Phospholipase C-related Catalytically Inactive Protein Is a New Modulator of Thermogenesis Promoted by β-Adrenergic Receptors in Brown Adipocytes

Journal of Biological Chemistry

Volumn 291, Issue 8, 2016, Pages 4185-4196

  Oue, Kana ^a   Zhang, Jun ^a   Harada Hada, Kae ^a   Asano, Satoshi ^a   Yamawaki, Yosuke ^a   Hayashiuchi, Masaki ^a   Furusho, Hisako ^a   Takata, Takashi ^a   Irifune, Masahiro ^a   Hirata, Masato ^b   Kanematsu, Takashi ^a,c  

^a HIROSHIMA UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; ENZYMES; GENE EXPRESSION; GENES; MAMMALS; METABOLISM; PHYSIOLOGY;

BETA ADRENERGIC RECEPTOR; ENERGY EXPENDITURE; HORMONE-SENSITIVE LIPASE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PROTEIN EXPRESSIONS; PROTEIN PHOSPHATASE; UNCOUPLING PROTEIN-1; WHITE ADIPOSE TISSUES;

PROTEINS;

BETA 3 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; GLUCOSE; INSULIN; MESSENGER RNA; PERILIPIN; PHOSPHOLIPASE C; PHOSPHOLIPASE C RELATED CATALYTICALLY INACTIVE PROTEIN; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; FAT INTAKE; ION CHANNEL; MITOCHONDRIAL PROTEIN; NCOA6 PROTEIN, MOUSE; NUCLEAR RECEPTOR COACTIVATOR; UCP1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; BROWN ADIPOCYTE; COLD EXPOSURE; CONTROLLED STUDY; DIO2 GENE; ENERGY EXPENDITURE; ENERGY METABOLISM; GENE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HISTOLOGY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; LIPOLYSIS; LOCOMOTION; MALE; MOUSE; NONHUMAN; OBESITY; PCG1 GENE; PHENOTYPE; PHOSPHORYLATION; PPAR GENE; PRIORITY JOURNAL; PRIP1 GENE; PRIP2 GENE; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE; THERMOGENESIS; UCP1 GENE; WILD TYPE MOUSE; ADVERSE EFFECTS; ANIMAL; CHEMICALLY INDUCED; FAT INTAKE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHARMACOLOGY;

ADIPOCYTES, BROWN; ANIMALS; DIETARY FATS; ION CHANNELS; LIPOLYSIS; MICE; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; NUCLEAR RECEPTOR COACTIVATORS; OBESITY; THERMOGENESIS; UNCOUPLING PROTEIN 1;

EID: 84964575888     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.705723     Document Type: Article

References (49)

1. Spiegelman, B. M., and Flier, J. S. (2001) Obesity and the regulation of energy balance. Cell 104, 531-543
2. Woods, S. C., and D'Alessio, D. A. (2008) Central control of body weight and appetite. J. Clin. Endocrinol. Metab. 93, S37-50
3. Harms, M., and Seale, P. (2013) Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19, 1252-1263
4. van 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
5. Virtanen, K. A., Lidell, M.E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., and Savisto, N. J., Enerbäck, S., and Nuutila, P. (2009) Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525
6. Cannon, B., and Nedergaard, J. (2004) Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359
7. Fedorenko, A., and Lishko, P. V., and Kirichok, Y. (2012) Mechanism of fattyacid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151, 400-413
8. Mottillo, E. P., and Bloch, A. E., Leff, T., and Granneman, J. G. (2012) Lipolytic products activate peroxisome proliferator-activated receptor (PPAR) α and δ in brown adipocytes to match fatty acid oxidation with supply. J. Biol. Chem. 287, 25038-25048
9. Granneman, J. G., and Moore, H. P., Krishnamoorthy, R., and Rathod, M. (2009) Perilipin controls lipolysis by regulating the interactions of AB-hydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). J. Biol. Chem. 284, 34538-34544
10. Anthonsen, M. W., Rönnstrand, L., Wernstedt, C., Degerman, E., and Holm, C. (1998) Identification of novel phosphorylation sites in hormone-sensitive lipase that are phosphorylated in response to isoproterenol and govern activation properties in vitro. J. Biol. Chem. 273, 215-221
11. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., and Spiegelman, B. M. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839
12. Cao, W., and Daniel, K. W., Robidoux, J., Puigserver, P., Medvedev, A. V., Bai, X., and Floering, L. M., Spiegelman, B. M., and Collins, S. (2004) 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
13. Wood, S. L., Emmison, N., Borthwick, A. C, and Yeaman, S. J. (1993) The protein phosphatases responsible for dephosphorylation of hormone-sensitive lipase in isolated rat adipocytes. Biochem. J. 295, 531-535
14. Clifford, G. M., and McCormick, D. K., Londos, C, and Vernon, R. G., and Yeaman, S. J. (1998) Dephosphorylation of perilipin by protein phosphatases present in rat adipocytes. FEBSLett. 435, 125-129
15. Kinney, B. P., Qiao, L., Levaugh, J. M., and Shao, J. (2010) B56α/protein phosphatase 2A inhibits adipose lipolysis in high-fat diet-induced obese mice. Endocrinology 151, 3624-3632
16. Kanematsu, T., Takeya, H., Watanabe, Y., Ozaki, S., Yoshida, M., Koga, T., Iwanaga, S., and Hirata, M. (1992) Putative inositol 1,4,5-trisphosphate binding proteins in rat brain cytosol. J. Biol. Chem. 267, 6518-6525
17. Yoshida, M., Kanematsu, T., Watanabe, Y., Koga, T., Ozaki, S., Iwanaga, S., and Hirata, M. (1994) D-myo-Inositol 1,4,5-trisphosphate-binding proteins in rat brain membranes. J. Biochem. 115, 973-980
18. Kanematsu, T., Misumi, Y., Watanabe, Y., Ozaki, S., Koga, T., Iwanaga, S., Ikehara, Y., and Hirata, M. (1996) A new inositol 1,4,5-trisphosphate binding protein similar to phospholipase C-S 1. Biochem. J. 313, 319-325
19. Takeuchi, H., Kanematsu, T., Misumi, Y., Yaakob, H. B., Yagisawa, H., Ikehara, Y., Watanabe, Y., Tan, Z., and Shears, S. B., and Hirata, M. (1996) Localization of a high-affinity inositol 1,4,5-trisphosphate/inositol 1,4,5,6-tetrakisphosphate binding domain to the pleckstrin homology module of a new 130 kDa protein: characterization of the determinants of structural specificity. Biochem. J. 318, 561-568
20. Kanematsu, T., Yoshimura, K., Hidaka, K., Takeuchi, H., Katan, M., and Hirata, M. (2000) Domain organization of p130, PLC-related catalytically inactive protein, and structural basis for the lack of enzyme activity. Eur. J. Biochem. 267, 2731-2737
21. Kitayama, T., Morita, K., Sultana, R., Kikushige, N., Mgita, K., Ueno, S., Hirata, M., and Kanematsu, T. (2013) Phospholipase C-related but catalytically inactive protein modulates pain behavior in a neuropathic pain model in mice. Mol. Pain. 9, 23
22. Umebayashi, H., Mizokami, A., Matsuda, M., Harada, K., Takeuchi, H., Tanida, I., Hirata, M., and Kanematsu, T. (2013) Phospholipase C-related catalytically inactive protein, a novel microtubule-associated protein 1 light chain 3-binding protein, negatively regulates autophagosome formation. Biochem. Biophys. Res. Commun. 432, 268-274
23. Harada-Hada, K., Harada, K., Kato, F., Hisatsune, J., Tanida, I., Ogawa, M., Asano, S., Sugai, M., Hirata, M., and Kanematsu, T. (2014) Phospholipase C-related catalytically inactive protein participates in the autophagic elimination of Staphylococcus aureus infecting mouse embryonic fibroblasts. PLoS ONE 9, e98285
24. Yoshimura, K., Takeuchi, H., Sato, O., Hidaka, K., Doira, N., Terunuma, M., Harada, K., Ogawa, Y., Ito, Y., Kanematsu, T., and Hirata, M. (2001) Interaction of p130 with, and consequent inhibition of, the catalytic sub-unit of protein phosphatase 1a. J. Biol. Chem. 276, 17908-17913
25. A receptor function. EMBOJ. 21, 1004-1011
26. A receptor phospho-dependent modulation is regulated by phospholipase C-related inactive protein type 1, a novel protein phosphatase 1 anchoring protein. J. Neurosci. 24, 7074-7084
27. A receptor phosphorylation and membrane trafficking by phospholipase C-related inactive protein/protein phosphatase 1 and 2A signaling complex underlying brain-derived neurotrophic factor-dependent regulation of GABAergic inhibition. J. Biol. Chem. 281, 22180-22189
28. A receptors to the cell surface. J. Neurosci. 27, 1692-1701
29. Fujii, M., Kanematsu, T., Ishibashi, H., Fukami, K., Takenawa, T., Nakayama, K. I., and Moss, S. J., Nabekura, J., and Hirata, M. (2010) Phospholipase C-related but catalytically inactive protein is required for insulin-induced cell surface expression of 7-aminobutyric acid type A receptors. J. Biol. Chem. 285, 4837-4846
30. Sugiyama, G., Takeuchi, H., Nagano, K., Gao, J., Ohyama, Y., Mori, Y., and Hirata, M. (2012) Regulated interaction of protein phosphatase 1 and protein phosphatase 2A with phospholipase C-related, but catalytically inactive protein. Biochemistry 51, 3394-3403
31. Okumura, T., Harada, K., Oue, K., Zhang, J., Asano, S., Hayashiuchi, M., Mizokami, A., Tanaka, H., Irifune, M., Kamata, N., Hirata, M., and Kanematsu, T. (2014) Phospholipase C-related catalytically inactive protein (PRIP) regulates lipolysis in adipose tissue by modulating the phosphorylation of hormone-sensitive lipase. PLoS ONE 9, e100559
32. Takenaka, K., Fukami, K., Otsuki, M., Nakamura, Y., Kataoka, Y., Wada, M., Tsuji, K., Nishikawa, S., Yoshida, N., and Takenawa, T. (2003) Role of phospholipase C-L2, a novel phospholipase C-like protein that lacks lipase activity, in B-cell receptor signaling. Mol. Cell. Biol. 23, 7329-7338
33. McLean, J. A. (1987) Analysis of gaseous exchange in open-circuit indirect calorimetry. Med. Biol. Eng. Comput. 25, 239-240
34. Hernandez, A., de Mena, R. M., Martin, E., and Obregon, M. J. (2011) Differences in the response of UCP1 mRNA to hormonal stimulation between rat and mouse primary cultures of brown adipocytes. Cell. Physiol. Biochem. 28, 969-980
35. Feldmann, H. M., Golozoubova, V., Cannon, B., and Nedergaard, J. (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 9, 203-209
36. Galmozzi, A., and Sonne, S. B., Altshuler-Keylin, S., Hasegawa, Y., Shinoda, K., Luijten, I. H., and Chang, J. W., Sharp, L. Z., Cravatt, B. F., Saez, E., and Kajimura, S. (2014) ThermoMouse: an in vivo model to identify modulators of UCP1 expression in brown adipose tissue. CellRep. 9, 1584-1593
37. Zurlo, F., Larson, K., Bogardus, C, and Ravussin, E. (1990) Skeletal muscle metabolism is a major determinant of resting energy expenditure. J. Clin. Invest. 86, 1423-1427
38. Lampidonis, A. D., Rogdakis, E., Voutsinas, G. E., and Stravopodis, D. J. (2011) The resurgence of hormone-sensitive lipase (HSL) in mammalian lipolysis. Gene 477, 1-11
39. Collins, S., and Surwit, R. S. (2001) The beta-adrenergic receptors and the control of adipose tissue metabolism and thermogenesis. Recent Prog. Horm. Res. 56, 309-328
40. Nicholls, D. G. (1974) Hamster brown-adipose-tissue mitochondria. The chloride permeability of the inner membrane under respiring conditions, the influence of purine nucleotides. Eur. J. Biochem. 49, 585-593
41. Kozak, U. C, Kopecky, J., Teisinger, J., Enerbäck, S., Boyer, B., and Kozak, L. P. (1994) An upstream enhancer regulating brown-fat-specific expression of the mitochondrial uncoupling protein gene. Mol. Cell. Biol. 14, 59-67
42. Hondares, E., Rosell, M., Díaz-Delfin, J., Olmos, Y., Monsalve, M., Iglesias, R., Villarroya, F., and Giralt, M. (2011) Peroxisome proliferator-activated receptor α (PPARα) induces PPAR7 coactivator 1alpha (PGC-1α) gene expression and contributes to thermogenic activation of brown fat: involvement of PRDM16. J. Biol. Chem. 286, 43112-43122
43. Barbera, M. J., Schluter, A., Pedraza, N., Iglesias, R., Villarroya, F., and Giralt, M. (2001) Peroxisome proliferator-activated receptor α activates transcription of the brown fat uncoupling protein-1 gene: a link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J. Biol. Chem. 276, 1486-1493
44. Kajimura, S., and Saito, M. (2014) A new era in brown adipose tissue biology: molecular control of brown fat development and energy homeostasis. Annu. Rev. Physiol. 76, 225-249
45. Rim, J. S., and Kozak, L. P. (2002) 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
46. Robidoux, J., Cao, W., Quan, H., Daniel, K. W., Moukdar, F., Bai, X., Floering, L. M., and Collins, S. (2005) Selective activation of mitogen-activated protein (MAP) kinase kinase 3 and p38α MAP kinase is essential for cyclic AMP-dependent UCP1 expression in adipocytes. Mol. Cell. Biol. 25, 5466-5479
47. Wu, Q., Kazantzis, M., Doege, H., Ortegon, A. M., Tsang, B., Falcon, A., and Stahl, A. (2006) Fatty acid transport protein 1 is required for non-shivering thermogenesis in brown adipose tissue. Diabetes 55, 3229-3237
48. Bartelt, A., and Bruns, O. T., Reimer, R., Hohenberg, H., Ittrich, H., Peldschus, K., Kaul, M. G., and Tromsdorf, U. I., Weller, H., Waurisch, C, Eychmüller, A., Gordts, P. L., Rinninger, F., Bruegelmann, K., Freund, B., Nielsen, P., Merkel, M., and Heeren, J. (2011) Brown adipose tissue activity controls triglyceride clearance. Nat Med. 17, 200-205
49. Hirata, M., Suzuki, M., Ishii, R., Satow, R., Uchida, T., Kitazumi, T., Sasaki, T., Kitamura, T., Yamaguchi, H., Nakamura, Y., and Fukami, K. (2011) Genetic defect in phospholipase CS1 protects mice from obesity by regulating thermogenesis and adipogenesis. Diabetes 60, 1926-1937