The lysyl oxidase inhibitor β-aminopropionitrile reduces body weight gain and improves the metabolic profile in diet-induced obesity in rats

DMM Disease Models and Mechanisms

Volumn 8, Issue 6, 2015, Pages 543-551

  Miana, María ^a,b   Galán, María ^c   Martínez Martínez, Ernesto ^a,b,d   Varona, Saray ^c   Jurado López, Raquel ^a,b   Bausa Miranda, Belén ^a,b   Antequera, Alfonso ^e   Luaces, María ^f   Martínez González, Joś ^c   Rodríguez, Cristina ^c   Cachofeiro, Victoria ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^c Institut Català de Ciències Cardiovasculars   (Spain)

^d Atención Primaria Y Promoción de La Salud   (Spain)

^e HOSPITAL UNIVERSITARIO DE FUENLABRADA   (Spain)

^f HOSPITAL CLÍNICO SAN CARLOS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOPROPIONITRILE; ADIPONECTIN; BETA ACTIN; COLLAGEN; DIPEPTIDYL PEPTIDASE IV; GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; PROCOLLAGEN C PROTEINASE; PROTEIN LYSINE 6 OXIDASE; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRIACYLGLYCEROL; ENZYME INHIBITOR; SLC2A4 PROTEIN, RAT;

3T3 CELL LINE; ADIPOCYTE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET INDUCED OBESITY; DOWN REGULATION; EPIDIDYMIS FAT; EXTRACELLULAR MATRIX; FAT MASS; FEMALE; FIBROSIS; GLUCOSE TRANSPORT; HUMAN; INTRAABDOMINAL FAT; MALE; METABOLIC PARAMETERS; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; WEIGHT REDUCTION; WHITE ADIPOSE TISSUE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL SIZE; DRUG EFFECTS; INSULIN RESISTANCE; LIPID DIET; METABOLISM; METABOLOME; MOUSE; SIGNAL TRANSDUCTION; WEIGHT GAIN; WISTAR RAT;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

3T3-L1 CELLS; ADIPOCYTES; ADIPONECTIN; ADIPOSITY; AMINOPROPIONITRILE; ANIMALS; CELL SIZE; COLLAGEN; DIET, HIGH-FAT; ENZYME INHIBITORS; FEMALE; FIBROSIS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MALE; METABOLOME; MICE; MODELS, BIOLOGICAL; OBESITY; PROTEIN-LYSINE 6-OXIDASE; RATS, WISTAR; SIGNAL TRANSDUCTION; WEIGHT GAIN;

EID: 84930584864     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.020107     Document Type: Article

References (50)

1. Abdennour, M., Reggio, S., Le Naour, G., Liu, Y., Poitou, C., Aron-Wisnewsky, J., Charlotte, F., Bouillot, J.-L., Torcivia, A., Sasso, M. et al. (2014). Association of adipose tissue and liver fibrosis with tissue stiffness in morbid obesity: links with diabetes and BMI loss after gastric bypass. J. Clin. Endocrinol. Metab. 99, 898-907.
2. Ahsan, T., Lottman, L. M., Harwood, F., Amiel, D. and Sah, R. L. (1999). Integrative cartilage repair: inhibition by beta-aminopropionitrile. J. Orthop. Res. 17, 850-857.
3. Alligier, M., Meugnier, E., Debard, C., Lambert-Porcheron, S., Chanseaume, E., Sothier, M., Loizon, E., Hssain, A. A., Brozek, J., Scoazec, J.-Y. et al. (2012). Subcutaneous adipose tissue remodelling during the initial phase of weight gain induced by overfeeding in humans. J. Clin. Endocrinol. Metab. 97, E183-E192.
4. Brasselet, C., Durand, E., Addad, F., Al Haj Zen, A., Smeets, M. B., Laurent-Maquin, D., Bouthors, S., Bellon, G., de Kleijn, D., Godeau, G. et al. (2005). Collagen and elastin cross-linking: a mechanism of constrictive remodelling after arterial injury. Am. J. Physiol. Heart Circ. Physiol. 289, H2228-H2233.
5. Dasler, W. (1954). Isolation of toxic crystals from sweet peas (Lathyrus odoratus). Science 120, 307-308.
6. Dimaculangan, D. D., Chawla, A., Boak, A., Kagan, H. M. and Lazar, M. A. (1994). Retinoic acid prevents downregulation of ras recision gene/lysyl oxidase early in adipocyte differentiation. Differentiation 58, 47-52.
7. Divoux, A., Tordjman, J., Lacasa, D., Veyrie, N., Hugol, D., Aissat, A., Basdevant, A., Guerre-Millo, M., Poitou, C., Zucker, J.-D. et al. (2010). Fibrosis in human adipose tissue: composition, distribution, and link with lipid metabolism and fat mass loss. Diabetes 59, 2817-2825.
8. Eckel, R. H. (2011). The complex metabolic mechanisms relating obesity to hypertriglyceridemia. Arterioscler. Thromb. Vasc. Biol. 31, 1946-1948.
9. Emanuelli, B., Peraldi, P., Filloux, C., Chavey, C., Freidinger, K., Hilton, D. J., Hotamisligil, G. S. and Van, O. E. (2001). SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor-alpha in the adipose tissue of obese mice. J. Biol. Chem. 276, 47944-47949.
10. Erler, J. T., Bennewith, K. L., Nicolau, M., Dornhöfer, N., Kong, C., Le, Q.-T., Chi, J.-T. A., Jeffrey, S. S. and Giaccia, A. J. (2006). Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440, 1222-1226.
11. Goossens, G. H. (2008). The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol. Behav. 94, 206-218.
12. Guilherme, A., Virbasius, J. V., Puri, V. and Czech, M. P. (2008). Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9, 367-377.
13. Halberg, N., Khan, T., Trujillo, M. E., Wernstedt-Asterholm, I., Attie, A. D., Sherwani, S., Wang, Z. V., Landskroner-Eiger, S., Dineen, S., Magalang, U. J. et al. (2009). Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol. Cell. Biol. 29, 4467-4483.
14. Henegar, C., Tordjman, J., Achard, V., Lacasa, D., Cremer, I., Guerre-Millo, M., Poitou, C., Basdevant, A., Stich, V., Viguerie, N. et al. (2008). Adipose tissue transcriptomic signature highlights the pathological relevance of extracellular matrix in human obesity. Genome Biol. 9, R14.
15. Hornstra, I. K., Birge, S., Starcher, B., Bailey, A. J., Mecham, R. P. and Shapiro, S. D. (2003). Lysyl oxidase is required for vascular and diaphragmatic development in mice. J Biol Chem. 278, 14387-14393.
16. Huang, H., Song, T.-J., Li, X., Hu, L., He, Q., Liu, M., Lane, M. D. and Tang, Q.-Q. (2009). BMP signaling pathway isrequired for commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proc. Natl. Acad. Sci. USA 106, 12670-12675.
17. Kadowaki, T., Yamauchi, T., Kubota, N., Hara, K., Ueki, K. and Tobe, K. (2006). Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J. Clin. Invest. 116, 1784-1792.
18. Kanatani, Y., Usui, I., Ishizuka, K., Bukhari, A., Fujisaka, S., Urakaze, M., Haruta, T., Kishimoto, T., Naka, T. and Kobayashi, M. (2007). Effects of pioglitazone on suppressor of cytokine signaling 3 expression: potential mechanisms for its effects on insulin sensitivity and adiponectin expression. Diabetes 56, 795-803.
19. Kern, P. A., Di Gregorio, G. B., Lu, T., Rassouli, N. and Ranganathan, G. (2003). Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes 52, 1779-1785.
20. Khan, T., Muise, E. S., Iyengar, P., Wang, Z. V., Chandalia, M., Abate, N., Zhang, B. B., Bonaldo, P., Chua, S. and Scherer, P. E. (2009). Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol. Cell. Biol. 29, 1575-1591.
21. Kothapalli, D., Liu, S.-L., Bae, Y. H., Monslow, J., Xu, T., Hawthorne, E. A., Byfield, F. J., Castagnino, P., Rao, S., Rader, D. J. et al. (2012). Cardiovascular protection by ApoE and ApoE-HDL linked to suppression of ECM gene expression and arterial stiffening. Cell Rep. 2, 1259-1271.
22. Lamers, D., Famulla, S., Wronkowitz, N., Hartwig, S., Lehr, S., Ouwens, D. M., Eckardt, K., Kaufman, J. M., Ryden, M., Muller, S. et al. (2011). Dipeptidyl peptidase 4 is a novel adipokine potentially linking obesity to the metabolic syndrome. Diabetes 60, 1917-1925.
23. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F. T., Csiszar, K., Giaccia, A., Weninger, W. et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906.
24. Mäki, J. M., Räsänen, J., Tikkanen, H., Sormunen, R., Mäkikallio, K., Kivirikko, K. I. and Soininen, R. (2002). Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation 106, 2503-2509.
25. Martínez-Martínez, E., Jurado-López, R., Valero-Muñoz, M., Bartolomé, M. V., Ballesteros, S., Luaces, M., Briones, A. M., López-Andrés, N., Miana, M. and Cachofeiro, V. (2014a). Leptin induces cardiac fibrosis through galectin-3, mTOR and oxidative stress: potential role in obesity. J. Hypertens. 32, 1104-1114.
26. Martínez-Martínez, E., Miana, M., Jurado-López, R., Bartolomé, M. V., Souza Neto, F. V., Salaices, M., López-Andrés, N. and Cachofeiro, V. (2014b). The potential role of leptin in the vascular remodelling associated with obesity. Int. J. Obes. (Lond.) 38, 1565-1572.
27. Miana, M., de Las Heras, N., Rodriguez, C., Sanz-Rosa, D., Martin-Fernandez, B., Mezzano, S., Lahera, V., Martinez-Gonzalez, J. and Cachofeiro, V. (2011). Effect of eplerenone on hypertension-associated renal damage in rats: potential role of peroxisome proliferator activated receptor gamma (PPAR-gamma). J. Physiol. Pharmacol. 62, 87-94.
28. Mutch, D. M., Rouault, C., Keophiphath, M., Lacasa, D. and Clément, K. (2009). Using gene expression to predict the secretome of differentiating human preadipocytes. Int. J. Obes. (Lond.) 33, 354-363.
29. Nave, A. H., Mižíková, I., Niess, G., Steenbock, H., Reichenberger, F., Talavera, M. L., Veit, F., Herold, S., Mayer, K., Vadász, I. et al. (2014). Lysyl oxidases play a causal role in vascular remodelling in clinical and experimental pulmonary arterial hypertension. Arterioscler. Thromb. Vasc. Biol. 34, 1446-1458.
30. Orriols, M., Guadall, A., Galán, M., Martí-Pàmies, I., Varona, S., Rodríguez-Calvo, R., Briones, A. M., Navarro, M. A., de Diego, A., Osada, J. et al. (2014). Lysyl oxidase (LOX) in vascular remodelling. Insight from a new animal model. Thromb. Haemost. 112, 812-824.
31. Palanivel, R., Fullerton, M. D., Galic, S., Honeyman, J., Hewitt, K. A., Jorgensen, S. B. and Steinberg, G. R. (2012). Reduced Socs3 expression in adipose tissue protects female mice against obesity-induced insulin resistance. Diabetologia 55, 3083-3093.
32. Raposo, B., Rodríguez, C., Martínez-González, J. and Badimon, L. (2004). High levels of homocysteine inhibit lysyl oxidase (LOX) and downregulate LOX expression in vascular endothelial cells. Atherosclerosis 177, 1-8.
33. Rodríguez, C., Raposo, B., Martínez-González, J., Casaní, L. and Badimon, L. (2002). Low density lipoproteins downregulate lysyl oxidase in vascular endothelial cells and the arterial wall. Arterioscler. Thromb. Vasc. Biol. 22, 1409-1414.
34. Rodríguez, C., Martinez-Gonzalez, J., Raposo, B., Alcudia, J. F., Guadall, A. and Badimon, L. (2008a). Regulation of lysyl oxidase in vascular cells: lysyl oxidase as a new player in cardiovascular diseases. Cardiovasc. Res. 79, 7-13.
35. Rodríguez, C., Rodríguez-Sinovas, A. and Martínez-González, J. (2008b). Lysyl oxidase as a potential therapeutic target. Drug News Perspect. 21, 218-224.
36. Rodriguez, C., Alcudia, J. F., Martinez-Gonzalez, J., Guadall, A., Raposo, B., Sanchez-Gomez, S. and Badimon, L. (2009). Statins normalize vascular lysyl oxidase down-regulation induced by proatherogenic risk factors. Cardiovasc. Res. 83, 595-603.
37. Sell, H., Bluher, M., Kloting, N., Schlich, R., Willems, M., Ruppe, F., Knoefel, W. T., Dietrich, A., Fielding, B. A., Arner, P. et al. (2013). Adipose dipeptidyl peptidase-4 and obesity: correlation with insulin resistance and depot-specific release from adipose tissue in vivo and in vitro. Diabetes Care. 36, 4083-4090.
38. Sethi, J. K. and Hotamisligil, G. S. (1999). The role of TNF alpha in adipocyte metabolism. Semin. Cell Dev. Biol. 10, 19-29.
39. Shepherd, P. R. and Kahn, B. B. (1999). Glucose transporters and insulin action-implications for insulin resistance and diabetes mellitus. N. Engl. J. Med. 341, 248-257.
40. Spencer, P. S. and Schaumburg, H. H. (1983). Lathyrism: a neurotoxic disease. Neurobehav. Toxicol. Teratol. 5, 625-629.
41. Stefanon, I., Valero-Muñoz, M., Fernandes, A. A., Ribeiro, R. F., Jr, Rodríguez, C., Miana, M., Martínez-González, J., Spalenza, J. S., Lahera, V., Vassallo, P. F. et al. (2013). Left and right ventricle late remodelling following myocardial infarction in rats. PLoS ONE 8, e64986.
42. Stephens, J. M., Lee, J. and Pilch, P. F. (1997). Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J. Biol. Chem. 272, 971-976.
43. Tam, C. S., Tordjman, J., Divoux, A., Baur, L. A. and Cle?ent, K. (2012). Adipose tissue remodelling in children: the link between collagen deposition and age-related adipocyte growth. J. Clin. Endocrinol. Metab. 97, 1320-1327.
44. Tang, S. S., Trackman, P. C. and Kagan, H. M. (1983). Reaction of aortic lysyl oxidase with beta-aminopropionitrile. J. Biol. Chem. 258, 4331-4338.
45. Taskinen, M.-R., Adiels, M., Westerbacka, J., Soderlund, S., Kahri, J., Lundbom, N., Lundbom, J., Hakkarainen, A., Olofsson, S.-O., Orho-Melander, M. et al. (2011). Dual metabolic defects are required to produce hypertriglyceridemia in obese subjects. Arterioscler. Thromb. Vasc. Biol. 31, 2144-2150.
46. Trayhurn, P. (2013). Hypoxia and adipose tissue function and dysfunction in obesity. Physiol. Rev. 93, 1-21.
47. Turecek, C., Fratzl-Zelman, N., Rumpler, M., Buchinger, B., Spitzer, S., Zoehrer, R., Durchschlag, E., Klaushofer, K., Paschalis, E. P. and Varga, F. (2008). Collagen cross-linking influences osteoblastic differentiation. Calcif. Tissue Int. 82, 392-400.
48. Virtue, S. and Vidal-Puig, A. (2010). Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome-an allostatic perspective. Biochim. Biophys. Acta 1801, 338-349.
49. Walker, R. W., Allayee, H., Inserra, A., Fruhwirth, R., Alisi, A., Devito, R., Carey, M. E., Sinatra, F., Goran, M. I. and Nobili, V. (2014). Macrophages and fibrosis in adipose tissue are linked to liver damage and metabolic risk in obese children. Obesity(Silver Spring) 22, 1512-1519.
50. Wang, Z., Zhou, Y.-T., Kakuma, T., Lee, Y., Kalra, S. P. and Kalra, P. S. (2000). Leptin resistance of adipocytes in obesity: role of suppressors of cytokine signaling. Biochem. Biophys. Res. Commun. 277, 20-26.