Improved metabolic regulation is associated with retinoblastoma protein gene haploinsufficiency in mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 308, Issue 2, 2015, Pages E172-E183

  Petrov, Petar D ^a   Ribot, Joan ^a   Palou, Andreu ^a   Bonet, M Luisa ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

Author keywords

Browning; Fat tolerance; Insulin sensitivity; Retinoblastoma

Indexed keywords

FATTY ACID; GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; LEPTIN; LIPID; RETINOBLASTOMA PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY FAT; BODY WEIGHT; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; FATTY ACID OXIDATION; FEMALE; GENE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GROUPS BY AGE; HAPLOINSUFFICIENCY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULINEMIA; LIPID BLOOD LEVEL; MALE; METABOLIC REGULATION; METABOLIC STRESS; MOUSE; NONHUMAN; NUTRITIONAL TOLERANCE; PRIORITY JOURNAL; RETINOBLASTOMA PROTEIN GENE; SKELETAL MUSCLE; WEANING; WHITE ADIPOSE TISSUE; WILD TYPE; ADIPOGENESIS; AGING; ANIMAL; BLOOD; BODY TEMPERATURE; C57BL MOUSE; CALORIC INTAKE; CALORIMETRY; GENE EXPRESSION PROFILING; GENETICS; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY;

ADIPOGENESIS; AGING; ANIMALS; BODY TEMPERATURE; CALORIMETRY, INDIRECT; ENERGY INTAKE; GENE EXPRESSION PROFILING; GLUCOSE TOLERANCE TEST; HAPLOINSUFFICIENCY; IMMUNOHISTOCHEMISTRY; INSULIN; LEPTIN; MALE; MICE; MICE, INBRED C57BL; RETINOBLASTOMA PROTEIN;

EID: 84921467633     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00308.2014     Document Type: Article

References (50)

1. Amengual J, Petrov P, Bonet ML, Ribot J, Palou A. Induction of carnitine palmitoyl transferase 1 and fatty acid oxidation by retinoic acid in HepG2 cells. Int J Biochem Cell Biol44: 2019–2027, 2012.
2. Annicotte JS, Blanchet E, Chavey C, Iankova I, Costes S, Assou S, Teyssier J, Dalle S, Sardet C, Fajas L. The CDK4-pRB-E2F1 pathway controls insulin secretion. Nat Cell Biol11: 1017–1023, 2009.
3. Astrup A, Raben A, Buemann B, Toubro S. Fat metabolism in the predisposition to obesity. Ann NY Acad Sci827: 417–430, 1997.
4. Blanchet E, Annicotte JS, Lagarrigue S, Aguilar V, Clape C, Chavey C, Fritz V, Casas F, Apparailly F, Auwerx J, Fajas L. E2F transcription factor-1 regulates oxidative metabolism. Nat Cell Biol13: 1146–1152, 2011.
5. Bonet ML, Oliver P, Palou A. Pharmacological and nutritional agents promoting browning of white adipose tissue. Biochim Biophys Acta1831: 969–985, 2013.
6. Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol94: 2467–2474, 1999.
7. Cai EP, Wu X, Schroer SA, Elia AJ, Nostro MC, Zacksenhaus E, Woo M. Retinoblastoma tumor suppressor protein in pancreatic progenitors controls alpha- and beta-cell fate. Proc Natl Acad Sci USA110: 14723– 14728, 2013.
8. Calo E, Quintero-Estades JA, Danielian PS, Nedelcu S, Berman SD, Lees JA. Rb regulates fate choice and lineage commitment in vivo. Nature466: 1110–1114, 2010.
9. Capasso S, Alessio N, Di Bernardo G, Cipollaro M, Melone MA, Peluso G, Giordano A, Galderisi U. Silencing of RB1 and RB2/P130 during adipogenesis of bone marrow stromal cells results in dysregulated differentiation. Cell Cycle13: 482–490, 2014.
10. Chen P, Riley DJ, Chen Y, Lee W. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs. Genes Dev10: 2794–2804, 1996.
11. Classon M, Kennedy BK, Mulloy R, Harlow E. Opposing roles of pRB and p107 in adipocyte differentiation. Proc Natl Acad Sci USA97: 10826–10831, 2000.
12. Dali-Youcef N, Mataki C, Coste A, Messaddeq N, Giroud S, Blanc S, Koehl C, Champy MF, Chambon P, Fajas L, Metzger D, Schoonjans K, Auwerx J. Adipose tissue-specific inactivation of the retinoblastoma protein protects against diabesity because of increased energy expenditure. Proc Natl Acad Sci USA104: 10703–10708, 2007.
13. Dieguez C, Vazquez MJ, Romero A, Lopez M, Nogueiras R. Hypo-thalamic control of lipid metabolism: focus on leptin, ghrelin and mela-nocortins. Neuroendocrinology94: 1–11, 2011.
14. Fajas L. Re-thinking cell cycle regulators: the cross-talk with metabolism (Abstract). Front Oncol3: 4, 2013.
15. Fajas L, Egler V, Reiter R, Hansen J, Kristiansen K, Debril MB, Miard S, Auwerx J. The retinoblastoma-histone deacetylase 3 complex inhibits PPARgamma and adipocyte differentiation. Dev Cell3: 903–910, 2002.
16. Fajas L, Landsberg RL, Huss-Garcia Y, Sardet C, Lees JA, Auwerx J. E2Fs regulate adipocyte differentiation. Dev Cell3: 39–49, 2002.
17. Flachs P, Rossmeisl M, Kuda O, Kopecky J. Stimulation of mitochon-drial oxidative capacity in white fat independent of UCP1: a key to lean phenotype. Biochim Biophys Acta1831: 986–1003, 2013.
18. Gabriely I, Ma XH, Yang XM, Rossetti L, Barzilai N. Leptin resistance during aging is independent of fat mass. Diabetes51: 1016–1021, 2002.
19. Hansen JB, Jorgensen C, Petersen RK, Hallenborg P, De Matteis R, Boye HA, Petrovic N, Enerback S, Nedergaard J, Cinti S, te Riele H, Kristiansen K. Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation. Proc Natl Acad Sci USA 101: 4112–4117, 2004.
20. Hsieh MC, Das D, Sambandam N, Zhang MQ, Nahle Z. Regulation of the PDK4 isozyme by the Rb-E2F1 complex. J Biol Chem283: 27410– 27417, 2008.
21. Hsu SM, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem29: 577– 580, 1981.
22. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA. Effects of an Rb mutation in the mouse. Nature359: 295–300, 1992.
23. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature444: 840–846, 2006.
24. Konner AC, Bruning JC. Selective insulin and leptin resistance in metabolic disorders. Cell Metab16: 144–152, 2012.
25. Kranenburg O, van der Eb AJ, Zantema A. Cyclin-dependent kinases and pRb: regulators of the proliferation-differentiation switch. FEBS Lett367: 103–106, 1995.
26. Lu Z, Marcelin G, Bauzon F, Wang H, Fu H, Dun SL, Zhao H, Li X, Jo YH, Wardlaw S, Dun N, Chua S Jr, Zhu L. pRb is an obesity suppressor in hypothalamus and high-fat diet inhibits pRb in this location. Embo J32: 844–857, 2013.
27. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia28: 412–419, 1985.
28. Mercader J, Madsen L, Felipe F, Palou A, Kristiansen K, Bonet ML. All-trans retinoic acid increases oxidative metabolism in mature adi-pocytes. Cell Physiol Biochem20: 1061–1072, 2007.
29. Mercader J, Ribot J, Murano I, Feddersen S, Cinti S, Madsen L, Kristiansen K, Bonet ML, Palou A. Haploinsufficiency of the retino-blastoma protein gene reduces diet-induced obesity, insulin resistance, and hepatosteatosis in mice. Am J Physiol Endocrinol Metab297: E184–E193, 2009.
30. Mercader J, Ribot J, Murano I, Felipe F, Cinti S, Bonet ML, Palou A. Remodeling of white adipose tissue after retinoic acid administration in mice. Endocrinology147: 5325–5332, 2006.
31. Moreno-Navarrete JM, Petrov P, Serrano M, Ortega F, Garcia-Ruiz E, Oliver P, Ribot J, Ricart W, Palou A, Bonet ML, Fernandez-Real JM. Decreased RB1 mRNA, protein, and activity reflect obesity-induced altered adipogenic capacity in human adipose tissue. Diabetes62: 1923– 1931, 2013.
32. Perseghin G, Caumo A, Caloni M, Testolin G, Luzi L. Incorporation of the fasting plasma FFA concentration into QUICKI improves its association with insulin sensitivity in nonobese individuals. J Clin Endocrinol Metab86: 4776–4781, 2001.
33. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR (Abstract). Nucleic Acids Res29: e45, 2001.
34. Puigserver P, Nadal-Ginard B, Palou A. Expression and interaction of C/EBPalpha adipogenic transcription factor and retinoblastoma protein in adipocytes during differentiation (Abstract). Int J Obes Relat Metab Disord18: 113, 1994.
35. Puigserver P, Ribot J, Serra F, Gianotti M, Bonet ML, Nadal-Ginard B, Palou A. Involvement of the retinoblastoma protein in brown and white adipocyte cell differentiation: functional and physical association with the adipogenic transcription factor C/EBPalpha. Eur J Cell Biol77: 117–123, 1998.
36. Richon VM, Lyle RE, McGehee RE Jr. Regulation and expression of retinoblastoma proteins p107 and p130 during 3T3–L1 adipocyte differentiation. J Biol Chem272: 10117–10124, 1997.
37. Rodriguez-Sureda V, Peinado-Onsurbe J. A procedure for measuring triacylglyceride and cholesterol content using a small amount of tissue. Anal Biochem343: 277–282, 2005.
38. Rosenkilde M, Nordby P, Nielsen LB, Stallknecht BM, Helge JW. Fat oxidation at rest predicts peak fat oxidation during exercise and metabolic phenotype in overweight men. Int J Obes (Lond)34: 871–877, 2010.
39. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data (Abstract). Nucleic Acids Res37: e45, 2009.
40. Sanchez J, Priego T, Palou M, Tobaruela A, Palou A, Pico C. Oral supplementation with physiological doses of leptin during lactation in rats improves insulin sensitivity and affects food preferences later in life. Endocrinology149: 733–740, 2008.
41. Scarpace PJ, Zhang Y. Leptin resistance: a prediposing factor for diet-induced obesity. Am J Physiol Regul Integr Comp Physiol296: R493–R500, 2009.
42. Schrauwen P, Hesselink MK. The role of uncoupling protein 3 in fatty acid metabolism: protection against lipotoxicity? Proc Nutr Soc63: 287–292, 2004.
43. Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, Ishibashi J, Cohen P, Cinti S, Spiegelman BM. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest121: 96–105, 2011.
44. Steger G. Thermal denaturation of double-stranded nucleic acids: prediction of temperatures critical for gradient gel electrophoresis and polymer-ase chain reaction. Nucleic Acids Res22: 2760–2768, 1994.
45. Su JW, Nzekwu MM, Cabezas MC, Redgrave T, Proctor SD. Methods to assess impaired post-prandial metabolism and the impact for early detection of cardiovascular disease risk. Eur J Clin Invest 39: 741–754, 2009.
46. Sugden MC, Holness MJ. Mechanisms underlying regulation of the expression and activities of the mammalian pyruvate dehydrogenase kinases. Arch Physiol Biochem112: 139–149, 2006.
47. Thomas DM, Yang HS, Alexander K, Hinds PW. Role of the retino-blastoma protein in differentiation and senescence. Cancer Biol Ther2: 124–130, 2003.
48. Wajchenberg BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev21: 697–738, 2000.
49. Wang ZW, Pan WT, Lee Y, Kakuma T, Zhou YT, Unger RH. The role of leptin resistance in the lipid abnormalities of aging. FASEB J15: 108–114, 2001.
50. Zhang Y, Scarpace PJ. The role of leptin in leptin resistance and obesity. Physiol Behav88: 249–256, 2006.