Apolipoprotein-D expression is increased during development and maturation of the human prefrontal cortex

Journal of Neurochemistry

Volumn 109, Issue 4, 2009, Pages 1053-1066

  Kim, Woojin S ^a,b   Wong, Jenny ^a,b   Weickert, Cynthia Shannon ^a,b   Webster, Maree J ^c   Bahn, Sabine ^d   Garner, Brett ^a,b  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c Stanley Medical Research Institute   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apolipoprotein D; Brain development; Lipid transport; Oxidative stress

Indexed keywords

4 HYDROXYNONENAL; APOLIPOPROTEIN D; APOLIPOPROTEIN E; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 3; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 8; MESSENGER RNA; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ADULTHOOD; AGED; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN DEVELOPMENT; BRAIN MATURATION; CHILD; CORRELATION ANALYSIS; FEMALE; GENE; GROUPS BY AGE; HUMAN; HUMAN EXPERIMENT; INFANT; LIPID PEROXIDATION; MALE; MICROARRAY ANALYSIS; NEWBORN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; QUANTITATIVE ANALYSIS; WESTERN BLOTTING;

ADOLESCENT; ADULT; AGING; ALDEHYDES; ANTIOXIDANTS; APOLIPOPROTEINS D; APOLIPOPROTEINS E; BLOTTING, WESTERN; CHILD; CHILD, PRESCHOOL; CYSTEINE PROTEINASE INHIBITORS; GENE EXPRESSION; GLUTATHIONE PEROXIDASE; HUMANS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREFRONTAL CORTEX; RECEPTORS, LIPOPROTEIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPEROXIDE DISMUTASE; YOUNG ADULT;

EID: 65649125678     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06031.x     Document Type: Article

References (95)

1. Andersson M., Aberg F., Teclebrhan H., Edlund C. Appelkvist E. L. (1995) Age-dependent modifications in the metabolism of mevalonate pathway lipids in rat brain. Mech. Ageing Dev. 85, 1 14. (Pubitemid 26021798)
2. Assadi A. H., Zhang G., Beffert U. et al. (2003) Interaction of reelin signaling and Lis1 in brain development. Nat. Genet. 35, 270 276. (Pubitemid 37363182)
3. Babin P. J., Thisse C., Durliat M., Andre M., Akimenko M. A. Thisse B. (1997) Both apolipoprotein E and A-I genes are present in a nonmammalian vertebrate and are highly expressed during embryonic development. Proc. Natl Acad. Sci. USA 94, 8622 8627. (Pubitemid 27335089)
4. Beffert U., Stolt P. C. Herz J. (2004) Functions of lipoprotein receptors in neurons. J. Lipid Res. 45, 403 409. (Pubitemid 38337986)
5. Beffert U., Durudas A., Weeber E. J., Stolt P. C., Giehl K. M., Sweatt J. D., Hammer R. E. Herz J. (2006) Functional dissection of Reelin signaling by site-directed disruption of Disabled-1 adaptor binding to apolipoprotein E receptor 2: distinct roles in development and synaptic plasticity. J. Neurosci. 26, 2041 2052. (Pubitemid 43295856)
6. Benavides S. H., Monserrat A. J., Farina S. Porta E. A. (2002) Sequential histochemical studies of neuronal lipofuscin in human cerebral cortex from the first to the ninth decade of life. Arch. Gerontol. Geriatr. 34, 219 231. (Pubitemid 34224163)
7. Boschert U., Merlo-Pich E., Higgins G., Roses A. D. Catsicas S. (1999) Apolipoprotein E expression by neurons surviving excitotoxic stress. Neurobiol. Dis. 6, 508 514. (Pubitemid 30036620)
8. Boyles J. K., Zoellner C. D., Anderson L. J. et al. (1989) A role for apolipoprotein E, apolipoprotein A-I, and low density lipoprotein receptors in cholesterol transport during regeneration and remyelination of the rat sciatic nerve. J. Clin. Invest. 83, 1015 1031. (Pubitemid 19080637)
9. Boyles J. K., Notterpek L. M. Anderson L. J. (1990a) Accumulation of apolipoproteins in the regenerating and remyelinating mammalian peripheral nerve. Identification of apolipoprotein D, apolipoprotein A-IV, apolipoprotein E, and apolipoprotein A-I. J. Biol. Chem. 265, 17805 17815. (Pubitemid 20355936)
10. Boyles J. K., Notterpek L. M., Wardell M. R. Rall Jr. S. C. (1990b) Identification, characterization, and tissue distribution of apolipoprotein D in the rat. J. Lipid Res. 31, 2243 2256.
11. Cabreiro F., Picot C. R., Friguet B. Petropoulos I. (2006) Methionine sulfoxide reductases: relevance to aging and protection against oxidative stress. Ann. N Y Acad. Sci. 1067, 37 44. (Pubitemid 43806307)
12. Calabrese V., Scapagnini G., Ravagna A., Colombrita C., Spadaro F., Butterfield D. A. Giuffrida Stella A. M. (2004) Increased expression of heat shock proteins in rat brain during aging: relationship with mitochondrial function and glutathione redox state. Mech. Ageing Dev. 125, 325 335. (Pubitemid 38438512)
13. Charron J. B., Ouellet F., Houde M. Sarhan F. (2008) The plant Apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biol. 8, 86.
14. Cini M. Moretti A. (1995) Studies on lipid peroxidation and protein oxidation in the aging brain. Neurobiol. Aging 16, 53 57.
15. Cristiano F., de Haan J. B., Iannello R. C. Kola I. (1995) Changes in the levels of enzymes which modulate the antioxidant balance occur during aging and correlate with cellular damage. Mech. Ageing Dev. 80, 93 105.
16. D'Arcangelo G., Homayouni R., Keshvara L., Rice D. S., Sheldon M. Curran T. (1999) Reelin is a ligand for lipoprotein receptors. Neuron 24, 471 479. (Pubitemid 29508420)
17. Dietschy J. M. Turley S. D. (2004) Thematic review series: brain Lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J. Lipid Res. 45, 1375 1397.
18. Dilley W. G., Haagensen D. E., Cox C. E. Wells Jr. S. A. (1990) Immunologic and steroid binding properties of the GCDFP-24 protein isolated from human breast gross cystic disease fluid. Breast Cancer Res. Treat. 16, 253 260.
19. Do Carmo S., Seguin D., Milne R. Rassart E. (2002) Modulation of apolipoprotein D and apolipoprotein E mRNA expression by growth arrest and identification of key elements in the promoter. J. Biol. Chem. 277, 5514 5523.
20. Do Carmo S., Levros Jr. L. C. Rassart E. (2007) Modulation of apolipoprotein D expression and translocation under specific stress conditions. Biochim. Biophys. Acta 1773, 954 969. (Pubitemid 46839140)
21. Do Carmo S., Jacomy H., Talbot P. J. Rassart E. (2008) Neuroprotective effect of apolipoprotein D against human coronavirus OC43-induced encephalitis in mice. J. Neurosci. 28, 10330 10338.
22. Double K. L., Dedov V. N., Fedorow H., Kettle E., Halliday G. M., Garner B. Brunk U. T. (2008) The comparative biology of neuromelanin and lipofuscin in the human brain. Cell. Mol. Life Sci. 65, 1669 1682.
23. Droge W. Schipper H. M. (2007) Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell 6, 361 370. (Pubitemid 46785141)
24. Eichinger A., Nasreen A., Kim H. J. Skerra A. (2007) Structural insight into the dual ligand specificity and mode of high density lipoprotein association of apolipoprotein D. J. Biol. Chem. 282, 31068 31075. (Pubitemid 350035183)
25. Ganfornina M. D., Do Carmo S., Lora J. M., Torres-Schumann S., Vogel M., Allhorn M., Gonzalez C., Bastiani M. J., Rassart E. Sanchez D. (2008) Apolipoprotein D is involved in the mechanisms regulating protection from oxidative stress. Aging Cell 7, 506 515.
26. Garner B., Waldeck A. R., Witting P. K., Rye K. A. Stocker R. (1998a) Oxidation of high density lipoproteins II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. J. Biol. Chem. 273, 6088 6095. (Pubitemid 28144688)
27. Garner B., Witting P. K., Waldeck A. R., Christison J. K., Raftery M. Stocker R. (1998b) Oxidation of high density lipoproteins I. Formation of methionine sulfoxide in apolipoproteins AI and AII is an early event that accompanies lipid peroxidation and can be enhanced by alpha-tocopherol. J. Biol. Chem. 273, 6080 6087. (Pubitemid 28144687)
28. Gupta A., Hasan M., Chander R. Kapoor N. K. (1991) Age-related elevation of lipid peroxidation products: diminution of superoxide dismutase activity in the central nervous system of rats. Gerontology 37, 305 309.
29. Haynes R. L., Folkerth R. D., Szweda L. I., Volpe J. J. Kinney H. C. (2006) Lipid peroxidation during human cerebral myelination. J. Neuropathol. Exp. Neurol. 65, 894 904. (Pubitemid 44371235)
30. Herz J. Bock H. H. (2002) Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71, 405 434.
31. Herz J. Chen Y. (2006) Reelin, lipoprotein receptors and synaptic plasticity. Nat. Rev. Neurosci. 7, 850 859. (Pubitemid 44624177)
32. Ignatius M. J., Gebicke-Harter P. J., Skene J. H., Schilling J. W., Weisgraber K. H., Mahley R. W. Shooter E. M. (1986) Expression of apolipoprotein E during nerve degeneration and regeneration. Proc. Natl Acad. Sci. USA 83, 1125 1129. (Pubitemid 16086425)
33. Kalaria R. N. Andorn A. C. (1991) Adrenergic receptors in aging and Alzheimer's disease: decreased alpha 2-receptors demonstrated by [3H]p-aminoclonidine binding in prefrontal cortex. Neurobiol. Aging 12, 131 136.
34. Kalman J., McConathy W., Araoz C., Kasa P. Lacko A. G. (2000) Apolipoprotein D in the aging brain and in Alzheimer's dementia. Neurol. Res. 22, 330 336. (Pubitemid 30409586)
35. Kozlovsky N., Shanon-Weickert C., Tomaskovic-Crook E., Kleinman J. E., Belmaker R. H. Agam G. (2004) Reduced GSK-3beta mRNA levels in postmortem dorsolateral prefrontal cortex of schizophrenic patients. J. Neural Transm. 111, 1583 1592. (Pubitemid 40064475)
36. LaDu M. J., Gilligan S. M., Lukens J. R., Cabana V. G., Reardon C. A., Van Eldik L. J. Holtzman D. M. (1998) Nascent astrocyte particles differ from lipoproteins in CSF. J. Neurochem. 70, 2070 2081. (Pubitemid 28207831)
37. Ladu M. J., Reardon C., Van Eldik L., Fagan A. M., Bu G., Holtzman D. Getz G. S. (2000) Lipoproteins in the central nervous system. Ann. N Y Acad. Sci. 903, 167 175. (Pubitemid 30251555)
38. Lea O. A. (1988) Binding properties of progesterone-binding Cyst protein, PBCP. Steroids 52, 337 338.
39. Lesne S., Koh M. T., Kotilinek L., Kayed R., Glabe C. G., Yang A., Gallagher M. Ashe K. H. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352 357.
40. Lewandowski N. M. Small S. A. (2005) Brain microarray: finding needles in molecular haystacks. J. Neurosci. 25, 10341 10346. (Pubitemid 41628434)
41. Lewis D. A. Gonzalez-Burgos G. (2006) Pathophysiologically based treatment interventions in schizophrenia. Nat. Med. 12, 1016 1022. (Pubitemid 44353381)
42. Li Y., Lu W., Marzolo M. P. Bu G. (2001) Differential functions of members of the low density lipoprotein receptor family suggested by their distinct endocytosis rates. J. Biol. Chem. 276, 18000 18006. (Pubitemid 37411362)
43. Lipska B. K., Deep-Soboslay A., Weickert C. S., Hyde T. M., Martin C. E., Herman M. M. Kleinman J. E. (2006) Critical factors in gene expression in postmortem human brain: focus on studies in schizophrenia. Biol. Psychiatry 60, 650 658. (Pubitemid 44402385)
44. Loerch P. M., Lu T., Dakin K. A. et al. (2008) Evolution of the aging brain transcriptome and synaptic regulation. PLoS ONE 3, e3329.
45. Lu T., Pan Y., Kao S. Y., Li C., Kohane I., Chan J. Yankner B. A. (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429, 883 891. (Pubitemid 38843301)
46. Lynch J. R., Tang W., Wang H., Vitek M. P., Bennett E. R., Sullivan P. M., Warner D. S. Laskowitz D. T. (2003) APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response. J. Biol. Chem. 278, 48529 48533. (Pubitemid 41079490)
47. McCarthy M. M. (2008) Estradiol and the developing brain. Physiol. Rev. 88, 91 124.
48. Mexal S., Berger R., Adams C. E., Ross R. G., Freedman R. Leonard S. (2006) Brain pH has a significant impact on human postmortem hippocampal gene expression profiles. Brain Res. 1106, 1 11. (Pubitemid 44163309)
49. Mimmack M. L., Ryan M., Baba H. et al. (2002) Gene expression analysis in schizophrenia: reproducible up-regulation of several members of the apolipoprotein L family located in a high-susceptibility locus for schizophrenia on chromosome 22. Proc. Natl Acad. Sci. USA 99, 4680 4685. (Pubitemid 34286044)
50. Miyata M. Smith J. D. (1996) Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and beta-amyloid peptides. Nat. Genet. 14, 55 61. (Pubitemid 26301547)
51. Morais Cabral J. H., Atkins G. L., Sanchez L. M., Lopez-Boado Y. S., Lopez-Otin C. Sawyer L. (1995) Arachidonic acid binds to apolipoprotein D: implications for the protein's function. FEBS Lett. 366, 53 56.
52. Moskovitz J. (2005) Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochim. Biophys. Acta 1703, 213 219. (Pubitemid 40170444)
53. Mouchel Y., Lefrancois T., Fages C. Tardy M. (1995) Apolipoprotein E gene expression in astrocytes: developmental pattern and regulation. Neuroreport 7, 205 208. (Pubitemid 26077227)
54. Muffat J., Walker D. W. Benzer S. (2008) Human ApoD, an apolipoprotein up-regulated in neurodegenerative diseases, extends lifespan and increases stress resistance in Drosophila. Proc. Natl Acad. Sci. USA 105, 7088 7093.
55. Murray C. A. Lynch M. A. (1998) Evidence that increased hippocampal expression of the cytokine interleukin-1 beta is a common trigger for age- and stress-induced impairments in long-term potentiation. J. Neurosci. 18, 2974 2981. (Pubitemid 28163227)
56. Navarro A., Tolivia J., Astudillo A. del Valle E. (1998) Pattern of apolipoprotein D immunoreactivity in human brain. Neurosci. Lett. 254, 17 20. (Pubitemid 28430614)
57. O'Donnell E. Lynch M. A. (1998) Dietary antioxidant supplementation reverses age-related neuronal changes. Neurobiol. Aging 19, 461 467. (Pubitemid 29065495)
58. Ong W. Y., He Y., Suresh S. Patel S. C. (1997) Differential expression of apolipoprotein D and apolipoprotein E in the kainic acid-lesioned rat hippocampus. Neuroscience 79, 359 367. (Pubitemid 27232395)
59. Ong W. Y., Lau C. P., Leong S. K., Kumar U., Suresh S. Patel S. C. (1999) Apolipoprotein D gene expression in the rat brain and light and electron microscopic immunocytochemistry of apolipoprotein D expression in the cerebellum of neonatal, immature and adult rats. Neuroscience 90, 913 922. (Pubitemid 29156756)
60. Ordonez C., Navarro A., Perez C., Astudillo A., Martinez E. Tolivia J. (2006) Apolipoprotein D expression in substantia nigra of Parkinson disease. Histol. Histopathol. 21, 361 366.
61. Patel S. C., Asotra K., Patel Y. C., McConathy W. J., Patel R. C. Suresh S. (1995) Astrocytes synthesize and secrete the lipophilic ligand carrier apolipoprotein D. Neuroreport 6, 653 657.
62. Patel R. C., Lange D., McConathy W. J., Patel Y. C. Patel S. C. (1997) Probing the structure of the ligand binding cavity of lipocalins by fluorescence spectroscopy. Protein Eng. 10, 621 625. (Pubitemid 27332068)
63. Pearlman W. H., Gueriguian J. L. Sawyer M. E. (1973) A specific progesterone-binding component of human breast cyst fluid. J. Biol. Chem. 248, 5736 5741.
64. Peitsch M. C. Boguski M. S. (1990) Is apolipoprotein D a mammalian bilin-binding protein? New Biol. 2, 197 206. (Pubitemid 20210040)
65. Perez-Garcia C. G., Tissir F., Goffinet A. M. Meyer G. (2004) Reelin receptors in developing laminated brain structures of mouse and human. Eur. J. Neurosci. 20, 2827 2832. (Pubitemid 39573799)
66. Pitas R. E., Boyles J. K., Lee S. H., Hui D. Weisgraber K. H. (1987) Lipoproteins and their receptors in the central nervous system. Characterization of the lipoproteins in cerebrospinal fluid and identification of apolipoprotein B,E(LDL) receptors in the brain. J. Biol. Chem. 262, 14352 14360. (Pubitemid 17152101)
67. Porta E. A. (2002) Pigments in aging: an overview. Ann. N Y Acad. Sci. 959, 57 65. (Pubitemid 34457552)
68. Provost P. R., Villeneuve L., Weech P. K., Milne R. W., Marcel Y. L. Rassart E. (1991) Localization of the major sites of rabbit apolipoprotein D gene transcription by in situ hybridization. J. Lipid Res. 32, 1959 1970.
69. Quan G., Xie C., Dietschy J. M. Turley S. D. (2003) Ontogenesis and regulation of cholesterol metabolism in the central nervous system of the mouse. Brain Res. Dev. Brain Res. 146, 87 98. (Pubitemid 37474113)
70. Quinn C. M., Kagedal K., Terman A., Stroikin U., Brunk U. T., Jessup W. Garner B. (2004) Induction of fibroblast apolipoprotein E expression during apoptosis, starvation-induced growth arrest and mitosis. Biochem. J. 378, 753 761. (Pubitemid 38406850)
71. Rassart E., Bedirian A., Do Carmo S., Guinard O., Sirois J., Terrisse L. Milne R. (2000) Apolipoprotein D. Biochim. Biophys. Acta 1482, 185 198.
72. Rickhag M., Deierborg T., Patel S., Ruscher K. Wieloch T. (2008) Apolipoprotein D is elevated in oligodendrocytes in the peri-infarct region after experimental stroke: influence of enriched environment. J. Cereb. Blood Flow Metab. 28, 551 562.
73. Salimi K., Glantz L. A., Hamer R. M., German T. T., Gilmore J. H. Jarskog L. F. (2008) Regulation of complexin 1 and complexin 2 in the developing human prefrontal cortex. Synapse 62, 273 282.
74. Sanchez D., Lopez-Arias B., Torroja L., Canal I., Wang X., Bastiani M. J. Ganfornina M. D. (2006) Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Curr. Biol. 16, 680 686.
75. Savaskan N. E., Borchert A., Brauer A. U. Kuhn H. (2007a) Role for glutathione peroxidase-4 in brain development and neuronal apoptosis: specific induction of enzyme expression in reactive astrocytes following brain injury. Free Radic. Biol. Med. 43, 191 201. (Pubitemid 46977163)
76. Savaskan N. E., Ufer C., Kuhn H. Borchert A. (2007b) Molecular biology of glutathione peroxidase 4: from genomic structure to developmental expression and neural function. Biol. Chem. 388, 1007 1017. (Pubitemid 47584303)
77. Snipes G. J., McGuire C. B., Norden J. J. Freeman J. A. (1986) Nerve injury stimulates the secretion of apolipoprotein E by nonneuronal cells. Proc. Natl Acad. Sci. USA 83, 1130 1134. (Pubitemid 16086426)
78. Sohal R. S. Brunk U. T. (1989) Lipofuscin as an indicator of oxidative stress and aging. Adv. Exp. Med. Biol. 266, 17 26.
79. Spreyer P., Schaal H., Kuhn G., Rothe T., Unterbeck A., Olek K. Muller H. W. (1990) Regeneration-associated high level expression of apolipoprotein D mRNA in endoneurial fibroblasts of peripheral nerve. EMBO J. 9, 2479 2484. (Pubitemid 20218345)
80. Stadtman E. R., Van Remmen H., Richardson A., Wehr N. B. Levine R. L. (2005) Methionine oxidation and aging. Biochim. Biophys. Acta 1703, 135 140. (Pubitemid 40170436)
81. Terrisse L., Poirier J., Bertrand P., Merched A., Visvikis S., Siest G., Milne R. Rassart E. (1998) Increased levels of apolipoprotein D in cerebrospinal fluid and hippocampus of Alzheimer's patients. J. Neurochem. 71, 1643 1650. (Pubitemid 28443037)
82. Terrisse L., Seguin D., Bertrand P., Poirier J., Milne R. Rassart E. (1999) Modulation of apolipoprotein D and apolipoprotein E expression in rat hippocampus after entorhinal cortex lesion. Brain Res. Mol. Brain Res. 70, 26 35. (Pubitemid 29278604)
83. Thomas E. A., Dean B., Pavey G. Sutcliffe J. G. (2001) Increased CNS levels of apolipoprotein D in schizophrenic and bipolar subjects: implications for the pathophysiology of psychiatric disorders. Proc. Natl Acad. Sci. USA 98, 4066 4071. (Pubitemid 32249899)
84. Thomas E. A., Laws S. M., Sutcliffe J. G., Harper C., Dean B., McClean C., Masters C., Lautenschlager N., Gandy S. E. Martins R. N. (2003) Apolipoprotein D levels are elevated in prefrontal cortex of subjects with Alzheimer's disease: no relation to apolipoprotein E expression or genotype. Biol. Psychiatry 54, 136 141. (Pubitemid 36859773)
85. Uauy R., Mena P. Rojas C. (2000) Essential fatty acids in early life: structural and functional role. Proc. Nutr. Soc. 59, 3 15. (Pubitemid 30316601)
86. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A. Speleman F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034.
87. Walker D. W., Muffat J., Rundel C. Benzer S. (2006) Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Curr. Biol. 16, 674 679.
88. Webster M. J., Weickert C. S., Herman M. M. Kleinman J. E. (2002) BDNF mRNA expression during postnatal development, maturation and aging of the human prefrontal cortex. Brain Res. Dev. Brain Res. 139, 139 150. (Pubitemid 35453900)
89. Weickert C. S., Webster M. J., Gondipalli P., Rothmond D., Fatula R. J., Herman M. M., Kleinman J. E. Akil M. (2007) Postnatal alterations in dopaminergic markers in the human prefrontal cortex. Neuroscience 144, 1109 1119. (Pubitemid 46019839)
90. Weickert C. S., Elashoff M., Richards A. B., Sinclair D., Bahn S., Paabo S., Khaitchovitch P. Webster M. J. (2009) Transcriptome analysis of male-female differences in prefrontal cortical development. Mol. Psychiatry (In press).
91. Whitney K. D., Watson M. A., Collins J. L., Benson W. G., Stone T. M., Numerick M. J., Tippin T. K., Wilson J. G., Winegar D. A. Kliewer S. A. (2002) Regulation of cholesterol homeostasis by the liver X receptors in the central nervous system. Mol. Endocrinol. 16, 1378 1385. (Pubitemid 34621083)
92. Yang C. Y., Gu Z. W., Blanco-Vaca F., Gaskell S. J., Yang M., Massey J. B., Gotto Jr. A. M. Pownall H. J. (1994) Structure of human apolipoprotein D: locations of the intermolecular and intramolecular disulfide links. Biochemistry 33, 12451 12455. (Pubitemid 24340450)
93. Yankner B. A., Lu T. Loerch P. (2008) The aging brain. Annu. Rev. Pathol. 3, 41 66.
94. Yoritaka A., Hattori N., Uchida K., Tanaka M., Stadtman E. R. Mizuno Y. (1996) Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl Acad. Sci. USA 93, 2696 2701. (Pubitemid 26114311)
95. Zhu Y., Carvey P. M. Ling Z. (2006) Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res. 1090, 35 44. (Pubitemid 43817938)