Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle

Meat Science

Volumn 86, Issue 1, 2010, Pages 103-109

  Du, Min ^a   Yin, Jingdong ^b   Zhu, Mei J ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Adipogenesis; Marbling; Meat; Mesenchymal stem cells; Signaling; Skeletal muscle

Indexed keywords

ADIPOGENESIS; ANIMAL; DOMESTIC ANIMAL; FAT INTAKE; MEAT; MESENCHYMAL STEM CELL; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIME;

ADIPOGENESIS; ANIMALS; ANIMALS, DOMESTIC; DIETARY FATS; MEAT; MESENCHYMAL STEM CELLS; MUSCLE, SKELETAL; SIGNAL TRANSDUCTION; TIME FACTORS;

COLUMBA; ERINACEIDAE;

EID: 77954385613     PISSN: 03091740     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meatsci.2010.04.027     Document Type: Review

References (103)

1. Al-Khalili L., Chibalin A.V., Yu M., Sjodin B., Nylen C., Zierath J.R., et al. MEF2 activation in differentiated primary human skeletal muscle cultures requires coordinated involvement of parallel pathways. American Journal of Physiology Cell Physiology 2004, 286:C1410-C1416.
2. Armstrong D.D., Esser K.A. Wnt/beta-catenin signaling activates growth-control genes during overload-induced skeletal muscle hypertrophy. American Journal of Physiology Cell Physiology 2005, 289:C853-C859.
3. Aschenbach W.G., Hirshman M.F., Fujii N., Sakamoto K., Howlett K.F., Goodyear L.J. Effect of AICAR treatment on glycogen metabolism in skeletal muscle. Diabetes 2002, 51:567-573.
4. Beri R.K., Marley A.E., See C.G., Sopwith W.F., Aguan K., Carling D., et al. Molecular-cloning, expression and chromosomal localization of human AMP-activated. FEBS Letters 1994, 356:117-121.
5. Borello U., Berarducci B., Murphy P., Bajard L., Buffa V., Piccolo S., et al. The Wnt/beta-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development 2006, 133:3723-3732.
6. Borycki A., Brown A.M., Emerson C.P. Shh and Wnt signaling pathways converge to control Gli gene activation in avian somites. Development 2000, 127:2075-2087.
7. Bray S.J. Notch signalling: A simple pathway becomes complex. Nature Reviews Molecular Cell Biology 2006, 7:678-689.
8. Capdevila J., Tabin C., Johnson R.L. Control of dorsoventral somite patterning by Wnt-1 and beta-catenin. Developmental Biology 1998, 193:182-194.
9. Chen P.L., Riley D.J., Chen Y., Lee W.H. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs. Genes and Development 1996, 10:2794-2804.
10. Cheung P.C.F., Salt I.P., Davies S.P., Hardie D.G., Carling D. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochemical Journal 2000, 346:659-669.
11. Clarke S.L., Robinson C.E., Gimble J.M. CAAT/enhancer binding proteins directly modulate transcription from the peroxisome proliferator-activated receptor gamma 2 promoter. Biochemical and Biophysical Research Communications 1997, 240:99-103.
12. Cousin W., Fontaine C., Dani C., Peraldi P. Hedgehog and adipogenesis: Fat and fiction. Biochimie 2007, 89:1447-1453.
13. Dagon Y., Avraham Y., Berry E.M. AMPK activation regulates apoptosis, adipogenesis, and lipolysis by eIF2alpha in adipocytes. Biochemical and Biophysical Research Communications 2006, 340:43-47.
14. Davies S.P., Hawley S.A., Woods A., Carling D., Haystead T.A., Hardie D.G. Purification of the AMP-activated protein kinase on ATP-gamma-sepharose and analysis of its subunit structure. European Journal of Biochemistry 1994, 223:351-357.
15. Dierick H., Bejsovec A. Cellular mechanisms of wingless/Wnt signal transduction. Current Topics in Developmental Biology 1999, 43:153-190.
16. Du M., Zhu M.J. Fetal programming of skeletal muscle development. Applied muscle biology and meat science 2009, 81-96. CRC Press, Boca Raton, FL. M. Du, R.J. McCormick (Eds.).
17. Du M., Yan X., Tong J.F., Zhao J., Zhu M.J. Maternal obesity, inflammation, and fetal skeletal muscle development. Biology of Reproduction 2010, 82:4-12.
18. Du M., Tong J., Zhao J.F., Zhao J., Underwood K.R., Zhu M., Ford S.P., Nathanielsz P.W. Fetal programming of skeletal muscle development in ruminant animals. Journal of Animal Science 2010, 88:E51-E60.
19. Dyck J.R., Gao G., Widmer J., Stapleton D., Fernandez C.S., Kemp B.E., et al. Regulation of 5'AMP-activated protein kinase activity by the noncatalytic beta and gamma subunits. Journal of Biological Chemistry 1996, 271:17798-17803.
20. Essers M.A., de Vries-Smits L.M., Barker N., Polderman P.E., Burgering B.M., Korswagen H.C. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 2005, 308:1181-1184.
21. Feng X., Adiarte E.G., Devoto S.H. Hedgehog acts directly on the zebrafish dermomyotome to promote myogenic differentiation. Developmental Biology 2006, 300:736-746.
22. Fernyhough M.E., Okine E., Hausman G., Vierck J.L., Dodson M.V. PPARΓ and GLUT-4 expression as developmental regulators/markers for preadipocyte differentiation into an adipocyte. Domestic Animal Endocrinology 2007, 33:367-378.
23. Feve B. Adipogenesis: Cellular and molecular aspects. Best Practice and Research Clinical Endocrinology and Metabolism 2005, 19:483-499.
24. Fontaine C., Cousin W., Plaisant M., Dani C., Peraldi P. Hedgehog signaling alters adipocyte maturation of human mesenchymal stem cells. Stem Cells 2008, 26:1037-1046.
25. Frohnert B.I., Hui T.Y., Bernlohr D.A. Identification of a functional peroxisome proliferator-responsive element in the murine fatty acid transport protein gene. Journal of Biological Chemistry 1999, 274:3970-3977.
26. Garces C., Ruiz-Hidalgo M.J., Font de Mora J., Park C., Miele L., Goldstein J., et al. Notch-1 controls the expression of fatty acid-activated transcription factors and is required for adipogenesis. Journal of Biological Chemistry 1997, 272:29729-29734.
27. Giri S., Rattan R., Haq E., Khan M., Yasmin R., Won J.S., et al. AICAR inhibits adipocyte differentiation in 3T3L1 and restores metabolic alterations in diet-induced obesity mice model. Nutrition & Metabolism 2006, 3:31-51.
28. Gnanalingham M.G., Mostyn A., Symonds M.E., Stephenson T. Ontogeny and nutritional programming of adiposity in sheep: Potential role of glucocorticoid action and uncoupling protein-2. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 2005, 289:R1407-R1415.
29. Gotoh T., Albrecht E., Teuscher F., Kawabata K., Sakashita K., Iwamoto H., et al. Differences in muscle and fat accretion in Japanese Black and European cattle. Meat Science 2009, 82:300-308.
30. Greenwood P.L., Slepetis R.M., Hermanson J.W., Bell A.W. Intrauterine growth retardation is associated with reduced cell cycle activity, but not myofibre number, in ovine fetal muscle. Reproduction, Fertility, and Development 1999, 11:281-291.
31. Grohmann M., Sabin M., Holly J., Shield J., Crowne E., Stewart C. Characterization of differentiated subcutaneous and visceral adipose tissue from children: The influences of TNF-alpha and IGF-I. Journal of Lipid Research 2005, 46:93-103.
32. Gustafsson M.K., Pan H., Pinney D.F., Liu Y., Lewandowski A., Epstein D.J., et al. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes & Development 2002, 16:114-126.
33. Habinowski S.A., Witters L.A. The effects of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochemical and Biophysical Research Communications 2001, 286:852-856.
34. Hardie D.G. AMPK: A key regulator of energy balance in the single cell and the whole organism. International Journal of Obesity 2008, 32:S7-S12.
35. Hardie D.G., Carling D., Carlson M. The AMP-activated/SNF1 protein kinase subfamily: Metabolic sensors of the eukaryotic cell?. Annual Review of Biochemistry 1998, 67:821-855.
36. Harper G.S., Pethick D.W. How might marbling begin?. Australian Journal of Experimental Agriculture 2004, 44:653-662.
37. Hata K., Nishimura R., Ikeda F., Yamashita K., Matsubara T., Nokubi T., et al. Differential roles of Smad1 and p38 kinase in regulation of peroxisome proliferator-activating receptor gamma during bone morphogenetic protein 2-induced adipogenesis. Molecular Biology of the Cell 2003, 14:545-555.
38. Hausman G.J., Dodson M.V., Ajuwon K., Azain M., Barnes K.M., Guan L.L., et al. Board-invited review: The biology and regulation of preadipocytes and adipocytes in meat animals. Journal of Animal Science 2009, 87:1218-1246.
39. Hecht A., Kemler R. Curbing the nuclear activities of beta-catenin. Control over Wnt target gene expression. EMBO Reports 2000, 1:24-28.
40. Hirai S., Matsumoto H., Hino N., Kawachi H., Matsui T., Yano H. Myostatin inhibits differentiation of bovine preadipocyte. Domestic Animal Endocrinology 2007, 32:1-14.
41. Hirai S., Matsumoto H., Hino N., Kawachi H., Matsui T., Yano H. Follistatin rescues the inhibitory effect of activin A on the differentiation of bovine preadipocytes. Domestic Animal Endocrinology 2007, 33:269-280.
42. Hocquette J.F., Gondret F., Baeza E., Medale F., Jurie C., Pethick D.W. Intramuscular fat content in meat-producing animals: Development, genetic and nutritional control, and identification of putative markers. Animal 2010, 4:303-319.
43. Hoogeboom D., Essers M.A., Polderman P.E., Voets E., Smits L.M., Burgering B.M. Interaction of FOXO with beta-catenin inhibits beta-catenin/T cell factor activity. Journal of Biological Chemistry 2008, 283:9224-9230.
44. Hu Y., Davies G.E. Berberine increases expression of GATA-2 and GATA-3 during inhibition of adipocyte differentiation. Phytomedicine 2009, 16:864-873.
45. Hu E., Kim J.B., Sarraf P., Spiegelman B.M. Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARgamma. Science 1996, 274:2100-2103.
46. Huelsken J., Birchmeier W. New aspects of Wnt signaling pathways in higher vertebrates. Current Opinion in Genetics & Development 2001, 11:547-553.
47. Hwang J.T., Park I.J., Shin J.I., Lee Y.K., Lee S.K., Baik H.W., et al. Genistein, EGCG, and capsaicin inhibit adipocyte differentiation process via activating AMP-activated protein kinase. Biochemical and Biophysical Research Communications 2005, 338:694-699.
48. IJpenberg A., Jeannin E., Wahli W., Desvergne B. Polarity and specific sequence requirements of peroxisome proliferator-activated receptor (PPAR)/retinoid×receptor heterodimer binding to DNA. A functional analysis of the malic enzyme gene PPAR response element. Journal of Biological Chemistry 1997, 272:20108-20117.
49. Jin W., Takagi T., Kanesashi S.N., Kurahashi T., Nomura T., Harada J., et al. Schnurri-2 controls BMP-dependent adipogenesis via interaction with Smad proteins. Developmental Cell 2006, 10:461-471.
50. Johnson M.L., Rajamannan N. Diseases of Wnt signaling. Reviews in Endocrine & Metabolic Disorders 2006, 7:41-49.
51. Kajimura S., Seale P., Kubota K., Lunsford E., Frangioni J.V., Gygi S.P., et al. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature 2009, 460:1154-1158.
52. Katanaev V.L., Ponzielli R., Semeriva M., Tomlinson A. Trimeric G protein-dependent frizzled signaling in Drosophila. Cell 2005, 120:111-122.
53. Kim J.B., Spiegelman B.M. ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes & Development 1996, 10:1096-1107.
54. Kliewer S.A., Lenhard J.M., Willson T.M., Patel I., Morris D.C., Lehmann J.M. A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 1995, 83:813-819.
55. Krishnan V., Elberg G., Tsai M.J., Tsai S.Y. Identification of a novel sonic hedgehog response element in the chicken ovalbumin upstream promoter-transcription factor II promoter. Molecular Endocrinology 1997, 11:1458-1466.
56. Krishnan V., Pereira F.A., Qiu Y., Chen C.H., Beachy P.A., Tsai S.Y., et al. Mediation of Sonic hedgehog-induced expression of COUP-TFII by a protein phosphatase. Science 1997, 278:1947-1950.
57. Liu X., Rubin J.S., Kimmel A.R. Rapid, Wnt-induced changes in GSK3beta associations that regulate beta-catenin stabilization are mediated by Galpha proteins. Current Biology 2005, 15:1989-1997.
58. Manolagas S.C., Almeida M. Gone with the Wnts: Beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Molecular Endocrinology 2007, 21:2605-2614.
59. Mermelstein C.S., Portilho D.M., Mendes F.A., Costa M.L., Abreu J.G. Wnt/beta-catenin pathway activation and myogenic differentiation are induced by cholesterol depletion. Differentiation; Research in Biological Diversity 2007, 75:184-192.
60. Mitchelhill K.I., Stapleton D., Gao G., House C., Michell B., Katsis F., et al. Mammalian AMP-activated protein kinase shares structural and functional homology with the catalytic domain of yeast Snf1 protein kinase. Journal of Biological Chemistry 1994, 269:2361-2364.
61. Morin S., Charron F., Robitaille L., Nemer M. GATA-dependent recruitment of MEF2 proteins to target promoters. EMBO Journal 2000, 19:2046-2055.
62. Muhlhausler B.S., Duffield J.A., McMillen I.C. Increased maternal nutrition stimulates Peroxisome Proliferator Activated Receptor-gamma (PPARgamma), adiponectin and leptin mRNA expression in adipose tissue before birth. Endocrinology 2006, 148:878-885.
63. Nagy L., Tontonoz P., Alvarez J.G., Chen H., Evans R.M. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell 1998, 93:229-240.
64. Nedergaard J., Petrovic N., Lindgren E.M., Jacobsson A., Cannon B. PPARgamma in the control of brown adipocyte differentiation. Biochimica et Biophysica Acta 2005, 1740:293-304.
65. Nichols A.M., Pan Y., Herreman A., Hadland B.K., De Strooper B., Kopan R., et al. Notch pathway is dispensable for adipocyte specification. Genesis 2004, 40:40-44.
66. Nieuwenhuis E., Motoyama J., Barnfield P.C., Yoshikawa Y., Zhang X., Mo R., et al. Mice with a targeted mutation of patched2 are viable but develop alopecia and epidermal hyperplasia. Molecular and Cellular Biology 2006, 26:6609-6622.
67. Nueda M.L., Baladron V., Sanchez-Solana B., Ballesteros M.A., Laborda J. The EGF-like protein dlk1 inhibits notch signaling and potentiates adipogenesis of mesenchymal cells. Journal of Molecular Biology 2007, 367:1281-1293.
68. Okamura M., Kudo H., Wakabayashi K., Tanaka T., Nonaka A., Uchida A., et al. COUP-TFII acts downstream of Wnt/beta-catenin signal to silence PPARgamma gene expression and repress adipogenesis. Proceedings of the National Academy of Science of the United States of America 2009, 106:5819-5824.
69. Pan W., Jia Y., Wang J., Tao D., Gan X., Tsiokas L., et al. Beta-catenin regulates myogenesis by relieving I-mfa-mediated suppression of myogenic regulatory factors in P19 cells. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:17378-17383.
70. Park H.L., Bai C., Platt K.A., Matise M.P., Beeghly A., Hui C.C., et al. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 2000, 127:1593-1605.
71. Persson M., Stamataki D., te Welscher P., Andersson E., Bose J., Ruther U., et al. Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes & Development 2002, 16:2865-2878.
72. Polesskaya A., Seale P., Rudnicki M.A. Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 2003, 113:841-852.
73. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
74. Ridgeway A.G., Skerjanc I.S. Pax3 is essential for skeletal myogenesis and the expression of Six1 and Eya2. Journal of Biological Chemistry 2001, 276:19033-19039.
75. Rosen E.D., MacDougald O.A. Adipocyte differentiation from the inside out. Nature Reviews Molecular Cell Biology 2006, 7:885-896.
76. Rosen E.D., Hsu C.H., Wang X., Sakai S., Freeman M.W., Gonzalez F.J., et al. C/EBPalpha induces adipogenesis through PPARgamma: A unified pathway. Genes & Development 2002, 16:22-26.
77. Russell R.G., Oteruelo F.T. An ultrastructural study of the differentiation of skeletal muscle in the bovine fetus. Anatomy and Embryology 1981, 162:403-417.
78. Schopfer F.J., Lin Y., Baker P.R., Cui T., Garcia-Barrio M., Zhang J., et al. Nitrolinoleic acid: An endogenous peroxisome proliferator-activated receptor gamma ligand. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:2340-2345.
79. Schupp M., Cristancho A.G., Lefterova M.I., Hanniman E.A., Briggs E.R., Steger D.J., et al. Re-expression of GATA2 cooperates with peroxisome proliferator-activated receptor-gamma depletion to revert the adipocyte phenotype. Journal of Biological Chemistry 2009, 284:9458-9464.
80. Seale P., Bjork B., Yang W., Kajimura S., Chin S., Kuang S., et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 2008, 454:961-967.
81. Shang Y.C., Zhang C., Wang S.H., Xiong F., Zhao C.P., Peng F.N., et al. Activated beta-catenin induces myogenesis and inhibits adipogenesis in BM-derived mesenchymal stromal cells. Cytotherapy 2007, 9:667-681.
82. Shao D., Rangwala S.M., Bailey S.T., Krakow S.L., Reginato M.J., Lazar M.A. Interdomain communication regulating ligand binding by PPAR-gamma. Nature 1998, 396:377-380.
83. Smith S.B., Kawachi H., Choi C.B., Choi C.W., Wu G., Sawyer J.E. Cellular regulation of bovine intramuscular adipose tissue development and composition. Journal of Animal Science 2009, 87:E72-E82.
84. Spinella-Jaegle S., Rawadi G., Kawai S., Gallea S., Faucheu C., Mollat P., et al. Sonic hedgehog increases the commitment of pluripotent mesenchymal cells into the osteoblastic lineage and abolishes adipocytic differentiation. Journal of Cell Science 2001, 114:2085-2094.
85. Stapleton D., Woollatt E., Mitchelhill K.I., Nicholl J.K., Fernandez C.S., Michell B.J., et al. AMP-activated protein kinase isoenzyme family: Subunit structure and chromosomal location. FEBS Letters 1997, 409:452-456.
86. Suh J.M., Gao X., McKay J., McKay R., Salo Z., Graff J.M. Hedgehog signaling plays a conserved role in inhibiting fat formation. Cell Metabolism 2006, 3:25-34.
87. Tong J., Zhu M.J., Underwood K.R., Hess B.W., Ford S.P., Du M. AMP-activated protein kinase and adipogenesis in sheep fetal skeletal muscle and 3T3-L1 cells. Journal of Animal Science 2008, 86:1296-1305.
88. Tong J.F., Yan X., Zhu M.J., Ford S.P., Nathanielsz P.W., Du M. Maternal obesity downregulates myogenesis and {beta}-catenin signaling in fetal skeletal muscle. American Journal of Physiology, Endocrinology and Metabolism 2009, 296:E917-E924.
89. Tsai J., Tong Q., Tan G., Chang A.N., Orkin S.H., Hotamisligil G.S. The transcription factor GATA2 regulates differentiation of brown adipocytes. EMBO Reports 2005, 6:879-884.
90. Tseng Y.H., Butte A.J., Kokkotou E., Yechoor V.K., Taniguchi C.M., Kriauciunas K.M., et al. Prediction of preadipocyte differentiation by gene expression reveals role of insulin receptor substrates and necdin. Nature Cell Biology 2005, 7:601-611.
91. Tseng Y.H., Kokkotou E., Schulz T.J., Huang T.L., Winnay J.N., Taniguchi C.M., et al. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 2008, 454:1000-1004.
92. Underwood K.R., Means W.J., Zhu M.J., Ford S.P., Hess B.W., Du M. AMP-activated protein kinase is negatively associated with intramuscular fat content in longissimus dorsi muscle of beef cattle. Meat Science 2007, 79:394-402.
93. Underwood K.R., Tong J., Zhu M.J., Shen Q.W., Means W.J., Ford S.P., et al. Relationship between kinase phosphorylation, muscle fiber typing, and glycogen accumulation in longissimus muscle of beef cattle with high and low intramuscular fat. Journal of Agricultural and Food Chemistry 2007, 55:9698-9703.
94. Wang Y., Kim K.A., Kim J.H., Sul H.S. Pref-1, a preadipocyte secreted factor that inhibits adipogenesis. Journal of Nutrition 2006, 136:2953-2956.
95. Woods A., Cheung P.C., Smith F.C., Davison M.D., Scott J., Beri R.K., et al. Characterization of AMP-activated protein kinase beta and gamma subunits. Assembly of the heterotrimeric complex in vitro. Journal of Biological Chemistry 1996, 271:10282-10290.
96. Wu Z., Rosen E.D., Brun R., Hauser S., Adelmant G., Troy A.E., et al. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Molecular Cell 1999, 3:151-158.
97. Xu Z., Yu S., Hsu C.H., Eguchi J., Rosen E.D. The orphan nuclear receptor chicken ovalbumin upstream promoter-transcription factor II is a critical regulator of adipogenesis. Proceedings of the National Academy of Science of the United States of America 2008, 105:2421-2426.
98. Yamanouchi K., Hosoyama T., Murakami Y., Nishihara M. Myogenic and adipogenic properties of goat skeletal muscle stem cells. Journal of Reproduction and Development 2007, 53:51-58.
99. Zawel L., Dai J.L., Buckhaults P., Zhou S., Kinzler K.W., Vogelstein B., et al. Human Smad3 and Smad4 are sequence-specific transcription activators. Molecular Cell 1998, 1:611-617.
100. Zehentner B.K., Leser U., Burtscher H. BMP-2 and sonic hedgehog have contrary effects on adipocyte-like differentiation of C3H10T1/2 cells. DNA and Cell Biology 2000, 19:275-281.
101. Zhu M.J., Han B., Tong J., Ma C., Kimzey J.M., Underwood K.R., et al. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. Journal of Physiology 2008, 586:2651-2664.
102. Ziouzenkova O., Plutzky J. Retinoid metabolism and nuclear receptor responses: New insights into coordinated regulation of the PPAR-RXR complex. FEBS Letters 2008, 582:32-38.
103. Ziouzenkova O., Orasanu G., Sukhova G., Lau E., Berger J.P., Tang G., et al. Asymmetric cleavage of beta-carotene yields a transcriptional repressor of retinoid×receptor and peroxisome proliferator-activated receptor responses. Molecular Endocrinology 2007, 21:77-88.