Cell-Autonomous Brown-Like Adipogenesis of Preadipocytes From Retinoblastoma Haploinsufficient Mice

Journal of Cellular Physiology

Volumn 231, Issue 9, 2016, Pages 1941-1952

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

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARNITINE PALMITOYLTRANSFERASE I; CD137 ANTIGEN; FATTY ACID TRANSPORTER 4; HOXC9 PROTEIN; OSTEOGENIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PROTEIN PRDM16; PROTEIN SHOX2; PROTEIN TBX1; PROTEIN TMEM26; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADIPOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BROWN ADIPOCYTE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GLUCOSE TRANSPORT; HAPLOINSUFFICIENCY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN EXPRESSION; SIBLING; UPREGULATION; WHITE ADIPOSE TISSUE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION; GENETICS; HAPLOTYPE; KNOCKOUT MOUSE; METABOLISM; OBESITY; PHYSIOLOGY; RETINOBLASTOMA; THERMOGENESIS; TUMOR SUPPRESSOR GENE;

ADIPOCYTES, BROWN; ADIPOGENESIS; ADIPOSE TISSUE, WHITE; ANIMALS; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION; GENES, RETINOBLASTOMA; HAPLOTYPES; MALE; MICE; MICE, KNOCKOUT; OBESITY; PHENOTYPE; RETINOBLASTOMA; RETINOBLASTOMA PROTEIN; THERMOGENESIS; TRANSCRIPTION FACTORS;

EID: 84954290016     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25299     Document Type: Article

References (64)

1. Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, Eychmuller A, Gordts PL, Rinninger F, Bruegelmann K, Freund B, Nielsen P, Merkel M, Heeren J. 2011. Brown adipose tissue activity controls triglyceride clearance. Nat Med 17:200-205.
2. Bonet ML, Oliver P, Palou A. 2013. Pharmacological and nutritional agents promoting browning of white adipose tissue. Biochim Biophys Acta 1831:969-985.
3. Boon MR, van den Berg SA, Wang Y, van den Bossche J, Karkampouna S, Bauwens M, De Saint-Hubert M, van der Horst G, Vukicevic S, de Winther MP, Havekes LM, Jukema JW, Tamsma JT, van der Pluijm G, van Dijk KW, Rensen PC. 2013. BMP7 activates brown adipose tissue and reduces diet-induced obesity only at subthermoneutrality. PLoS ONE 8:e74083.
4. Cannon B, Nedergaard J. 2004. Brown adipose tissue: Function and physiological significance. Physiol Rev 84:277-359.
5. Cederberg A, Gronning LM, Ahren B, Tasken K, Carlsson P, Enerback S. 2001. FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell 106:563-573.
6. Cereijo R, Giralt M, Villarroya F. 2014. Thermogenic brown and beige/brite adipogenesis in humans. Ann Med 47:169-177.
7. Cohen P, Levy JD, Zhang Y, Frontini A, Kolodin DP, Svensson KJ, Lo JC, Zeng X, Ye L, Khandekar MJ, Wu J, Gunawardana SC, Banks AS, Camporez JP, Jurczak MJ, Kajimura S, Piston DW, Mathis D, Cinti S, Shulman GI, Seale P, Spiegelman BM. 2014. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 156:304-316.
8. Chaussepied M, Ginsberg D. 2005. E2F and signal transduction pathways. Cell Cycle 4:392-396.
9. 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. 2007. Adipose tissue-specific inactivation of the retinoblastoma protein protects against diabesity because of increased energy expenditure. Proc Natl Acad Sci USA 104:10703-10708.
10. Elsen M, Raschke S, Tennagels N, Schwahn U, Jelenik T, Roden M, Romacho T, Eckel J. 2014. BMP4 and BMP7 induce the white-to-brown transition of primary human adipose stem cells. Am J Physiol Cell Physiol 306:C431-C440.
11. Fajas L, Egler V, Reiter R, Hansen J, Kristiansen K, Debril MB, Miard S, Auwerx J. 2002. The retinoblastoma-histone deacetylase 3 complex inhibits PPARgamma and adipocyte differentiation. Dev Cell 3:903-910.
12. Fisher FM, Kleiner S, Douris N, Fox EC, Mepani RJ, Verdeguer F, Wu J, Kharitonenkov A, Flier JS, Maratos-Flier E, Spiegelman BM. 2012. FGF21 regulates PGC-1alpha and browning of white adipose tissues in adaptive thermogenesis. Genes Dev 26:271-281.
13. Gao CL, Liu GL, Liu S, Chen XH, Ji CB, Zhang CM, Xia ZK, Guo XR. 2012. Overexpression of PGC-1beta improves insulin sensitivity and mitochondrial function in 3T3-L1 adipocytes. Mol Cell Biochem 353:215-223.
14. Gubelmann C, Schwalie PC, Raghav SK, Roder E, Delessa T, Kiehlmann E, Waszak SM, Corsinotti A, Udin G, Holcombe W, Rudofsky G, Trono D, Wolfrum C, Deplancke B. 2014. Identification of the transcription factor ZEB1 as a central component of the adipogenic gene regulatory network. Elife 3:e03346.
15. 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. 2004. Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation. Proc Natl Acad Sci USA 101:4112-4117.
16. Hansen JB, Kristiansen K. 2006. Regulatory circuits controlling white versus brown adipocyte differentiation. Biochem J 398:153-168.
17. Harms M, Seale P. 2013. Brown and beige fat: Development, function and therapeutic potential. Nat Med 19:1252-1263.
18. Himms-Hagen J, Melnyk A, Zingaretti MC, Ceresi E, Barbatelli G, Cinti S. 2000. Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol 279:C670-C681.
19. Hollenberg AN, Susulic VS, Madura JP, Zhang B, Moller DE, Tontonoz P, Sarraf P, Spiegelman BM, Lowell BB. 1997. Functional antagonism between CCAAT/enhancer binding protein-alpha and peroxisome proliferator-activated receptor-gamma on the leptin promoter. J Biol Chem 272:5283-5290.
20. Ji H, Lu RH, Chang ZG, Su SS, Yang GS. 2011. PGC-1beta modulates the expression of genes involved in mitochondrial function and adipogenesis during preadipocyte differentiation. Reprod Domest Anim 47:419-427.
21. Jokinen R, Marttinen P, Sandell HK, Manninen T, Teerenhovi H, Wai T, Teoli D, Loredo-Osti JC, Shoubridge EA, Battersby BJ. 2010. Gimap3 regulates tissue-specific mitochondrial DNA segregation. PLoS Genet 6:e1001161.
22. Kajimura S, Seale P, Spiegelman BM. 2010. Transcriptional control of brown fat development. Cell Metab 11:257-262.
23. Karamanlidis G, Karamitri A, Docherty K, Hazlerigg DG, Lomax MA. 2007. C/EBPbeta reprograms white 3T3-L1 preadipocytes to a brown adipocyte pattern of gene expression. J Biol Chem 282:24660-24669.
24. Karnieli E, Armoni M. 2008. Transcriptional regulation of the insulin-responsive glucose transporter GLUT4 gene: From physiology to pathology. Am J Physiol Endocrinol Metab 295:E38-E45.
25. Koh YJ, Park BH, Park JH, Han J, Lee IK, Park JW, Koh GY. 2009. Activation of PPAR gamma induces profound multilocularization of adipocytes in adult mouse white adipose tissues. Exp Mol Med 41:880-895.
26. Lee KY, Yamamoto Y, Boucher J, Winnay JN, Gesta S, Cobb J, Bluher M, Kahn CR. 2013. Shox2 is a molecular determinant of depot-specific adipocyte function. Proc Natl Acad Sci USA 110:11409-11414.
27. Lee YH, Petkova AP, Mottillo EP, Granneman JG. 2012. In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding. Cell Metab 15:480-491.
28. Leonardsson G, Steel JH, Christian M, Pocock V, Milligan S, Bell J, So PW, Medina-Gomez G, Vidal-Puig A, White R, Parker MG. 2004. Nuclear receptor corepressor RIP140 regulates fat accumulation. Proc Natl Acad Sci USA 101:8437-8442.
29. Lidell ME, Seifert EL, Westergren R, Heglind M, Gowing A, Sukonina V, Arani Z, Itkonen P, Wallin S, Westberg F, Fernandez-Rodriguez J, Laakso M, Nilsson T, Peng XR, Harper ME, Enerback S. 2011. The adipocyte-expressed forkhead transcription factor Foxc2 regulates metabolism through altered mitochondrial function. Diabetes 60:427-435.
30. Long JZ, Svensson KJ, Tsai L, Zeng X, Roh HC, Kong X, Rao RR, Lou J, Lokurkar I, Baur W, Castellot JJ, Jr., Rosen ED, Spiegelman BM. 2014. A smooth muscle-like origin for beige adipocytes. Cell Metab 19:810-820.
31. Lundgren M, Svensson M, Lindmark S, Renstrom F, Ruge T, Eriksson JW. 2007. Fat cell enlargement is an independent marker of insulin resistance and 'hyperleptinaemia.' Diabetologia 50:625-633.
32. Mercader J, Madsen L, Felipe F, Palou A, Kristiansen K, Bonet ML. 2007. All-trans retinoic acid increases oxidative metabolism in mature adipocytes. Cell Physiol Biochem 20:1061-1072.
33. Mercader J, Palou A, Bonet ML. 2010. Induction of uncoupling protein-1 in mouse embryonic fibroblast-derived adipocytes by retinoic acid. Obesity (Silver Spring) 18:655-662.
34. Mercader J, Ribot J, Murano I, Feddersen S, Cinti S, Madsen L, Kristiansen K, Bonet ML, Palou A. 2009. Haploinsufficiency of the retinoblastoma protein gene reduces diet-induced obesity, insulin resistance, and hepatosteatosis in mice. Am J Physiol Endocrinol Metab 297:E184-E193.
35. Mercader J, Ribot J, Murano I, Felipe F, Cinti S, Bonet ML, Palou A. 2006. Remodeling of white adipose tissue after retinoic acid administration in mice. Endocrinology 147:5325-5332.
36. 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. 2013. Decreased RB1 mRNA, protein, and activity reflect obesity-induced altered adipogenic capacity in human adipose tissue. Diabetes 62:1923-1931.
37. Mossenbock K, Vegiopoulos A, Rose AJ, Sijmonsma TP, Herzig S, Schafmeier T. 2014. Browning of white adipose tissue uncouples glucose uptake from insulin signaling. PLoS ONE 9:e110428.
38. Oxburgh L. 2009. Control of the bone morphogenetic protein 7 gene in developmental and adult life. Curr Genomics 10:223-230.
39. Pan D, Fujimoto M, Lopes A, Wang YX. 2009. Twist-1 is a PPARdelta-inducible, negative-feedback regulator of PGC-1alpha in brown fat metabolism. Cell 137:73-86.
40. Petrov PD, Ribot J, Lopez-Mejia IC, Fajas L, Palou A, Bonet ML. 2016. Retinoblastoma protein knockdown favors oxidative metabolism and glucose and fatty acid disposal in muscle cells. J Cell Physiol 231:708-718.
41. Petrov PD, Ribot J, Palou A, Bonet ML. 2015. Improved metabolic regulation is associated with retinoblastoma protein gene haploinsufficiency in mice. Am J Physiol Endocrinol Metab 308:E172-E183.
42. Petrovic N, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. 2008. Thermogenically competent nonadrenergic recruitment in brown preadipocytes by a PPARgamma agonist. Am J Physiol Endocrinol Metab 295:E287-E296.
43. Petrovic N, Walden TB, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. 2010. Chronic peroxisome proliferator-activated receptor gamma (PPARgamma) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J Biol Chem 285:7153-7164.
44. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
45. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839.
46. Qian SW, Tang Y, Li X, Liu Y, Zhang YY, Huang HY, Xue RD, Yu HY, Guo L, Gao HD, Sun X, Li YM, Jia WP, Tang QQ. 2013. BMP4-mediated brown fat-like changes in white adipose tissue alter glucose and energy homeostasis. Proc Natl Acad Sci USA 110:E798-E807.
47. Rajakumari S, Wu J, Ishibashi J, Lim HW, Giang AH, Won KJ, Reed RR, Seale P. 2013. EBF2 determines and maintains brown adipocyte identity. Cell Metab 17:562-574.
48. Rong JX, Klein JL, Qiu Y, Xie M, Johnson JH, Waters KM, Zhang V, Kashatus JA, Remlinger KS, Bing N, Crosby RM, Jackson TK, Witherspoon SM, Moore JT, Ryan TE, Neill SD, Strum JC. 2011. Rosiglitazone induces mitochondrial biogenesis in differentiated murine 3T3-L1 and C3H/10T1/2 adipocytes. PPAR Res 2011:179454.
49. Rosen ED, Spiegelman BM. 2014. What we talk about when we talk about fat. Cell 156:20-44.
50. Rutledge RG, Stewart D. 2008. A kinetic-based sigmoidal model for the polymerase chain reaction and its application to high-capacity absolute quantitative real-time PCR. BMC Biotechnol 8:47.
51. Scime A, Grenier G, Huh MS, Gillespie MA, Bevilacqua L, Harper ME, Rudnicki MA. 2005. Rb and p107 regulate preadipocyte differentiation into white versus brown fat through repression of PGC-1alpha. Cell Metab 2:283-295.
52. Schulz TJ, Huang TL, Tran TT, Zhang H, Townsend KL, Shadrach JL, Cerletti M, McDougall LE, Giorgadze N, Tchkonia T, Schrier D, Falb D, Kirkland JL, Wagers AJ, Tseng YH. 2011. Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proc Natl Acad Sci USA 108:143-148.
53. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM. 2008. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454:961-967.
54. Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, Ishibashi J, Cohen P, Cinti S, Spiegelman BM. 2011. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 121:96-105.
55. Seale P, Kajimura S, Yang W, Chin S, Rohas LM, Uldry M, Tavernier G, Langin D, Spiegelman BM. 2007. Transcriptional control of brown fat determination by PRDM16. Cell Metab 6:38-54.
56. Sharp LZ, Shinoda K, Ohno H, Scheel DW, Tomoda E, Ruiz L, Hu H, Wang L, Pavlova Z, Gilsanz V, Kajimura S. 2012. Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS ONE 7:e49452.
57. Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM, Tran TT, Suzuki R, Espinoza DO, Yamamoto Y, Ahrens MJ, Dudley AT, Norris AW, Kulkarni RN, Kahn CR. 2008. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454:1000-1004.
58. Uldry M, Yang W, St-Pierre J, Lin J, Seale P, Spiegelman BM. 2006. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab 3:333-341.
59. Walden TB, Hansen IR, Timmons JA, Cannon B, Nedergaard J. 2012. Recruited vs. nonrecruited molecular signatures of brown, "brite, " and white adipose tissues. Am J Physiol Endocrinol Metab 302:E19-E31.
60. Wang J, Liu R, Wang F, Hong J, Li X, Chen M, Ke Y, Zhang X, Ma Q, Wang R, Shi J, Cui B, Gu W, Zhang Y, Zhang Z, Wang W, Xia X, Liu M, Ning G. 2013. Ablation of LGR4 promotes energy expenditure by driving white-to-brown fat switch. Nat Cell Biol 15:1455-1463.
61. Wang W, Kissig M, Rajakumari S, Huang L, Lim HW, Won KJ, Seale P. 2014. Ebf2 is a selective marker of brown and beige adipogenic precursor cells. Proc Natl Acad Sci USA 111:14466-14471.
62. Whittle AJ, Jiang M, Peirce V, Relat J, Virtue S, Ebinuma H, Fukamachi I, Yamaguchi T, Takahashi M, Murano T, Tatsuno I, Takeuchi M, Nakaseko C, Jin W, Jin Z, Campbell M, Schneider WJ, Vidal-Puig A, Bujo H. 2015. Soluble LR11/SorLA represses thermogenesis in adipose tissue and correlates with BMI in humans. Nat Commun 6:8951.
63. Wiczer BM, Bernlohr DA. 2009. A novel role for fatty acid transport protein 1 in the regulation of tricarboxylic acid cycle and mitochondrial function in 3T3-L1 adipocytes. J Lipid Res 50:2502-2513.
64. Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerback S, Schrauwen P, Spiegelman BM. 2012. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150:366-376.