Hypothalamic proteoglycan syndecan-3 is a novel cocaine addiction resilience factor

Nature Communications

Volumn 4, Issue , 2013, Pages

  Chen, Jihuan ^a   Repunte Canonigo, Vez ^a   Kawamura, Tomoya ^a   Lefebvre, Celine ^b   Shin, William ^b   Howell, Leonard L ^c   Hemby, Scott E ^d   Harvey, Brandon K ^e   Califano, Andrea ^b   Morales, Marisela ^e   Koob, George F ^a   Sanna, Pietro Paolo ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c EMORY UNIVERSITY   (United States)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; PARVOVIRUS VECTOR; PROTEIN RET; SYNDECAN 3; VANDETANIB; SUCROSE;

BRAIN; DRUG USER; NEUROLOGY; RODENT; SIGNALING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR EFFECT; COCAINE DEPENDENCE; CONTROLLED STUDY; DOSE RESPONSE; DRUG SELF ADMINISTRATION; GENE EXPRESSION; HEART RATE; LATERAL HYPOTHALAMUS; LOCOMOTION; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; RAT; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SUCROSE PREFERENCE TEST; VIRAL GENE DELIVERY SYSTEM; ANIMAL; DEFICIENCY; DRUG EFFECTS; FEEDING BEHAVIOR; HYPOTHALAMUS; KNOCKOUT MOUSE; METABOLISM; RHESUS MONKEY; WISTAR RAT; DRUG EFFECT;

ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; FEEDING BEHAVIOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HYPOTHALAMUS; MACACA MULATTA; MALE; MICE; MICE, KNOCKOUT; RATS; RATS, WISTAR; SUCROSE; SYNDECAN-3;

EID: 84891607200     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2955     Document Type: Article

References (35)

1. Nader, M. A., Czoty, P. W., Gould, R. W. & Riddick, N. V. Review. Positron emission tomography imaging studies of dopamine receptors in primate models of addiction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 3223-3232 (2008).
2. Volkow, N. D., Wang, G. J., Fowler, J. S., Tomasi, D. & Telang, F. Addiction: beyond dopamine reward circuitry. Proc. Natl Acad. Sci. USA 108, 15037-15042 (2011).
3. Koob, G. F. A role for brain stress systems in addiction. Neuron 59, 11-34 (2008).
4. Bernfield, M. et al. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777 (1999).
5. Streuli, C. H. & Akhtar, N. Signal co-operation between integrins and other receptor systems. Biochem. J. 418, 491-506 (2009).
6. Bespalov, M. M. et al. Heparan sulfate proteoglycan syndecan-3 is a novel receptor for GDNF, neurturin, and artemin. J. Cell Biol. 192, 153-169 (2011).
7. Diamantopoulou, Z., Kitsou, P., Menashi, S., Courty, J. & Katsoris, P. Loss of receptor protein tyrosine phosphatase beta/zeta (RPTPbeta/zeta) promotes prostate cancer metastasis. J. Biol. Chem. 287, 40339-40349 (2012).
8. Koob, G. F. & Volkow, N. D. Neurocircuitry of addiction. Neuropsychopharmacology 35, 217-238 (2010).
9. Ahmed, S. H. et al. Gene expression evidence for remodeling of lateral hypothalamic circuitry in cocaine addiction. Proc. Natl Acad. Sci. USA 102, 11533-11538 (2005).
10. Piazza, P. V., Deroche-Gamonent, V., Rouge-Pont, F. & Le Moal, M. Vertical shifts in self-administration dose-response functions predict a drug-vulnerable phenotype predisposed to addiction. J. Neurosci. 20, 4226-4232 (2000).
11. Zheng, Q. et al. Enhanced anorexigenic signaling in lean obesity resistant syndecan-3 null mice. Neuroscience 171, 1032-1040 (2010).
12. Strader, A. D., Reizes, O., Woods, S. C., Benoit, S. C. & Seeley, R. J. Mice lacking the syndecan-3 gene are resistant to diet-induced obesity. J. Clin. Invest. 114, 1354-1360 (2004).
13. Manon-Jensen, T., Itoh, Y. & Couchman, J. R. Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J. 277, 3876-3889 (2010).
14. Pickens, C. L., Airavaara, M., Theberge, F., Fanous, S., Hope, B. T. & Shaham, Y. Neurobiology of the incubation of drug craving. Trends. Neurosci. 34, 411-420 (2011).
15. Kawamoto, Y., Nakamura, S., Matsuo, A., Akiguchi, I. & Shibasaki, H. Immunohistochemical localization of glial cell line-derived neurotrophic factor in the human central nervous system. Neuroscience 100, 701-712 (2000).
16. Green-Sadan, T., Kinor, N., Roth-Deri, I., Geffen-Aricha, R., Schindler, C. J. & Yadid, G. Transplantation of glial cell line-derived neurotrophic factor-expressing cells into the striatum and nucleus accumbens attenuates acquisition of cocaine self-administration in rats. Eur. J. Neurosci. 18, 2093-2098 (2003).
17. Carlomagno, F. et al. ZD6474, an orally available inhibitor of KDR tyrosine kinase activity, efficiently blocks oncogenic RET kinases. Cancer. Res. 62, 7284-7290 (2002).
18. Bock, R. et al. Strengthening the accumbal indirect pathway promotes resilience to compulsive cocaine use. Nat. Neurosci. 16, 632-638 (2013).
19. Vassoler, F. M., White, S. L., Schmidt, H. D., Sadri-Vakili, G. & Pierce, R. C. Epigenetic inheritance of a cocaine-resistance phenotype. Nat. Neurosci. 16, 42-47 (2013).
20. Stellar, E. The physiology of motivation. Psychol. Rev. 61, 5-22 (1954).
21. Olds, J. Hypothalamic substrates of reward. Physiol. Rev. 42, 554-604 (1962).
22. Gabbott, P. L., Warner, T. A., Jays, P. R., Salway, P. & Busby, S. J. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol. 492, 145-177 (2005).
23. Barbas, H. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res. Bull. 52, 319-330 (2000).
24. Humphries, M. D. & Prescott, T. J. The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. Prog. Neurobiol. 90, 385-417 (2010).
25. Risold, P. Y., Thompson, R. H. & Swanson, L. W. The structural organization of connections between hypothalamus and cerebral cortex. Brain Res. Brain Res. Rev. 24, 197-254 (1997).
26. Marchant, N. J., Millan, E. Z. & McNally, G. P. The hypothalamus and the neurobiology of drug seeking. Cell Mol. Life Sci. 69, 581-597 (2012).
27. Kenny, P. J. Brain reward systems and compulsive drug use. Trends Pharmacol. Sci. 28, 135-141 (2007).
28. Stanley, B. G., Willett, 3rd V. L., Donias, H. W., Ha, L. H. & Spears, L. C. The lateral hypothalamus: a primary site mediating excitatory amino acid-elicited eating. Brain Res. 630, 41-49 (1993).
29. Stricker, E. M., Swerdloff, A. F. & Zigmond, M. J. Intrahypothalamic injections of kainic acid produce feeding and drinking deficits in rats. Brain Res. 158, 470-473 (1978).
30. Velley, L. The role of intrinsic neurons in lateral hypothalamic self-stimulation. Behav. Brain Res. 22, 141-152 (1986).
31. Richardson, N. R. & Roberts, D. C. Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J. Neurosci. Methods 66, 1-11 (1996).
32. Lewis, S. R., Ahmed, S., Dym, C., Khaimova, E., Kest, B. & Bodnar, R. J. Inbred mouse strain survey of sucrose intake. Physiol. Behav. 85, 546-556 (2005).
33. Reizes, O. et al. Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell 106, 105-116 (2001).
34. Lu, L. et al. Role of ventral tegmental area glial cell line-derived neurotrophic factor in incubation of cocaine craving. Biol. Psychiatry 66, 137- 145 (2009).
35. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).