Prenatal exposure to ethanol stimulates hypothalamic CCR2 chemokine receptor system: Possible relation to increased density of orexigenic peptide neurons and ethanol drinking in adolescent offspring

Neuroscience

Volumn 310, Issue , 2015, Pages 163-175

  Chang, G Q ^a   Karatayev, O ^a   Leibowitz, S F ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

CCL2; CCR2; Lateral hypothalamus; Melanin concentrating hormone; Neurogenesis; Prenatal ethanol

Indexed keywords

CHEMOKINE RECEPTOR CCR2; MELANIN CONCENTRATING HORMONE; MONOCYTE CHEMOTACTIC PROTEIN 1; ALCOHOL; CCL2 PROTEIN, RAT; CCR2 PROTEIN, RAT; CENTRAL DEPRESSANT AGENT; ENOLASE; HYPOPHYSIS HORMONE; HYPOTHALAMUS HORMONE; MELANIN; MELANIN-CONCENTRATING HORMONE;

ADOLESCENT; ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL DENSITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; LATERAL HYPOTHALAMUS; MALE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; AGE; ANIMAL; CHEMICALLY INDUCED; DRINKING BEHAVIOR; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; HYPOTHALAMUS; METABOLISM; NERVE CELL; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY; SPRAGUE DAWLEY RAT;

AGE FACTORS; ALCOHOL DRINKING; ANIMALS; ANIMALS, NEWBORN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CHEMOKINE CCL2; ETHANOL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYPOTHALAMIC HORMONES; HYPOTHALAMUS; INFANT, NEWBORN; MALE; MELANINS; NEURONS; PHOSPHOPYRUVATE HYDRATASE; PITUITARY HORMONES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CCR2;

EID: 84942871169     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.09.020     Document Type: Article

References (88)

1. Abel E.L., York J.L. Absence of effect of prenatal ethanol on adult emotionality and ethanol consumption in rats. J Stud Alcohol 1979, 40:547-553.
2. Alati R., Al Mamun A., Williams G.M., O'Callaghan M., Najman J.M., Bor W. In utero alcohol exposure and prediction of alcohol disorders in early adulthood: a birth cohort study. Arch Gen Psychiatry 2006, 63:1009-1016.
3. Altman J., Bayer S.A. Development of the diencephalon in the rat. II. Correlation of the embryonic development of the hypothalamus with the time of origin of its neurons. J Comp Neurol 1978, 182:973-993.
4. Altman J., Bayer S.A. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 1990, 301:365-381.
5. Baer J.S., Sampson P.D., Barr H.M., Connor P.D., Streissguth A.P. A 21-year longitudinal analysis of the effects of prenatal alcohol exposure on young adult drinking. Arch Gen Psychiatry 2003, 60:377-385.
6. Banisadr G., Queraud-Lesaux F., Boutterin M.C., Pelaprat D., Zalc B., Rostene W., Haour F., Parsadaniantz S.M. Distribution, cellular localization and functional role of CCR2 chemokine receptors in adult rat brain. J Neurochem 2002, 81:257-269.
7. Banisadr G., Gosselin R.D., Mechighel P., Kitabgi P., Rostene W., Parsadaniantz S.M. Highly regionalized neuronal expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) in rat brain: evidence for its colocalization with neurotransmitters and neuropeptides. J Comp Neurol 2005, 489:275-292.
8. Barson J.R., Karatayev O., Chang G.Q., Johnson D.F., Bocarsly M.E., Hoebel B.G., Leibowitz S.F. Positive relationship between dietary fat, ethanol intake, triglycerides, and hypothalamic peptides: counteraction by lipid-lowering drugs. Alcohol 2009, 43:433-441.
9. Barson J.R., Karatayev O., Gaysinskaya V., Chang G.Q., Leibowitz S.F. Effect of dietary fatty acid composition on food intake, triglycerides, and hypothalamic peptides. Regul Pept 2012, 173:13-20.
10. Barson J.R., Morganstern I., Leibowitz S.F. Neurobiology of consummatory behavior: mechanisms underlying overeating and drug use. ILAR J 2012, 53:35-58.
11. Barson J.R., Ho H.T., Leibowitz S.F. Anterior thalamic paraventricular nucleus is involved in intermittent access ethanol drinking: role of orexin receptor 2. Addict Biol 2014.
12. Barson J.R., Ho H.T., Leibowitz S.F. Anterior thalamic paraventricular nucleus is involved in intermittent access ethanol drinking: role of orexin receptor 2. Addict Biol 2015, 20:469-481.
13. Blednov Y.A., Bergeson S.E., Walker D., Ferreira V.M., Kuziel W.A., Harris R.A. Perturbation of chemokine networks by gene deletion alters the reinforcing actions of ethanol. Behav Brain Res 2005, 165:110-125.
14. Boulanger L.M. Immune proteins in brain development and synaptic plasticity. Neuron 2009, 64:93-109.
15. Brischoux F., Fellmann D., Risold P.Y. Ontogenetic development of the diencephalic MCH neurons: a hypothalamic 'MCH area' hypothesis. Eur J Neurosci 2001, 13:1733-1744.
16. Caetano R., Cunradi C. Alcohol dependence: a public health perspective. Addiction 2002, 97:633-645.
17. Carneiro L.M., Diogenes J.P., Vasconcelos S.M., Aragao G.F., Noronha E.C., Gomes P.B., Viana G.S. Behavioral and neurochemical effects on rat offspring after prenatal exposure to ethanol. Neurotoxicol Teratol 2005, 27:585-592.
18. Carta M., Mameli M., Valenzuela C.F. Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J Neurosci 2004, 24:3746-3751.
19. Chang G.Q., Gaysinskaya V., Karatayev O., Leibowitz S.F. Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 2008, 28:12107-12119.
20. Chang G.Q., Karatayev O., Liang S.C., Barson J.R., Leibowitz S.F. Prenatal ethanol exposure stimulates neurogenesis in hypothalamic and limbic peptide systems: possible mechanism for offspring ethanol overconsumption. Neuroscience 2012, 222:417-428.
21. Chang G.Q., Karatayev O., Leibowitz S.F. Prenatal exposure to nicotine stimulates neurogenesis of orexigenic peptide-expressing neurons in hypothalamus and amygdala. J Neurosci 2013, 33:13600-13611.
22. Chintawar S., Cayrol R., Antel J., Pandolfo M., Prat A. Blood-brain barrier promotes differentiation of human fetal neural precursor cells. Stem Cells 2009, 27:838-846.
23. Chometton S., Franchi-Bernard G., Houdayer C., Mariot A., Poncet F., Fellmann D., Risold P.Y. Melanin-concentrating hormone expression in the rat hypothalamus is not affected in an experiment of prenatal alcohol exposure. Brain Res Bull 2014, 107:102-109.
24. Chotro M.G., Arias C. Prenatal exposure to ethanol increases ethanol consumption: a conditioned response?. Alcohol 2003, 30:19-28.
25. Chotro M.G., Arias C., Laviola G. Increased ethanol intake after prenatal ethanol exposure: studies with animals. Neurosci Biobehav Rev 2007, 31:181-191.
26. Cippitelli A., Karlsson C., Shaw J.L., Thorsell A., Gehlert D.R., Heilig M. Suppression of alcohol self-administration and reinstatement of alcohol seeking by melanin-concentrating hormone receptor 1 (MCH1-R) antagonism in Wistar rats. Psychopharmacology 2010, 211:367-375.
27. Crews F.T., Zou J., Qin L. Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 2011, 25(Suppl 1):S4-S12.
28. Cullen C.L., Burne T.H., Lavidis N.A., Moritz K.M. Low dose prenatal ethanol exposure induces anxiety-like behaviour and alters dendritic morphology in the basolateral amygdala of rat offspring. PLoS ONE 2013, 8:e54924.
29. Cullere M.E., Spear N.E., Molina J.C. Prenatal ethanol increases sucrose reinforcement, an effect strengthened by postnatal association of ethanol and sucrose. Alcohol 2014, 48:25-33.
30. Diaz-Cenzano E., Chotro M.G. Prenatal binge ethanol exposure on gestation days 19-20, but not on days 17-18, increases postnatal ethanol acceptance in rats. Behav Neurosci 2010, 124:362-369.
31. DiLeone R.J., Georgescu D., Nestler E.J. Lateral hypothalamic neuropeptides in reward and drug addiction. Life Sci 2003, 73:759-768.
32. Drew P.D., Johnson J.W., Douglas J.C., Phelan K.D., Kane C.J. Pioglitazone blocks ethanol induction of microglial activation and immune responses in the hippocampus, cerebellum, and cerebral cortex in a mouse model of fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2015, 39:445-454.
33. Duncan E.A., Proulx K., Woods S.C. Central administration of melanin-concentrating hormone increases alcohol and sucrose/quinine intake in rats. Alcohol Clin Exp Res 2005, 29:958-964.
34. El-Hage N., Wu G., Ambati J., Bruce-Keller A.J., Knapp P.E., Hauser K.F. CCR2 mediates increases in glial activation caused by exposure to HIV-1 Tat and opiates. J Neuroimmunol 2006, 178:9-16.
35. Fabio M.C., March S.M., Molina J.C., Nizhnikov M.E., Spear N.E., Pautassi R.M. Prenatal ethanol exposure increases ethanol intake and reduces c-Fos expression in infralimbic cortex of adolescent rats. Pharmacol Biochem Behav 2013, 103:842-852.
36. Fabio M.C., Nizhnikov M.E., Spear N.E., Pautassi R.M. Binge ethanol intoxication heightens subsequent ethanol intake in adolescent, but not adult, rats. Dev Psychobiol 2013.
37. Fabio M.C., Macchione A.F., Nizhnikov M.E., Pautassi R.M. Prenatal ethanol increases ethanol intake throughout adolescence, alters ethanol-mediated aversive learning, and affects mu but not delta or kappa opioid receptor mRNA expression. Eur J Neurosci 2015, 41:1569-1579.
38. Foresti M.L., Arisi G.M., Katki K., Montanez A., Sanchez R.M., Shapiro L.A. Chemokine CCL2 and its receptor CCR2 are increased in the hippocampus following pilocarpine-induced status epilepticus. J Neuroinflamm 2009, 6:40.
39. Gatto G.J., McBride W.J., Murphy J.M., Lumeng L., Li T.K. Ethanol self-infusion into the ventral tegmental area by alcohol-preferring rats. Alcohol 1994, 11:557-564.
40. Gil-Mohapel J., Boehme F., Kainer L., Christie B.R. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: insights from different rodent models. Brain Res Rev 2010, 64:283-303.
41. He J., Crews F.T. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 2008, 210:349-358.
42. Hong Y.R., Lee H., Park M.H., Lee J.K., Lee J.Y., Suh H.D., Jeong M.S., Bae J.S., Jin H.K. CCL2 induces neural stem cell proliferation and neuronal differentiation in Niemann-Pick type C mice. J Vet Med Sci 2015.
43. Imamura F., Greer C.A. Segregated labeling of olfactory bulb projection neurons based on their birthdates. Eur J Neurosci 2015, 41:147-156.
44. Jonsson S., Ericson M., Soderpalm B. Modest long-term ethanol consumption affects expression of neurotransmitter receptor genes in the rat nucleus accumbens. Alcohol Clin Exp Res 2014, 38:722-729.
45. Kane C.J., Phelan K.D., Douglas J.C., Wagoner G., Johnson J.W., Xu J., Drew P.D. Effects of ethanol on immune response in the brain: region-specific changes in aged mice. J Neuroinflamm 2013, 10:66.
46. Kane C.J., Phelan K.D., Douglas J.C., Wagoner G., Johnson J.W., Xu J., Phelan P.S., Drew P.D. Effects of ethanol on immune response in the brain: region-specific changes in adolescent versus adult mice. Alcohol Clin Exp Res 2014, 38:384-391.
47. Karlsson C., Zook M., Ciccocioppo R., Gehlert D.R., Thorsell A., Heilig M., Cippitelli A. Melanin-concentrating hormone receptor 1 (MCH1-R) antagonism: reduced appetite for calories and suppression of addictive-like behaviors. Pharmacol Biochem Behav 2012, 102:400-406.
48. Kim A.K., Brown R.M., Lawrence A.J. The role of orexins/hypocretins in alcohol use and abuse: an appetitive-reward relationship. Front Behav Neurosci 2012, 6:78.
49. Koob G.F., Roberts A.J., Schulteis G., Parsons L.H., Heyser C.J., Hyytia P., Merlo-Pich E., Weiss F. Neurocircuitry targets in ethanol reward and dependence. Alcohol Clin Exp Res 1998, 22:3-9.
50. Lakaye B., Coumans B., Harray S., Grisar T. Melanin-concentrating hormone and immune function. Peptides 2009, 30:2076-2080.
51. Lawrence D.M., Seth P., Durham L., Diaz F., Boursiquot R., Ransohoff R.M., Major E.O. Astrocyte differentiation selectively upregulates CCL2/monocyte chemoattractant protein-1 in cultured human brain-derived progenitor cells. Glia 2006, 53:81-91.
52. Li M., Ransohoff R.M. Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog Neurobiol 2008, 84:116-131.
53. Li J., Hu Z., de Lecea L. The hypocretins/orexins: integrators of multiple physiological functions. Br J Pharmacol 2014, 171:332-350.
54. Liu X.S., Zhang Z.G., Zhang R.L., Gregg S.R., Wang L., Yier T., Chopp M. Chemokine ligand 2 (CCL2) induces migration and differentiation of subventricular zone cells after stroke. J Neurosci Res 2007, 85:2120-2125.
55. Livy D.J., Miller E.K., Maier S.E., West J.R. Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol Teratol 2003, 25:447-458.
56. Magge S.N., Malik S.Z., Royo N.C., Chen H.I., Yu L., Snyder E.Y., O'Rourke D.M., Watson D.J. Role of monocyte chemoattractant protein-1 (MCP-1/CCL2) in migration of neural progenitor cells toward glial tumors. J Neurosci Res 2009, 87:1547-1555.
57. Malone S.M., McGue M., Iacono W.G. Mothers' maximum drinks ever consumed in 24 hours predicts mental health problems in adolescent offspring. J Child Psychol Psychiatry 2010, 51:1067-1075.
58. March S.M., Abate P., Spear N.E., Molina J.C. Fetal exposure to moderate ethanol doses: heightened operant responsiveness elicited by ethanol-related reinforcers. Alcohol Clin Exp Res 2009, 33:1981-1993.
59. McBride W.J., Murphy J.M., Lumeng L., Li T.K. Serotonin, dopamine and GABA involvement in alcohol drinking of selectively bred rats. Alcohol 1990, 7:199-205.
60. McGorry P.D., Purcell R., Goldstone S., Amminger G.P. Age of onset and timing of treatment for mental and substance use disorders: implications for preventive intervention strategies and models of care. Curr Opin Psychiatry 2011, 24:301-306.
61. McMillin M., Frampton G., Thompson M., Galindo C., Standeford H., Whittington E., Alpini G., DeMorrow S. Neuronal CCL2 is upregulated during hepatic encephalopathy and contributes to microglia activation and neurological decline. J Neuroinflamm 2014, 11:121.
62. Mihic S.J., Sanna E., Whiting P.J., Harris R.A. Pharmacology of recombinant GABAA receptors. Adv Biochem Psychopharmacol 1995, 48:17-40.
63. Miller M.W. Effect of pre- or postnatal exposure to ethanol on the total number of neurons in the principal sensory nucleus of the trigeminal nerve: cell proliferation and neuronal death. Alcohol Clin Exp Res 1995, 19:1359-1363.
64. Miller M.W. Expression of transforming growth factor-beta in developing rat cerebral cortex: effects of prenatal exposure to ethanol. J Comp Neurol 2003, 460:410-424.
65. Morganstern I., Chang G.Q., Barson J.R., Ye Z., Karatayev O., Leibowitz S.F. Differential effects of acute and chronic ethanol exposure on orexin expression in the perifornical lateral hypothalamus. Alcohol Clin Exp Res 2010, 34:886-896.
66. Morganstern I., Chang G.Q., Chen Y.W., Barson J.R., Zhiyu Y., Hoebel B.G., Leibowitz S.F. Role of melanin-concentrating hormone in the control of ethanol consumption: Region-specific effects revealed by expression and injection studies. Physiol Behav 2010, 101:428-437.
67. Nanji A.A., Jokelainen K., Fotouhinia M., Rahemtulla A., Thomas P., Tipoe G.L., Su G.L., Dannenberg A.J. Increased severity of alcoholic liver injury in female rats: role of oxidative stress, endotoxin, and chemokines. Am J Physiol Gastrointest Liver Physiol 2001, 281:G1348-G1356.
68. Orikasa C., Kondo Y., Usui S., Sakuma Y. Similar numbers of neurons are generated in the male and female rat preoptic area in utero. Neurosci Res 2010, 68:9-14.
69. Pascual M., Balino P., Aragon C.M., Guerri C. Cytokines and chemokines as biomarkers of ethanol-induced neuroinflammation and anxiety-related behavior: role of TLR4 and TLR2. Neuropharmacology 2015, 89:352-359.
70. Poon K., Ho H.T., Barson J.R., Leibowitz S.F. Stimulatory role of the chemokine CCL2 in the migration and peptide expression of embryonic hypothalamic neurons. J Neurochem 2014.
71. Pueta M., Abate P., Haymal O.B., Spear N.E., Molina J.C. Ethanol exposure during late gestation and nursing in the rat: effects upon maternal care, ethanol metabolism and infantile milk intake. Pharmacol Biochem Behav 2008, 91:21-31.
72. Qiang M., Wang M.W., Elberger A.J. Second trimester prenatal alcohol exposure alters development of rat corpus callosum. Neurotoxicol Teratol 2002, 24:719-732.
73. Qin L., He J., Hanes R.N., Pluzarev O., Hong J.S., Crews F.T. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflamm 2008, 5:10.
74. Reyes E., Garcia K.D., Jones B.C. Effects of the maternal consumption of alcohol on alcohol selection in rats. Alcohol 1985, 2:323-326.
75. Richards J.K., Simms J.A., Steensland P., Taha S.A., Borgland S.L., Bonci A., Bartlett S.E. Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology 2008, 199:109-117.
76. Roberson R., Kuddo T., Benassou I., Abebe D., Spong C.Y. Neuroprotective peptides influence cytokine and chemokine alterations in a model of fetal alcohol syndrome. Am J Obstet Gynecol 2012, 207(499):e491-e495.
77. Sarkar D.K., Kuhn P., Marano J., Chen C., Boyadjieva N. Alcohol exposure during the developmental period induces beta-endorphin neuronal death and causes alteration in the opioid control of stress axis function. Endocrinology 2007, 148:2828-2834.
78. Shoblock J.R., Welty N., Aluisio L., Fraser I., Motley S.T., Morton K., Palmer J., Bonaventure P., Carruthers N.I., Lovenberg T.W., Boggs J., Galici R. Selective blockade of the orexin-2 receptor attenuates ethanol self-administration, place preference, and reinstatement. Psychopharmacology 2011, 215:191-203.
79. Simms J.A., Steensland P., Medina B., Abernathy K.E., Chandler L.J., Wise R., Bartlett S.E. Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats. Alcohol Clin Exp Res 2008, 32:1816-1823.
80. Simms J.A., Bito-Onon J.J., Chatterjee S., Bartlett S.E. Long-Evans rats acquire operant self-administration of 20% ethanol without sucrose fading. Neuropsychopharmacology 2010, 35:1453-1463.
81. Stettner G.M., Kubin L., Volgin D.V. Antagonism of orexin 1 receptors eliminates motor hyperactivity and improves homing response acquisition in juvenile rats exposed to alcohol during early postnatal period. Behav Brain Res 2011, 221:324-328.
82. Tabakoff B., Saba L., Printz M., Flodman P., Hodgkinson C., Goldman D., Koob G., Richardson H.N., Kechris K., Bell R.L., Hubner N., Heinig M., Pravenec M., Mangion J., Legault L., Dongier M., Conigrave K.M., Whitfield J.B., Saunders J., Grant B., Hoffman P.L., State WISo, Trait Markers of A Genetical genomic determinants of alcohol consumption in rats and humans. BMC Biol 2009, 7:70.
83. Umhau J.C., Schwandt M., Solomon M.G., Yuan P., Nugent A., Zarate C.A., Drevets W.C., Hall S.D., George D.T., Heilig M. Cerebrospinal fluid monocyte chemoattractant protein-1 in alcoholics: support for a neuroinflammatory model of chronic alcoholism. Alcohol Clin Exp Res 2014, 38:1301-1306.
84. Vengeliene V., Bilbao A., Molander A., Spanagel R. Neuropharmacology of alcohol addiction. Br J Pharmacol 2008, 154:299-315.
85. Vink J., Auth J., Abebe D.T., Brenneman D.E., Spong C.Y. Novel peptides prevent alcohol-induced spatial learning deficits and proinflammatory cytokine release in a mouse model of fetal alcohol syndrome. Am J Obstet Gynecol 2005, 193:825-829.
86. Wang S., Xu M., Li F., Wang X., Bower K.A., Frank J.A., Lu Y., Chen G., Zhang Z., Ke Z., Shi X., Luo J. Ethanol promotes mammary tumor growth and angiogenesis: the involvement of chemoattractant factor MCP-1. Breast Cancer Res Treat 2012, 133:1037-1048.
87. Williamson L.L., Bilbo S.D. Chemokines and the hippocampus: a new perspective on hippocampal plasticity and vulnerability. Brain Behav Immun 2013, 30:186-194.
88. Youngentob S.L., Glendinning J.I. Fetal ethanol exposure increases ethanol intake by making it smell and taste better. Proc Natl Acad Sci USA 2009, 106:5359-5364.