Loss of Magel2 impairs the development of hypothalamic Anorexigenic circuits

Human Molecular Genetics

Volumn 25, Issue 15, 2016, Pages 3208-3215

  Maillard, Julien ^a,b,c   Park, Soyoung ^a,c   Croizier, Sophie ^a,c   Vanacker, Charlotte ^b,c   Cook, Joshua H ^a,c   Prevot, Vincent ^b,c   Tauber, Maithe ^a,b,c   Bouret, Sebastien G ^a,b,c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b INSERM   (France)

^c HÔPITAL DES ENFANTS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI RELATED PROTEIN; ALPHA INTERMEDIN; GHRELIN; LEPTIN; MAGEL2 PROTEIN; MELANOMA ANTIGEN 2; PROOPIOMELANOCORTIN; UNCLASSIFIED DRUG; MAGEL2 PROTEIN, MOUSE; PROTEIN; TUMOR ANTIGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; AXON; CELL DENSITY; CONTROLLED STUDY; IN VITRO STUDY; MOUSE; NERVE PROJECTION; NEURITE OUTGROWTH; NEWBORN; NONHUMAN; PATHOGENESIS; PRADER WILLI SYNDROME; PRIORITY JOURNAL; ANIMAL; EMBRYOLOGY; GENETICS; HYPOTHALAMUS; METABOLISM; MUTANT MOUSE STRAIN;

ANIMALS; ANTIGENS, NEOPLASM; GHRELIN; HYPOTHALAMUS; LEPTIN; MICE; MICE, MUTANT STRAINS; PRADER-WILLI SYNDROME; PROTEINS;

EID: 85014333510     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw169     Document Type: Article

References (47)

1. Hanel, M. and Wevrick, R. (2001) The role of genomic imprinting in human developmental disorders: lessons from Prader-Willi syndrome. Clin. Genet., 59, 156-164.
2. Lee, S., Kozlov, S., Hernandez, L., Chamberlain, S.J., Brannan, C.I., Stewart, C.L. and Wevrick, R. (2000) Expression and imprinting of MAGEL2 suggest a role in Prader-Willi syndrome and the homologous murine imprinting phenotype. Hum. Mol. Genet., 9, 1813-1819.
3. Lee, S., Walker, C.L. and Wevrick, R. (2003) Prader-Willi syndrome transcripts are expressed in phenotypically significant regions of the developing mouse brain. Gene Expr. Patterns, 3, 599-609.
4. Kozlov, S.V., Bogenpohl, J.W., Howell, M.P., Wevrick, R., Panda, S., Hogenesch, J.B., Muglia, L.J., Van Gelder, R.N., Herzog, E.D. and Stewart, C.L. (2007) The imprinted gene Magel2 regulates normal circadian output. Nat. Genet., 39, 1266-1272.
5. Grill, H.J. (2006) Distributed neural control of energy balance: contributions from hindbrain and hypothalamus. Obesity, 14, 216S-221S.
6. Broberger, C., Johansen, J., Johansson, C., Schalling, M. and Hokfelt, T. (1998) The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc. Natl. Acad. Sci. USA., 95, 15043-15048.
7. Cone, R.D. (2005) Anatomy and regulation of the central melanocortin system. Nat. Neurosci., 8, 571-578.
8. Levin, B.E. (2000) The obesity epidemic: metabolic imprinting on genetically susceptible neural circuits. Obesity Res., 8, 342-347.
9. Horvath, T.L. and Bruning, J.C. (2006) Developmental programming of the hypothalamus: a matter of fat. Nat. Med., 12, 52-53.
10. Bouret, S., Levin, B.E. and Ozanne, S.E. (2015) Geneenvironment interactions controlling energy and glucose homeostasis and the developmental origins of obesity. Physiol. Rev., 95, 47-82.
11. Kirk, S.L., Samuelsson, A.M., Argenton, M., Dhonye, H., Kalamatianos, T., Poston, L., Taylor, P.D. and Coen, C.W. (2009) Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS One, 4, e5870.
12. Grayson, B.E., Levasseur, P.R., Williams, S.M., Smith, M.S., Marks, D.L. and Grove, K.L. (2010) Changes in melanocortin expression and inflammatory pathways in fetal offspring of nonhuman primates fed a high-fat diet. Endocrinology, 151, 1622-1632.
13. Bouret, S.G., Gorski, J.N., Patterson, C.M., Chen, S., Levin, B.E. and Simerly, R.B. (2008) Hypothalamic neural projections are permanently disrupted in diet-induced obese rats. Cell Metab., 7, 179-185.
14. LaBelle, D.R., Cox, J.M., Dunn-Meynell, A.A., Levin, B.E. and Flanagan-Cato, L.M. (2009) Genetic and dietary effects on dendrites in the rat hypothalamic ventromedial nucleus. Physiol. Behav., 98, 511-516.
15. Cummings, D.E., Clement, K., Purnell, J.Q., Vaisse, C., Foster, K.E., Frayo, R.S., Schwartz, M.W., Basdevant, A. and Weigle, D.S. (2002) Elevated plasma ghrelin levels in Prader-Willi syndrome. Nat. Med., 8, 643-644.
16. Feigerlová, E., Diene, G., Conte-Auriol, F., Molinas, C., Gennero, I., Salles, J.P., Arnaud, C. and Tauber, M. (2008) Hyperghrelinemia precedes obesity in Prader-Willi syndrome. J. Clin. Endocrinol. Metab., 93, 2800-28005.
17. Kweh, F.A., Miller, J.L., Sulsona, C.R., Wasserfall, C., Atkinson, M., Shuster, J.J., Goldstone, A.P. and Driscoll, D.J. (2015) Hyperghrelinemia in Prader-Willi syndrome begins in early infancy long before the onset of hyperphagia. Am. J. Med. Genet. Part A., 167, 69-79.
18. Bouret, S.G., Draper, S.J. and Simerly, R.B. (2004) Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J. Neurosci., 24, 2797-2805.
19. Bischof, J.M., Stewart, C.L. and Wevrick, R. (2007) Inactivation of the mouse Magel2 gene results in growth abnormalities similar to Prader-Willi syndrome. Hum. Mol. Genet., 16, 2713-2719.
20. Schaller, F., Watrin, F., Sturny, R., Massacrier, A., Szepetowski, P. and Muscatelli, F. (2010) A single postnatal injection of oxytocin rescues the lethal feeding behaviour in mouse newborns deficient for the imprinted Magel2 gene. Hum. Mol. Genet., 19, 4895-4905.
21. Bervini, S. and Herzog, H. (2013) Mouse models of Prader-Willi Syndrome: a systematic review. Front. Neuroendocrinol., 34, 107-119.
22. Cassidy, S.B., Schwartz, S., Miller, J.L. and Driscoll, D.J. (2012) Prader-Willi syndrome. Genet. Med., 14, 10-26.
23. Steculorum, S.M.C.G., Coupe, B., Croizier, S., Andrews, Z., Jarosch, F., Klussmann, S. and Bouret, S.G. (2015) Ghrelin programs development of hypothalamic feeding circuits. J. Clin. Invest., 125, 846-858.
24. Bouret, S.G., Draper, S.J. and Simerly, R.B. (2004) Trophic action of leptin on hypothalamic neurons that regulate feeding. Science, 304, 108-110.
25. Bouret, S.G., Bates, S.H., Chen, S., Myers, M.G. and Simerly, R.B. (2012) Distinct roles for specific leptin receptor signals in the development of hypothalamic feeding circuits. J. Neurosci., 32, 1244-1252.
26. Tennese, A.A. and Wevrick, R. (2011) Impaired hypothalamic regulation of endocrine function and delayed counterregulatory response to hypoglycemia in Magel2-null mice. Endocrinology, 152, 967-978.
27. Mercer, R.E., Michaelson, S.D., Chee, M.J.S., Atallah, T.A., Wevrick, R. and Colmers, W.F. (2013) Magel2 is required for leptin-mediated depolarization of POMC neurons in the hypothalamic arcuate nucleus in mice. PLoS Genet., 9, e1003207.
28. Pravdivyi, I., Ballanyi, K., Colmers, W.F. and Wevrick, R. (2015) Progressive postnatal decline in leptin sensitivity of arcuate hypothalamic neurons in the Magel2-null mouse model of Prader-Willi syndrome. Hum. Mol. Genet., 24, 4276-4283.
29. Bazeley, P., Shepelev, V., Talebizadeh, Z., Butler, M.G., Fedorova, L. and Filatov, V. A. F., (2008) snoTARGET shows that human orphan snoRNA targets locate close to alternative splice junctions. Gene, 408, 172-179.
30. Boccaccio, I., Glatt-Deeley, H., Watrin, F., Röeckel, N., Lalande, M. and Muscatelli, F. (1999) The human Magel2 gene and its mouse homologue are paternally expressed and mapped to the Prader-Willi region. Hum. Mol. Genet., 8, 2497-2505.
31. Doyle, J.M., Gao, J., Wang, J., Yang, M. and Potts, P.R. (2010) MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol. Cell, 39, 963-974.
32. Devos, J., Weselake, S.V. and Wevrick, R. (2011) Magel2, a Prader-Willi syndrome candidate gene, modulates the activities of circadian rhythm proteins in cultured cells. J. Circadian Rhythms, 9, 12-12.
33. Jay, P., Rougeulle, C., Massacrier, A., Moncla, A., Mattel, M.G., Malzac, P., Roeckel, N., Taviaux, S., Berge Lefranc, J.L., Cau, P. et al. (1997) The human necdin gene, NDN, is maternally imprinted and located in the Prader-Willi syndrome chromosomal region. Nat. Genet., 17, 357-361.
34. Kuwako, K., Hosokawa, A., Nishimura, I., Uetsuki, T., Yamada, M., Nada, S., Okada, M. and Yoshikawa, K. (2005) Disruption of the paternal Necdin gene diminishes TrkA signaling for sensory neuron survival. J. Neurosci., 25, 7090-7099.
35. Tcherpakov, M., Bronfman, F.C., Conticello, S.G., Vaskovsky, A., Levy, Z., Niinobe, M., Yoshikawa, K., Arenas, E. and Fainzilber, M. (2002) The p75 neurotrophin receptor interacts with multiple MAGE proteins. J. Biol. Chem., 277, 49101-49104.
36. Pagliardini, S., Ren, J., Wevrick, R. and Greer, J.J. (2005) Developmental abnormalities of neuronal structure and function in prenatal mice lacking the Prader-Willi syndrome gene necdin. Am. J. Pathol., 167, 175-191.
37. Lee, S., Walker, C.L., Karten, B., Kuny, S.L., Tennese, A.A., O'Neill, M.A. and Wevrick, R. (2005) Essential role for the Prader-Willi syndrome protein necdin in axonal outgrowth. Hum. Mol. Genet., 14, 627-637.
38. Mercer, R.E., Kwolek, E.M., Bischof, J.M., van Eede, M., Henkelman, R.M. and Wevrick, R. (2009) Regionally reduced brain volume, altered serotonin neurochemistry, and abnormal behavior in mice null for the circadian rhythm output gene Magel2. Am. J. Med. Genet. B Neuropsychiatr. Genet., 150B, 1085-1099.
39. Miller, J.L., Couch, J.A., Schmalfuss, I., He, G., Liu, Y. and Driscoll, D.J. (2007) Intracranial abnormalities detected by three-dimensional magnetic resonance imaging in Prader-Willi syndrome. Am. J. Med. Genet. Part A., 143A, 476-483.
40. Shapira, N.A., Lessig, M.C., He, A.G., James, G.A., Driscoll, D.J. and Liu, Y. (2005) Satiety dysfunction in Prader-Willi syndrome demonstrated by fMRI. J. Neurol. Neurosurg. Psychiatry, 76, 260-262.
41. Holsen, L.M., Zarcone, J.R., Brooks, W.M., Butler, M.G., Thompson, T.I., Ahluwalia, J.S., Nollen, N.L. and Savage, C.R. (2006) Neural mechanisms underlying hyperphagia in Prader-Willi syndrome. Obesity, 14, 1028-1037.
42. Swaab, D.F., Purba, J.S. and Hofman, M.A. (1995) Alterations in the hypothalamic paraventricular nucleus and its oxytocin neurons (putative satiety cells) in Prader-Willi syndrome: a study of five cases. J. Clin. Endocrinol. Metab., 80, 573-579.
43. Meziane, H., Schaller, F., Bauer, S., Villard, C., Matarazzo, V., Riet, F., Guillon, G., Lafitte, D., Desarmenien, M.G., Tauber, M. et al. (2015) An early postnatal oxytocin treatment prevents social and learning deficits in adult mice deficient for magel2, a gene involved in Prader-Willi syndrome and autism. Biol. Psychiatry, 78, 85-94.
44. Goldstone, A.P., Unmehopa, U.A., Bloom, S.R. and Swaab, D.F. (2002) Hypothalamic NPY and agouti-related protein are increased in human illness but not in Prader-Willi syndrome and other obese subjects. J. Clin. Endocrinol. Metab., 87, 927-937.
45. Goldstone, A.P., Unmehopa, U.A. and Swaab, D.F. (2003) Hypothalamic growth hormone-releasing hormone (GHRH) cell number is increased in human illness, but is not reduced in Prader-Willi syndrome or obesity. Clin. Endocrinol., 58, 743-755.
46. Fronczek, R., Lammers, G.J., Balesar, R., Unmehopa, U.A. and Swaab, D.F. (2005) The number of hypothalamic hypocretin (Orexin) neurons is not affected in Prader-Willi syndrome. J. Clin. Endocrinol. Metab., 90, 5466-5470.
47. Collden, G., Balland, E., Parkash, J., Caron, E., Langlet, F., Prevot, V. and Bouret, S.G. (2015) Neonatal overnutrition causes early alterations in the central response to peripheral ghrelin. Mol. Metab., 4, 15-24.