Myeloid-Cell-Derived VEGF Maintains Brain Glucose Uptake and Limits Cognitive Impairment in Obesity

Cell

Volumn 165, Issue 4, 2016, Pages 882-895

  Jais, Alexander ^a,b,c   Solas, Maite ^a,b,c   Backes, Heiko ^a   Chaurasia, Bhagirath ^a   Kleinridders, André ^a,d,e   Theurich, Sebastian ^a,b,c   Mauer, Jan ^a,b,c   Steculorum, Sophie M ^a,b,c   Hampel, Brigitte ^a,b,c   Goldau, Julia ^a,b,c   Alber, Jens ^a,b,c   Förster, Carola Y ^f   Eming, Sabine A ^c,g   Schwaninger, Markus ^h   Ferrara, Napoleone ⁱ   Karsenty, Gerard ^j   Brüning, Jens C ^a,b,c,e  

^a MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

^d GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^e GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^f UNIVERSITY OF WÜRZBURG   (Germany)

^g UNIVERSITY OF COLOGNE   (Germany)

^h UNIVERSITY OF LÜBECK   (Germany)

ⁱ UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^j Columbia University ^*  (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; GLUCOSE TRANSPORTER 1; SATURATED FATTY ACID; VASCULOTROPIN; GLUCOSE; SLC2A1 PROTEIN, MOUSE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BONE MARROW CELL; COGNITION; COGNITIVE DEFECT; ENDOTHELIUM CELL; GLUCOSE BRAIN LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; INDIRECT CALORIMETRY; LIPID DIET; MACROPHAGE ACTIVATION; MORRIS WATER MAZE TEST; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BRAIN; GENETICS; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; COGNITION; DIET, HIGH-FAT; ENDOTHELIAL CELLS; FATTY ACIDS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; MICE; MYELOID CELLS; OBESITY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84964595404     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.03.033     Document Type: Article

References (57)

1. U. Andersson, and K.J. Tracey Reflex principles of immunological homeostasis Annu. Rev. Immunol. 30 2012 313 335
2. M.C. Arkan, A.L. Hevener, F.R. Greten, S. Maeda, Z.W. Li, J.M. Long, A. Wynshaw-Boris, G. Poli, J. Olefsky, and M. Karin IKK-beta links inflammation to obesity-induced insulin resistance Nat. Med. 11 2005 191 198
3. M. Bencherif, P.M. Lippiello, R. Lucas, and M.B. Marrero Alpha7 nicotinic receptors as novel therapeutic targets for inflammation-based diseases Cell. Mol. Life Sci. 68 2011 931 949
4. S.C. Benoit, C.J. Kemp, C.F. Elias, W. Abplanalp, J.P. Herman, S. Migrenne, A.L. Lefevre, C. Cruciani-Guglielmacci, C. Magnan, F. Yu, and et al. Palmitic acid mediates hypothalamic insulin resistance by altering PKC-theta subcellular localization in rodents J. Clin. Invest. 119 2009 2577 2589
5. G. Boden Role of fatty acids in the pathogenesis of insulin resistance and NIDDM Diabetes 46 1997 3 10
6. B.E. Clausen, C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster Conditional gene targeting in macrophages and granulocytes using LysMcre mice Transgenic Res. 8 1999 265 277
7. D.C. De Vivo, R.R. Trifiletti, R.I. Jacobson, G.M. Ronen, R.A. Behmand, and S.I. Harik Defective glucose transport across the blood-brain barrier as a cause of persistent hypoglycorrhachia, seizures, and developmental delay N. Engl. J. Med. 325 1991 703 709
8. C. Förster, C. Silwedel, N. Golenhofen, M. Burek, S. Kietz, J. Mankertz, and D. Drenckhahn Occludin as direct target for glucocorticoid-induced improvement of blood-brain barrier properties in a murine in vitro system J. Physiol. 565 2005 475 486
9. A.J. Freemerman, A.R. Johnson, G.N. Sacks, J.J. Milner, E.L. Kirk, M.A. Troester, A.N. Macintyre, P. Goraksha-Hicks, J.C. Rathmell, and L. Makowski Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype J. Biol. Chem. 289 2014 7884 7896
10. I. Galea, K. Palin, T.A. Newman, N. Van Rooijen, V.H. Perry, and D. Boche Mannose receptor expression specifically reveals perivascular macrophages in normal, injured, and diseased mouse brain Glia 49 2005 375 384
11. L. Gautron, J.K. Elmquist, and K.W. Williams Neural control of energy balance: translating circuits to therapies Cell 161 2015 133 145
12. H.P. Gerber, K.J. Hillan, A.M. Ryan, J. Kowalski, G.A. Keller, L. Rangell, B.D. Wright, F. Radtke, M. Aguet, and N. Ferrara VEGF is required for growth and survival in neonatal mice Development 126 1999 1149 1159
13. C.X. Gong, F. Liu, I. Grundke-Iqbal, and K. Iqbal Impaired brain glucose metabolism leads to Alzheimer neurofibrillary degeneration through a decrease in tau O-GlcNAcylation J. Alzheimers Dis. 9 2006 1 12
14. M.F. Gregor, and G.S. Hotamisligil Inflammatory mechanisms in obesity Annu. Rev. Immunol. 29 2011 415 445
15. H. He, J. Xu, C.M. Warren, D. Duan, X. Li, L. Wu, and M.L. Iruela-Arispe Endothelial cells provide an instructive niche for the differentiation and functional polarization of M2-like macrophages Blood 120 2012 3152 3162
16. C. Heilig, F. Brosius, B. Siu, L. Concepcion, R. Mortensen, K. Heilig, M. Zhu, R. Weldon, G. Wu, and D. Conner Implications of glucose transporter protein type 1 (GLUT1)-haplodeficiency in embryonic stem cells for their survival in response to hypoxic stress Am. J. Pathol. 163 2003 1873 1885
17. N. Horwood, and D.C. Davies Immunolabelling of hippocampal microvessel glucose transporter protein is reduced in Alzheimer's disease Virchows Arch. 425 1994 69 72
18. G.S. Hotamisligil Inflammation and metabolic disorders Nature 444 2006 860 867
19. J.L. Jankowsky, D.J. Fadale, J. Anderson, G.M. Xu, V. Gonzales, N.A. Jenkins, N.G. Copeland, M.K. Lee, L.H. Younkin, S.L. Wagner, and et al. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase Hum. Mol. Genet. 13 2004 159 170
20. R.N. Kalaria, and S.I. Harik Reduced glucose transporter at the blood-brain barrier and in cerebral cortex in Alzheimer disease J. Neurochem. 53 1989 1083 1088
21. S. Kälin, F.L. Heppner, I. Bechmann, M. Prinz, M.H. Tschöp, and C.X. Yi Hypothalamic innate immune reaction in obesity Nat. Rev. Endocrinol. 11 2015 339 351
22. C. Karschin, C. Ecke, F.M. Ashcroft, and A. Karschin Overlapping distribution of K(ATP) channel-forming Kir6.2 subunit and the sulfonylurea receptor SUR1 in rodent brain FEBS Lett. 401 1997 59 64
23. A. Kleinridders, A.C. Könner, and J.C. Brüning CNS-targets in control of energy and glucose homeostasis Curr. Opin. Pharmacol. 9 2009 794 804
24. A. Kleinridders, D. Schenten, A.C. Könner, B.F. Belgardt, J. Mauer, T. Okamura, F.T. Wunderlich, R. Medzhitov, and J.C. Brüning MyD88 signaling in the CNS is required for development of fatty acid-induced leptin resistance and diet-induced obesity Cell Metab. 10 2009 249 259
25. S. Lee, T.T. Chen, C.L. Barber, M.C. Jordan, J. Murdock, S. Desai, N. Ferrara, A. Nagy, K.P. Roos, and M.L. Iruela-Arispe Autocrine VEGF signaling is required for vascular homeostasis Cell 130 2007 691 703
26. Y.S. Lee, P. Li, J.Y. Huh, I.J. Hwang, M. Lu, J.I. Kim, M. Ham, S. Talukdar, A. Chen, W.J. Lu, and et al. Inflammation is necessary for long-term but not short-term high-fat diet-induced insulin resistance Diabetes 60 2011 2474 2483
27. B.E. Levin, A.A. Dunn-Meynell, and V.H. Routh Brain glucose sensing and body energy homeostasis: role in obesity and diabetes Am. J. Physiol. 276 1999 R1223 R1231
28. S.L. Macauley, M. Stanley, E.E. Caesar, S.A. Yamada, M.E. Raichle, R. Perez, T.E. Mahan, C.L. Sutphen, and D.M. Holtzman Hyperglycemia modulates extracellular amyloid-β concentrations and neuronal activity in vivo J. Clin. Invest. 125 2015 2463 2467
29. A.N. Macintyre, V.A. Gerriets, A.G. Nichols, R.D. Michalek, M.C. Rudolph, D. Deoliveira, S.M. Anderson, E.D. Abel, B.J. Chen, L.P. Hale, and J.C. Rathmell The glucose transporter Glut1 is selectively essential for CD4 T cell activation and effector function Cell Metab. 20 2014 61 72
30. N. Mani, A. Khaibullina, J.M. Krum, and J.M. Rosenstein Activation of receptor-mediated angiogenesis and signaling pathways after VEGF administration in fetal rat CNS explants J. Cereb. Blood Flow Metab. 23 2003 1420 1429
31. A.D. Mooradian, H.C. Chung, and G.N. Shah GLUT-1 expression in the cerebra of patients with Alzheimer's disease Neurobiol. Aging 18 1997 469 474
32. P. Pekala, M. Marlow, D. Heuvelman, and D. Connolly Regulation of hexose transport in aortic endothelial cells by vascular permeability factor and tumor necrosis factor-alpha, but not by insulin J. Biol. Chem. 265 1990 18051 18054
33. A. Peters, U. Schweiger, L. Pellerin, C. Hubold, K.M. Oltmanns, M. Conrad, B. Schultes, J. Born, and H.L. Fehm The selfish brain: competition for energy resources Neurosci. Biobehav. Rev. 28 2004 143 180
34. D.A. Ridder, M.F. Lang, S. Salinin, J.P. Röderer, M. Struss, C. Maser-Gluth, and M. Schwaninger TAK1 in brain endothelial cells mediates fever and lethargy J. Exp. Med. 208 2011 2615 2623
35. M. Rosas-Ballina, and K.J. Tracey The neurology of the immune system: neural reflexes regulate immunity Neuron 64 2009 28 32
36. G. Sabio, M. Das, A. Mora, Z. Zhang, J.Y. Jun, H.J. Ko, T. Barrett, J.K. Kim, and R.J. Davis A stress signaling pathway in adipose tissue regulates hepatic insulin resistance Science 322 2008 1539 1543
37. R. Schlich, M. Willems, S. Greulich, F. Ruppe, W.T. Knoefel, D.M. Ouwens, B. Maxhera, A. Lichtenberg, J. Eckel, and H. Sell VEGF in the crosstalk between human adipocytes and smooth muscle cells: depot-specific release from visceral and perivascular adipose tissue Mediators Inflamm. 2013 2013 982458
38. G. Seidner, M.G. Alvarez, J.I. Yeh, K.R. O'Driscoll, J. Klepper, T.S. Stump, D. Wang, N.B. Spinner, M.J. Birnbaum, and D.C. De Vivo GLUT-1 deficiency syndrome caused by haploinsufficiency of the blood-brain barrier hexose carrier Nat. Genet. 18 1998 188 191
39. H. Sone, B.K. Deo, and A.K. Kumagai Enhancement of glucose transport by vascular endothelial growth factor in retinal endothelial cells Invest. Ophthalmol. Vis. Sci. 41 2000 1876 1884
40. L. Steinbusch, G. Labouèbe, and B. Thorens Brain glucose sensing in homeostatic and hedonic regulation Trends Endocrinol. Metab. 26 2015 455 466
41. K. Takata, T. Kasahara, M. Kasahara, O. Ezaki, and H. Hirano Erythrocyte/HepG2-type glucose transporter is concentrated in cells of blood-tissue barriers Biochem. Biophys. Res. Commun. 173 1990 67 73
42. J.P. Thaler, C.X. Yi, E.A. Schur, S.J. Guyenet, B.H. Hwang, M.O. Dietrich, X. Zhao, D.A. Sarruf, V. Izgur, K.R. Maravilla, and et al. Obesity is associated with hypothalamic injury in rodents and humans J. Clin. Invest. 122 2012 153 162
43. S. Tovar, L. Paeger, S. Hess, D.A. Morgan, A.C. Hausen, H.S. Brönneke, B. Hampel, P.J. Ackermann, N. Evers, H. Büning, and et al. K(ATP)-channel-dependent regulation of catecholaminergic neurons controls BAT sympathetic nerve activity and energy homeostasis Cell Metab. 18 2013 445 455
44. E. Tsaousidou, L. Paeger, B.F. Belgardt, M. Pal, C.M. Wunderlich, H. Brönneke, U. Collienne, B. Hampel, F.T. Wunderlich, M. Schmidt-Supprian, and et al. Distinct roles for JNK and IKK activation in Agouti-related peptide neurons in the development of obesity and insulin resistance Cell Rep. 9 2014 1495 1506
45. S.J. Vannucci, F. Maher, E. Koehler, and I.A. Simpson Altered expression of GLUT-1 and GLUT-3 glucose transporters in neurohypophysis of water-deprived or diabetic rats Am. J. Physiol. 267 1994 E605 E611
46. M.C. Vogt, and J.C. Brüning CNS insulin signaling in the control of energy homeostasis and glucose metabolism - from embryo to old age Trends Endocrinol. Metab. 24 2013 76 84
47. D. Wang, J.M. Pascual, H. Yang, K. Engelstad, X. Mao, J. Cheng, J. Yoo, J.L. Noebels, and D.C. De Vivo A mouse model for Glut-1 haploinsufficiency Hum. Mol. Genet. 15 2006 1169 1179
48. X. Wang, Z. Yang, B. Xue, and H. Shi Activation of the cholinergic antiinflammatory pathway ameliorates obesity-induced inflammation and insulin resistance Endocrinology 152 2011 836 846
49. J. Wei, J. Shimazu, M.P. Makinistoglu, A. Maurizi, D. Kajimura, H. Zong, T. Takarada, T. Iezaki, J.E. Pessin, E. Hinoi, and G. Karsenty Glucose uptake and Runx2 synergize to orchestrate osteoblast differentiation and bone formation Cell 161 2015 1576 1591
50. K.W. Williams, and J.K. Elmquist From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior Nat. Neurosci. 15 2012 1350 1355
51. K. Williams, X. Alvarez, and A.A. Lackner Central nervous system perivascular cells are immunoregulatory cells that connect the CNS with the peripheral immune system Glia 36 2001 156 164
52. E.A. Winkler, Y. Nishida, A.P. Sagare, S.V. Rege, R.D. Bell, D. Perlmutter, J.D. Sengillo, S. Hillman, P. Kong, A.R. Nelson, and et al. GLUT1 reductions exacerbate Alzheimer's disease vasculo-neuronal dysfunction and degeneration Nat. Neurosci. 18 2015 521 530
53. F.T. Wunderlich, T. Luedde, S. Singer, M. Schmidt-Supprian, J. Baumgartl, P. Schirmacher, M. Pasparakis, and J.C. Brüning Hepatic NF-kappa B essential modulator deficiency prevents obesity-induced insulin resistance but synergizes with high-fat feeding in tumorigenesis Proc. Natl. Acad. Sci. USA 105 2008 1297 1302
54. W.L. Yeh, C.J. Lin, and W.M. Fu Enhancement of glucose transporter expression of brain endothelial cells by vascular endothelial growth factor derived from glioma exposed to hypoxia Mol. Pharmacol. 73 2008 170 177
55. C.X. Yi, M. Gericke, M. Krüger, A. Alkemade, D.G. Kabra, S. Hanske, J. Filosa, P. Pfluger, N. Bingham, S.C. Woods, and et al. High calorie diet triggers hypothalamic angiopathy Mol. Metab. 1 2012 95 100
56. C.X. Yi, M.H. Tschöp, S.C. Woods, and S.M. Hofmann High-fat-diet exposure induces IgG accumulation in hypothalamic microglia Dis. Model. Mech. 5 2012 686 690
57. Y. Zhang, R. Proenca, M. Maffei, M. Barone, L. Leopold, and J.M. Friedman Positional cloning of the mouse obese gene and its human homologue Nature 372 1994 425 432