Heparanase affects food intake and regulates energy balance in mice

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Karlsson Lindahl, Linda ^a   Schmidt, Linnéa ^a   Haage, David ^b   Hansson, Caroline ^a   Taube, Magdalena ^a   Egeciouglu, Emil ^a   Tan, Ying xia ^e   Admyre, Therese ^c   Jansson, John Olov ^a   Vlodavsky, Israel ^d   Li, Jin Ping ^e   Lindahl, Ulf ^e   Dickson, Suzanne L ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c ASTRAZENECA R AND D   (Sweden)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARANASE; MELANOCORTIN 4 RECEPTOR; AGOUTI RELATED PROTEIN; AGRP PROTEIN, MOUSE; ALPHA INTERMEDIN; BETA GLUCURONIDASE; MC4R PROTEIN, MOUSE; SYNDECAN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY FAT; BODY WEIGHT; CONTROLLED STUDY; ENERGY BALANCE; FOOD INTAKE; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PROTEIN FUNCTION; WILD TYPE; ANIMAL; C57BL MOUSE; CROSS BREEDING; EATING; ENERGY METABOLISM; FAT INTAKE; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AGOUTI; MUS;

AGOUTI-RELATED PROTEIN; ALPHA-MSH; ANIMALS; BODY COMPOSITION; BODY WEIGHT; CROSSES, GENETIC; DIETARY FATS; EATING; ENERGY METABOLISM; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONIDASE; INFUSIONS, INTRAVENTRICULAR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTOR, MELANOCORTIN, TYPE 4; SIGNAL TRANSDUCTION; SYNDECAN-3;

EID: 84858991292     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034313     Document Type: Article

References (41)

1. Wang Y, Beydoun MA, (2007) 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: 6-28.
2. Woods SC, D'Alessio DA, (2008) Central control of body weight and appetite. J Clin Endocrinol Metab 93: S37-50.
3. Coll AP, Farooqi IS, O'Rahilly S, (2007) The hormonal control of food intake. Cell 129: 251-262.
4. Schwartz MW, Morton GJ, (2002) Obesity: keeping hunger at bay. Nature 418: 595-597.
5. Tolle V, Low MJ, (2008) In vivo evidence for inverse agonism of Agouti-related peptide in the central nervous system of proopiomelanocortin-deficient mice. Diabetes 57: 86-94.
6. Yeo GS, Farooqi IS, Aminian S, Halsall DJ, Stanhope RG, et al. (1998) A frameshift mutation in MC4R associated with dominantly inherited human obesity. Nat Genet 20: 111-112.
7. Krude H, Biebermann H, Luck W, Horn R, Brabant G, et al. (1998) Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat Genet 19: 155-157.
8. Huszar D, Lynch CA, Fairchild-Huntress V, Dunmore JH, Fang Q, et al. (1997) Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88: 131-141.
9. Gropp E, Shanabrough M, Borok E, Xu AW, Janoschek R, et al. (2005) Agouti-related peptide-expressing neurons are mandatory for feeding. Nat Neurosci 8: 1289-1291.
10. Ollmann MM, Wilson BD, Yang YK, Kerns JA, Chen Y, et al. (1997) Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 278: 135-138.
11. Wortley KE, Anderson KD, Yasenchak J, Murphy A, Valenzuela D, et al. (2005) Agouti-related protein-deficient mice display an age-related lean phenotype. Cell Metab 2: 421-427.
12. Farooqi IS, Keogh JM, Yeo GS, Lank EJ, Cheetham T, et al. (2003) Clinical spectrum of obesity and mutations in the melanocortin 4 receptor gene. N Engl J Med 348: 1085-1095.
13. Reizes O, Clegg DJ, Strader AD, Benoit SC, (2006) A role for syndecan-3 in the melanocortin regulation of energy balance. Peptides 27: 274-280.
14. Lindahl U, Li J-p, (2009) Interactions between heparan sulfate and proteins- design and functional implications. Intern Rev Cell Mol Biol 276: 105-159.
15. Bishop JR, Schuksz M, Esko JD, (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446: 1030-1037.
16. Reizes O, Lincecum J, Wang Z, Goldberger O, Huang L, et al. (2001) Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell 106: 105-116.
17. Strader AD, Reizes O, Woods SC, Benoit SC, Seeley RJ, (2004) Mice lacking the syndecan-3 gene are resistant to diet-induced obesity. J Clin Invest 114: 1354-1360.
18. Reizes O, Benoit SC, Strader AD, Clegg DJ, Akunuru S, et al. (2003) Syndecan-3 modulates food intake by interacting with the melanocortin/AgRP pathway. Ann N Y Acad Sci 994: 66-73.
19. Ogren S, Lindahl U, (1975) Cleavage of macromolecular heparin by an enzyme from mouse mastocytoma. J Biol Chem 250: 2690-2697.
20. Butler AA, (2006) The melanocortin system and energy balance. Peptides 27: 281-290.
21. Zcharia E, Jia J, Zhang X, Baraz L, Lindahl U, et al. (2009) Newly generated heparanase knock-out mice unravel co-regulation of heparanase and matrix metalloproteinases. PLoS One 4: e5181.
22. Zcharia E, Metzger S, Chajek-Shaul T, Aingorn H, Elkin M, et al. (2004) Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior. FASEB J 18: 252-263.
23. Vlodavsky I, Ilan N, Naggi A, Casu B, (2007) Heparanase: structure, biological functions, and inhibition by heparin-derived mimetics of heparan sulfate. Curr Pharm Des 13: 2057-2073.
24. Ha E, Kim MJ, Choi BK, Rho JJ, Oh DJ, et al. (2006) Positive association of obesity with single nucleotide polymorphisms of syndecan 3 in the Korean population. J Clin Endocrinol Metab 91: 5095-5099.
25. Nogueiras R, Wiedmer P, Perez-Tilve D, Veyrat-Durebex C, Keogh JM, et al. (2007) The central melanocortin system directly controls peripheral lipid metabolism. J Clin Invest 117: 3475-3488.
26. Pierroz DD, Ziotopoulou M, Ungsunan L, Moschos S, Flier JS, et al. (2002) Effects of acute and chronic administration of the melanocortin agonist MTII in mice with diet-induced obesity. Diabetes 51: 1337-1345.
27. Bluher S, Mantzoros CS, (2004) The role of leptin in regulating neuroendocrine function in humans. J Nutr 134: 2469S-2474S.
28. Garza JC, Kim CS, Liu J, Zhang W, Lu XY, (2008) Adeno-associated virus-mediated knockdown of melanocortin-4 receptor in the paraventricular nucleus of the hypothalamus promotes high-fat diet-induced hyperphagia and obesity. J Endocrinol 197: 471-482.
29. Butler AA, Marks DL, Fan W, Kuhn CM, Bartolome M, et al. (2001) Melanocortin-4 receptor is required for acute homeostatic responses to increased dietary fat. Nat Neurosci 4: 605-611.
30. Bode L, Salvestrini C, Park PW, Li JP, Esko JD, et al. (2008) Heparan sulfate and syndecan-1 are essential in maintaining murine and human intestinal epithelial barrier function. J Clin Invest 118: 229-238.
31. Coll AP, (2007) Effects of pro-opiomelanocortin (POMC) on food intake and body weight: mechanisms and therapeutic potential? Clin Sci (Lond) 113: 171-182.
32. Wikberg JE, Mutulis F, (2008) Targeting melanocortin receptors: an approach to treat weight disorders and sexual dysfunction. Nat Rev Drug Discov 7: 307-323.
33. Mul JD, van Boxtel R, Bergen DJ, Brans MA, Brakkee JH, et al. (2011) Melanocortin Receptor 4 Deficiency Affects Body Weight Regulation, Grooming Behavior, and Substrate Preference in the Rat. Obesity.
34. Farooqi IS, O'Rahilly S, (2005) Monogenic obesity in humans. Annu Rev Med 56: 443-458.
35. Thorleifsson G, Walters GB, Gudbjartsson DF, Steinthorsdottir V, Sulem P, et al. (2009) Genome-wide association yields new sequence variants at seven loci that associate with measures of obesity. Nat Genet 41: 18-24.
36. Chambers JC, Elliott P, Zabaneh D, Zhang W, Li Y, et al. (2008) Common genetic variation near MC4R is associated with waist circumference and insulin resistance. Nat Genet 40: 716-718.
37. Loos RJ, Lindgren CM, Li S, Wheeler E, Zhao JH, et al. (2008) Common variants near MC4R are associated with fat mass, weight and risk of obesity. Nat Genet 40: 768-775.
38. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, et al. (2005) Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123: 493-505.
39. Ailenberg M, Silverman M, (2000) Controlled hot start and improved specificity in carrying out PCR utilizing touch-up and loop incorporated primers (TULIPS). Biotechniques 29: 1018-1020, 1022-1014.
40. Nardella C, Lahm A, Pallaoro M, Brunetti M, Vannini A, et al. (2004) Mechanism of activation of human heparanase investigated by protein engineering. Biochemistry 43: 1862-1873.
41. Nadir Y, Brenner B, Zetser A, Ilan N, Shafat I, et al. (2006) Heparanase induces tissue factor expression in vascular endothelial and cancer cells. J Thromb Haemost 4: 2443-2451.