Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding

Cell

Volumn 156, Issue 3, 2014, Pages 495-509

  Vogt, Merly C ^a,b   Paeger, Lars ^b   Hess, Simon ^b   Steculorum, Sophie M ^a,b   Awazawa, Motoharu ^a,b   Hampel, Brigitte ^a,b   Neupert, Susanne ^b   Nicholls, Hayley T ^a,b   Mauer, Jan ^a,b   Hausen, A Christine ^a,b   Predel, Reinhard ^b   Kloppenburg, Peter ^b   Horvath, Tamas L ^d   Brüning, Jens C ^a,b,c  

^a MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI RELATED PROTEIN; INSULIN; MELANOCORTIN; NEUROPEPTIDE; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; PROTIRELIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; BODY FAT; BODY WEIGHT; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DISEASE SEVERITY; FAT INTAKE; FEMALE; GESTATIONAL AGE; GLUCOSE HOMEOSTASIS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN RESISTANCE; LACTATION; LIPID DIET; MATERNAL NUTRITION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOTONEURON; MOUSE; NERVE CELL; NEWBORN PERIOD; NONHUMAN; OBESITY; OVERNUTRITION; PANCREAS ISLET BETA CELL; PARASYMPATHETIC INNERVATION; PHENOTYPE; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; DISEASE PREDISPOSITION; HYPERINSULINEMIA; NERVE CELL MEMBRANE POTENTIAL; NERVOUS SYSTEM ELECTROPHYSIOLOGY;

AGOUTI; MUS;

ANIMALS; AXONS; DIET, HIGH-FAT; FEMALE; HYPERGLYCEMIA; HYPOTHALAMUS; INSULIN; LACTATION; MALE; METABOLIC DISEASES; MICE; MICE, INBRED C57BL; NEURONS; OBESITY; PREGNANCY; PRO-OPIOMELANOCORTIN; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84893463340     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.01.008     Document Type: Article

References (76)

1. V. Anna, H.P. van der Ploeg, N.W. Cheung, R.R. Huxley, and A.E. Bauman Sociodemographic correlates of the increasing trend in prevalence of gestational diabetes mellitus in a large population of women between 1995 and 2005 Diabetes Care 31 2008 2288 2293
2. N. Balthasar, R. Coppari, J. McMinn, S.M. Liu, C.E. Lee, V. Tang, C.D. Kenny, R.A. McGovern, S.C. Chua Jr.; J.K. Elmquist, and B.B. Lowell Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis Neuron 42 2004 983 991
3. P. Baum, D. Petroff, J. Classen, W. Kiess, and S. Blüher Dysfunction of autonomic nervous system in childhood obesity: a cross-sectional study PLoS ONE 8 2013 e54546
4. B.F. Belgardt, and J.C. Brüning CNS leptin and insulin action in the control of energy homeostasis Ann. N Y Acad. Sci. 1212 2010 97 113
5. J. Biag, Y. Huang, L. Gou, H. Hintiryan, A. Askarinam, J.D. Hahn, A.W. Toga, and H.W. Dong Cyto- and chemoarchitecture of the hypothalamic paraventricular nucleus in the C57BL/6J male mouse: a study of immunostaining and multiple fluorescent tract tracing J. Comp. Neurol. 520 2012 6 33
6. A. Bonnin, and P. Levitt Fetal, maternal, and placental sources of serotonin and new implications for developmental programming of the brain Neuroscience 197 2011 1 7
7. S.G. Bouret, S.J. Draper, and R.B. Simerly 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 2004 279 2805
8. S.G. Bouret, S.J. Draper, and R.B. Simerly Trophic action of leptin on hypothalamic neurons that regulate feeding Science 304 2004 108 110
9. S.G. Bouret, J.N. Gorski, C.M. Patterson, S. Chen, B.E. Levin, and R.B. Simerly Hypothalamic neural projections are permanently disrupted in diet-induced obese rats Cell Metab. 7 2008 179 185
10. K. Bouyer, and R.B. Simerly Neonatal leptin exposure specifies innervation of presympathetic hypothalamic neurons and improves the metabolic status of leptin-deficient mice J. Neurosci. 33 2013 840 851
11. C. Broberger, and T. Hökfelt Hypothalamic and vagal neuropeptide circuitries regulating food intake Physiol. Behav. 74 2001 669 682
12. J.C. Brüning, M.D. Michael, J.N. Winnay, T. Hayashi, D. Hörsch, D. Accili, L.J. Goodyear, and C.R. Kahn A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance Mol. Cell 2 1998 559 569
13. P.M. Catalano, L. Presley, J. Minium, and S. Hauguel-de Mouzon Fetuses of obese mothers develop insulin resistance in utero Diabetes Care 32 2009 1076 1080
14. H. Chen, D. Simar, K. Lambert, J. Mercier, and M.J. Morris Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism Endocrinology 149 2008 5348 5356
15. T.D. Clausen, E.R. Mathiesen, T. Hansen, O. Pedersen, D.M. Jensen, J. Lauenborg, and P. Damm High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational diabetes mellitus or type 1 diabetes: the role of intrauterine hyperglycemia Diabetes Care 31 2008 340 346
16. M.A. Cowley, J.L. Smart, M. Rubinstein, M.G. Cerdán, S. Diano, T.L. Horvath, R.D. Cone, and M.J. Low Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus Nature 411 2001 480 484
17. J.W. Creemers, L.E. Pritchard, A. Gyte, P. Le Rouzic, S. Meulemans, S.L. Wardlaw, X. Zhu, D.F. Steiner, N. Davies, and D. Armstrong et al. Agouti-related protein is posttranslationally cleaved by proprotein convertase 1 to generate agouti-related protein (AGRP)83-132: interaction between AGRP83-132 and melanocortin receptors cannot be influenced by syndecan-3 Endocrinology 147 2006 1621 1631
18. A.L. Deierlein, A.M. Siega-Riz, K. Chantala, and A.H. Herring The association between maternal glucose concentration and child BMI at age 3 years Diabetes Care 34 2011 480 484
19. C. Fekete, G. Legradi, E. Mihaly, Q.H. Huang, J.B. Tatro, W.M. Rand, C.H. Emerson, and R.M. Lechan α-Melanocyte-stimulating hormone is contained in nerve terminals innervating thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus and prevents fasting-induced suppression of prothyrotropin-releasing hormone gene expression J. Neurosci. 20 2000 1550 1558
20. C. Fekete, J. Kelly, E. Mihály, S. Sarkar, W.M. Rand, G. Légrádi, C.H. Emerson, and R.M. Lechan Neuropeptide Y has a central inhibitory action on the hypothalamic-pituitary-thyroid axis Endocrinology 142 2001 2606 2613
21. K.B.J. Franklin, and G. Paxinos The Mouse Brain in Stereotactic Coordinates 1997 Academic Press San Diego
22. M.M. Glavas, M.A. Kirigiti, X.Q. Xiao, P.J. Enriori, S.K. Fisher, A.E. Evans, B.E. Grayson, M.A. Cowley, M.S. Smith, and K.L. Grove Early overnutrition results in early-onset arcuate leptin resistance and increased sensitivity to high-fat diet Endocrinology 151 2010 1598 1610
23. J.N. Gorski, A.A. Dunn-Meynell, T.G. Hartman, and B.E. Levin Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 2006 R768 R778
24. W.F. Grant, L.E. Nicol, S.R. Thorn, K.L. Grove, J.E. Friedman, and D.L. Marks Perinatal exposure to a high-fat diet is associated with reduced hepatic sympathetic innervation in one-year old male Japanese macaques PLoS ONE 7 2012 e48119
25. C. Gravena, A.E. Andreazzi, F.T. Mecabo, S. Grassiolli, V.M. Scantamburlo, and P.C. Mathias Protein restriction during lactation alters the autonomic nervous system control on glucose-induced insulin secretion in adult rats Nutr. Neurosci. 10 2007 79 87
26. B.E. Grayson, S.E. Allen, S.K. Billes, S.M. Williams, M.S. Smith, and K.L. Grove Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate Neuroscience 143 2006 975 986
27. J.R. Greenfield, and L.V. Campbell Role of the autonomic nervous system and neuropeptides in the development of obesity in humans: targets for therapy? Curr. Pharm. Des. 14 2008 1815 1820
28. E. Gropp, M. Shanabrough, E. Borok, A.W. Xu, R. Janoschek, T. Buch, L. Plum, N. Balthasar, B. Hampel, and A. Waisman et al. Agouti-related peptide-expressing neurons are mandatory for feeding Nat. Neurosci. 8 2005 1289 1291
29. K.L. Grove, and M.A. Cowley Is ghrelin a signal for the development of metabolic systems? J. Clin. Invest. 115 2005 3393 3397
30. K.L. Grove, B.E. Grayson, M.M. Glavas, X.Q. Xiao, and M.S. Smith Development of metabolic systems Physiol. Behav. 86 2005 646 660
31. A. Gupta, M. Srinivasan, S. Thamadilok, and M.S. Patel Hypothalamic alterations in fetuses of high fat diet-fed obese female rats J. Endocrinol. 200 2009 293 300
32. A. Habbout, N. Li, L. Rochette, and C. Vergely Postnatal overfeeding in rodents by litter size reduction induces major short- and long-term pathophysiological consequences J. Nutr. 143 2013 553 562
33. T. Harder, A. Rake, W. Rohde, G. Doerner, and A. Plagemann Overweight and increased diabetes susceptibility in neonatally insulin-treated adult rats Endocr. Regul. 33 1999 25 31
34. T.L. Horvath, and J.C. Bruning Developmental programming of the hypothalamus: a matter of fat Nat. Med. 12 2006 52 53 discussion 53
35. S.Y. Kim, J.L. England, J.A. Sharma, and T. Njoroge Gestational diabetes mellitus and risk of childhood overweight and obesity in offspring: a systematic review Exp. Diabetes Res. 2011 2011 541308
36. C.M. King, and S.T. Hentges Relative number and distribution of murine hypothalamic proopiomelanocortin neurons innervating distinct target sites PLoS ONE 6 2011 e25864
37. T. Klöckener, S. Hess, B.F. Belgardt, L. Paeger, L.A. Verhagen, A. Husch, J.W. Sohn, B. Hampel, H. Dhillon, and J.M. Zigman et al. High-fat feeding promotes obesity via insulin receptor/PI3K-dependent inhibition of SF-1 VMH neurons Nat. Neurosci. 14 2011 911 918
38. A.C. Könner, R. Janoschek, L. Plum, S.D. Jordan, E. Rother, X. Ma, C. Xu, P. Enriori, B. Hampel, and G.S. Barsh et al. Insulin action in AgRP-expressing neurons is required for suppression of hepatic glucose production Cell Metab. 5 2007 438 449
39. A.C. Könner, T. Klöckener, and J.C. Brüning Control of energy homeostasis by insulin and leptin: targeting the arcuate nucleus and beyond Physiol. Behav. 97 2009 632 638
40. Y. Koutcherov, J.K. Mai, and G. Paxinos Hypothalamus of the human fetus J. Chem. Neuroanat. 26 2003 253 270
41. D.S. Ludwig, and C.B. Ebbeling Type 2 diabetes mellitus in children: Primary care and public health considerations JAMA 286 2001 1427 1430
42. S. Luquet, F.A. Perez, T.S. Hnasko, and R.D. Palmiter NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates Science 310 2005 683 685
43. J.S. Marino, Y. Xu, and J.W. Hill Central insulin and leptin-mediated autonomic control of glucose homeostasis Trends Endocrinol. Metab. 22 2011 275 285
44. B.E. Metzger, L.P. Lowe, A.R. Dyer, E.R. Trimble, U. Chaovarindr, D.R. Coustan, D.R. Hadden, D.R. McCance, M. Hod, H.D. McIntyre HAPO Study Cooperative Research Group Hyperglycemia and adverse pregnancy outcomes N. Engl. J. Med. 358 2008 1991 2002
45. M.J. Morris, and H. Chen Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth Int. J. Obes. (Lond.) 33 2009 115 122
46. M. Mumtaz Gestational diabetes mellitus Malays. J. Med. Sci. 7 2000 4 9
47. J. Pedersen Diabetes mellitus and pregnancy: present status of the hyperglycaemia - hyperinsulinism theory and the weight of the newborn baby Postgrad. Med. J. Suppl 1971 66 67
48. A. Plagemann Perinatal programming: the state of the art 2012 De Gruyter Berlin, Boston
49. A. Plagemann, I. Heidrich, F. Götz, W. Rohde, and G. Dörner Lifelong enhanced diabetes susceptibility and obesity after temporary intrahypothalamic hyperinsulinism during brain organization Exp. Clin. Endocrinol. 99 1992 91 95
50. A. Plagemann, T. Harder, U. Janert, A. Rake, F. Rittel, W. Rohde, and G. Dörner Malformations of hypothalamic nuclei in hyperinsulinemic offspring of rats with gestational diabetes Dev. Neurosci. 21 1999 58 67
51. L.E. Pritchard, and A. White Neuropeptide processing and its impact on melanocortin pathways Endocrinology 148 2007 4201 4207
52. J. Rossi, P. Santamäki, M.S. Airaksinen, and K.H. Herzig Parasympathetic innervation and function of endocrine pancreas requires the glial cell line-derived factor family receptor alpha2 (GFRalpha2) Diabetes 54 2005 1324 1330
53. J. Rossi, N. Balthasar, D. Olson, M. Scott, E. Berglund, C.E. Lee, M.J. Choi, D. Lauzon, B.B. Lowell, and J.K. Elmquist Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis Cell Metab. 13 2011 195 204
54. M.A. Sabin, and J.P. Shield Childhood obesity Front. Horm. Res. 36 2008 85 96
55. A. Sasaki, W.C. de Vega, S. St-Cyr, P. Pan, and P.O. McGowan Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood Neuroscience 240 2013 1 12
56. R. Schechter, M. Abboud, and G. Johnson Brain endogenous insulin effects on neurite growth within fetal rat neuron cell cultures Brain Res. Dev. Brain Res. 116 1999 159 167
57. T.P. Segerson, H. Hoefler, H. Childers, H.J. Wolfe, P. Wu, I.M. Jackson, and R.M. Lechan Localization of thyrotropin-releasing hormone prohormone messenger ribonucleic acid in rat brain in situ hybridization Endocrinology 121 1987 98 107
58. J.W. Sohn, L.E. Harris, E.D. Berglund, T. Liu, L. Vong, B.B. Lowell, N. Balthasar, K.W. Williams, and J.K. Elmquist Melanocortin 4 receptors reciprocally regulate sympathetic and parasympathetic preganglionic neurons Cell 152 2013 612 619
59. S.M. Steculorum, and S.G. Bouret Maternal diabetes compromises the organization of hypothalamic feeding circuits and impairs leptin sensitivity in offspring Endocrinology 152 2011 4171 4179
60. S.M. Steculorum, M.C. Vogt, and J.C. Brüning Perinatal programming of metabolic diseases: role of insulin in the development of hypothalamic neurocircuits Endocrinol. Metab. Clin. North Am. 42 2013 149 164
61. E.L. Sullivan, and K.L. Grove Metabolic imprinting in obesity Forum Nutr. 63 2010 186 194
62. B. Sun, R.H. Purcell, C.E. Terrillion, J. Yan, T.H. Moran, and K.L. Tamashiro Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity Diabetes 61 2012 2833 2841
63. L.W. Swanson Brain Maps: Structure of the Rat Brain 1998 Academic Press San Diego
64. C.D. Toran-Allerand, L. Ellis, and K.H. Pfenninger Estrogen and insulin synergism in neurite growth enhancement in vitro: mediation of steroid effects by interactions with growth factors? Brain Res. 469 1988 87 100
65. M.H. Vickers, P.D. Gluckman, A.H. Coveny, P.L. Hofman, W.S. Cutfield, A. Gertler, B.H. Breier, and M. Harris Neonatal leptin treatment reverses developmental programming Endocrinology 146 2005 4211 4216
66. M.C. Vogt, and J.C. Brüning CNS insulin signaling in the control of energy homeostasis and glucose metabolism - from embryo to old age Trends Endocrinol. Metab. 24 2013 76 84
67. K.W. Williams, L.O. Margatho, C.E. Lee, M. Choi, S. Lee, M.M. Scott, C.F. Elias, and J.K. Elmquist Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons J. Neurosci. 30 2010 2472 2479
68. Z. Yu, S. Han, J. Zhu, X. Sun, C. Ji, and X. Guo Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: a systematic review and meta-analysis PLoS ONE 8 2013 e61627
69. N. Akaike, and N. Harata Nystatin perforated patch recording and its applications to analyses of intracellular mechanisms Jpn. J. Physiol. 44 1994 433 473
70. O.P. Hamill, A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches Pflugers Arch. 391 1981 85 100
71. R. Horn, and A. Marty Muscarinic activation of ionic currents measured by a new whole-cell recording method J. Gen. Physiol. 92 1988 145 159
72. D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, and R.C. Turner Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man Diabetologia 28 1985 412 419
73. J. Rae, K. Cooper, P. Gates, and M. Watsky Low access resistance perforated patch recordings using amphotericin B J. Neurosci. Methods 37 1991 15 26
74. J. Rappsilber, M. Mann, and Y. Ishihama Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips Nat. Protoc. 2 2007 1896 1906
75. Q. Tong, C.P. Ye, J.E. Jones, J.K. Elmquist, and B.B. Lowell Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance Nat. Neurosci. 11 2008 998 1000
76. J.H. Ye, J. Zhang, C. Xiao, and J.Q. Kong Patch-clamp studies in the CNS illustrate a simple new method for obtaining viable neurons in rat brain slices: glycerol replacement of NaCl protects CNS neurons J. Neurosci. Methods 158 2006 251 259