Beige differentiation of adipose depots in mice lacking prolactin receptor protects against high-fat-dietinduced obesity

FASEB Journal

Volumn 26, Issue 9, 2012, Pages 3728-3737

  Auffret, Julien ^a,b   Viengchareun, Say ^a,b   Carré, Nadège ^a,b   Denis, Raphaël G P ^c   Magnan, Christophe ^c   Marie, Pierre Yves ^d   Muscat, Adeline ^e   Fève, Bruno ^e   Lombès, Marc ^a,b,f   Binart, Nadine ^a,b,f  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITY HOSPITAL OF NANCY   (France)

^e CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^f BICÊTRE HOSPITAL   (France)

Author keywords

Adipocyte; Thermogenesis

Indexed keywords

FAT; PROLACTIN RECEPTOR; TRANSCRIPTION FACTOR FOXC2;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BROWN ADIPOSE TISSUE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; ENERGY BALANCE; ENERGY EXPENDITURE; GENE EXPRESSION; KIDNEY; LIPID DIET; LIPID STORAGE; METABOLIC RATE; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; SUBCUTANEOUS TISSUE;

ADIPOSE TISSUE, BROWN; ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CELL DIFFERENTIATION; DIETARY FATS; DNA PRIMERS; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; OBESITY; POSITRON-EMISSION TOMOGRAPHY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, PROLACTIN; THERMOGENESIS;

MUS; RODENTIA;

EID: 84865781554     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-204958     Document Type: Article

References (49)

1. Bole-Feysot, C., Goffin, V., Edery, M., Binart, N., and Kelly, P. A. (1998) Prolactin and its receptor: actions, signal transduction pathways and phenotypes observed in prolactin receptor knockout mice. Endocr. Rev. 19, 225-268
2. Goffin, V., Binart, N., Touraine, P., and Kelly, P. A. (2002) Prolactin: the new biology of an old hormone. Annu. Rev. Physiol. 64, 47-67
3. Ben Jonathan, N., Lapensee, C. R., and Lapensee, E. W. (2008) What can we learn from rodents about prolactin in humans? Endocr. Rev. 29, 1-41
4. Clevenger, C. V., Gadd, S. L., and Zheng, J. (2009) New mechanisms for PRLr action in breast cancer Trends Endocrinol. Metab. 20, 223-229
5. Binart, N., Bachelot, A., and Bouilly, J. (2010) Impact of prolactin receptor isoforms on reproduction. Trends Endocrinol. Metab. 21, 362-368
6. Freemark, M., Fleenor, D., Driscoll, P., Binart, N., and Kelly, P. A. (2001) Body weight and fat deposition in prolactin receptor-deficient mice. Endocrinology 142, 532-537
7. Fleenor, D., Oden, J., Kelly, P. A., Mohan, S., Alliouachene, S., Pende, M., Wentz, S., Kerr, J., and Freemark, M. (2005) Roles of the lactogens and somatogens in perinatal and postnatal metabolism and growth: studies of a novel mouse model combining lactogen resistance and growth hormone deficiency. Endocrinology 146, 103-112
8. Flint, D. J., Binart, N., Boumard, S., Kopchick, J. J., and Kelly, P. (2006) Developmental aspects of adipose tissue in GH receptor and prolactin receptor gene disrupted mice: site-specific effects upon proliferation, differentiation and hormone sensitivity. J. Endocrinol. 191, 101-111
9. Dos Santos Silva, C. M., Barbosa, F. R., Lima, G. A., Warszawski, L., Fontes, R., Domingues, R. C., and Gadelha, M. R. (2010) BMI and metabolic profile in patients with prolactinoma before and after treatment with dopamine agonists. Obesity (Silver Spring) 19, 800-805
10. Kok, P., Roelfsema, F., Frolich, M., van Pelt, J., Stokkel, M. P., Meinders, A. E., and Pijl, H. (2006) Activation of dopamine D2 receptors simultaneously ameliorates various metabolic features of obese women. Am. J. Physiol. Endocrinol. Metab. 291, E1038-E1043
11. Nanbu-Wakao, R., Fujitani, Y., Masuho, Y., Muramatu, M., and Wakao, H. (2000) Prolactin enhances CCAAT enhancer-binding protein-beta (C/EBP beta) and peroxisome proliferatoractivated receptor gamma (PPAR gamma) messenger RNA expression and stimulates adipogenic conversion of NIH-3T3 cells. Mol. Endocrinol. 14, 307-316
12. Brandebourg, T. D., Bown, J. L., and Ben Jonathan, N. (2007) Prolactin upregulates its receptors and inhibits lipolysis and leptin release in male rat adipose tissue. Biochem. Biophys. Res. Commun. 357, 408-413
13. Viengchareun, S., Bouzinba-Segard, H., Laigneau, J. P., Zennaro, M. C., Kelly, P. A., Bado, A., Lombes, M., and Binart, N. (2004) Prolactin potentiates insulin-stimulated leptin expression and release from differentiated brown adipocytes. J. Mol. Endocrinol. 33, 679-691
14. Viengchareun, S., Servel, N., Feve, B., Freemark, M., Lombes, M., and Binart, N. (2008) Prolactin receptor signaling is essential for perinatal brown adipocyte function: a role for insulinlike growth factor-2. PLoS ONE 3, e1535
15. Hugo, E. R., Borcherding, D. C., Gersin, K. S., Loftus, J., and Ben Jonathan, N. (2008) Prolactin release by adipose explants, primary adipocytes, and LS14 adipocytes. J. Clin. Endocrinol. Metab. 93, 4006-4012
16. Vegiopoulos, A., Muller-Decker, K., Strzoda, D., Schmitt, I., Chichelnitskiy, E., Ostertag, A., Berriel, D. M., Rozman, J., Hrabe, d. A., Nusing, R. M., Meyer, C. W., Wahli, W., Klingenspor, M., and Herzig, S. (2010) Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science 328, 1158-1161
17. Ishibashi, J., and Seale, P. (2010) Medicine. Beige can be slimming. Science 328, 1113-1114
18. Ormandy, C. J., Camus, A., Barra, J., Damotte, D., Lucas, B. K., Buteau, H., Edery, M., Brousse, N., Babinet, C., Binart, N., and Kelly, P. A. (1997) Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev. 11, 167-178
19. Carter, E. A., Bonab, A. A., Hamrahi, V., Pitman, J., Winter, D., Macintosh, L. J., Cyr, E. M., Paul, K., Yerxa, J., Jung, W., Tompkins, R. G., and Fischman, A. J. (2011) Effects of burn injury, cold stress and cutaneous wound injury on the morphology and energy metabolism of murine brown adipose tissue (BAT) in vivo. Life Sci. 89, 78-85
20. Fueger, B. J., Czernin, J., Hildebrandt, I., Tran, C., Halpern, B. S., Stout, D., Phelps, M. E., and Weber, W. A. (2006) Impact of animal handling on the results of 18F-FDG PET studies in mice. J. Nucl. Med. 47, 999-1006
21. Cannon, B., and Nedergaard, J. (2004) Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359
22. Seale, P., Conroe, H. M., Estall, J., Kajimura, S., Frontini, A., Ishibashi, J., Cohen, P., Cinti, S., and Spiegelman, B. M. (2011) Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J. Clin. Invest. 121, 96-105
23. Ohno, H., Shinoda, K., Spiegelman, B. M., and Kajimura, S. (2012) PPARgamma agonists induce a white-to-brown fat conversion through stabilization of PRDM16 protein. Cell Metab. 15, 395-404
24. Schroeder, M. D., Symowicz, J., and Schuler, L. A. (2002) PRL modulates cell cycle regulators in mammary tumor epithelial cells. Mol. Endocrinol. 16, 45-57
25. Calo, E., Quintero-Estades, J. A., Danielian, P. S., Nedelcu, S., Berman, S. D., and Lees, J. A. (2010) Rb regulates fate choice and lineage commitment in vivo. Nature 466, 1110-1114
26. Lidell, M. E., Seifert, E. L., Westergren, R., Heglind, M., Gowing, A., Sukonina, V., Arani, Z., Itkonen, P., Wallin, S., Westberg, F., Fernandez-Rodriguez, J., Laakso, M., Nilsson, T., Peng, X. R., Harper, M. E., and Enerback, S. (2011) The adipocyte-expressed forkhead transcription factor Foxc2 regulates metabolism through altered mitochondrial function. Diabetes 60, 427-435
27. Seale, P., and Lazar, M. A. (2009) Brown fat in humans: turning up the heat on obesity. Diabetes 58, 1482-1484
28. Kajimura, S., Seale, P., and Spiegelman, B. M. (2010) Transcriptional control of brown fat development. Cell Metab. 11, 257-262
29. Barbatelli, G., Murano, I., Madsen, L., Hao, Q., Jimenez, M., Kristiansen, K., Giacobino, J. P., De Matteis, R., and Cinti, S. (2010) The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am. J. Physiol. Endocrinol. Metab. 298, E1244-E1253
30. Schulz, T. J., Huang, T. L., Tran, T. T., Zhang, H., Townsend, K. L., Shadrach, J. L., Cerletti, M., McDougall, L. E., Giorgadze, N., Tchkonia, T., Schrier, D., Falb, D., Kirkland, J. L., Wagers, A. J., and Tseng, Y. H. (2011) Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proc. Natl. Acad. Sci. U. S. A. 108, 143-148
31. Seale, P., Kajimura, S., Yang, W., Chin, S., Rohas, L. M., Uldry, M., Tavernier, G., Langin, D., and Spiegelman, B. M. (2007) Transcriptional control of brown fat determination by PRDM16. Cell Metab. 6, 38-54
32. Kajimura, S., Seale, P., Tomaru, T., Erdjument-Bromage, H., Cooper, M. P., Ruas, J. L., Chin, S., Tempst, P., Lazar, M. A., and Spiegelman, B. M. (2008) Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev. 22, 1397-1409
33. Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scime, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H., Tempst, P., Rudnicki, M. A., Beier, D. R., and Spiegelman, B. M. (2008) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967
34. Scime, A., Grenier, G., Huh, M. S., Gillespie, M. A., Bevilacqua, L., Harper, M. E., and Rudnicki, M. A. (2005) Rb and p107 regulate preadipocyte differentiation into white versus brown fat through repression of PGC-1alpha. Cell Metab. 2, 283-295
35. Toh, S. Y., Gong, J., Du, G., Li, J. Z., Yang, S., Ye, J., Yao, H., Zhang, Y., Xue, B., Li, Q., Yang, H., Wen, Z., and Li, P. (2008) Up-regulation of mitochondrial activity and acquirement of brown adipose tissue-like property in the white adipose tissue of fsp27 deficient mice. PLoS ONE 3, e2890
36. Hansen, J. B., Jorgensen, C., Petersen, R. K., Hallenborg, P., De Matteis, R., Boye, H. A., Petrovic, N., Enerback, S., Nedergaard, J., Cinti, S., te Riele, H., and Kristiansen, K. (2004) Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 101, 4112-4117
37. Cederberg, A., Gronning, L. M., Ahren, B., Tasken, K., Carlsson, P., and Enerback, S. (2001) FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell 106, 563-573
38. Nybroe, O., Rosenkilde, P., and Ryttersgaard, L. (1985) Effects of hypophysectomy and substitution with growth hormone, prolactin, and thyroxine on growth and deposition in juvenile frogs, Xenopus laevis. Gen. Comp. Endocrinol. 57, 257-265
39. Roy, A. F., Benomar, Y., Bailleux, V., Vacher, C. M., Aubourg, A., Gertler, A., Djiane, J., and Taouis, M. (2007) Lack of cross-desensitization between leptin and prolactin signaling pathways despite the induction of suppressor of cytokine signaling 3 and PTP-1B. J. Endocrinol. 195, 341-350
40. Lisboa, P. C., Passos, M. C., Dutra, S. C., Bonomo, I. T., Denolato, A. T., Reis, A. M., and Moura, E. G. (2006) Leptin and prolactin, but not corticosterone, modulate body weight and thyroid function in protein-malnourished lactating rats. Horm. Metab. Res. 38, 295-299
41. Meyre, D., Delplanque, J., Chevre, J. C., Lecoeur, C., Lobbens, S., Gallina, S., Durand, E., Vatin, V., Degraeve, F., Proenca, C., Gaget, S., Korner, A., Kovacs, P., Kiess, W., Tichet, J., Marre, M., Hartikainen, A. L., Horber, F., Potoczna, N., Hercberg, S., Levy-Marchal, C., Pattou, F., Heude, B., Tauber, M., McCarthy, M. I., Blakemore, A. I., Montpetit, A., Polychronakos, C., Weill, J., Coin, L. J., Asher, J., Elliott, P., Jarvelin, M. R., Visvikis-Siest, S., Balkau, B., Sladek, R., Balding, D., Walley, A., Dina, C., and Froguel, P. (2009) Genome-wide association study for early-onset and morbid adult obesity identifies three new risk loci in European populations. Nat. Genet. 41, 157-159
42. Nilsson, L., Olsson, A. H., Isomaa, B., Groop, L., Billig, H., and Ling, C. (2011) A common variant near the PRL gene is associated with increased adiposity in males. Mol. Genet. Metab. 102, 78-81
43. Kok, P., Roelfsema, F., Frolich, M., Meinders, A. E., and Pijl, H. (2004) Prolactin release is enhanced in proportion to excess visceral fat in obese women. J. Clin. Endocrinol. Metab. 89, 4445-4449
44. Dos Santos Silva, C. M., Barbosa, F. R., Lima, G. A., Warszawski, L., Fontes, R., Domingues, R. C., and Gadelha, M. R. (2011) BMI and metabolic profile in patients with prolactinoma before and after treatment with dopamine agonists. Obesity 19, 800-805
45. Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., Savisto, N. J., Enerback, S., and Nuutila, P. (2009) Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525
46. Marken Lichtenbelt, W. D., Vanhommerig, J. W., Smulders, N. M., Drossaerts, J. M., Kemerink, G. J., Bouvy, N. D., Schrauwen, P., and Teule, G. J. (2009) Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 360, 1500-1508
47. Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y. H., Doria, A., Kolodny, G. M., and Kahn, C. R. (2009) Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517
48. Saito, M., Okamatsu-Ogura, Y., Matsushita, M., Watanabe, K., Yoneshiro, T., Nio-Kobayashi, J., Iwanaga, T., Miyagawa, M., Kameya, T., Nakada, K., Kawai, Y., and Tsujisaki, M. (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58, 1526-1531
49. Lee, P., Zhao, J. T., Swarbrick, M. M., Gracie, G., Bova, R., Greenfield, J. R., Freund, J., and Ho, K. K. (2011) High prevalence of brown adipose tissue in adult humans. J. Clin. Endocrinol. Metab. 96, 2450-2455