Prenatal ethanol exposure up-regulates the cholesterol transporters ATP-binding cassette A1 and G1 and reduces cholesterol levels in the developing rat brain

Alcohol and Alcoholism

Volumn 49, Issue 6, 2014, Pages 626-634

  Zhou, Chunyan ^a   Chen, Jing ^a   Zhang, Xiaolu ^b,c   Costa, Lucio G ^a,d   Guizzetti, Marina ^a,b,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c JESSE BROWN VA MEDICAL CENTER   (United States)

^d UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; ALCOHOL; CHOLESTEROL; PHOSPHOLIPID; ABC TRANSPORTER; ABCA1 PROTEIN, RAT; ABCG1 PROTEIN, RAT;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DAMAGE; BRAIN DEVELOPMENT; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FETAL ALCOHOL SYNDROME; FETUS; IN VITRO STUDY; IN VIVO STUDY; MALE; MENTAL DEFICIENCY; MICROCEPHALY; NEOCORTEX; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION; WEIGHT REDUCTION; ANIMAL; BRAIN; BRAIN CHEMISTRY; DRUG EFFECTS; EMBRYOLOGY; METABOLISM; PREGNANCY; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

RATTUS;

ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 1; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; BRAIN; BRAIN CHEMISTRY; CHOLESTEROL; ETHANOL; FEMALE; MALE; PHOSPHOLIPIDS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84937406825     PISSN: 07350414     EISSN: 14643502     Source Type: Journal    
DOI: 10.1093/alcalc/agu049     Document Type: Article

References (68)

1. Astley SJ, Clarren SK. (2000) Diagnosing the full spectrum of fetal alcohol-exposed individuals: introducing the 4-digit diagnostic code. Alcohol Alcohol 35:400-10.
2. Barcelo-Coblijn G, Wold LE, Ren J et al. (2013) Prenatal ethanol exposure increases brain cholesterol content in adult rats. Lipids 48: 1059-68.
3. Bochelen D, Langley K, Adamczyk M et al. (2000) 7betahydroxysterol is cytotoxic to neonatal rat astrocytes in primary culture when cAMP levels are increased. J Neurosci Res 62:99-111.
4. Boyles JK, Zoellner CD, Anderson LJ 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 83:1015-31.
5. Burdge GC, Postle AD. (1995) Phospholipid molecular species composition of developing fetal guinea pig brain. Lipids 30:719-24.
6. Chen J, Costa LG, Guizzetti M. (2011) Retinoic Acid isomers up-regulate ATP binding cassette A1 and g1 and cholesterol efflux in rat astrocytes: implications for their therapeutic and teratogenic effects. J Pharmacol Exp Ther 338:870-8.
7. Chen J, Zhang X, Kusumo H et al. (2013) Cholesterol efflux is differentially regulated in neurons and astrocytes: implications for brain cholesterol homeostasis. Biochim Biophys Acta 1831:263-75.
8. Clarren SK, Alvord EC, Jr, Sumi SM et al. (1978) Brain malformations related to prenatal exposure to ethanol. J Pediatr 92:64-7
9. Cohen MM, Jr, Shiota K. (2002) Teratogenesis of holoprosencephaly. Am J Med Genet 109:1-15.
10. Cooper MK, Wassif CA, Krakowiak PA et al. (2003) A defective response to Hedgehog signaling in disorders of cholesterol biosynthesis. Nat Genet 33:508-13.
11. Dehart DB, Lanoue L, Tint GS et al. (1997) Pathogenesis of malformations in a rodent model for Smith-Lemli-Opitz syndrome. Am J Med Genet 68:328-37.
12. Dietschy JM, Turley SD. (2001) Cholesterol metabolism in the brain. Curr Opin Lipidol 12:105-12.
13. Dietschy JM, Turley SD. (2004) Thematic review series: brain Lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 45:1375-97
14. Dobbing J, Sands J. (1973) Quantitative growth and development of human brain. Arch Dis Child 48:757-67
15. Duffy O, Menez JF, Floch HH et al. (1991) Changes in whole brain membranes of rats following pre- and post-natal exposure to ethanol. Alcohol Alcohol 26:605-13.
16. Famy C, Streissguth AP, Unis AS. (1998) Mental illness in adults with fetal alcohol syndrome or fetal alcohol effects. Am J Psychiatry 155:552-4.
17. Fan QW, Yu W, Gong JS et al. (2002) Cholesterol-dependent modulation of dendrite outgrowth and microtubule stability in cultured neurons. J Neurochem 80:178-90.
18. Glavas MM, Yu WK, Weinberg J. (2006) Effects of mineralocorticoid and glucocorticoid receptor blockade on hypothalamicpituitary-adrenal function in female rats prenatally exposed to ethanol. Alcohol Clin Exp Res 30:1916-24.
19. Glavas MM, Ellis L, Yu WK et al. (2007) Effects of prenatal ethanol exposure on basal limbic-hypothalamic-pituitary-adrenal regulation: role of corticosterone. Alcohol Clin Exp Res 31:1598-610.
20. Guizzetti M, Costa LG. (2005) Disruption of cholesterol homeostasis in the developing brain as a potential mechanism contributing to the developmental neurotoxicity of ethanol: an hypothesis. Med Hypotheses 64:563-7.
21. Guizzetti M, Costa LG. (2007) Cholesterol homeostasis in the developing brain: a possible new target for ethanol. Hum Exp Toxicol 26:355-60.
22. Guizzetti M, Chen J, Oram JF et al. (2007) Ethanol induces cholesterol efflux and up-regulates ATP-binding cassette cholesterol transporters in fetal astrocytes. J Biol Chem 282:18740-9.
23. Guizzetti M, Chen J, Costa LG. (2011) Disruption of cholesterol homeostasis in developmental neurotoxicity. In Gupta RC (ed). Reproductive and Developmental Toxicology. London: Academic Press, 855-62.
24. Hayashi H, Campenot RB, Vance DE et al. (2004) Glial lipoproteins stimulate axon growth of central nervous system neurons in compartmented cultures. J Biol Chem 279:14009-15.
25. Hayashi H, Campenot RB, Vance DE et al. (2009) Protection of neurons from apoptosis by apolipoprotein E-containing lipoproteins does not require lipoprotein uptake and involves activation of phospholipase Cgamma1 and inhibition of calcineurin. J Biol Chem 284:29605-13.
26. Hellemans KG, Verma P, Yoon E et al. (2010) Prenatal alcohol exposure and chronic mild stress differentially alter depressive- and anxiety-like behaviors in male and female offspring. Alcohol Clin Exp Res 34:633-45.
27. Herz J. (2001) The LDL receptor gene family: (un)expected signal transducers in the brain. Neuron 29:571-81.
28. Hirsch-Reinshagen V, Zhou S, Burgess BL et al. (2004) Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J Biol Chem 279:41197-207.
29. Incardona JP, Roelink H. (2000) The role of cholesterol in Shh signaling and teratogen-induced holoprosencephaly. Cell Mol Life Sci 57:1709-19.
30. Jurevics HA, Kidwai FZ, Morell P. (1997) Sources of cholesterol during development of the rat fetus and fetal organs. J Lipid Res 38:723-33.
31. Kim WS, Suryo Rahmanto A, Kamili A et al. (2007) Role of ABCG1 and ABCA1 in regulation of neuronal cholesterol efflux to apolipoprotein-E discs and suppression of amyloid-beta peptide generation. J Biol Chem282:2851-61.
32. Koldamova RP, Lefterov IM, Ikonomovic MD et al. (2003) 22R-hydroxycholesterol and 9-cis-retinoic acid induce ATP-binding cassette transporter A1 expression and cholesterol efflux in brain cells and decrease amyloid beta secretion. J Biol Chem 278: 13244-56.
33. LaDu MJ, Gilligan SM, Lukens JR et al. (1998) Nascent astrocyte particles differ from lipoproteins in CSF. J Neurochem70:2070-81.
34. Lalitha T, Kumar K, Ramakrishnan CV et al. (1988) Effect of maternal alcohol consumption on the lipid composition of CNS in the offspring. J Neurochem 50:1346-51.
35. Langan TJ, Slater MC. (1991) Quiescent astroglia in long-term primary cultures re-enter the cell cycle and require a non-sterol isoprenoid in late G1. Brain Res 548:9-17.
36. Lanoue L, Dehart DB, Hinsdale ME et al. (1997) Limb, genital, CNS, and facial malformations result from gene/environment-induced cholesterol deficiency: further evidence for a link to sonic hedgehog. Am J Med Genet 73:24-31.
37. Li Z, Vance DE. (2008) Phosphatidylcholine and choline homeostasis. J Lipid Res 49:1187-94.
38. Lund EG, Guileyardo JM, Russell DW. (1999) cDNA cloning of cholesterol 24-hydroxylase, a mediator of cholesterol homeostasis in the brain. Proc Natl Acad Sci USA 96:7238-43.
39. Marti E, Bovolenta P. (2002) Sonic hedgehog in CNS development: one signal, multiple outputs. Trends Neurosci 25:89-96.
40. Matsuo M, Campenot RB, Vance DE et al. (2011) Involvement of low-density lipoprotein receptor-related protein and ABCG1 in stimulation of axonal extension by apoE-containing lipoproteins. Biochim Biophys Acta 1811:31-8.
41. Mauch DH, Nagler K, Schumacher S et al. (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354-7.
42. May PA, Brooke L, Gossage JP et al. (2000) Epidemiology of fetal alcohol syndrome in a South African community in the Western Cape Province. Am J Public Health 90:1905-12.
43. Michikawa M, Yanagisawa K. (1999) Inhibition of cholesterol production but not of nonsterol isoprenoid products induces neuronal cell death. J Neurochem 72:2278-85.
44. Michikawa M, Fan QW, Isobe I et al. (2000) Apolipoprotein E exhibits isoform-specific promotion of lipid efflux from astrocytes and neurons in culture. J Neurochem 74:1008-16.
45. Miller MW. (1986) Effects of alcohol on the generation and migration of cerebral cortical neurons. Science 233:1308-11.
46. Miller MW, Potempa G. (1990) Numbers of neurons and glia in mature rat somatosensory cortex: effects of prenatal exposure to ethanol. J Comp Neurol 293:92-102.
47. Mooney SM, Miller MW. (2007) Nerve growth factor neuroprotection of ethanol-induced neuronal death in rat cerebral cortex is age dependent. Neuroscience 149:372-81.
48. Nowaczyk MJ, Whelan DT, Heshka TW et al. (1999) Smith-Lemli-Opitz syndrome: a treatable inherited error of metabolism causing mental retardation. Can Med Assoc J 161:165-70.
49. Oram JF, Heinecke JW. (2005) ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev 85:1343-72.
50. Pitas RE, Boyles JK, Lee SH et al. (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: 14352-60.
51. Porter JA, Young KE, Beachy PA. (1996) Cholesterol modification of hedgehog signaling proteins in animal development. Science 274:255-9.
52. Quan G, Xie C, Dietschy JM et al. (2003) Ontogenesis and regulation of cholesterol metabolism in the central nervous system of the mouse. Brain Res Dev Brain Res 146:87-98.
53. Raffai RL, Weisgraber KH. (2003) Cholesterol: from heart attacks to Alzheimer's disease. J Lipid Res 44:1423-30.
54. Riley EP, Infante MA, Warren KR. (2011) Fetal alcohol spectrum disorders: an overview. Neuropsychol Rev 21:73-80.
55. Roux C, Wolf C, Mulliez N et al. (2000) Role of cholesterol in embryonic development. Am J Clin Nutr 71:1270-9.
56. Soscia SJ, Tong M, Xu XJ et al. (2006) Chronic gestational exposure to ethanol causes insulin and IGF resistance and impairs acetylcholine homeostasis in the brain. Cell Mol Life Sci 63:2039-56.
57. Streissguth AP, O'Malley K. (2000) Neuropsychiatric implications and long-term consequences of fetal alcohol spectrum disorders. Semin Clin Neuropsychiatry 5:177-90.
58. Streissguth AP, Landesman-Dwyer S, Martin JC et al. (1980) Teratogenic effects of alcohol in humans and laboratory animals. Science 209:353-61.
59. Turley SD, Burns DK, Rosenfeld CR et al. (1996) Brain does not utilize low density lipoprotein-cholesterol during fetal and neonatal development in the sheep. J Lipid Res 37:1953-61.
60. Turley SD, Burns DK, Dietschy JM. (1998) Preferential utilization of newly synthesized cholesterol for brain growth in neonatal lambs. Am J Physiol 274:E1099-105.
61. Uban KA, Comeau WL, Ellis LA et al. (2013) Basal regulation of HPA and dopamine systems is altered differentially in males and females by prenatal alcohol exposure and chronic variable stress. Psychoneuroendocrinology 38:1953-66.
62. Vaughan AM, Oram JF. (2006) ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J Lipid Res 47:2433-43.
63. Verma P, Hellemans KG, Choi FY et al. (2010) Circadian phase and sex effects on depressive/anxiety-like behaviors and HPA axis responses to acute stress. Physiol Behav 99:276-85.
64. Wahrle SE, Jiang H, Parsadanian M et al. (2004) ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE. J Biol Chem 279:40987-93.
65. Wang H, Eckel RH. (2014) What are lipoproteins doing in the brain? Trends Endocrinol Metab 25:8-14.
66. Weinberg J. (1984) Nutritional issues in perinatal alcohol exposure. Neurobehav Toxicol Teratol 6:261-9.
67. Weinberg J, Sliwowska JH, Lan N et al. (2008) Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J Neuroendocrinol 20:470-88.
68. Yu C, Youmans KL, LaDu MJ. (2010) Proposed mechanism for lipoprotein remodelling in the brain. Biochim Biophys Acta 1801:819-23