Soluble LR11/SorLA represses thermogenesis in adipose tissue and correlates with BMI in humans

Nature Communications

Volumn 6, Issue , 2015, Pages

  Whittle, Andrew J ^a   Jiang, Meizi ^b,c   Peirce, Vivian ^a   Relat, Joana ^d   Virtue, Sam ^a   Ebinuma, Hiroyuki ^e   Fukamachi, Isamu ^e   Yamaguchi, Takashi ^b   Takahashi, Mao ^b   Murano, Takeyoshi ^b   Tatsuno, Ichiro ^b   Takeuchi, Masahiro ^f   Nakaseko, Chiaki ^f   Jin, Wenlong ^g   Jin, Zhehu ^g   Campbell, Mark ^a   Schneider, Wolfgang J ^h   Vidal Puig, Antonio ^a,i   Bujo, Hideaki ^b,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b TOHO UNIVERSITY   (Japan)

^c CHIBA UNIVERSITY   (Japan)

^d UNIVERSITY OF BARCELONA   (Spain)

^e SEKISUI CHEMICAL CO LTD   (Japan)

^f CHIBA UNIVERSITY HOSPITAL   (Japan)

^g YANBIAN UNIVERSITY   (China)

^h MEDICAL UNIVERSITY OF VIENNA   (Austria)

ⁱ WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ 2; BONE MORPHOGENETIC PROTEIN; CHOLESTEROL; FAT DROPLET; GLUCOSE; INSULIN; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; OSTEOGENIC PROTEIN 1; SMAD PROTEIN; SOLUBLE LR11 PROTEIN; SORTILIN; TRANSFORMING GROWTH FACTOR BETA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CARRIER PROTEIN; SORL1 PROTEIN, HUMAN; SORL1 PROTEIN, MOUSE;

BODY MASS; CELLS AND CELL COMPONENTS; DIET; HEAT PRODUCTION; MAMMAL; METABOLISM; OBESITY; PHYSIOLOGY; PROTEIN; RODENT;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; BROWN ADIPOCYTE; BROWN ADIPOSE TISSUE; CELL RESPIRATION; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; DIET INDUCED OBESITY; ENERGY EXPENDITURE; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; HUMAN; HYPERMETABOLISM; IN VIVO STUDY; LIPID OXIDATION; LIPID STORAGE; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SLEEP DISORDERED BREATHING; THERMOGENESIS; TRIACYLGLYCEROL BLOOD LEVEL; VASCULAR SMOOTH MUSCLE CELL; WEIGHT GAIN; WHITE ADIPOSE TISSUE; ANIMAL; BLOOD; C57BL MOUSE; DOWN REGULATION; ENERGY METABOLISM; FEMALE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY;

MAMMALIA; MUS;

ADIPOSE TISSUE, BROWN; ANIMALS; BODY MASS INDEX; DOWN-REGULATION; ENERGY METABOLISM; FEMALE; HUMANS; LDL-RECEPTOR RELATED PROTEINS; MALE; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OBESITY; RECEPTORS, LDL; THERMOGENESIS;

EID: 84947718853     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9951     Document Type: Article

References (40)

1. Bostrom, P. et al. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463-468 (2012).
2. Leonardsson, G. et al. Nuclear receptor corepressor RIP140 regulates fat accumulation. Proc. Natl Acad. Sci. USA 101, 8437-8442 (2004).
3. Whittle, A. J. et al. BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell 149, 871-885 (2012).
4. Cypess, A. M. et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517 (2009).
5. Nedergaard, J., Bengtsson, T., Cannon, B. Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 293, E444-E452 (2007).
6. Zingaretti, M. C. et al. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 23, 3113-3120 (2009).
7. Ouellet, V. et al. Outdoor temperature, age, sex, body mass index, and diabetic status determine the prevalence, mass, and glucose-uptake activity of 18F-FDGdetected BAT in humans. J. Clin. Endocrinol. Metab. 96, 192-199 (2011).
8. Lee, P. et al. Temperature-acclimated brown adipose tissue modulates insulin sensitivity in humans. Diabetes 63, 3686-3698 (2014).
9. Whittle, A. Searching for ways to switch on brown fat: are we getting warmer J. Mol. Endocrinol. 49, R79-R87 (2012).
10. Dodson, S. E. et al. Loss of LR11/SORLA enhances early pathology in a mouse model of amyloidosis: evidence for a proximal role in Alzheimer's disease. J. Neurosci. 28, 12877-12886 (2008).
11. Jiang, M. et al. Ang II-stimulated migration of vascular smooth muscle cells is dependent on LR11 in mice. J. Clin. Invest. 118, 2733-2746 (2008).
12. Ohwaki, K. et al. A secreted soluble form of LR11, specifically expressed in intimal smooth muscle cells, accelerates formation of lipid-laden macrophages. Arterioscler. Thromb. Vasc. Biol. 27, 1050-1056 (2007).
13. Taira, K. et al. LR11, a mosaic LDL receptor family member, mediates the uptake of ApoE-rich lipoproteins in vitro. Arterioscler. Thromb. Vasc. Biol. 21, 1501-1506 (2001).
14. Bartelt, A. et al. Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 17, 200-205 (2011).
15. Klinger, S. C. et al. SorLA regulates the activity of lipoprotein lipase by intracellular trafficking. J. Cell. Sci. 124, 1095-1105 (2011).
16. Nishii, K. et al. The soluble form of LR11 protein is a regulator of hypoxiainduced, urokinase-type plasminogen activator receptor (uPAR)-mediated adhesion of immature hematological cells. J. Biol. Chem. 288, 11877-11886 (2013).
17. Kanaki, T. et al. Developmental regulation of LR11 expression in murine brain. DNA Cell Biol. 17, 647-657 (1998).
18. Crossno, Jr. J. T., Majka, S. M., Grazia, T., Gill, R. G., Klemm, D. J. Rosiglitazone promotes development of a novel adipocyte population from bone marrowderived circulating progenitor cells. J. Clin. Invest. 116, 3220-3228 (2006).
19. Feldmann, H. M., Golozoubova, V., Cannon, B., Nedergaard, J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 9, 203-209 (2009).
20. Matsuo, M. et al. Development of an immunoassay for the quantification of soluble LR11, a circulating marker of atherosclerosis. Clin. Chem. 55, 1801-1808 (2009).
21. Cannon, B., Nedergaard, J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359 (2004).
22. Boon, M. R. et al. BMP7 activates brown adipose tissue and reduces dietinduced obesity only at subthermoneutrality. PLoS ONE 8, e74083 (2013).
23. Schulz, T. J. et al. Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature 495, 379-383 (2013).
24. Schulz, T. J. et al. Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proc. Natl Acad. Sci. USA 108, 143-148 (2011).
25. Tseng, Y. H. et al. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454, 1000-1004 (2008).
26. Bohm, C. et al. SorLA signaling by regulated intramembrane proteolysis. J. Biol. Chem. 281, 14547-14553 (2006).
27. Werling, M. et al. Increased postprandial energy expenditure may explain superior long term weight loss after Roux-en-Y gastric bypass compared to vertical banded gastroplasty. PLoS ONE 8, e60280 (2013).
28. Faria, S. L., Faria, O. P., Cardeal Mde, A., Ito, M. K., Buffington, C. Dietinduced thermogenesis and respiratory quotient after Roux-en-Y gastric bypass surgery: a prospective study. Surg. Obes. Relat. Dis. 10, 138-143 (2014).
29. Pottier, C. et al. High frequency of potentially pathogenic SORL1 mutations in autosomal dominant early-onset Alzheimer disease. Mol. Psychiatry 17, 875-879 (2012).
30. Takahashi, M. et al. Enhanced circulating soluble LR11 in patients with coronary organic stenosis. Atherosclerosis 210, 581-584 (2010).
31. Whittle, A., Relat-Pardo, J., Vidal-Puig, A. Pharmacological strategies for targeting BAT thermogenesis. Trends Pharmacol. Sci. 34, 347-355 (2013).
32. Christian, M. et al. RIP140-targeted repression of gene expression in adipocytes. Mol. Cell. Biol. 25, 9383-9391 (2005).
33. Gerhart-Hines, Z. et al. The nuclear receptor Rev-erbalpha controls circadian thermogenic plasticity. Nature 503, 410-413 (2013).
34. Virtue, S., Even, P., Vidal-Puig, A. Below thermoneutrality, changes in activity do not drive changes in total daily energy expenditure between groups of mice. Cell Metab. 16, 665-671 (2012).
35. Elia, M., Livesey, G. Energy expenditure and fuel selection in biological systems: the theory and practice of calculations based on indirect calorimetry and tracer methods. World Rev. Nutr. Diet. 70, 68-131 (1992).
36. Arch, J. R., Hislop, D., Wang, S. J., Speakman, J. R. Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int. J. Obes. (Lond.) 30, 1322-1331 (2006).
37. Asada, S. et al. Ceiling culture-derived proliferative adipocytes retain high adipogenic potential suitable for use as a vehicle for gene transduction therapy. Am. J. Physiol. Cell. Physiol. 301, C181-C185 (2011).
38. Murano, T., Sako, T., Oikawa, S., Shirai, K. The recovery of dysfunctional lipoprotein lipase (Asp204-Glu) activity by modification of substrate. Atherosclerosis 183, 101-107 (2005).
39. Fujimura, K. et al. Circulating LR11 is a novel soluble-receptor marker for early-stage clinical conditions in patients with non-Hodgkin's lymphoma. Clin. Chim. Acta 430, 48-54 (2014).
40. Nakata, Z. et al. Crystallization and preliminary crystallographic analysis of human LR11 Vps10p domain. Acta. Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 129-132 (2011)