Loss of hypothalamic response to leptin during pregnancy associated with development of melanocortin resistance

Journal of Neuroendocrinology

Volumn 21, Issue 5, 2009, Pages 449-456

  Ladyman, S R ^a   Tups, A ^a   Augustine, R A ^a   Swahn Azavedo, A ^a   Kokay, I C ^a   Grattan, David R ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Hypothalamus; Leptin resistance; POMC; STAT3

Indexed keywords

AGOUTI RELATED PROTEIN; ALPHA INTERMEDIN; LEPTIN; MELANOCORTIN; MESSENGER RNA; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FEMALE; FOOD INTAKE; HORMONE RESISTANCE; HORMONE RESPONSIVE ELEMENT; HYPOTHALAMUS; HYPOTHALAMUS FUNCTION DISORDER; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

AGOUTI-RELATED PROTEIN; ALPHA-MSH; ANIMALS; CRICETINAE; ENERGY METABOLISM; FEMALE; HYPOTHALAMUS; IN SITU HYBRIDIZATION; LACTATION; LEPTIN; MELANOCORTINS; NEURONS; NEUROPEPTIDE Y; PREGNANCY; PRO-OPIOMELANOCORTIN; RATS; RATS, SPRAGUE-DAWLEY; STAT3 TRANSCRIPTION FACTOR;

EID: 64849097385     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2009.01862.x     Document Type: Article

References (45)

1. Ladyman SR., Grattan DR. Region-specific reduction in leptin-induced phosphorylation of signal transducer and activator of transcription-3 (STAT3) in the rat hypothalamus is associated with leptin resistance during pregnancy. Endocrinology 2004; 145: 3704-3711.
2. Grattan DR, Ladyman SR, Augustine RA. Hormonal induction of leptin resistance during pregnancy. Physiol Behav 2007; 91: 366-374.
3. Ladyman SR. Leptin resistance during pregnancy in the rat. J Neuroendocrinol 2008; 20: 269-277.
4. Gavrilova O, Barr V, Marcus-Samuels B, Reitman M. Hyperleptinemia of pregnancy associated with the appearance of a circulating form of the leptin receptor. J Biol Chem 1997; 272: 30546-30551.
5. Seeber RM, Smith JT, Waddell BJ. Plasma leptin-binding activity and hypothalamic leptin receptor expression during pregnancy and lactation in the rat. Biol Reprod 2002; 66: 1762-1767.
6. Spiegelman BM, Flier JS. Obesity and the regulation of energy balance. Cell 2001; 104: 531-543.
7. Marsh DJ, Hollopeter G, Huszar D, Laufer R, Yagaloff KA, Fisher SL, Burn P, Palmiter RD. Response of melanocortin-4 receptor-deficient mice to anorectic and orexigenic peptides. Nat Genet 1999; 21: 119-122.
8. Poggioli R, Vergoni AV, Bertolini A. ACTH-(1-24) and alpha-MSH antagonize feeding behavior stimulated by kappa opiate agonists. Peptides 1986; 7: 843-848.
9. Thiele TE, van Dijk G, Yagaloff KA, Fisher SL, Schwartz M, Burn P, Seeley RJ. Central infusion of melanocortin agonist MTII in rats: assessment of c-Fos expression and taste aversion. Am J Physiol 1998; 274: R248-R254.
10. Yaswen L, Diehl N, Brennan MB, Hochgeschwender U. Obesity in the mouse model of pro-opiomelanocortin deficiency responds to peripheral melanocortin. Nat Med 1999; 5: 1066-1070.
11. Douglas AJ, Bicknell RJ, Leng G, Russell JA, Meddle SL. Beta-endorphin cells in the arcuate nucleus: Projections to the supraoptic nucleus and changes in expression during pregnancy and parturition. J Neuroendocrinol 2002; 14: 768-777.
12. Mann PE, Rubin BS, Bridges RS. Differential proopiomelanocortin gene expression in the medial basal hypothalamus of rats during pregnancy and lactation. Brain Res Mol Brain Res 1997; 46: 9-16.
13. Rocha M, Bing C, Williams G, Puerta M. Pregnancy-induced hyperphagia is associated with increased gene expression of hypothalamic agouti-related peptide in rats. Regul Pept 2003; 114: 159-165.
14. Khorram O, DePalatis LR, McCann SM. Changes in hypothalamic and pituitary content of immunoreactive alpha-melanocyte-stimulating hormone during the gestational and postpartum periods in the rat. Proc Soc Exp Biol Med 1984; 177: 318-326.
15. Wilding JP, Ajala MO, Lambert PD, Bloom SR. Additive effects of lactation and food restriction to increase hypothalamic neuropeptide Y mRNA in rats. J Endocrinol 1997; 152: 365-369.
16. Pierroz DD, Ziotopoulou M, Ungsunan L, Moschos S, Flier JS, Mantzoros CS. Effects of acute and chronic administration of the melanocortin agonist MTII in mice with diet-induced obesity. Diabetes 2002; 51: 1337-1345.
17. Scarpace PJ, Matheny M, Zolotukhin S, Tumer N, Zhang Y. Leptin-induced leptin resistant rats exhibit enhanced responses to the melanocortin agonist MT II. Neuropharmacology 2003; 45: 211-219.
18. Zhang Y, Matheny M, Tumer N, Scarpace PJ. Aged-obese rats exhibit robust responses to a melanocortin agonist and antagonist despite leptin resistance. Neurobiol Aging 2004; 25: 1349-1360.
19. Zhang Y, Scarpace PJ. Circumventing central leptin resistance: Lessons from central leptin and POMC gene delivery. Peptides 2006; 27: 350-364.
20. Mercer JG, Moar KM, Logie TJ, Findlay PA, Adam CL, Morgan PJ. Seasonally inappropriate body weight induced by food restriction: Effect on hypothalamic gene expression in male Siberian hamsters. Endocrinology 2001; 142: 4173-4181.
21. Mercer JG, Moar KM, Ross AW, Hoggard N, Morgan PJ. Photoperiod regulates arcuate nucleus POMC, AGRP, and leptin receptor mRNA in Siberian hamster hypothalamus. Am J Physiol Regul Integr Comp Physiol 2000; 278: R271-R281.
22. Mercer JG, Lawrence CB, Beck B, Burlet A, Atkinson T, Barrett P. Hypothalamic NPY and prepro-NPY mRNA in Djungarian hamsters: Effects of food deprivation and photoperiod. Am J Physiol 1995; 269: R1099-R1106.
23. Munzberg H, Huo L, Nillni EA, Hollenberg AN, Bjorbaek C. Role of signal transducer and activator of transcription 3 in regulation of hypothalamic proopiomelanocortin gene expression by leptin. Endocrinology 2003; 144: 2121-2131.
24. Ladyman SR, Grattan DR. Suppression of leptin receptor messenger ribonucleic acid and leptin responsiveness in the ventromedial nucleus of the hypothalamus during pregnancy in the rat. Endocrinology 2005; 146: 3868-3874.
25. Bagnol D, Lu XY, Kaelin CB, Day HE, Ollmann M, Gantz I, Akil H, Barsh GS, Watson SJ. Anatomy of an endogenous antagonist: Relationship between Agouti-related protein and proopiomelanocortin in brain. J Neurosci 1999; 19: RC26.
26. Munzberg H, Flier JS, Bjorbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 2004; 145: 4880-4889.
27. Erickson JC, Hollopeter G, Palmiter RD. Attenuation of the obesity syndrome of ob/ob mice by the loss of neuropeptide Y. Science 1996; 274: 1704-1707.
28. Amico JA, Thomas A, Crowley RS, Burmeister LA. Concentrations of leptin in the serum of pregnant, lactating, and cycling rats and of leptin messenger ribonucleic acid in rat placental tissue. Life Sci 1998; 63: 1387-1395.
29. Garcia MD, Casanueva FF, Dieguez C, Senaris RM. Gestational profile of leptin messenger ribonucleic acid (mRNA) content in the placenta and adipose tissue in the rat, and regulation of the mRNA levels of the leptin receptor subtypes in the hypothalamus during pregnancy and lactation. Biol Reprod 2000; 62: 698-703.
30. Kawai M, Yamaguchi M, Murakami T, Shima K, Murata Y, Kishi K. The placenta is not the main source of leptin production in pregnant rat: gestational profile of leptin in plasma and adipose tissues. Biochem Biophys Res Commun 1997; 240: 798-802.
31. Lopez-Soriano J, Carbo N, Lopez-Soriano FJ, Argiles JM. Leptin levels and gene expression during the perinatal phase in the rat. Eur J Obstet Gynecol Reprod Biol 1998; 81: 95-100.
32. Brunton PJ, Bales J, Russell JA. Neuroendocrine stress but not feeding responses to centrally administered neuropeptide Y are suppressed in pregnant rats. Endocrinology 2006; 147: 3737-3745.
33. Ciofi P, Fallon JH, Croix D, Polak JM, Tramu G. Expression of neuropeptide Y precursor-immunoreactivity in the hypothalamic dopaminergic tubero-infundibular system during lactation in rodents. Endocrinology 1991; 128: 823-834.
34. Bates SH, Myers MG. The role of leptin → STAT3 signaling in neuroendocrine function: An integrative perspective. J Mol Med 2004; 82: 12-20.
35. Abbott CR, Rossi M, Kim M, AlAhmed SH, Taylor GM, Ghatei MA, Smith DM, Bloom SR. Investigation of the melanocyte stimulating hormones on food intake. Lack Of evidence to support a role for the melanocortin-3-receptor. Brain Res 2000; 869: 203-210.
36. Kask A, Rago L, Wikberg JE, Schioth HB. Differential effects of melanocortin peptides on ingestive behaviour in rats: Evidence against the involvement of MC(3) receptor in the regulation of food intake. Neurosci Lett 2000; 283: 1-4.
37. Ludwig DS, Mountjoy KG, Tatro JB, Gillette JA, Frederich RC, Flier JS, Maratos-Flier E. Melanin-concentrating hormone: A functional melanocortin antagonist in the hypothalamus. Am J Physiol 1998; 274: E627-E633.
38. McMinn JE, Wilkinson CW, Havel PJ, Woods SC, Schwartz MW. Effect of intracerebroventricular alpha-MSH on food intake, adiposity, c-Fos induction, and neuropeptide expression. Am J Physiol Regul Integr Comp Physiol 2000; 279: R695-R703.
39. Tsujii S, Bray GA. Acetylation alters the feeding response to MSH and beta-endorphin. Brain Res Bull 1989; 23: 165-169.
40. Chen AS, Metzger JM, Trumbauer ME, Guan XM, Yu H, Frazier EG, Marsh DJ, Forrest MJ, Gopal-Truter S, Fisher J, Camacho RE, Strack AM, Mellin TN, MacIntyre DE, Chen HY, Van der Ploeg LH. Role of the melanocortin-4 receptor in metabolic rate and food intake in mice. Transgenic Res 2000; 9: 145-154.
41. Gantz I, Miwa H, Konda Y, Shimoto Y, Tashiro T, Watson SJ, DelValle J, Yamada T. Molecular cloning, expression, and gene localization of a fourth melanocortin receptor. J Biol Chem 1993; 268: 15174-15179.
42. Huszar D, Lynch CA, Fairchild-Huntress V, Dunmore JH, Fang Q, Berkemeier LR, Gu W, Kesterson RA, Boston BA, Cone RD, Smith FJ, Campfield LA, Burn P, Lee F. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 1997; 88: 131-141.
43. Mountjoy KG, Mortrud MT, Low MJ, Simerly RB, Cone RD. Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol Endocrinol 1994; 8: 1298-1308.
44. Grattan DR. The actions of prolactin in the brain during pregnancy and lactation. Prog Brain Res 2001; 133: 153-171.
45. Russell JA, Douglas AJ, Ingram CD. Brain preparations for maternity-adaptive changes in behavioral and neuroendocrine systems during pregnancy and lactation. An overview. Prog Brain Res 2001; 133: 1-38.