Blockade of VEGF-C and VEGF-D modulates adipose tissue inflammation and improves metabolic parameters under high-fat diet

Molecular Metabolism

Volumn 4, Issue 2, 2015, Pages 93-105

  Karaman, Sinem ^a   Hollmén, Maija ^a   Robciuc, Marius R ^b   Alitalo, Annamari ^a   Nurmi, Harri ^b   Morf, Bettina ^a   Buschle, Dorina ^a   Alkan, H Furkan ^a   Ochsenbein, Alexandra M ^a   Alitalo, Kari ^b   Wolfrum, Christian ^a   Detmar, Michael ^a  

^a ETH ZURICH   (Switzerland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Adipose tissue; Inflammation; Macrophages; Obesity; Vegfc

Indexed keywords

IMMUNOGLOBULIN; INSULIN; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 3;

3T3 CELL LINE; ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CELL SIZE; CHEMOTAXIS; CONTROLLED STUDY; EMBRYO; FLUORESCENCE ACTIVATED CELL SORTING; IN VITRO STUDY; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIPID DIET; LIPID LIVER LEVEL; LIPID STORAGE; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; METABOLIC PARAMETERS; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SUBCUTANEOUS FAT; WEIGHT GAIN; WILD TYPE MOUSE;

MURINAE; MUS;

EID: 84921848567     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2014.11.006     Document Type: Article

References (51)

1. Wang Y., Beydoun M.A., Liang L., Caballero B., Kumanyika S.K. Will all Americans become overweight or obese? Estimating the progression and cost of the US obesity epidemic. Obesity (Silver Spring) 2008, 16:2323-2330.
2. Olefsky J.M., Glass C.K. Macrophages, inflammation, and insulin resistance. Annual Review of Physiology 2010, 72:219-246.
3. Hotamisligil G.S., Shargill N.S., Spiegelman B.M. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993, 259:87-91.
4. Bastard J.P., Jardel C., Bruckert E., Blondy P., Capeau J., Laville M., et al. Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. Journal of Clinical Endocrinology and Metabolism 2000, 85:3338-3342.
5. Sartipy P., Loskutoff D. Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:7265-7270.
6. Kanda H., Tateya S., Tamori Y., Kotani K., Hiasa K., Kitazawa R., et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. Journal of Clinical Investigation 2006, 116:1494-1505.
7. Laurencikiene J., van Harmelen V., Arvidsson Nordstrom E., Dicker A., Blomqvist L., Naslund E., et al. NF-kappaB is important for TNF-alpha-induced lipolysis in human adipocytes. Journal of Lipid Research 2007, 48:1069-1077.
8. Hotamisligil G. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
9. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. Journal of Clinical Investigation 2003, 112:1796-1808.
10. Feuerer M., Herrero L., Cipolletta D., Naaz A., Wong J., Nayer A., et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nature Medicine 2009, 15:930-939.
11. Nishimura S., Manabe I., Nagasaki M., Eto K., Yamashita H., Ohsugi M., et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nature Medicine 2009, 15:914-920.
12. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends in Immunology 2004, 25:677-686.
13. Shapiro H., Lutaty A., Ariel A. Macrophages, meta-inflammation, and immuno-metabolism. ScientificWorldJournal 2011, 11:2509-2529.
14. Sica A., Mantovani A. Macrophage plasticity and polarization: invivo veritas. Journal of Clinical Investigation 2012, 122:787-795.
15. Lumeng C.N., Bodzin J.L., Saltiel A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. Journal of Clinical Investigation 2007, 117:175-184.
16. Kolattukudy P.E., Niu J. Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/CCR2 pathway. Circulation Research 2012, 110:174-189.
17. Nicholls H.T., Kowalski G., Kennedy D.J., Risis S., Zaffino L.A., Watson N., et al. Hematopoietic cell-restricted deletion of CD36 reduces high-fat diet-induced macrophage infiltration and improves insulin signaling in adipose tissue. Diabetes 2011, 60:1100-1110.
18. Gomez-Ambrosi J., Catalan V., Rodriguez A., Ramirez B., Silva C., Gil M.J., et al. Involvement of serum vascular endothelial growth factor family members in the development of obesity in mice and humans. Journal of Nutritional Biochemistry 2010, 21:774-780.
19. Silha J., Krsek M., Sucharda P., Murphy L. Angiogenic factors are elevated in overweight and obese individuals. International Journal of Obesity 2005, 29:1308-1314.
20. Wada H., Ura S., Kitaoka S., Satoh-Asahara N., Horie T., Ono K., et al. Distinct characteristics of circulating vascular endothelial growth factor-A and C levels in human subjects. PLoS One 2011, 6:e29351.
21. Alitalo K. The lymphatic vasculature in disease. Nature Medicine 2011, 17:1371-1380.
22. Cueni L., Detmar M. The lymphatic system in health and disease. Lymphatic Research and Biology 2008, 6:109-122.
23. Rockson S.G. Update on the biology and treatment of lymphedema. Current Treatment Options in Cardiovascular Medicine 2012, 14:184-192.
24. Greene A.K., Grant F.D., Slavin S.A. Lower-extremity lymphedema and elevated body-mass index. New England Journal of Medicine 2012, 366:2136-2137.
25. Blum K.S., Karaman S., Proulx S.T., Ochsenbein A.M., Luciani P., Leroux J.C., et al. Chronic high-fat diet impairs collecting lymphatic vessel function in mice. PLoS One 2014, 9:e94713.
26. Elias I., Franckhauser S., Ferre T., Vila L., Tafuro S., Munoz S., et al. Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes 2012, 61:1801-1813.
27. Sun K., Wernstedt Asterholm I., Kusminski C.M., Bueno A.C., Wang Z.V., Pollard J.W., et al. Dichotomous effects of VEGF-A on adipose tissue dysfunction. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:5874-5879.
28. Lijnen H.R., Frederix L., Van Hoef B., Dewerchin M. Deficiency of vascular endothelial growth factor-D does not affect murine adipose tissue development. Biochemical and Biophysical Research Communications 2009, 378:255-258.
29. Mäkinen T., Jussila L., Veikkola T., Karpanen T., Kettunen M., Pulkkanen K., et al. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nature Medicine 2001, 7:199-205.
30. Aschen S.Z., Farias-Eisner G., Cuzzone D.A., Albano N.J., Ghanta S., Weitman E.S., et al. Lymph node transplantation results in spontaneous lymphatic reconnection and restoration of lymphatic flow. Plastic and Reconstructive Surgery 2014, 133:301-310.
31. Alitalo A.K., Proulx S.T., Karaman S., Aebischer D., Martino S., Jost M., et al. VEGF-C and VEGF-D blockade inhibits inflammatory skin carcinogenesis. Cancer Research 2013, 73:4212-4221.
32. Livingston J.N., Cuatrecasa P., Lockwood D.H. Insulin insensitivity of large fat cells. Science 1972, 177:626-628.
33. Wallace T.M., Levy J.C., Matthews D.R. Use and abuse of HOMA modeling. Diabetes Care 2004, 27:1487-1495.
34. Lumeng C.N., DelProposto J.B., Westcott D.J., Saltiel A.R. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 2008, 57:3239-3246.
35. Kang K., Reilly S.M., Karabacak V., Gangl M.R., Fitzgerald K., Hatano B., et al. Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell Metabolism 2008, 7:485-495.
36. Constant V.A., Gagnon A., Landry A., Sorisky A. Macrophage-conditioned medium inhibits the differentiation of 3T3-L1 and human abdominal preadipocytes. Diabetologia 2006, 49:1402-1411.
37. Lacasa D., Taleb S., Keophiphath M., Miranville A., Clement K. Macrophage-secreted factors impair human adipogenesis: involvement of proinflammatory state in preadipocytes. Endocrinology 2007, 148:868-877.
38. Permana P.A., Menge C., Reaven P.D. Macrophage-secreted factors induce adipocyte inflammation and insulin resistance. Biochemical and Biophysical Research Communications 2006, 341:507-514.
39. Poulos S.P., Dodson M.V., Hausman G.J. Cell line models for differentiation: preadipocytes and adipocytes. Experimental Biology and Medicine 2010, 235:1185-1193.
40. Linde N., Lederle W., Depner S., van Rooijen N., Gutschalk C.M., Mueller M.M. Vascular endothelial growth factor-induced skin carcinogenesis depends on recruitment and alternative activation of macrophages. Journal of Pathology 2012, 227:17-28.
41. Skobe M., Hawighorst T., Jackson D.G., Prevo R., Janes L., Velasco P., et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nature Medicine 2001, 7:192-198.
42. Schoppmann S., Birner P., Stockl J., Kalt R., Ullrich R., Caucig C., et al. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. American Journal of Pathology 2002, 161:947-956.
43. Stepanova O.I., Krylov A.V., Lioudyno V.I., Kisseleva E.P. Gene expression for VEGF-A, VEGF-C, and their receptors in murine lymphocytes and macrophages. Biochemistry (Moscow) 2007, 72:1194-1198.
44. Zhang Y., Lu Y., Ma L., Cao X., Xiao J., Chen J., et al. Activation of vascular endothelial growth factor receptor-3 in macrophages restrains TLR4-NF-kappaB signaling and protects against endotoxin shock. Immunity 2014, 40:501-514.
45. Skobe M., Hamberg L.M., Hawighorst T., Schirner M., Wolf G.L., Alitalo K., et al. Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. American Journal of Pathology 2001, 159:893-903.
46. Zuniga L.A., Shen W.J., Joyce-Shaikh B., Pyatnova E.A., Richards A.G., Thom C., et al. IL-17 regulates adipogenesis, glucose homeostasis, and obesity. Journal of Immunology 2010, 185:6947-6959.
47. Kim D.H., Sandoval D., Reed J.A., Matter E.K., Tolod E.G., Woods S.C., et al. The role of GM-CSF in adipose tissue inflammation. American Journal of Physiology. Endocrinology and Metabolism 2008, 295:E1038-E1046.
48. Persaud K., Tille J.C., Liu M., Zhu Z., Jimenez X., Pereira D.S., et al. Involvement of the VEGF receptor 3 in tubular morphogenesis demonstrated with a human anti-human VEGFR-3 monoclonal antibody that antagonizes receptor activation by VEGF-C. Journal of Cell Science 2004, 117:2745-2756.
49. Meissburger B., Ukropec J., Roeder E., Beaton N., Geiger M., Teupser D., et al. Adipogenesis and insulin sensitivity in obesity are regulated by retinoid-related orphan receptor gamma. EMBO Molecular Medicine 2011, 3:637-651.
50. Hara A., Radin N.S. Lipid extraction of tissues with a low-toxicity solvent. Analytical Biochemistry 1978, 90:420-426.
51. Karpanen T., Heckman C.A., Keskitalo S., Jeltsch M., Ollila H., Neufeld G., et al. Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB Journal 2006, 20:1462-1472.