Protein kinase G controls brown fat cell differentiation and mitochondrial biogenesis

Science Signaling

Volumn 2, Issue 99, 2009, Pages

  Haas, Bodo ^a   Mayer, Peter ^b   Jennissen, Katja ^a   Scholz, Daniela ^a   Diaz, Mauricio Berriel ^c   Bloch, Wilhelm ^d   Herzig, Stephan ^c   Fässler, Reinhard ^e   Pfeifer, Alexander ^a  

^a UNIVERSITY OF BONN   (Germany)

^b FEDERAL INSTITUTE FOR DRUGS AND MEDICAL DEVICES   (Germany)

^c GERMAN CANCER RESEARCH CENTER   (Germany)

^d GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

^e MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; INSULIN; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCOUPLING PROTEIN 1; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN;

ADIPOGENESIS; ARTICLE; BIOGENESIS; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CONTROLLED STUDY; LIPID STORAGE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; THERMOGENESIS; ANIMAL; CYTOLOGY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ADIPOGENESIS; ADIPOSE TISSUE, BROWN; ANIMALS; CELL DIFFERENTIATION; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; INSULIN; ION CHANNELS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NITRIC OXIDE; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN;

EID: 77950361100     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000511     Document Type: Article

References (49)

1. S. Gesta, Y. H. Tseng, C. R. Kahn, Developmental origin of fat: Tracking obesity to its source. Cell 131, 242-256 (2007). (Pubitemid 47576146)
2. B. Cannon, J. Nedergaard, Brown adipose tissue: Function and physiological significance. Physiol. Rev. 84, 277-359 (2004). (Pubitemid 38054374)
3. A. M. Cypess, S. Lehman, G. Williams, I. Tal, D. Rodman, A. B. Goldfine, F. C. Kuo, E. L. Palmer, Y. H. Tseng, A. Doria, G. M. Kolodny, C. R. Kahn, Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517 (2009).
4. K. A. Virtanen, M. E. Lidell, J. Orava, M. Heglind, R. Westergren, T. Niemi, M. Taittonen, J. Laine, N. J. Savisto, S. Enerbäck, P. Nuutila, Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525 (2009).
5. J. Nedergaard, T. Bengtsson, B. Cannon, Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 293, E444-E452 (2007). (Pubitemid 47205086)
6. W. D. van Marken Lichtenbelt, J. W. Vanhommerig, N. M. Smulders, J. M. Drossaerts, G. J. Kemerink, N. D. Bouvy, P. Schrauwen, G. J. Teule, Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 360, 1500-1508 (2009).
7. M. Saito, Y. Okamatsu-Ogura, M. Matsushita, K. Watanabe, T. Yoneshiro, J. Nio- Kobayashi, T. Iwanaga, M. Miyagawa, T. Kameya, K. Nakada, Y. Kawai, M. Tsujisaki, High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes 58, 1526-1531 (2009).
8. Z. Wu, P. Puigserver, U. Andersson, C. Zhang, G. Adelmant, V. Mootha, A. Troy, S. Cinti, B. Lowell, R. C. Scarpulla, B. M. Spiegelman, Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124 (1999). (Pubitemid 29331201)
9. W. K. Alderton, C. E. Cooper, R. G. Knowles, Nitric oxide synthases: Structure, function and inhibition. Biochem. J. 357, 593-615 (2001). (Pubitemid 32735142)
10. E. Nisoli, E. Clementi, C. Paolucci, V. Cozzi, C. Tonello, C. Sciorati, R. Bracale, A. Valerio, M. Francolini, S. Moncada, M. O. Carruba, Mitochondrial biogenesis in mammals: The role of endogenous nitric oxide. Science 299, 896-899 (2003). (Pubitemid 36182449)
11. L. J. Ignarro, C. Napoli, J. Loscalzo, Nitric oxide donors and cardiovascular agents modulating the bioactivity of nitric oxide: An overview. Circ. Res. 90, 21-28 (2002). (Pubitemid 34074604)
12. F. Murad, Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development. N. Engl. J. Med. 355, 2003-2011 (2006). (Pubitemid 44708019)
13. D. L. Garbers, T. D. Chrisman, P. Wiegn, T. Katafuchi, J. P. Albanesi, V. Bielinski, B. Barylko, M. M. Redfield, J. C. Burnett Jr., Membrane guanylyl cyclase receptors: An update. Trends Endocrinol. Metab. 17, 251-258 (2006). (Pubitemid 44164281)
14. D. Koesling, M. Russwurm, E. Mergia, F. Mullershausen, A. Friebe, Nitric oxide-sensitive guanylyl cyclase: Structure and regulation. Neurochem. Int. 45, 813-819 (2004).
15. A. T. Bender, J. A. Beavo, Cyclic nucleotide phosphodiesterases: Molecular regulation to clinical use. Pharmacol. Rev. 58, 488-520 (2006).
16. R. Feil, S. M. Lohmann, H. de Jonge, U. Walter, F. Hofmann, Cyclic GMP-dependent protein kinases and the cardiovascular system: Insights from genetically modified mice. Circ. Res. 93, 907-916 (2003). (Pubitemid 37433228)
17. S. H. Francis, J. D. Corbin, Cyclic nucleotide-dependent protein kinases: Intracellular receptors for cAMP and cGMP action. Crit. Rev. Clin. Lab. Sci. 36, 275-328 (1999).
18. A. Pfeifer, P. Ruth, W. Dostmann, M. Sausbier, P. Klatt, F. Hofmann, Structure and function of cGMP-dependent protein kinases. Rev. Physiol. Biochem. Pharmacol. 135, 105-149 (1999).
19. A. Pfeifer, P. Klatt, S. Massberg, L. Ny, M. Sausbier, C. Hirneiss, G. X. Wang, M. Korth, A. Aszodi, K. E. Andersson, F. Krombach, A. Mayerhofer, P. Ruth, R. Fassler, F. Hofmann, Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J. 17, 3045-3051 (1998). (Pubitemid 28254377)
20. W. G. Heil, W. Landgraf, F. Hofmann, A catalytically active fragment of cGMP-dependent protein kinase. Occupation of its cGMP-binding sites does not affect its phosphotransferase activity. Eur. J. Biochem. 168, 117-121 (1987).
21. E. D. Rosen, C. J. Walkey, P. Puigserver, B. M. Spiegelman, Transcriptional regulation of adipogenesis. Genes Dev. 14, 1293-1307 (2000). (Pubitemid 30397073)
22. E. Nisoli, E. Clementi, C. Tonello, C. Sciorati, L. Briscini, M. O. Carruba, Effects of nitric oxide on proliferation and differentiation of rat brown adipocytes in primary cultures. Br. J. Pharmacol. 125, 888-894 (1998). (Pubitemid 28482634)
23. N. Sawada, H. Itoh, J. Yamashita, K. Doi, M. Inoue, K. Masatsugu, Y. Fukunaga, S. Sakaguchi, M. Sone, K. Yamahara, T. Yurugi, K. Nakao, cGMP-dependent protein kinase phosphorylates and inactivates RhoA. Biochem. Biophys. Res. Commun. 280, 798-805 (2001). (Pubitemid 32924500)
24. V. Sauzeau, H. Le Jeune, C. Cario-Toumaniantz, A. Smolenski, S. M. Lohmann, J. Bertoglio, P. Chardin, P. Pacaud, G. Loirand, Cyclic GMP-dependent protein kinase signaling pathway inhibits RhoA-induced Ca2+ sensitization of contraction in vascular smooth muscle. J. Biol. Chem. 275, 21722-21729 (2000). (Pubitemid 30481881)
25. R. Sordella, W. Jiang, G. C. Chen, M. Curto, J. Settleman, Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 113, 147-158 (2003). (Pubitemid 36514967)
26. R. McBeath, D. M. Pirone, C. M. Nelson, K. Bhadriraju, C. S. Chen, Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495 (2004). (Pubitemid 38456178)
27. A. J. Ridley, A. Hall, The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399 (1992).
28. M. Fasshauer, J. Klein, K. M. Kriauciunas, K. Ueki, M. Benito, C. R. Kahn, Essential role of insulin receptor substrate 1 in differentiation of brown adipocytes. Mol. Cell. Biol. 21, 319-329 (2001).
29. A. M. Valverde, M. Arribas, C. Mur, P. Navarro, S. Pons, A. M. Cassard-Doulcier, C. R. Kahn, M. Benito, Insulin-induced up-regulated uncoupling protein-1 expression is mediated by insulin receptor substrate 1 through the phosphatidylinositol 3-kinase/ Akt signaling pathway in fetal brown adipocytes. J. Biol. Chem. 278, 10221-10231 (2003). (Pubitemid 36800283)
30. N. Begum, O. A. Sandu, M. Ito, S. M. Lohmann, A. Smolenski, Active Rho kinase (ROK-a) associates with insulin receptor substrate-1 and inhibits insulin signaling in vascular smooth muscle cells. J. Biol. Chem. 277, 6214-6222 (2002). (Pubitemid 34968412)
31. N. Furukawa, P. Ongusaha, W. J. Jahng, K. Araki, C. S. Choi, H. J. Kim, Y. H. Lee, K. Kaibuchi, B. B. Kahn, H. Masuzaki, J. K. Kim, S. W. Lee, Y. B. Kim, Role of Rhokinase in regulation of insulin action and glucose homeostasis. Cell Metab. 2, 119-129 (2005).
32. A. M. Valverde, M. Benito, M. Lorenzo, The brown adipose cell: A model for understanding the molecular mechanisms of insulin resistance. Acta Physiol. Scand. 183, 59-73 (2005). (Pubitemid 40188036)
33. J. S. Boehm, J. J. Zhao, J. Yao, S. Y. Kim, R. Firestein, I. F. Dunn, S. K. Sjostrom, L. A. Garraway, S. Weremowicz, A. L. Richardson, H. Greulich, C. J. Stewart, L. A. Mulvey, R. R. Shen, L. Ambrogio, T. Hirozane-Kishikawa, D. E. Hill, M. Vidal, M. Meyerson, J. K. Grenier, G. Hinkle, D. E. Root, T. M. Roberts, E. S. Lander, K. Polyak, W. C. Hahn, Integrative genomic approaches identify IKBKE as a breast cancer oncogene. Cell 129, 1065-1079 (2007).
34. J. A. Engelman, A. H. Berg, R. Y. Lewis, A. Lin, M. P. Lisanti, P. E. Scherer, Constitutively active mitogen-activated protein kinase kinase 6 (MKK6) or salicylate induces spontaneous 3T3-L1 adipogenesis. J. Biol. Chem. 274, 35630-35638 (1999).
35. J. E. Reusch, L. A. Colton, D. J. Klemm, CREB activation induces adipogenesis in 3T3-L1 cells. Mol. Cell. Biol. 20, 1008-1020 (2000).
36. W. Cao, K. W. Daniel, J. Robidoux, P. Puigserver, A. V. Medvedev, X. Bai, L. M. Floering, B. M. Spiegelman, S. Collins, p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol. Cell. Biol. 24, 3057-3067 (2004).
37. M. R. Hodges, G. J. Tattersall, M. B. Harris, S. D. McEvoy, D. N. Richerson, E. S. Deneris, R. L. Johnson, Z. F. Chen, G. B. Richerson, Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J. Neurosci. 28, 2495-2505 (2008).
38. S. Enerbäck, A. Jacobsson, E. M. Simpson, C. Guerra, H. Yamashita, M. E. Harper, L. P. Kozak, Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387, 90-94 (1997).
39. J. Lin, P. H. Wu, P. T. Tarr, K. S. Lindenberg, J. St-Pierre, C. Y. Zhang, V. K. Mootha, S. Jager, C. R. Vianna, R. M. Reznick, L. Cui, M. Manieri, M. X. Donovan, Z. Wu, M. P. Cooper, M. C. Fan, L. M. Rohas, A. M. Zavacki, S. Cinti, G. I. Shulman, B. B. Lowell, D. Krainc, B. M. Spiegelman, Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1a null mice. Cell 119, 121-135 (2004).
40. M. Noguchi, K. Hosoda, J. Fujikura, M. Fujimoto, H. Iwakura, T. Tomita, T. Ishii, N. Arai, M. Hirata, K. Ebihara, H. Masuzaki, H. Itoh, S. Narumiya, K. Nakao, Genetic and pharmacological inhibition of Rho-associated kinase II enhances adipogenesis. J. Biol. Chem. 282, 29574-29583 (2007).
41. T. Gudi, D. E. Casteel, C. Vinson, G. R. Boss, R. B. Pilz, NO activation of fos promoter elements requires nuclear translocation of G-kinase I and CREB phosphorylation but is independent of MAP kinase activation. Oncogene 19, 6324-6333 (2000).
42. M. Armoni, C. Harel, S. Karni, H. Chen, F. Bar-Yoseph, M. R. Ver, M. J. Quon, E. Karnieli, FOXO1 represses peroxisome proliferator-activated receptor-g1 and -g2 gene promoters in primary adipocytes. A novel paradigm to increase insulin sensitivity. J. Biol. Chem. 281, 19881-19891 (2006).
43. W. Fan, T. Imamura, N. Sonoda, D. D. Sears, D. Patsouris, J. J. Kim, J. M. Olefsky, FOXO1 transrepresses peroxisome proliferator-activated receptor g transactivation, coordinating an insulin-induced feed-forward response in adipocytes. J. Biol. Chem. 284, 12188-12197 (2009).
44. X. D. Peng, P. Z. Xu, M. L. Chen, A. Hahn-Windgassen, J. Skeen, J. Jacobs, D. Sundararajan, W. S. Chen, S. E. Crawford, K. G. Coleman, N. Hay, Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 17, 1352-1365 (2003).
45. S. Herzig, F. Long, U. S. Jhala, S. Hedrick, R. Quinn, A. Bauer, D. Rudolph, G. Schutz, C. Yoon, P. Puigserver, B. Spiegelman, M. Montminy, CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413, 179-183 (2001). (Pubitemid 32867880)
46. J. S. Rim, L. P. Kozak, Regulatory motifs for CREB-binding protein and Nfe2l2 transcription factors in the upstream enhancer of the mitochondrial uncoupling protein 1 gene. J. Biol. Chem. 277, 34589-34600 (2002).
47. Y. Zhu, C. Qi, J. R. Korenberg, X. N. Chen, D. Noya, M. S. Rao, J. K. Reddy, Structural organization of mouse peroxisome proliferator-activated receptor g (mPPARg) gene: Alternative promoter use and different splicing yield two mPPARg isoforms. Proc. Natl. Acad. Sci. U.S.A. 92, 7921-7925 (1995).
48. A. Pfeifer, E. P. Brandon, N. Kootstra, F. H. Gage, I. M. Verma, Delivery of the Cre recombinase by a self-deleting lentiviral vector: Efficient gene targeting in vivo. Proc. Natl. Acad. Sci. U.S.A. 98, 11450-11455 (2001).
49. We are grateful to L. Naldini, D. Trono, and W. C. Hahn, for providing plasmids. We thank S. Kipschull and A. Ziegler for excellent technical assistance and M. Ahmad for help with the generation of the PKGI floxed mice. This study was supported by a grant from the Federal Institute for Drugs and Medical Devices to A.P., the Max Planck Society to R.F., and the Deutsche Forschungsgemeinschaft to S.H., R.F., and A.P. B.H., K.J., D.S., P.M., M.B.D., and W.B. performed the experiments. A.P. and B.H. wrote the paper, A.P., S.H., and R.F. conceived and designed experiments.