Maternal perinatal undernutrition programs a "brown-like" phenotype of gonadal white fat in male rat at weaning

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 1, 2010, Pages

  Delahaye, Fabien ^a   Lukaszewski, Marie Amélie ^a   Wattez, Jean Sébastien ^a   Cisse, Ouma ^a   Dutriez Casteloot, Isabelle ^a   Fajardy, Isabelle ^a   Montel, Valérie ^a   Dickes Coopman, Anne ^a   Laborie, Christine ^a   Lesage, Jean ^a   Breton, Christophe ^a   Vieau, Didier ^a  

^a UNIVERSITÉ DE LILLE   (France)

Author keywords

Adipose tissue programming; Maternal undernutrition; Neuropeptide Y; Peroxisome proliferator activated receptor coactivator 1 ; Uncoupling protein 1

Indexed keywords

LEPTIN; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; UNCOUPLING PROTEIN 1;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIET RESTRICTION; ENERGY METABOLISM; GENE EXPRESSION; GENE OVEREXPRESSION; HYPERPHAGIA; IMMUNOHISTOCHEMISTRY; MALE; MALNUTRITION; METABOLIC REGULATION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROGENY; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WEANING; WHITE ADIPOSE TISSUE;

EID: 77954397668     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00604.2009     Document Type: Article

References (60)

1. Ahima RS. Adipose tissue as an endocrine organ. Obesity 14, Suppl 5: 242S-249S, 2006.
2. Ailhaud G, Hauner H. Development of White Adipose Tissue (2nd Ed.). New York: Dekker, 2004.
3. Aslanidi G, Kroutov V, Philipsberg G, Lamb K, Campbell-Thompson M, Walter G, Kureno S, Aguirre I, Keller P, Hankenson K, Mac-Dougald O, Zolotukhin S. Ectopic expression of Wnt10b decreases adiposity and improves glucose homeostasis in obese rats. Am J Physiol Endocrinol Metab 293: E726-E736, 2007.
4. Barbera MJ, Schluter A, Pedraza N, Iglesias R, Villarroya F, Giralt M. Peroxysome proliferator-activated receptor α activates transcription of the brown fat uncoupling protein-1 gene. A link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J Biol Chem 276: 1486-1493, 2001.
5. Barker DJ. The developmental origins of chronic adult disease. Acta Paediatr 93: 26-33, 2004.
6. Bieswal F, Hay SM, McKinnon C, Reusens B, Cuignet M, Rees WD, Remacle C. Prenatal protein restriction does not affect the proliferation and differentiation of rat preadipocytes. J Nutr 134: 1493-1499, 2004.
7. Bol VV, Delattre AI, Reusens B, Raes M, Remacle C. Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol 297: R291-R299, 2009.
8. Breton C, Lukaszewski MA, Risold PY, Enache M, Guillemot J, Rivière G, Delahaye F, Lesage J, Dutriez-Casteloot I, Laborie C, Vieau D. Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Am J Physiol Endocrinol Metab 296: E462-E472, 2009.
9. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359, 2004.
10. Cinti S. Adipose tissues and obesity. Ital J Anat Embryol 104: 37-51, 1999.
11. Cinti S. Adipocyte differentiation and transdifferentiation: plasticity of the adipose organ. J Endocrinol Invest 25: 823-835, 2002.
12. Cinti S. Transdifferentiation properties of adipocytes in the adipose organ. Am J Physiol Endocrinol Metab 297: E977-E986, 2009.
13. Ciofi P, Garret M, Lapirot O, Lafon P, Loyens A, Prévot V, Levine JE. Brain-endocrine interactions: a microvascular route in the mediobasal hypothalamus. Endocrinology 150: 5509-5519, 2009.
14. Cousin B, Cinti S, Morroni M, Raimbault S, Ricquier D, Penicaud L, Casteilla L. Occurrence of brown adipocytes in white fat adipose tissue: molecular and morphological characterization. J Cell Sci 103: 931-942, 1992.
15. Delahaye F, Breton C, Risold PY, Enache M, Dutriez-Casteloot I, Laborie C, Lesage J, Vieau D. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology 149: 470-475, 2008.
16. De Matteis R, Ricquier D, Cinti S. Th-, NPY-, SP-, and CGRP-immunoreactive nerves in interscapular brown adipose tissue of adult rats acclimated at different temperatures: an immunohistochemical study. J Neurocytol 27: 877-886, 1998.
17. Desai M, Gayle D, Han G, Ross MG. Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reprod Sci 14: 329-337, 2007.
18. Gluckman PD, Hanson MA, Spencer HG, Bateson P. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc Biol Sci 272: 671-677, 2005.
19. Granneman JG, Li P, Zhu Z, Lu Y. Metabolic and cellular plasticity in white adipose tissue. I. Effects of beta 3-adrenergic receptor activation. Am J Physiol Endocrinol Metab 289: E608-E616, 2005.
20. Guan H, Arany E, van Beek JP, Chamson-Reig A, Thyssen S, Hill DJ, Yang K. Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal protein-restricted rats. Am J Physiol Endocrinol Metab 288: E663-E6673, 2005.
21. Guerra C, Koza RA, Yamashita H, Walsh K, Kozak L. Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity. J Clin Invest 102: 412-420, 1998.
22. Hauner H, Schmid P, Pfeiffer EF. Glucocorticoids and insulin promote the differentiation of human adipocyte precursor cells into fat cells. J Clin Endocrinol Metab 64: 832-835, 1987.
23. Himms-Hagen J, Melnyk A, Zingaretti MC, Ceresi E, Barbatelli G, Cinti S. Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol 279: C670-C681, 2000.
24. Huan JN, Li J, Han Y, Chen K, Wu N, Zhao AZ. Adipocyte-selective reduction of the leptin receptors induced by antisense RNA leads to increased adiposity, dyslipidemia, and insulin resistance. J Biol Chem 278: 45638-45650, 2003.
25. Kakuma T, Wang ZW, Pan W, Unger RH, Zhou YT. Role of leptin in peroxisome proliferator-activated receptor gamma coactivator-1 expression. Endocrinology 141: 4576-4582, 2000.
26. Kim S, Moustaid-Moussa N. Secretory, endocrine and autocrine/paracrine function of the adipocyte. J Nutr 130: 3110S-3115S, 2000.
27. Klaus S, Ely M, Encke D, Heldmaier G. Functional assessment of white and brown adipocyte development and energy metabolism in cell culture. Dissociation of terminal differentiation and thermogenesis in brown adipocytes. J Cell Sci 108: 3171-3180, 1995.
28. Kos K, Harte AL, James S, Snead DR, O'Hare JP, McTernan PG, Kumar S. Secretion of neuropeptide Y in human adipose tissue and its role in maintenance of adipose tissue mass. Am J Physiol Endocrinol Metab 293: E1335-E1340, 2007.
29. Kuo LE, Kitlinska JB, Tilan JU, Li L, Baker SB, Johnson MD, Lee EW, Burnett MS, Fricke ST, Kvetnansky R, Herzog H, Zukowska Z. Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome. Nat Med 13: 803-811, 2007.
30. Lehr L, Canola K, Léger B, Giacobino JP. Differentiation and characterization in primary culture of white adipose tissue brown adipocyte-like cells. Int J Obes 33: 680-686, 2009.
31. Léonhardt M, Lesage J, Dufourny L, Dickes-Coopman A, Montel V, Dupouy JP. Perinatal maternal food restriction induces alterations in hypothalamo-pituitary-adrenal axis activity and in plasma corticosterone-binding globulin capacity of weaning rat pups. Neuroendocrinology 75: 45-54, 2002.
32. Lopez M, Seoane LM, Tovar S, Garcia MC, Nogueiras R, Dieguez C, Senaris RM. A possible role of neuropeptide Y, agouti-related protein and leptin receptor isoforms in hypothalamic programming by perinatal feeding in the rat. Diabetologia 48: 140-148, 2005.
33. Lumbers ER, Yu ZY, Gibson KJ. The selfish brain and the Barker hypothesis. Clin Exp Pharmacol Physiol 28: 942-947, 2001.
34. Molendi-Coste O, Grumolato L, Laborie C, Lesage J, Maubert E, Ghzili H, Vaudry H, Anouar Y, Breton C, Vieau D. Maternal perinatal undernutrition alters neuronal and neuroendocrine differentiation in the rat adrenal medulla at weaning. Endocrinology 147: 3050-3059, 2006.
35. Mullier A, Bouret SG, Prévot V, Dehouck B. Differential distribution of tight junction proteins suggests a role for tanycytes in blood-hypothalamus barrier regulation in the adult mouse brain. J Comp Neurol 518: 943-962, 2010.
36. Norsted E, Gömüç B, Meister B. Protein components of the blood-brain barrier (BBB) in the mediobasal hypothalamus. J Chem Neuroanat 36: 107-121, 2008.
37. Plagemann A, Harder T, Melchior K, Rake A, Rohde W, Dörner G. Elevation of hypothalamic neuropeptide Y neurons in adult offspring of diabetic mother rats. Neuroreport 10: 3211-3216, 1999.
38. Plagemann A, Harder T, Rake A, Janert U, Melchior K, Rohde W, Dörner G. Morphological alterations of hypothalamic nuclei due to intrahypothalamic hyperinsulinism in newborn rats. Int J Dev Neurosci 17: 37-44, 1999.
39. Plagemann A, Harder T, Rake A, Waas T, Melchior K, Rohde W, Dörner G. Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 130: 2582-2589, 2000.
40. Plagemann A, Waas T, Harder T, Rittel F, Ziska T, Rohde W. Hypothalamic neuropeptide Y levels in weaning offspring of low-protein malnourished mother rats. Neuropeptides 34: 1-6, 2000.
41. Rajakumar PA, He J, Simmons RA, Devaskar SU. Effects of uteroplacental insufficiency upon brain neuropeptide Y and corticotrophin-releasing factor gene expression and concentrations. Pediatr Res 44: 168-174, 1998.
42. Remacle C, Bieswal F, Reusens B. Programming of obesity and cardiovascular disease. Int J Obes Relat Metab Disord 3: S46-S53, 2004.
43. Rodriguez EM, Blazquez JL, Guerra M. The design of barriers in the hypothalamus allows the median eminence and the arcuate nucleus to enjoy private milieus: the former opens to the portal blood and the latter to the cerebrospinal fluid. Peptides 31: 757-776, 2010.
44. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scimè A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM. PRDM16 controls a brown fat/skeletal muscle switch. Nature 45: 961-967, 2008.
45. Siegrist-Kaiser CA, Pauli V, Juge-Aubry CE, Boss O, Pernin A, Chin WW, Cusin I, Rohner-Jeanrenaud F, Burger AG, Zapf J, Meier CA. Direct effects of leptin on brown and white adipose tissue. J Clin Invest 100: 2858-2864, 1997.
46. Simmons R. Developmental origins of adult metabolic disease. Endocrinol Metab Clin North Am 35: 193-204, 2006.
47. Simon MA, Calle C. Adrenergic receptors are not mediators in the lipolytic effect of somatostatin in rat adipocytes. Life Sci 41: 2411-2417, 1987.
48. Sinclair KD, Lea RG, Rees WD, Young LE. The developmental origins of health and disease: current theories and epigenetic mechanisms. Soc Reprod Fertil Suppl 64: 425-443, 2007.
49. Skala J, Barnard T, Lindberg O. Changes in interscapular brown adipose tissue of the rat during perinatal and early postnatal development and after cold acclimatation. II. Mitochondrial changes. Comp Biochem Physiol 33: 509-528, 1970.
50. Song CK, Schwartz GJ, Bartness TJ. Anterograde transneuronal viral tract tracing reveals central sensory circuits from white adipose tissue. Am J Physiol Regul Integr Comp Physiol 296: R501-R511, 2009.
51. Symonds ME, Mostyn A, Pearce S, Budge H, Stephenson T. Endocrine and nutritional regulation of fetal adipose tissue development. J Endocrinol 179: 293-299, 2003.
52. Tiraby C, Tavernier G, Lefort C, Larrouy D, Bouillaud F, Ricquier D, Langin D. Acquirement of brown fat cell features by human white adipocytes. J Biol Chem 278: 33370-33376, 2003.
53. Valet P, Berlan M, Beauville M, Crampes F, Montastruc JL, Lafontan M. Neuropeptide Y and peptide YY inhibit lipolysis in human and dog fat cells through a pertussis toxin-sensitive G protein. J Clin Invest 85: 291-295, 1990.
54. Waki H, Tontonoz P. Endocrine functions of adipose tissue. Annu Rev Pathol 2: 31-56, 2007.
55. Wang P, Mariman E, Renes J, Keijer J. The secretory function of adipocytes in the physiology of white adipose tissue. J Cell Physiol 216: 3-13, 2008.
56. Xue B, Rim JS, Hogan JC, Coulter AA, Koza RA, Kozak LP. Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. J Lipid Res 48: 41-51, 2007.
57. Yang K, Guan H, Arany E, Hill DJ, Cao X. Neuropeptide Y is produced in visceral tissue and promotes proliferation of adipocyte precursor cells via the Y1 receptor. FASEB J 22: 2452-2464, 2008.
58. Yang YS, Song HD, Li RY, Zhou LB, Zhu ZD, Hu RM, Han ZG, Chen JL. The gene expression profiling of human visceral adipose tissue and its secretory functions. Biochem Biophys Res Commun 300: 839-846, 2003.
59. Young P, Arch JR, Ashwell M. Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Lett 167: 10-14, 1984.
60. Zhang T, Guan H, Arany E, Hill DJ, Yang K. Maternal protein restriction permanently programs adipocyte growth and development in adult male rat offspring. J Cell Biochem 101: 381-388, 2007.