Long-term hypoxia modulates expression of key genes regulating adipose function in the late-gestation ovine fetus

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 294, Issue 4, 2008, Pages

  Myers, Dean A ^a   Hanson, Krista ^a   Mlynarczyk, Malgorzata ^b   Kaushal, Kanchan M ^b   Ducsay, Charles A ^b  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b LOMA LINDA UNIVERSITY   (United States)

Author keywords

Cortisol; Uncoupling protein

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; BETA 3 ADRENERGIC RECEPTOR; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; THYROID HORMONE; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FETUS; FETUS HYPOXIA; GENE EXPRESSION REGULATION; NONHUMAN; NONSHIVERING THERMOGENESIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEEP;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ABDOMINAL FAT; ACCLIMATIZATION; ALTITUDE; ANIMALS; ANOXIA; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GESTATIONAL AGE; HYDROCORTISONE; IODIDE PEROXIDASE; ION CHANNELS; MITOCHONDRIAL PROTEINS; PPAR ALPHA; PPAR GAMMA; PREGNANCY; RECEPTORS, ADRENERGIC, BETA-3; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; SHEEP; THERMOGENESIS; TIME FACTORS;

EID: 41749107727     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00004.2008     Document Type: Article

References (43)

1. Adachi K, Umezaki H, Kaushal KM, Ducsay CA. Long-term hypoxia alters ovine fetal endocrine and physiological responses to hypotension. Am J Physiol Regul Integr Comp Physiol 287: R209-R217, 2004.
2. Araki O, Morimura T, Ogiwara T, Mizuma H, Mori M, Murakami M. Expression of type 2 iodothyronine deiodinase in corticotropin-secreting mouse pituitary tumor cells is stimulated by glucocorticoid and corticotropin- releasing hormone. Endocrinology 144: 4459-4465, 2003.
3. Barbera MJ, Schluter A, Pedraza N, Iglesias R, Villarroya F, Giralt M. Peroxisome proliferator-activated receptor alpha 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.
4. Berger JP. Role of PPARγ, transcriptional cofactors, and adiponectin in the regulation of nutrient metabolism, adipogenesis and insulin action: view from the chair. Int J Obes Relat Metab Disord 29: S3-S4, 2005.
5. Bianco AC, Kim BW. Deiodinases: implications of the local control of thyroid hormone action. J Clin Invest 116: 2571-2579, 2006.
6. Brand MD, Esteves TC. Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab 2: 85-93, 2004.
7. Cannon B, Nedergaard JAN. Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359, 2004.
8. Cassard-Doulcier AM, Gelly C, Bouillaud F, Ricquier D. A 211-bp enhancer of the rat uncoupling protein-1 (UCP-1) gene controls specific and regulated expression in brown adipose tissue. Biochem J 333: 243-246, 1998.
9. Casteilla L, Forest C, Robelin J, Ricquier D, Lombet A, Ailhaud G. Characterization of mitochondrial-uncoupling protein in bovine fetus and newborn calf. Am J Physiol Endocrinol Metab 252: E627-E636, 1987.
10. Clarke I, Heasman L, Symonds ME. Influence of maternal dexamethasone administration on thermoregulation in lambs delivered by caesarean section. J Endocrinol 156: 307-314, 1998.
11. Clarke L, Bryant MJ, Lomax MA, Symonds ME. Maternal manipulation of brown adipose tissue and liver development in the ovine fetus during late gestation. Br J Nutr 77: 781-883, 1997.
12. Clarke L, Buss DS, Juniper DT, Lomax MA, Symonds ME. Adipose tissue development during early postnatal life in ewe-reared lambs. Exp Physiol 82: 1015-1027, 1997.
13. Clarke L, Heasman L, Firth K, Symonds ME. Influence of route of delivery and ambient temperature on thermoregulation in newborn lambs. Am J Physiol Regul Integr Comp Physiol 272: R1931-R1939, 1997.
14. De Vos P, Saladin R, Auwerx J, Staels B. Induction of ob gene expression by corticosteroids is accompanied by body weight loss and reduced food intake. J Biol Chem 270: 15958-15961, 1995.
15. Devaskar SU, Anthony R, Hay W Jr. Ontogeny and insulin regulation of fetal ovine white adipose tissue leptin expression. Am J Physiol Regul Integr Comp Physiol 282: R431-R438, 2002.
16. Ducsay CA, Hyatt K, Mlynarczyk M, Kaushal KM, Myers DA. Long-term hypoxia increases leptin receptors and plasma leptin concentrations in the late-gestation ovine fetus. Am J Physiol Regul Integr Comp Physiol 291: R1406-R1413, 2006.
17. Gnanalingham MG, Giussani DA, Sivathondan P, Forhead AJ, Stephenson T, Symonds ME, Gardner DS. Chronic umbilical cord compression results in accelerated maturation of lung and brown adipose tissue in the sheep fetus during late gestation. Am J Physiol Endocrinol Metab 289: E456-E465, 2005.
18. Gnanalingham MG, Mostyn A, Forhead AJ, Fowden AL, Symonds ME, Stephenson T. Increased uncoupling protein-2 mRNA abundance and glucocorticoid action in adipose tissue in the sheep fetus during late gestation is dependent on plasma cortisol and triiodothyronine. J Physiol 567: 283-292, 2005.
19. Gnanalingham MG, Mostyn A, Symonds ME, Stephenson T. Ontogeny and nutritional programming of adiposity in sheep: potential role of glucocorticoid action and uncoupling protein-2. Am J Physiol Regul Integr Comp Physiol 289: R1407-R1415, 2005.
20. Granneman JG, Burnazi M, Zhu Z, Schwamb LA. White adipose tissue contributes to UCP1-independent thermogenesis. Am J Physiol Endocrinol Metab 285: E1230-E1236, 2003.
21. Grujic D, Susulic VS, Harper ME, Himms-Hagen J, Cunningham BA, Corkey BE, Lowell BB. β3-Adrenergic receptors on white and brown adipocytes mediate β3-selective agonist-induced effects on energy expenditure, insulin secretion, and food intake. A study using transgenic and gene knockout mice. J Biol Chem 272: 17686-17693, 1997.
22. Guerra C, Roncero C, Porras A, Fernandez M, Benito M. Triiodothyronine induces the transcription of the uncoupling protein gene and stabilizes its mRNA in fetal rat brown adipocyte primary cultures. J Biol Chem 271: 2076-2081, 1996.
23. Harvey LM, Gilbert RD, Longo LD, Ducsay CA. Changes in ovine fetal adrenocortical responsiveness after long-term hypoxemia. Am J Physiol Endocrinol Metab 264: E741-E747, 1993.
24. Imamura T, Umezak iH, Kaushal KM, Ducsay CA. Long-term hypoxia alters endocrine and physiological responses to umbilical cord occlusion in the ovine fetus. J Soc Gynecol Invest 11: 131-140, 2004.
25. Ip MS, Lam KS, Ho C, Tsang KW, Lam W. Serum leptin and vascular risk factors in obstructive sleep apnea. Chest 118: 580-586, 2000.
26. Kato A, Umezak iH, Imamura T, Kaushal KM, Mlynarczyk M, Gilbert RD, Buccholz J, Longo LD, Ducsay CA. Catecholamine and cardiovascular responses to superimposed hypoxia following carotid body denervation in the long-term hypoxemic ovine fetus. In: Proceedings of the Forty-ninth Annual Meeting of the Society for Gynecologic Investigation Abstract Volume 380: 21, 2002.
27. Kelly LJ, Vicario PP, Thompson GM, Candelore MR, Doebber TW, Ventre J, Wu MS, Meurer R, Forrest MJ, Conner MW, Cascieri MA, Moller DE. Peroxisome proliferator-activated receptors γ and α mediate in vivo regulation of uncoupling protein (UCP-1, UCP-2, UCP-3) gene expression. Endocrinology 139: 4920-4927, 1998.
28. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W. Peroxisome proliferatorñactivated receptor α mediates the adaptive response to fasting. J Clin Invest 103: 1489-1498, 1999.
29. Masaki T, Yoshimichi G, Chiba S, Yasuda T, Noguchi H, Kakuma T, Sakata T, Yoshimatsu H. Corticotropin-releasing hormone-mediated pathway of leptin to regulate feeding, adiposity, and uncoupling protein expression in mice. Endocrinology 144: 3547-3554, 2003.
30. Mostyn A, Pearce S, Budge H, Elmes M, Forhead AJ, Fowden AL, Stephenson T, Symonds ME. Influence of cortisol on adipose tissue development in the fetal sheep during late gestation. J Endocrinol 176: 23-30, 2003.
31. Mostyn A, Pearce S, Stephenson T, Symonds ME. Hormonal and nutritional regulation of adipose tissue development and function in the newborn. Exp Clin Endocrinol Diabetes 112: 2-9, 2004.
32. Muzzin P, Revelli JP, Kuhne F, Gocayne JD, McCombie WR, Venter JC, Giacobino JP, Fraser CM. An adipose tissue-specific beta-adrenergic receptor. Molecular cloning and down-regulation in obesity. J Biol Chem 266: 24053-24058, 1991.
33. Myers DA, Bell PA, Hyatt K, Mlynarczyk M, Ducsay CA. Long-term hypoxia enhances proopiomelanocortin processing in the near-term ovine fetus. Am J Physiol Regul Integr Comp Physiol 288: R1178-R1184, 2005.
34. Myers DA, Hyatt K, Mlynarczyk M, Bird IM, Ducsay CA. Long-term hypoxia represses the expression of key genes regulating cortisol biosynthesis in the near-term ovine fetus. Am J Physiol Regul Integr Comp Physiol 289: R1707-R1714, 2005.
35. Pearce S, Mostyn A, Alves-Guerra MC, Pecqueur C, Miroux B, Webb R, Stephenson T, Symond M. Prolactin, prolactin receptor and uncoupling proteins during fetal and neonatal development. Proc Nutr Soc 62: 421-427, 2003.
36. Polotsky VY, Li J, Punjabi NM, Rubin AE, Smith PL, Schwartz AR, O'Donnell CP. Intermittent hypoxia increases insulin resistance in genetically obese mice. J Physiol 552: 253-264, 2003.
37. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839, 1998.
38. Rosen ED, Spiegelman BM. PPARγ: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 276: 37731-37734, 2001.
39. Scarpace PJ, Matheny M. Leptin induction of UCP1 gene expression is dependent on sympathetic innervation. Am J Physiol Endocrinol Metab 275: E259-E264, 1998.
40. 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.
41. Tschop M, Strasburger CJ, Hartmann G, Biollaz J, Bartsch P. Raised leptin concentrations at high altitude associated with loss of appetite. Lancet 352: 1119-1120, 1998.
42. Villarroya F, Iglesias R, Giralt M. PPARs in the control of uncoupling proteins gene expression (Online). PPAR Research Volume 2007 (2007), 12 pages, doi:10.1155/2007/74364.2007.
43. Yuen BSJ, Owens PC, Muhlhausler BS, Roberts CT, Symonds ME, Keisler DH, McFarlane JR, Kauter KG, Evens Y, McMillen IC. Leptin alters the structural and functional characteristics of adipose tissue before birth. FASEB J 17: 1102-1104, 2003.