Adolescent morphine exposure affects long-term microglial function and later-life relapse liability in a model of addiction

Journal of Neuroscience

Volumn 33, Issue 3, 2013, Pages 961-971

  Schwarz, Jaclyn M ^a   Bilbo, Staci D ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD14 ANTIGEN; IBUDILAST; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MORPHINE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4;

ADOLESCENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG SEEKING BEHAVIOR; DRUG SENSITIZATION; EXPOSURE; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MORPHINE ADDICTION; NONHUMAN; NUCLEOTIDE SEQUENCE; NUCLEUS ACCUMBENS; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REINFORCEMENT; RELAPSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

AGE FACTORS; ANIMALS; CONDITIONING, OPERANT; DISEASE MODELS, ANIMAL; DRUG-SEEKING BEHAVIOR; MICROGLIA; MINOCYCLINE; MORPHINE; NARCOTICS; NUCLEUS ACCUMBENS; OPIOID-RELATED DISORDERS; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECURRENCE; TOLL-LIKE RECEPTOR 4;

EID: 84872362714     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2516-12.2013     Document Type: Article

References (27)

1. Baumrind D (1987) A developmental perspective on adolescent risk taking in contemporary America. New Dir Child Dev 37:93-125. Medline
2. Bilbo SD (2010) Early-life infection is a vulnerability factor for aging-related glial alterations and cognitive decline. Neurobiol Learn Mem 94:57-64. CrossRef Medline
3. Bilbo SD, Tsang V (2010) Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J 24:2104-2115. CrossRef Medline
4. Bland ST, Beckley JT, Watkins LR, Maier SF, Bilbo SD (2010a) Neonatal Escherichia coli infection alters glial, cytokine, and neuronal gene expression in response to acute amphetamine in adolescent rats. Neurosci Lett 474:52-57. CrossRef Medline
5. Bland ST, Beckley JT, Young S, Tsang V, Watkins LR, Maier SF, Bilbo SD (2010b) Enduring consequences of early-life infection on glial and neural cell genesis within cognitive regions of the brain. Brain Behav Immun 24:329-338. CrossRef Medline
6. Casula M, Iyer AM, Spliet WG, Anink JJ, Steentjes K, Sta M, Troost D, Aronica E (2011) Toll-like receptor signaling in amyotrophic lateral sclerosis spinal cord tissue. Neuroscience 179:233-243. CrossRef Medline
7. Cunningham CL, Gremel CM, Groblewski PA (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1:1662-1670. CrossRef Medline
8. Galvan A, Hare TA, Parra CE, Penn J, Voss H, Glover G, Casey BJ (2006) Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci 26: 6885-6892. CrossRef Medline
9. Gorina R, Font-Nieves M, Márquez-Kisinousky L, Santalucia T, Planas AM (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways. Glia 59:242-255. CrossRef Medline
10. Hutchinson MR, Northcutt AL, Chao LW, Kearney JJ, Zhang Y, Berkelhammer DL, Loram LC, Rozeske RR, Bland ST, Maier SF, Gleeson TT, Watkins LR (2008) Minocycline suppresses morphine-induced respiratory depression, suppresses morphine-induced reward, and enhances systemic morphine-induced analgesia. Brain Behav Immun 22:1248-1256. CrossRef Medline
11. Hutchinson MR, Zhang Y, Shridhar M, Evans JH, Buchanan MM, Zhao TX, Slivka PF, Coats BD, Rezvani N, Wieseler J, Hughes TS, Landgraf KE, Chan S, Fong S, Phipps S, Falke JJ, Leinwand LA, Maier SF, Yin H, Rice KC, Watkins LR (2010) Evidence that opioids may have Toll-like receptor 4 and MD-2 effects. Brain Behav Immun 24:83-95. CrossRef Medline
12. Hutchinson MR, Northcutt AL, Hiranita T, Wang X, Lewis SS, Thomas J, van Steeg K, Kopajtic TA, Loram LC, Sfregola C, Galer E, Miles NE, Bland ST, Amat J, Rozeske RR, Maslanik T, Chapman TR, Strand KA, Fleshner M, Bachtell RK, Somogyi AA, Yin H, Katz JL, Rice KC, Maier SF, Watkins LR. (2012) Opioid activation of Toll-like receptor 4 contributes to drug reinforcement. J Neurosci 32:11187-11200. CrossRef Medline
13. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S (1996) A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 224:855-862. CrossRef Medline
14. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, Ed 5. New York: Academic.
15. Robins LN, Przybeck TR (1985) Age of onset of drug use as a factor in drug and other disorders. NIDA Res Monogr 56:178-192. Medline
16. Saito O, Svensson CI, Buczynski MW, Wegner K, Hua XY, Codeluppi S, Schaloske RH, Deems RA, Dennis EA, Yaksh TL (2010) Spinal glial TLR4-mediated nociception and production of prostaglandin E(2) and TNF. Br J Pharmacol 160:1754-1764. CrossRef Medline
17. Santos-Galindo M, Acaz-Fonseca E, Bellini MJ, Garcia-Segura LM (2011) Sex differences in the inflammatory response of primary astrocytes to lipopolysaccharide. Biol Sex Differ 2:7. CrossRef Medline
18. Schwarz JM, Bilbo SD (2011) LPS elicits a much larger and broader inflammatory response than Escherichia coli infection within the hippocampus of neonatal rats. Neurosci Lett 497:110-115. CrossRef Medline
19. Schwarz JM, Hutchinson MR, Bilbo SD (2011) Early-life experience decreases drug-induced reinstatement of morphine CPP in adulthood via microglial-specific epigenetic programming of anti-inflammatory IL-10 expression. J Neurosci 31:17835-17847. CrossRef Medline
20. Simoni-Wastila L, Yang HK (2006) Psychoactive drug abuse in older adults. Am J Geriatr Pharmacother 4:380-394. CrossRef Medline
21. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463. CrossRef Medline
22. Wang X, Loram LC, Ramos K, de Jesus AJ, Thomas J, Cheng K, Reddy A, Somogyi AA, Hutchinson MR, Watkins LR, Yin H (2012) Morphine activates neuroinflammation in a manner parallel to endotoxin. Proc Natl Acad Sci U S A 109:6325-6330. CrossRef Medline
23. Williamson LL, Sholar PW, Mistry RM, Smith SH, Bilbo SD (2011) Microglia and memory: modulation by early-life infection. J Neurosci 31:15511-15521. CrossRef Medline
24. Wills TA, Vaccaro D, McNamara G (1994) Novelty seeking, risk taking, and related constructs as predictors of adolescent substance use: an application of Cloninger's theory. J Subst Abuse 6:1-20. CrossRef Medline
25. Wills TA, Vaccaro D, McNamara G, Hirky AE (1996) Escalated substance use: a longitudinal grouping analysis from early to middle adolescence. J Abnorm Psychol 105:166-180. CrossRef Medline
26. Yoo KY, Yoo DY, Hwang IK, Park JH, Lee CH, Choi JH, Kwon SH, Her S, Lee YL, Won MH (2011) Time-course alterations of Toll-like receptor 4 and NF-kappaB p65, and their coexpression in the gerbil hippocampal CA1 region after transient cerebral ischemia. Neurochem Res 36:2417-2426. CrossRef Medline
27. Zurolo E, Iyer A, Maroso M, Carbonell C, Anink JJ, Ravizza T, Fluiter K, Spliet WG, van Rijen PC, Vezzani A, Aronica E (2011) Activation of Toll-like receptor, RAGE and HMGB1 signalling in malformations of cortical de-velopment. Brain 134:1015-1032. CrossRef Medline