: NADPH and steroid dependence. Archives of Biochemistry and Biophysics 317 412-416. (doi:10.1006/abbi.1995.1182)
69. Ray PD, Huang BW & Tsuji Y 2012 Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cellular Signalling 24 981-990. (doi:10.1016/j.cellsig.2012.01.008)
70. Reshmi-Skarja S, Huebner A, Handschug K, Finegold DN, Clark AJ & Gollin SM 2003 Chromosomal fragility in patients with triple A syndrome. American Journal of Medical Genetics. Part A 117A 30-36. (doi:10.1002/ajmg.a.10846)
71. van Roermund CW, Visser WF, Ijlst L, van Cruchten A, Boek M, Kulik W, Waterham HR & Wanders RJ 2008 The human peroxisomal ABC half transporter ALDP functions as a homodimer and accepts acyl-CoA esters. FASEB Journal 22 4201-4208. (doi:10.1096/fj.08-110866)
72. Rossmeisl M, Rim JS, Koza RA & Kozak LP 2003 Variation in type 2 diabetes - related traits in mouse strains susceptible to diet-induced obesity. Diabetes 52 1958-1966. (doi:10.2337/diabetes.52.8.1958)
73. Sena LA & Chandel NS 2012 Physiological roles of mitochondrial reactive oxygen species. Molecular Cell 48 158-167. (doi:10.1016/j.molcel.2012. 09.025)
74. Shi Z, Feng Y, Wang J, Zhang H, Ding L & Dai J 2010 Perfluorododecanoic acid-induced steroidogenic inhibition is associated with steroidogenic acute regulatory protein and reactive oxygen species in cAMP-stimulated Leydig cells. Toxicological Sciences 114 285-294. (doi:10.1093/toxsci/kfq014)
75. Storr HL, Clark AJ, Priestley JV &Michael GJ 2005 Identification of the sites of expression of triple A syndrome mRNA in the rat using in situ hybridisation. Neuroscience 131 113-123. (doi:10.1016/j.neuroscience. 2004.10.029)
76. Storr HL, Kind B, Parfitt DA, Chapple JP, Lorenz M, Koehler K, Huebner A & Clark AJ 2009 Deficiency of ferritin heavy-chain nuclear import in triple a syndrome implies nuclear oxidative damage as the primary disease mechanism. Molecular Endocrinology 23 2086-2094. (doi:10.1210/me. 2009-0056)
77. Svirbely JL & Szent-Gyorgyi A 1932 The chemical nature of vitamin C. Biochemical Journal 26 865-870.
78. Toye AA, Lippiat JD, Proks P, Shimomura K, Bentley L, Hugill A, Mijat V, Goldsworthy M, Moir L, Haynes A et al. 2005 A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice. Diabetologia 48 675-686. (doi:10.1007/s00125-005-1680-z)
79. Troffer-Charlier N, Doerflinger N, Metzger E, Fouquet F, Mandel JL & Aubourg P 1998 Mirror expression of adrenoleukodystrophy and adrenoleukodystrophy related genes in mouse tissues and human cell lines. European Journal of Cell Biology 75 254-264. (doi:10.1016/S0171-9335(98)80121-0)
80. Vallet AE, Verschueren A, Petiot P, Vandenberghe N, Nicolino M, Roman S, Pouget J & Vial C 2012 Neurological features in adult triple-A (Allgrove) syndrome. Journal of Neurology 259 39-46. (doi:10.1007/s00415-011-6115-9)
81. Watabe S, Makino Y, Ogawa K, Hiroi T, Yamamoto Y & Takahashi SY 1999 Mitochondrial thioredoxin reductase in bovine adrenal cortex its purification, properties, nucleotide/amino acid sequences, and identification of selenocysteine. European Journal of Biochemistry 264 74-84. (doi:10.1046/j.1432-1327.1999.00578.x)
82. Wichers-Rother M, Grigull A, Sokolowski P, Stoffel-Wagner B & Kohler W 2005 Adrenal steroids in adrenomyeloneuropath. Dehydroepiandrosterone sulfate, androstenedione and 17a-hydroxyprogesterone. Journal of Neurology 252 1525-1529. (doi:10.1007/s00415-005-0908-7)
83. Wong N, Blair AR, Morahan G & Andrikopoulos S 2010 The deletion variant of nicotinamide nucleotide transhydrogenase (Nnt) does not affect insulin secretion or glucose tolerance. Endocrinology 151 96-102. (doi:10.1210/en.2009-0887)
84. Woo HA, Chae HZ, Hwang SC, Yang KS, Kang SW, Kim K & Rhee SG 2003 Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300 653-656. (doi:10.1126/science.1080273)
85. Zhang H, Go YM & Jones DP 2007 Mitochondrial thioredoxin-2/peroxiredoxin-3 system functions in parallel with mitochondrial GSH system in protection against oxidative stress. Archives of Biochemistry and Biophysics 465 119-126. (doi:10.1016/j.abb.2007.05.001)
86. Zhao Y, Ao H, Chen L, Sottas CM, Ge RS, Li L & Zhang Y 2012 Mono- (2-ethylhexyl) phthalate affects the steroidogenesis in rat Leydig cells through provoking ROS perturbation. Toxicology In Vitro 26 950-955. (doi:10.1016/j.tiv.2012.04.003)
87. Ziegler GA, Vonrhein C, Hanukoglu I & Schulz GE 1999 The structure of adrenodoxin reductase of mitochondrial P450 systems: electron transfer for steroid biosynthesis. Journal of Molecular Biology 289 981-990. (doi:10.1006/jmbi.1999.2807)