Preclinical models for obesity research

DMM Disease Models and Mechanisms

Volumn 9, Issue 11, 2016, Pages 1245-1255

  Barrett, Perry ^a   Mercer, Julian G ^a   Morgan, Peter J ^a  

^a ROWETT RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Binge eating; Epigenetics; Obesity; Transgenics

Indexed keywords

TRACE ELEMENT;

APPETITE; BINGE EATING DISORDER; BODY FAT; CAFETERIA DIET; CALORIC INTAKE; CARDIOVASCULAR DISEASE; DIET; ELECTROMAGNETIC RADIATION; EPIDEMIC; FAST FOOD; FEEDING; FOOD INTAKE; GENETIC MODEL; HUMAN; MACRONUTRIENT; MATERNAL NUTRITION; MATERNAL OBESITY; MEAL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OPTOGENETICS; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; PROGENY; REVIEW; SUGAR INTAKE; WEIGHT GAIN; ANIMAL; BIOLOGICAL MODEL; DISEASE MODEL; GENETICS; MEDICAL RESEARCH; PATHOLOGY; TRANSLATIONAL RESEARCH;

ANIMALS; BIOMEDICAL RESEARCH; DIET; DISEASE MODELS, ANIMAL; HUMANS; MODELS, GENETIC; OBESITY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84994792209     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.026443     Document Type: Review

References (102)

1. Adan, R. A. H., Tiesjema, B., Hillebrand, J. J. G., la Fleur, S. E., Kas, M. J. H. and de Krom, M. (2006). The MC4 receptor and control of appetite. Br. J. Pharmacol. 149, 815-827.
2. Aponte, Y., Atasoy, D. and Sternson, S. M. (2011). AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat. Neurosci. 14, 351-355.
3. Armbruster, B. N., Li, X., Pausch, M. H., Herlitze, S. and Roth, B. L. (2007). Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 104, 5163-5168.
4. Atasoy, D., Aponte, Y., Su, H. H. and Sternson, S. M. (2008). A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28, 7025-7030.
5. Atasoy, D., and Betley., J. N., Su, H. H. and Sternson, S.M. (2012). Deconstruction of a neural circuit for hunger. Nature 488, 172-177.
6. Bake, T., and Duncan., J. S., Morgan, D. G. A. and Mercer, J. G. (2013). Arcuate nucleus homeostatic systems are not altered immediately prior to the scheduled consumption of large, binge-type meals of palatable solid or liquid diet in rats and mice. J. Neuroendocrinol. 25, 357-371.
7. Bake, T., Murphy, M., Morgan, D. G. A. and Mercer, J. G. (2014a). Large, bingetype meals of high fat diet change feeding behaviour and entrain food anticipatory activity in mice. Appetite 77, 62-73.
8. Bake, T., Morgan, D. G. A. and Mercer, J. G. (2014b). Feeding and metabolic consequences of scheduled consumption of large, binge-type meals of high fat diet in the Sprague-Dawley rat. Physiol. Behav. 128, 70-79.
9. Benjamin, S. and Spener, F. (2009). Conjugated linoleic acids as functional food: an insight into their health benefits. Nutr. Metab. 6, 36.
10. Berner, L. A., Avena, N.M. and Hoebel, B. G. (2008). Bingeing, self-restriction, and increased body weight in rats with limited access to a sweet-fat diet. Obesity 16, 1998-2002.
11. Berthoud, H.-R., Lenard, N. R. and Shin, A. C. (2011). Food reward, hyperphagia and obesity. Am. J. Physiol. Regul. Integr.Comp. Physiol. 300, R1266-R1277.
12. Betley, J. N., Cao, Z. F. H., Ritola, K. D. and Sternson, S. M. (2013). Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell 155, 1337-1350.
13. Betley, J. N., Xu, S., Cao, Z. F. H., Gong, R., Magnus, C. J., Yu, Y. and Sternson, S. M. (2015). Neurons for hunger and thirst transmit a negative-valence teaching signal. Nature 521, 180-185.
14. Biran, J., Tahor, M., Wircer, E. and Levkowitz, G. (2015). Role of developmental factors in hypothalamic function. Front. Neuroanat. 9, 47.
15. Blackshaw, S., Scholpp, S., Placzek, M., Ingraham, H., Simerly, R. and Shimogori, T. (2010). Molecular pathways controlling development of thalamus and hypothalamus: from neural specification to circuit formation. J. Neurosci. 30, 14925-14930.
16. Bolborea, M. and Dale, N. (2013). Hypothalamic tanycytes: potential roles in the control of feeding and energy balance. Trends Neurosci. 36, 91-100.
17. Bouret, S. G. and Simerly, R. B. (2006). Developmental programming of hypothalamic feeding circuits. Clin. Genet. 70, 295-301.
18. 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.
19. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. and Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268.
20. Brenseke, B., Bahamonde, J., Talanian, M., Kornfeind, E., Daly, J., Cobb, G., Zhang, J., and Prater., M. R., Davis, G. C. and Good, D. J. (2015). Mitigating or exacerbating effects of maternal-fetal programming of female mice through the food choice environment. Endocrinology 156, 182-192.
21. Breslow, M. J., Min-Lee, K., Brown, D. R., and Chacko., V. P., Palmer, D. and Berkowitz, D. E. (1999). Effect of leptin deficiency on metabolic rate in ob/ob mice. Am. J. Physiol. 276, E443-E449.
22. Buettner, R., Scholmerich, J. and Bollheimer, L. C. (2007). High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity 15, 798-808.
23. Byerly, M. S., and Swanson., R. D., Wong, G. W. and Blackshaw, S. (2013). Stage-specific inhibition of Trk B activity leads to long-lasting and sexually dimorphic effects on body weight and hypothalamic gene expression. PLoS ONE 8, e80781.
24. Carlin, J. L., George, R. and Reyes, T. M. (2013). Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. PLoS ONE 8, e63549.
25. Cedar, H. and Bergman, Y. (2009). Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304.
26. Chang, G.-Q., Gaysinskaya, V., Karatayev, O. and Leibowitz, S. F. (2008). Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J. Neuosci. 28, 12107-12119.
27. Chaumontet, C., and Even., P. C., Schwarz, J., Simonin-Foucault, A., Piedcoq, J., Fromentin, G., Azzout-Marniche, D. and Tome, D. (2015). High dietary protein decreases fat deposition induced by high-fat and high-sucrose diet in rats. Br. J. Nutr. 114, 1132-1142.
28. Cheetham, S. C. and Jackson, H. C. (2012). Rodent models to evaluate antiobesity drugs. In 'TRP Channels in Drug Discovery', Methods in Pharmacology and Toxicology, Eds Arpad Szallasi and Tamas Biro. pp. 351-376. Humana Press, Springer Science+Business Media, LLC.
29. Chen, Y., Lin, Y.-C., Kuo, T.-W. and Knight, Z. A. (2015). Sensory detection of food rapidly modulates arcuate feeding circuits. Cell 160, 829-841.
30. Church, C., Moir, L., McMurray, F., Girard, C., and Banks., G. T., Teboul, L., Wells, S., Bruning, J. C., and Nolan., P. M., Ashcroft, F. M. et al. (2010). Overexpression of Fto leads to increased food intake and results in obesity. Nat. Genet. 42, 1086-1092.
31. Coleman, D. L. (1978). Obese and diabetes: two mutant genes causing diabetes-obesity syndromes in mice. Diabetologia 14, 141-148.
32. Conklin, B. R., and Hsiao., E. C., Claeysen, S., Dumuis, A., Srinivasan, S., and Forsayeth., J. R., Guettier, J.-M., and Chang., W. C., Pei, Y., McCarthy, K. D. et al. (2008). Engineering GPCR signaling pathways with RASSLs. Nat. Methods 5, 673-678.
33. Corwin, R. L., Wojnicki, F. H. E., Fisher, J. O., and Dimitriou., S. G., Rice, H. B. and Young, M. A. (1998). Limited access to a dietary fat option affects ingestive behavior but not body composition in male rats. Physiol. Behav. 65, 545-553.
34. Corwin, R. L., Avena, N. M. and Boggiano, M. M. (2011). Feeding and reward: perspectives from three rat models of binge eating. Physiol. Behav. 104, 87-97.
35. Cowley, M. A., and Smart., J. L., Rubinstein, M., Cerdan, M. G., Diano, S., and Horvath., T. L., Cone, R. D. and Low, M. J. (2001). Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411, 480-484.
36. Cummings, D. E., and Purnell., J. Q., Frayo, R. S., Schmidova, K., Wisse, B. E. and Weigle, D. S. (2001). A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50, 1714-1719.
37. D'Agostino, G., Lyons, D. J., Cristiano, C., and Burke., L. K., Madara, J. C., Campbell, J. N., and Garcia., A. P., Land, B. B., Lowell, B. B., Dileone, R. J. et al. (2016). Appetite controlled by a cholecystokinin nucleus of the solitary tract to hypothalamus neurocircuit. eLife 5, e12225.
38. Desai, M., Li, T. and Ross, M. G. (2011). Hypothalamic neurosphere progenitor cells in low birth-weight rat newborns: neurotrophic effects of leptin and insulin. Brain Res. 1378, 29-42.
39. Drewnowski, A. and Darmon, N. (2005). The economics of obesity: dietary energy density and energy cost. Am. J. Clin. Nutr. 82, 1 Suppl., 265S-273S.
40. Ellenbroek, B. and Youn, J. (2016). Rodent models in neuroscience research: is it a rat race? Dis Model Mech. 9, 1079-1087.
41. Enriori, P. J., Sinnayah, P., Simonds, S. E., Garcia Rudaz, C. and Cowley, M. A. (2011). Leptin action in the dorsomedial hypothalamus increases sympathetic tone to brown adipose tissue in spite of systemic leptin resistance. J. Neurosci. 31, 12189-12197.
42. Erickson, J. C., Clegg, K. E. and Palmiter, R. D. (1996). Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 381, 415-418.
43. Farooqi, I. S., and Keogh., J. M., Yeo, G. S., Lank, E. J., Cheetham, T. and O'Rahilly, S. (2003). Clinical spectrum of obesity and mutations in the melanocortin 4 receptor gene. N. Engl. J. Med. 348, 1085-1095.
44. Ferguson, A. V., Latchford, K. J. and Samson, W. K. (2008). The paraventricular nucleus of the hypothalamus: a potential target for integrative treatment of autonomic dysfunction. Expert Opin. Ther. Targets 12, 717-727.
45. Garcia, A. P., Palou, M., Priego, T., Sanchez, J., Palou, A. and Pico, C. (2010). Moderate caloric restriction during gestation results in lower arcuate nucleus NPY-and αMSH-neurons and impairs hypothalamic response to fed/fasting conditions in weaned rats. Diabetes Obs. Metab. 12, 403-413.
46. Graham, M., and Shutter., J. R., Sarmiento, U., Sarosi, I. and Stark, K. L. (1997). Overexpression of Agrt leads to obesity in transgenic mice. Nat. Genet. 17, 273-274.
47. Grove, K. L., and Grayson., B. E., Glavas, M. M., Xiao, X. Q. and Smith, M. S. (2005). Development of metabolic systems. Physiol. Behav. 86, 646-660.
48. Huang, Z. J. and Zeng, H. (2013). Genetic approaches to neural circuits in the mouse. Annu. Rev. Neurosci. 36, 183-215.
49. Huszar, D., and Lynch., C. A., Fairchild-Huntress, V., Dunmore, J. H., Fang, Q., and Berkemeier., L. R., Gu, W., Kesterson, R. A., and Boston., B. A., Cone, R. D. et al. (1997). Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88, 131-141.
50. Ikenasio-Thorpe, B. A., Breier, B. H., Vickers, M. H. and Fraser, M. (2007). Prenatal influences on susceptibility to diet-induced obesity are mediated by altered neuroendocrine gene expression. J. Endocrinol. 193, 31-37.
51. Johnson, P. M. and Kenny, P. J. (2010). Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat. Neurosci. 13, 635-641.
52. Johnstone, L. E., Fong, T. M. and Leng, G. (2006). Neuronal activation in the hypothalamus and brainstem during feeding in rats. Cell Metab. 4, 313-321.
53. Kaakoush, N. O., and Martire., S. I., Raipuria, M., Mitchell, H. M., Nielsen, S., Westbrook, R. F. and Morris, M. J. (2016). Alternating orcontinuous exposure to cafeteria diet leads to similar shifts in gut 1 microbiota compared to chow diet. Mol. Nutr. Food Res. [Epub ahead of print] doi:10.1002/mnfr.201500815.
54. Kang, J. G. and Park, C.-Y. (2012). Anti-obesity drugs: a review about their effects and safety. Diabetes Metab. J. 36, 13-25.
55. Krashes, M. J., Koda, S., Ye, C. P., and Rogan., S. C., Adams, A. C., Cusher, D. S., Maratos-Flier, E., Roth, B. L. and Lowell, B. B. (2011). Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J. Clin. Invest. 121, 1424-1428.
56. Krashes, M. J., and Shah., B. P., Koda, S. and Lowell, B. B. (2013). Rapid versus delayed stimulation of feeding by the endogenously released AgRP neuron mediators GABA, NPY, and AgRP. Cell Metab. 18, 588-595.
57. la Fleur, S. E., Luijendijk, M. C. M., van der Zwaal, E. M., Brans, M. A. D. and Adan, R. A. H. (2014). The snacking rat as model of human obesity: effects of a free-choice high-fat high-sugar diet on meal patterns. Int. J. Obesity 38, 643-649.
58. Lee, D. A., Bedont, J.L., Pak, T., Wang, H., Song, J., Miranda-Angulo, A., Takiar, V., Charubhumi, V., Balordi, F., Takebayashi, H. et al. (2012). Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat. Neurosci. 15, 700-702.
59. Leibowitz, S. F. (1991). Brain neuropeptide Y: an integrator of endocrine, metabolic and behavioral processes. Brain Res. Bull. 27, 333-337.
60. Luquet, S., and Perez., F. A., Hnasko, T. S. and Palmiter, R. D. (2005). NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310, 683-685.
61. Lutz, T. A. and Woods, S. C. (2012). Overview of animal models of obesity. Curr. Protoc. Pharmacol. 58:5.61:5.61.1-55.61.61.18.
62. Marsh, D. J., and Miura., G. I., Yagaloff, K. A., Schwartz, M. W., Barsh, G. S. and Palmiter, R. D. (1999). Effects of neuropeptide Y deficiency on hypothalamic agouti-related protein expression and responsiveness to melanocortin analogues. Brain Res. 848, 66-77.
63. Martire, S. I., Westbrook, R. F. and Morris, M. J. (2015). Effects of long-term cycling between palatable cafeteria diet and regular chow on intake, eating patterns, and response to saccharin and sucrose. Physiol. Behav. 139, 80-88.
64. Mayer, J., Bates, M. W. and Dickie, M. M. (1951). Hereditary diabetes in genetically obese mice. Science 113, 746-747.
65. McNay, D. E. G., Briançon, N., Kokoeva, M. V., Maratos-Flier, E. and Flier, J. S. (2012). Remodeling of the arcuate nucleus energy-balance circuit is inhibited in obese mice. J. Clin. Invest. 122, 142-152.
66. Mercer, J. G. and Archer, Z. A. (2008). Putting the diet back into diet-induced obesity: diet-induced hypothalamic gene expression. Eur. J. Pharmacol. 585, 31-37.
67. Myers, M. G., Jr and Olson, D. P. (2012). Central nervous system control of metabolism. Nature 491, 357-363.
68. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P. and Bamberg, E. (2003). Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100, 13940-13945.
69. Nilsson, C, Raun, K., Yan, F.-F., Larsen, M. O. and Tang-Christensen, M. (2012). Laboratory animals as surrogate models of human obesity. Acta Pharmacol. Sin. 33, 173-181.
70. Ong, Z. Y. and Muhlhausler, B. S. (2011). Maternal "junk-food" feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. FASEB J. 25, 2167-2179.
71. Ong, Z. Y., and Wanasuria., A. F., Lin, M. Z. P., Hiscock, J. and Muhlhausler, B. S. (2013). Chronic intake of a cafeteria diet and subsequent abstinence. Sex-specific effects on gene expression in the mesolimbic reward system. Appetite 65, 189-199.
72. Petrovich, G. D. (2013). Forebrain networks and the control of feeding by environmental learned cues. Physiol. Behav. 121, 10-18.
73. Pierce, A. A. and Xu, A. W. (2010). De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J. Neurosci. 30, 723-730.
74. Pinto, S., and Roseberry., A. G., Liu, H., Diano, S., Shanabrough, M., Cai, X., Friedman, J. M. and Horvath, T. L. (2004). Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304, 110-115.
75. Qian, S., Chen, H., Weingarth, D., Trumbauer, M. E., and Novi., D. E., Guan, X., Yu, H., Shen, Z., Feng, Y., Frazier, E. et al. (2002). Neither agouti-related protein nor neuropeptide Y is critically required for the regulation of energy homeostasis in mice. Mol. Cell. Biol. 22, 5027-5035.
76. Robins, S. C, Stewart, I., and McNay., D. E., Taylor, V., Giachino, C, Goetz, M., Ninkovic, J., Briancon, N., Maratos-Flier, E., Flier, J. S. et al. (2013). α-tanycytes of the adult hypothalamic third ventricle include distinct populations of FGF-responsive neural progenitors. Nat.Comm. 4, 2049.
77. Rodriguez, E. M., and Blazquez., J. L., Pastor, F. E., Pelaez, B., Pena, P., Peruzzo, B. and Amat, P. (2005). Hypothalamic tanycytes: a key component of brain-endocrine interaction. Int. Rev. Cytol. 247, 89-164.
78. Rolls, E. T. (2005). Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol. Behav. 85, 45-56.
79. Roman, C. W., Derkach, V. A. and Palmiter, R. D. (2016). Genetically and functionally defined NTS to PBN brain circuits mediating anorexia. Nature 7, 11905.
80. Rothwell, N. J., Saville, M. E. and Stock, M. J. (1982). Effects of feeding a "cafeteria" diet on energy balance and diet-induced thermogenesis in four strains of rat. J. Nutr. 112, 1515-1524.
81. Sasaki, H., Hattori, Y., Ikeda, Y., Kamagata, M. and Shibata, S. (2015). Eating meals before wheel-running exercise attenuate high fat diet-driven obesity in mice under two meals per day schedule. Chronobiol. Int. 32, 677-686.
82. Schwartz, M. W., Woods, S. C, Porte, D., Seeley, R. J. and Baskin, D. G. (2000). Central nervous system control of food intake. Nature 404, 661-671.
83. Shi, Y.-C., Lau, J., Lin, Z., Zhang, H., Zhai, L., Sperk, G., Heilbronn, R., Mietzsch, M., Weger, S., Huang, X.-F. et al. (2013). Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN. Cell Metab. 17, 236-248.
84. Slimani, N., Deharveng, G., Southgate, D. A. T., Biessy, C., Chajes, V., van Bakel, M. M. E, Boutron-Ruault, M. C., McTaggart, A., Grioni, S., Verkaik-Kloosterman, J. et al. (2009). Contribution of highly industrially processed foods to the nutrient intakes and patterns of middle-aged populations in the European Prospective Investigation into Cancer and Nutrition study. Eur. J. Clin. Nutr. 63 Suppl. 4, S206-S225.
85. Speakman, J., Hambly, C., Mitchell, S. and Krol, E. (2008). The contribution of animal models to the study of obesity. Lab. Anim. 42, 413-432.
86. Speliotes, E. K., and Willer., C. J., Berndt, S. I., Monda, K. L., Thorleifsson, G., and Jackson., A. U., Allen, H. L., Lindgren, C. M., Luan, J., Magi, R. et al. (2010). Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat. Genet. 42, 937-948.
87. Stanley, S. A., Kelly, L., Latcha, K. N., and Schmidt., S. F., Yu, X., Nectow, A. R., Sauer, J., and Dyke., J. P., Dordick, J. S. and Friedman, J. M. (2016). Bidirectional electromagnetic control of the hypothalamus regulates feeding and metabolism. Nature 531, 647-650.
88. Steculorum, S. M., Collden, G., Coupe, B., Croizier, S., Lockie, S., Andrews, Z. B., Jarosch, F., Klussman, S. and Bouret, S. (2015). Neonatal ghrelin programs development of hypothalamic feeding circuits. J. Clin. Invest. 125, 846-858.
89. Sternson, S. M., Atasoy, D., Betley, J. N., Henry, F. E. and Xu, S. (2016). An emerging technology framework for the neurobiology of appetite. Cell Metab. 23, 234-253.
90. Takahashi, K. A. and Cone, R.D. (2004). Fasting inducesa large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/agouti-related protein neurons. Endocrinology 146, 1043-1047.
91. Tartaglia, L. A., Dembski, M., Weng, X., Deng, N., Culpepper, J., Devos, R., Richards, G. J., and Campfield., L. A., Clark, F. T., Deeds, J. et al. (1995). Identification and expression cloning of a leptin receptor, OB-R. Cell 83, 1263-1271.
92. United States Department of Agriculture (2012). Nutritional Quality of Food Prepared at Home and Away From Home, 1977-2008. http://www.ers.usda.gov/publications/eib-economic-information-bulletin/eib105.aspx.
93. United States Department of Agriculture. (2014). American budget shares devoted to food have flattened in recent years. http://www.ers.usda.gov/data-products/chart-gallery/detail.aspx?chartId=40094&ref=collection&embed=True.
94. van de Giessen, E., la Fleur, S. E., de Bruin, K., van den Brink, W. and Booij, J. (2012). Free-choice and no-choice high-fat diets affect striatal dopamine D2/3 receptor availability, caloric intake, and adiposity. Obesity 20, 1738-1740.
95. Vogt, M. C., Paeger, L., Hess, S., Steculorum, S. M., Awazawa, M., Hampel, B., Neupert, S., Nicholls, H. T. Mauer, J., Hausen, A. C. et al. (2014). Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding. Cell 156, 495-509.
96. Waterland, R. A. (2014). Epigenetic mechanisms affecting regulation of energy balance: many questions, few answers. Annu. Rev. Nutr. 34, 337-355.
97. Waterson, M. J. and Horvath, T. L. (2015). Neuronal regulation of energy homeostasis: beyond the hypothalamus and feeding. Cell Metab. 22, 962-970.
98. Williams, L. M., and Campbell., F. M., Drew, J. E., Koch, C., Hoggard, N., and Rees., W. D., Kamolrat, T., Thi Ngo, H., Steffensen, I.-L., Gray, S. R. et al. (2014). The development of diet-induced obesity and glucose intolerance in C57BL/6 mice on a high-fat diet consists of distinct phases. PLoS ONE 9, e106159.
99. Yazdi, F. T., Clee, S. M. and Meyre, D. (2015). Obesity genetics in mouse and human: back and forth, and back again. Peer J 3, e856.
100. Zambrano, E., Ibanez, C., Martinez-Samayoa, P. M., Lomas-Soria, C., Durand-Carbajal, M. and Rodriguez-Gonzalez, G. L. (2016). Maternal obesity: lifelong metabolic outcomes for offspring from poor developmental trajectories during the perinatal period. Arch. Med. Res. 47, 1-12.
101. Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L. and Friedman, J. M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425-432.
102. Zhang, X., Yang, R., Jia, Y., Cai, D., Zhou, B., Qu, X., Han, H., Xu, L., Wang, L., Yoa, Y. et al. (2014). Hypermethylation of SP1 binding site suppresses hypothalamic POMC in neonates and may contribute to metabolic disorders in adults: impact of maternal dietary CLAs. Diabetes 63, 1475-1487.