Regulation of metabolism by cGMP

Pharmacology and Therapeutics

Volumn 140, Issue 1, 2013, Pages 81-91

  Pfeifer, Alexander ^a   Kilić, Ana ^a   Hoffmann, Linda Sarah ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Brown adipose tissue; Browning; cGMP; Metabolism; Obesity; White adipose tissue

Indexed keywords

BEIGE FAT; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; FAT; GUANYLATE CYCLASE; NATRIURETIC FACTOR; NITRIC OXIDE; PHOSPHODIESTERASE; PHOSPHODIESTERASE V INHIBITOR; PROTEIN KIONASE G; SILDENAFIL; TADALAFIL; UNCLASSIFIED DRUG; VARDENAFIL;

ADIPOSE TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL METABOLISM; CENTRAL NERVOUS SYSTEM; ENERGY EXPENDITURE; ERECTILE DYSFUNCTION; HUMAN; LIVER; METABOLIC DISORDER; METABOLISM; MUSCLE; NONHUMAN; OBESITY; PANCREAS; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; WHITE ADIPOSE TISSUE;

BROWN ADIPOSE TISSUE; BROWNING; CGMP; METABOLISM; OBESITY; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE; ANIMALS; CENTRAL NERVOUS SYSTEM; CYCLIC GMP; ENERGY METABOLISM; HUMANS; LIVER; PANCREAS; SIGNAL TRANSDUCTION;

EID: 84884138893     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2013.06.001     Document Type: Review

References (138)

1. M. Ahmadian, Y. Wang, and H.S. Sul Lipolysis in adipocytes Int J Biochem Cell Biol 42 2010 555 559
2. A.A. Alfadda, and R.M. Sallam Reactive oxygen species in health and disease J Biomed Biotechnol 2012 2012 8
3. Z. An, J.J. Winnick, M.C. Moore, B. Farmer, M. Smith, and J.M. Irimia A cyclic guanosine monophosphate-dependent pathway can regulate net hepatic glucose uptake in vivo Diabetes 61 2012 2433 2441
4. J. Antunes-Rodrigues, S.M. McCann, L.C. Rogers, and W.K. Samson Atrial natriuretic factor inhibits dehydration- and angiotensin II-induced water intake in the conscious, unrestrained rat Proc Natl Acad Sci U S A 82 1985 8720 8723
5. A. Armani, V. Marzolla, G.M. Rosano, A. Fabbri, and M. Caprio Phosphodiesterase type 5 (PDE5) in the adipocyte: a novel player in fat metabolism? Trends Endocrinol Metab 22 2011 404 411
6. R. Atit, S.K. Sgaier, O.A. Mohamed, M.M. Taketo, D. Dufort, and A.L. Joyner Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse Dev Biol 296 2006 164 176
7. A. Aversa, M. Caprio, A. Antelmi, A. Armani, M. Brama, and E.A. Greco Exposure to phosphodiesterase type 5 inhibitors stimulates aromatase expression in human adipocytes in vitro J Sex Med 8 2011 696 704
8. J.E. Ayala, D.P. Bracy, B.M. Julien, J.N. Rottman, P.T. Fueger, and D.H. Wasserman Chronic treatment with sildenafil improves energy balance and insulin action in high fat-fed conscious mice Diabetes 56 2007 1025 1033
9. J. Azer, R. Hua, K. Vella, and R.A. Rose Natriuretic peptides regulate heart rate and sinoatrial node function by activating multiple natriuretic peptide receptors J Mol Cell Cardiol 53 2012 715 724
10. G. Barbatelli, I. Murano, L. Madsen, Q. Hao, M. Jimenez, and K. Kristiansen 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 2010 E1244 E1253
11. A. Bartelt, O.T. Bruns, R. Reimer, H. Hohenberg, H. Ittrich, and K. Peldschus Brown adipose tissue activity controls triglyceride clearance Nat Med 17 2011 200 205
12. M. Bellingham, and T.J. Evans The alpha2beta1 isoform of guanylyl cyclase mediates plasma membrane localized nitric oxide signalling Cell Signal 19 2007 2183 2193 (Epub 2007 Jun 2129)
13. C. Beyer, N. Reich, S.C. Schindler, A. Akhmetshina, C. Dees, and M. Tomcik Stimulation of soluble guanylate cyclase reduces experimental dermal fibrosis Ann Rheum Dis 71 2012 1019 1026
14. M. Biel, and S. Michalakis Cyclic nucleotide-gated channels Handb Exp Pharmacol 111-136 2009
15. A.L. Birkenfeld, P. Budziarek, M. Boschmann, C. Moro, F. Adams, and G. Franke Atrial natriuretic peptide induces postprandial lipid oxidation in humans Diabetes 57 2008 3199 3204
16. P. Bogdanski, J. Suliburska, K. Grabanska, K. Musialik, A. Cieslewicz, and A. Skoluda Effect of 3-month l-arginine supplementation on insulin resistance and tumor necrosis factor activity in patients with visceral obesity Eur Rev Med Pharmacol Sci 16 2012 816 823
17. M. Bordicchia, D. Liu, E.Z. Amri, G. Ailhaud, P. Dessi-Fulgheri, and C. Zhang Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes J Clin Invest 122 2012 1022 1036
18. J. Budworth, S. Meillerais, I. Charles, and K. Powell Tissue distribution of the human soluble guanylate cyclases Biochem Biophys Res Commun 263 1999 696 701
19. W. Cao, K.W. Daniel, J. Robidoux, P. Puigserver, A.V. Medvedev, and X. Bai 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 2004 3057 3067
20. B.Y. Chen, R. Tie, P. Qu, M.Z. Zhu, X.X. Zhu, and J. Jin Vasonatrin peptide, a new regulator of adiponectin and interleukin-6 production in adipocytes J Endocrinol Invest 34 2011 742 746
21. H.H. Chen, and J.C. Burnett Jr. C-type natriuretic peptide: the endothelial component of the natriuretic peptide system J Cardiovasc Pharmacol 32 Suppl. 3 1998 S22 S28
22. Y. Chen, F. Siegel, S. Kipschull, B. Haas, H. Frohlich, and G. Meister miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit Nat Commun 4 2013 1769
23. H. Chusho, N. Tamura, Y. Ogawa, A. Yasoda, M. Suda, and T. Miyazawa Dwarfism and early death in mice lacking C-type natriuretic peptide Proc Natl Acad Sci U S A 98 2001 4016 4021
24. M. Conti, and J. Beavo Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling Annu Rev Biochem 76 2007 481 511
25. L.C. Costello-Boerrigter Cardiac natriuretic peptides: contributors to cardiac cachexia or possible anti-obesity agents or both? Diabetes 61 2012 2403 2404
26. A.M. Cypess, S. Lehman, G. Williams, I. Tal, D. Rodman, and A.B. Goldfine Identification and importance of brown adipose tissue in adult humans N Engl J Med 360 2009 1509 1517
27. A.M. Cypess, A.P. White, C. Vernochet, T.J. Schulz, R. Xue, and C.A. Sass Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat Nat Med 19 2013 635 639
28. S. Daff NO synthase: structures and mechanisms Nitric Oxide 23 2010 1 11
29. A.J. de Bold, H.B. Borenstein, A.T. Veress, and H. Sonnenberg A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats Life Sci 28 1981 89 94
30. E. Degerman, P. Belfrage, and V.C. Manganiello Structure, localization, and regulation of cGMP-inhibited phosphodiesterase (PDE3) J Biol Chem 272 1997 6823 6826
31. S.A. Doggrell Phosphodiesterase 5A as a target in cardiac disease Expert Opin Ther Targets 9 2005 1097 1100
32. S. Enerback Human brown adipose tissue Cell Metab 11 2010 248 252
33. G.J. Etgen Jr., C.M. Wilson, J. Jensen, S.W. Cushman, and J.L. Ivy Glucose transport and cell surface GLUT-4 protein in skeletal muscle of the obese Zucker rat Am J Physiol 271 1996 E294 E301
34. R. Feil, S.M. Lohmann, H. de Jonge, U. Walter, and F. Hofmann Cyclic GMP-dependent protein kinases and the cardiovascular system: insights from genetically modified mice Circ Res 93 2003 907 916
35. K.M. Flegal, B.K. Kit, H. Orpana, and B.I. Graubard Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis JAMA 309 2013 71 82
36. U. Forstermann, and W.C. Sessa Nitric oxide synthases: regulation and function Eur Heart J 33 2012 829 837
37. S.H. Francis, M.A. Blount, and J.D. Corbin Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms and physiological functions Physiol Rev 91 2011 651 690
38. S.H. Francis, J.L. Busch, and J.D. Corbin cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action Pharmacol Rev 62 2010 525 563
39. A. Friebe, and D. Koesling The function of NO-sensitive guanylyl cyclase: what we can learn from genetic mouse models Nitric Oxide 21 2009 149 156
40. A. Frontini, and S. Cinti Distribution and development of brown adipocytes in the murine and human adipose organ Cell Metab 11 2010 253 256
41. S. Gesta, Y.H. Tseng, and C.R. Kahn Developmental origin of fat: tracking obesity to its source Cell 131 2007 242 256
42. B. Haas, P. Mayer, K. Jennissen, D. Scholz, M.B. Diaz, and W. Bloch Protein kinase g controls brown fat cell differentiation and mitochondrial biogenesis Sci Signal 2 2009 ra78
43. Y.M. Haidar, and B.C. Cosman Obesity epidemiology Clin Colon Rectal Surg 24 2011 205 210
44. Y. Hara, S. Wakino, Y. Tanabe, M. Saito, H. Tokuyama, and N. Washida Rho and Rho-kinase activity in adipocytes contributes to a vicious cycle in obesity that may involve mechanical stretch Sci Signal 4 2011 ra3
45. J. Hassi, H. Rintamaki, H. Ruskoaho, J. Leppaluoto, and O. Vuolteenaho Plasma levels of endothelin-1 and atrial natriuretic peptide in men during a 2-hour stay in a cold room Acta Physiol Scand 142 1991 481 485
46. S.L. Henry, J.G. Bensley, R.J. Wood-Bradley, L.A. Cullen-McEwen, J.F. Bertram, and J.A. Armitage White adipocytes: more than just fat depots Int J Biochem Cell Biol 44 2012 435 440
47. Y. Higaki, M.F. Hirshman, N. Fujii, and L.J. Goodyear Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle Diabetes 50 2001 241 247
48. A.J. Hobbs, and J.P. Stasch Soluble Guanylate Cyclase: Allosteric Activation and Redox Regulation 2nd ed. 2009 Academic Press Burlington, MA, USA
49. F. Hofmann The biology of cyclic GMP-dependent protein kinases J Biol Chem 280 2005 1 4
50. F. Hofmann, A. Ammendola, and J. Schlossmann Rising behind NO: cGMP-dependent protein kinases J Cell Sci 113 Pt 10 2000 1671 1676
51. G.S. Hotamisligil Inflammation and metabolic disorders Nature 444 2006 860 867
52. M. Inuzuka, N. Tamura, N. Yamada, G. Katsuura, N. Oyamada, and D. Taura C-type natriuretic peptide as a new regulator of food intake and energy expenditure Endocrinology 151 2010 3633 3642
53. L. Jeandel, H. Okamura, M. Belles-Isles, J.G. Chabot, F. Dihl, and G. Morel Immunocytochemical localization, binding, and effects of atrial natriuretic peptide in rat adipocytes Mol Cell Endocrinol 62 1989 69 78
54. K. Jennissen, F. Siegel, M. Liebig-Gonglach, M.R. Hermann, S. Kipschull, and S. van Dooren A VASP-Rac-soluble guanylyl cyclase pathway controls cGMP production in adipocytes Sci Signal 5 2012 ra62
55. S. Kajimura, P. Seale, and B.M. Spiegelman Transcriptional control of brown fat development Cell Metab 11 2010 257 262
56. Y. Kaneko, T. Ishikawa, S. Amano, and K. Nakayama Dual effect of nitric oxide on cytosolic Ca2+ concentration and insulin secretion in rat pancreatic beta-cells Am J Physiol Cell Physiol 284 2003 C1215 C1222
57. R.E. Keesey, and T.L. Powley Body energy homeostasis Appetite 51 2008 442 445
58. D.P. Kelly, and R.C. Scarpulla Transcriptional regulatory circuits controlling mitochondrial biogenesis and function Genes Dev 18 2004 357 368
59. A.K. Kiemer, T. Gerwig, A.L. Gerbes, H. Meissner, M. Bilzer, and A.M. Vollmar Kupffer-cell specific induction of heme oxygenase 1 (hsp32) by the atrial natriuretic peptide - role of cGMP J Hepatol 38 2003 490 498
60. A.K. Kiemer, N.C. Weber, R. Furst, N. Bildner, S. Kulhanek-Heinze, and A.M. Vollmar Inhibition of p38 MAPK activation via induction of MKP-1: atrial natriuretic peptide reduces TNF-alpha-induced actin polymerization and endothelial permeability Circ Res 90 2002 874 881
61. E. Kiskinis, M. Hallberg, M. Christian, M. Olofsson, S.M. Dilworth, and R. White RIP140 directs histone and DNA methylation to silence Ucp1 expression in white adipocytes EMBO J 26 2007 4831 4840
62. T. Kleppisch, and R. Feil cGMP signalling in the mammalian brain: role in synaptic plasticity and behaviour Handb Exp Pharmacol 549-579 2009
63. M. Klingenspor Cold-induced recruitment of brown adipose tissue thermogenesis Exp Physiol 88 2003 141 148
64. M. Klingenspor, T. Fromme, D.A. Hughes Jr., L. Manzke, E. Polymeropoulos, and T. Riemann An ancient look at UCP1 Biochim Biophys Acta 1777 2008 637 641
65. M. Klingenspor, S. Herzig, and A. Pfeifer Brown fat develops a brite future Obes Facts 5 2012 890 896
66. A. Knorr, C. Hirth-Dietrich, C. Alonso-Alija, M. Harter, M. Hahn, and Y. Keim Nitric oxide-independent activation of soluble guanylate cyclase by BAY 60-2770 in experimental liver fibrosis Arzneimittelforschung 58 2008 71 80 10.1055/s-0031-1296471
67. K.J. Koller, D.G. Lowe, G.L. Bennett, N. Minamino, K. Kangawa, and H. Matsuo Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP) Science 252 1991 120 123
68. A. Kosteli, E. Sugaru, G. Haemmerle, J.F. Martin, J. Lei, and R. Zechner Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue J Clin Invest 120 2010 3466 3479
69. M. Kuhn Molecular physiology of natriuretic peptide signalling Basic Res Cardiol 99 2004 76 82
70. C.Y. Lee, H. Lieu, and J.C. Burnett Jr. Designer natriuretic peptides J Investig Med 57 2009 18 21
71. Y.H. Lee, A.P. Petkova, E.P. Mottillo, and J.G. Granneman In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding Cell Metab 15 2012 480 491
72. V. Leiss, A. Friebe, A. Welling, F. Hofmann, and R. Lukowski Cyclic GMP kinase I modulates glucagon release from pancreatic alpha-cells Diabetes 60 2011 148 156
73. B.R. Lindman, A. Zajarias, J.A. Madrazo, J. Shah, B.F. Gage, and E. Novak Effects of phosphodiesterase type 5 inhibition on systemic and pulmonary hemodynamics and ventricular function in patients with severe symptomatic aortic stenosis Circulation 125 2012 2353 2362
74. O. Lisy, B.K. Huntley, D.J. McCormick, P.A. Kurlansky, and J.C. Burnett Jr. Design, synthesis, and actions of a novel chimeric natriuretic peptide: CD-NP J Am Coll Cardiol 52 2008 60 68
75. K.A. Lucas, G.M. Pitari, S. Kazerounian, I. Ruiz-Stewart, J. Park, and S. Schulz Guanylyl cyclases and signaling by cyclic GMP Pharmacol Rev 52 2000 375 414
76. P. Lucotti, E. Setola, L.D. Monti, E. Galluccio, S. Costa, and E.P. Sandoli Beneficial effects of a long-term oral l-arginine treatment added to a hypocaloric diet and exercise training program in obese, insulin-resistant type 2 diabetic patients Am J Physiol Endocrinol Metab 291 2006 E906-912 (Epub 2006 Jun 2013)
77. C.N. Lumeng, J.L. Bodzin, and A.R. Saltiel Obesity induces a phenotypic switch in adipose tissue macrophage polarization J Clin Invest 117 2007 175 184
78. S.Z. Lutz, A.M. Hennige, S. Feil, A. Peter, A. Gerling, and J. Machann Genetic ablation of cGMP-dependent protein kinase type I causes liver inflammation and fasting hyperglycemia Diabetes 60 2011 1566 1576
79. T. Maack Receptors of atrial natriuretic factor Annu Rev Physiol 54 1992 11 27
80. V.O. Melichar, D. Behr-Roussel, U. Zabel, L.O. Uttenthal, J. Rodrigo, and A. Rupin Reduced cGMP signaling associated with neointimal proliferation and vascular dysfunction in late-stage atherosclerosis Proc Natl Acad Sci U S A 101 2004 16671 16676
81. G. Mensink, A. Schienkiewitz, and C. Scheidt-Nave Overweight and obesity in Germany: are we getting fatter? Bundesgesundheitsblatt 980-990 2012
82. S. Meurer, S. Pioch, T. Pabst, N. Opitz, P.M. Schmidt, and T. Beckhaus Nitric oxide-independent vasodilator rescues heme-oxidized soluble guanylate cyclase from proteasomal degradation Circ Res 105 2009 33 41
83. M.M. Mitschke, L.S. Hoffmann, T. Gnad, D. Scholz, K. Kruithoff, and P. Mayer Increased cGMP promotes healthy expansion and browning of white adipose tissue FASEB J 27 2013 1621 1630
84. K. Miyashita, H. Itoh, H. Tsujimoto, N. Tamura, Y. Fukunaga, and M. Sone Natriuretic peptides/cGMP/cGMP-dependent protein kinase cascades promote muscle mitochondrial biogenesis and prevent obesity Diabetes 58 2009 2880 2892
85. M. Mori, H. Nakagami, G. Rodriguez-Araujo, K. Nimura, and Y. Kaneda Essential role for miR-196a in brown adipogenesis of white fat progenitor cells PLoS Biol 10 2012 e1001314
86. K. Morino, S. Neschen, S. Bilz, S. Sono, D. Tsirigotis, and R.M. Reznick Muscle-specific IRS-1 Ser→Ala transgenic mice are protected from fat-induced insulin resistance in skeletal muscle Diabetes 57 2008 2644 2651
87. C. Moro, E. Klimcakova, M. Lafontan, M. Berlan, and J. Galitzky Phosphodiesterase-5A and neutral endopeptidase activities in human adipocytes do not control atrial natriuretic peptide-mediated lipolysis Br J Pharmacol 152 2007 1102 1110
88. C. Moro, and M. Lafontan Natriuretic peptides and cGMP signaling control of energy homeostasis Am J Physiol Heart Circ Physiol 304 2012 30
89. D.L. Morris, and L. Rui Recent advances in understanding leptin signaling and leptin resistance Am J Physiol Endocrinol Metab 297 2009 E1247 E1259
90. F. Murad Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development N Engl J Med 355 2006 2003 2011
91. J. Nedergaard, and B. Cannon The changed metabolic world with human brown adipose tissue: therapeutic visions Cell Metab 11 2010 268 272
92. E. Nisoli, E. Clementi, S. Moncada, and M.O. Carruba Mitochondrial biogenesis as a cellular signaling framework Biochem Pharmacol 67 2004 1 15
93. E. Nisoli, E. Clementi, C. Paolucci, V. Cozzi, C. Tonello, and C. Sciorati Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide Science 299 2003 896 899
94. E. Nisoli, E. Clementi, C. Tonello, C. Sciorati, L. Briscini, and M.O. Carruba Effects of nitric oxide on proliferation and differentiation of rat brown adipocytes in primary cultures Br J Pharmacol 125 1998 888 894
95. N. Petrovic, T.B. Walden, I.G. Shabalina, J.A. Timmons, B. Cannon, and J. Nedergaard 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 2010 7153 7164
96. A. Pfeifer, P. Klatt, S. Massberg, L. Ny, M. Sausbier, and C. Hirneiss Defective smooth muscle regulation in cGMP kinase I-deficient mice EMBO J 17 1998 3045 3051
97. A. Pfeifer, and H. Lehmann Pharmacological potential of RNAi - focus on miRNA Pharmacol Ther 126 2010 217 227
98. A. Pfeifer, P. Ruth, W. Dostmann, M. Sausbier, P. Klatt, and F. Hofmann Structure and function of cGMP-dependent protein kinases Rev Physiol Biochem Pharmacol 135 1999 105 149
99. O. Pivovarova, O. Gogebakan, N. Kloting, A. Sparwasser, M.O. Weickert, and I. Haddad Insulin up-regulates natriuretic peptide clearance receptor expression in the subcutaneous fat depot in obese subjects: a missing link between CVD risk and obesity? J Clin Endocrinol Metab 97 2012 E731 E739
100. J. Polak, C. Moro, E. Klimcakova, M. Kovacikova, M. Bajzova, and M. Vitkova The atrial natriuretic peptide- and catecholamine-induced lipolysis and expression of related genes in adipose tissue in hypothyroid and hyperthyroid patients Am J Physiol Endocrinol Metab 293 2007 E246 E251
101. L.R. Potter, S. Abbey-Hosch, and D.M. Dickey Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions Endocr Rev 27 2006 47 72
102. P. Puigserver, Z. Wu, C.W. Park, R. Graves, M. Wright, and B.M. Spiegelman A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis Cell 92 1998 829 839
103. A.B. Ropero, S. Soriano, E. Tuduri, L. Marroqui, N. Tellez, and B. Gassner The atrial natriuretic peptide and guanylyl cyclase-A system modulates pancreatic beta-cell function Endocrinology 151 2010 3665 3674
104. E.D. Rosen, and O.A. MacDougald Adipocyte differentiation from the inside out Nat Rev Mol Cell Biol 7 2006 885 896
105. N.J. Rothwell, and M.J. Stock A role for brown adipose tissue in diet-induced thermogenesis Nature 281 1979 31 35
106. N.B. Ruderman, S.H. Schneider, and P. Berchtold The "metabolically- obese," normal-weight individual Am J Clin Nutr 34 1981 1617 1621
107. P. Ruth, A. Pfeifer, S. Kamm, P. Klatt, W.R. Dostmann, and F. Hofmann Identification of the amino acid sequences responsible for high affinity activation of cGMP kinase Ialpha J Biol Chem 272 1997 10522 10528
108. M. Saito, Y. Okamatsu-Ogura, M. Matsushita, K. Watanabe, T. Yoneshiro, and J. Nio-Kobayashi High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity Diabetes 58 2009 1526 1531
109. H.H. Schmidt, P.M. Schmidt, and J.P. Stasch NO- and haem-independent soluble guanylate cyclase activators Handb Exp Pharmacol 309-339 2009
110. S. Schulz, S. Singh, R.A. Bellet, G. Singh, D.J. Tubb, and H. Chin The primary structure of a plasma membrane guanylate cyclase demonstrates diversity within this new receptor family Cell 58 1989 1155 1162
111. P. Seale, B. Bjork, W. Yang, S. Kajimura, S. Chin, and S. Kuang PRDM16 controls a brown fat/skeletal muscle switch Nature 454 2008 961 967
112. C. Sengenes, A. Zakaroff-Girard, A. Moulin, M. Berlan, A. Bouloumie, and M. Lafontan Natriuretic peptide-dependent lipolysis in fat cells is a primate specificity Am J Physiol Regul Integr Comp Physiol 283 2002 R257 R265
113. W. Shen, J. Hao, Z. Feng, C. Tian, W. Chen, and L. Packer Lipoamide or lipoic acid stimulates mitochondrial biogenesis in 3T3-L1 adipocytes via the endothelial NO synthase-cGMP-protein kinase G signalling pathway Br J Pharmacol 162 2011 1213 1224
114. A. Shore, A. Karamitri, P. Kemp, J.R. Speakman, and M.A. Lomax Role of Ucp1 enhancer methylation and chromatin remodelling in the control of Ucp1 expression in murine adipose tissue Diabetologia 53 2010 1164 1173
115. J.P. Stasch, and A.J. Hobbs NO-independent, haem-dependent soluble guanylate cyclase stimulators Handb Exp Pharmacol 277-308 2009
116. D.J. Stuehr, H.J. Cho, N.S. Kwon, M.F. Weise, and C.F. Nathan Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: an FAD- and FMN-containing flavoprotein Proc Natl Acad Sci U S A 88 1991 7773 7777
117. S. Suga, K. Nakao, K. Hosoda, M. Mukoyama, Y. Ogawa, and G. Shirakami Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide Endocrinology 130 1992 229 239
118. S. Suga, K. Nakao, H. Itoh, Y. Komatsu, Y. Ogawa, and N. Hama Endothelial production of C-type natriuretic peptide and its marked augmentation by transforming growth factor-beta. Possible existence of "vascular natriuretic peptide system" J Clin Invest 90 1992 1145 1149
119. K. Sun, C.M. Kusminski, and P.E. Scherer Adipose tissue remodeling and obesity J Clin Invest 121 2011 2094 2101
120. L. Sun, H. Xie, M.A. Mori, R. Alexander, B. Yuan, and S.M. Hattangadi Mir193b-365 is essential for brown fat differentiation Nat Cell Biol 13 2011 958 965
121. B.A. Swinburn, G. Sacks, K.D. Hall, K. McPherson, D.T. Finegood, and M.L. Moodie The global obesity pandemic: shaped by global drivers and local environments Lancet 378 2010 804 814
122. N. Tamura, L.K. Doolittle, R.E. Hammer, J.M. Shelton, J.A. Richardson, and D.L. Garbers Critical roles of the guanylyl cyclase B receptor in endochondral ossification and development of female reproductive organs Proc Natl Acad Sci U S A 101 2004 17300 17305
123. W. Tang, D. Zeve, J.M. Suh, D. Bosnakovski, M. Kyba, and R.E. Hammer White fat progenitor cells reside in the adipose vasculature Science 322 2008 583 586
124. S. Tateya, N.O. Rizzo, P. Handa, A.M. Cheng, V. Morgan-Stevenson, and G. Daum Endothelial NO/cGMP/VASP signaling attenuates Kupffer cell activation and hepatic insulin resistance induced by high-fat feeding Diabetes 60 2011 2792 2801
125. M. Trajkovski, K. Ahmed, C.C. Esau, and M. Stoffel MyomiR-133 regulates brown fat differentiation through Prdm16 Nat Cell Biol 14 2012 1330 1335
126. A.B. Vaandrager, E.M. Ehlert, T. Jarchau, S.M. Lohmann, and H.R. de Jonge N-terminal myristoylation is required for membrane localization of cGMP-dependent protein kinase type II J Biol Chem 271 1996 7025 7029
127. W.D. van Marken Lichtenbelt, J.W. Vanhommerig, N.M. Smulders, J.M. Drossaerts, G.J. Kemerink, and N.D. Bouvy Cold-activated brown adipose tissue in healthy men N Engl J Med 360 2009 1500 1508
128. E.J. Verspohl, and I.K. Bernemann Atrial natriuretic peptide (ANP)-induced inhibition of glucagon secretion: mechanism of action in isolated rat pancreatic islets Peptides 17 1996 1023 1029
129. G. Vila, G. Grimm, M. Resl, B. Heinisch, E. Einwallner, and H. Esterbauer B-type natriuretic peptide modulates ghrelin, hunger, and satiety in healthy men Diabetes 61 2012 2592 2596
130. K.A. Virtanen, M.E. Lidell, J. Orava, M. Heglind, R. Westergren, and T. Niemi Functional brown adipose tissue in healthy adults N Engl J Med 360 2009 1518 1525
131. T.J. Wang, M.G. Larson, D. Levy, E.J. Benjamin, E.P. Leip, and P.W. Wilson Impact of obesity on plasma natriuretic peptide levels Circulation 109 2004 594 600
132. Y. Wang, and M.A. Beydoun The obesity epidemic in the United States - gender, age, socioeconomic, racial/ethnic, and geographic characteristics: a systematic review and meta-regression analysis Epidemiol Rev 29 2007 6 28
133. J. Wu, P. Bostrom, L.M. Sparks, L. Ye, J.H. Choi, and A.H. Giang Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human Cell 150 2012 366 376
134. J. Wu, P. Cohen, and B.M. Spiegelman Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev 27 2013 234 250
135. H. You, and S.G. Laychock Long-term treatment with atrial natriuretic peptide inhibits ATP production and insulin secretion in rat pancreatic islets Am J Physiol Endocrinol Metab 300 2011 E435 E444
136. M.E. Young, and B. Leighton Fuel oxidation in skeletal muscle is increased by nitric oxide/cGMP - evidence for involvement of cGMP-dependent protein kinase FEBS Lett 424 1998 79 83
137. M.E. Young, G.K. Radda, and B. Leighton Nitric oxide stimulates glucose transport and metabolism in rat skeletal muscle in vitro Biochem J 322 Pt 1 1997 223 228
138. X. Zhang, J. Ji, G. Yan, J. Wu, X. Sun, and J. Shen Sildenafil promotes adipogenesis through a PKG pathway Biochem Biophys Res Commun 396 2010 1054 1059