The blood-brain barrier as a regulator of the gut-brain axis

Frontiers of Hormone Research

Volumn 42, Issue , 2014, Pages 29-49

  Schaeffer, Marie ^a,b,c   Hodson, David J ^a,b,c,d   Mollard, Patrice ^a,b,c  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b INSERM   (France)

^c UNIV MONTPELLIER   (France)

^d Section of Cell Biology   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APPETITE STIMULANT; CHOLECYSTOKININ; GASTRIC INHIBITORY POLYPEPTIDE; GASTROINTESTINAL HORMONE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GROWTH HORMONE RELEASING FACTOR; INSULIN; LEPTIN; OXYNTOMODULIN; PANCREAS POLYPEPTIDE; PEPTIDE HORMONE; PEPTIDE YY; PREPROGLUCAGON;

ACTIVE TRANSPORT; ADAPTIVE BEHAVIOR; ARCUATE NUCLEUS; ARTICLE; BIOLOGICAL ACTIVITY; BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN BLOOD VESSEL; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM FUNCTION; CHOROID PLEXUS; ENERGY BALANCE; FEEDING BEHAVIOR; FOOD INTAKE; GASTROINTESTINAL TRACT FUNCTION; GUT BRAIN AXIS; HOMEOSTASIS AND REGULATION; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS; LONG TERM CARE; METABOLIC DISORDER; NEUROMODULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS SECRETION; PERIPHERAL CIRCULATION; PRIORITY JOURNAL; SATIETY; VASCULAR ACCESS; CIRCUMVENTRICULAR ORGAN; GASTROINTESTINAL TRACT; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; EATING; HOMEOSTASIS; METABOLISM; PHYSIOLOGY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; EATING; GASTROINTESTINAL HORMONES; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMANS;

EID: 84903825319     PISSN: 03013073     EISSN: 16623762     Source Type: Book Series    
DOI: 10.1159/000358313     Document Type: Article

References (92)

1. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG: Central nervous system control of food intake. Nature 2000; 404: 661-671. (Pubitemid 30205071)
2. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, Wren AM, Brynes AE, Low MJ, Ghatei MA, Cone RD, Bloom SR: Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 2002; 418: 650-654.
3. Stanley S, Wynne K, McGowan B, Bloom S: Hormonal regulation of food intake. Physiol Rev 2005; 85: 1131-1158. (Pubitemid 41363743)
4. Skibicka KP, Dickson SL: Ghrelin and food reward: The story of potential underlying substrates. Peptides 2011;32: 2265-2273.
5. Schwartz GJ: Brainstem integrative function in the central nervous system control of food intake. Forum Nutr 2010; 63: 141-151.
6. Blouet C, Schwartz GJ: Brainstem nutrient sensing in the nucleus of the solitary tract inhibits feeding. Cell Metabolism 2012; 16: 579-587.
7. Gibbs J, Young RC, Smith GP: Cholecystokinin decreases food intake in rats. J Comp Physiol Psychol 1973; 84: 488-495.
8. Chaudhri O, Small C, Bloom S: Gastrointestinal hormones regulating appetite. Philos Trans R Soc Lond B Biol Sci 2006; 361: 1187-1209. (Pubitemid 44874228)
9. Strader AD, Woods SC: Gastrointestinal hormones and food intake. Gastroenterology 2005; 128: 175-191. (Pubitemid 40039969)
10. Tschöp M, Smiley DL, Heiman ML: Ghrelin induces adiposity in rodents. Nature 2000; 407: 908-913.
11. Otto B, Cuntz U, Fruehauf E, Wawarta R, Folwaczny C, Riepl RL, Heiman ML, Lehnert P, Fichter M, Tschöp M: Weight gain decreases elevated plasma ghrelin concentrations of patients with anorexia nervosa. Eur J Endocrinol 2001; 145:R5-R9. (Pubitemid 33061915)
12. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K: Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999; 402: 656-660. (Pubitemid 129516334)
13. Van der Lely AF, Tschöp M, Heiman ML, Ghigo E: Biological, physiological, pathophysiological, and pharmacological aspects of ghrelin. Endocr Rev 2004; 25: 426-457. (Pubitemid 38780667)
14. Harrold JA, Dovey T, Cai XJ, Halford JCG, Pinkney J: Autoradiographic analysis of ghrelin receptors in the rat hypothalamus. Brain Res 2008; 1196: 59-64.
15. Cowley MA, Smith RG, Diano S, Tschop M, Pronchuk N, Grove KL, Strasburger CJ, Bidlingmaier M, Esterman M, Heiman ML, Garcia-Segura LM, Nillni EA, Mendez P, Low MJ, Sotonyi P, Friedman JM, Liu H, Pinto S, Colmers WF, Cone RD, Horvath TL: The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 2003; 37: 649-661. (Pubitemid 36262986)
16. Sakata I, Nakano Y, Osborne-Lawrence S, Rovinsky SA, Lee CE, Perello M, Anderson JG, Coppari R, Xiao G, Lowell BB, Elmquist JK, Zigman JM: Characterization of a novel ghrelin cell reporter mouse. Regul Pept 2009; 155: 91-98.
17. Schaeffer M, Langlet F, Lafont C, Molino F, Hodson DJ, Roux T, Lamarque L, Verdie P, Bourrier E, Dehouck B, Baneres JL, Martinez J, Mery PF, Marie J, Trinquet E, Fehrentz JA, Prevot V, Mollard P: Rapid sensing of circulating ghrelin by hypothalamic appetite- modifying neurons. Proc Natl Acad Sci USA 2013; 110: 1512-1517.
18. Cui RJ, Li XJ, Appleyard SM: Ghrelin inhibits visceral afferent activation of catecholamine neurons in the solitary tract nucleus. J Neurosci 2011; 31: 3484-3492.
19. Fry M, Ferguson AV: Ghrelin modulates electrical activity of area postrema neurons. Am J Physiol Regul Integr Comp Physiol 2009; 296:R485-R492.
20. Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK: Expression of ghrelin receptor MRNA in the rat and the mouse brain. J Comp Neurol 2006; 494: 528-548. (Pubitemid 41791000)
21. Kern A, Albarran-Zeckler R, Walsh HE, Smith RG: Apo-ghrelin receptor forms heteromers with DRD2 in hypothalamic neurons and is essential for anorexigenic effects of DRD2 agonism. Neuron 2012; 73: 317-332.
22. Sun YX, Ahmed S, Smith RG: Deletion of ghrelin impairs neither growth nor appetite. Mol Cell Biol 2003; 23: 7973-7981. (Pubitemid 37377491)
23. Wren AM, Small CJ, Abbott CR, Dhillo WS, Seal LJ, Cohen MA, Batterham RL, Taheri S, Stanley SA, Ghatei MA, Bloom SR: Ghrelin causes hyperphagia and obesity in rats. Diabetes 2001; 50: 2540-2547. (Pubitemid 33642772)
24. Grouselle D, Chaillou E, Caraty A, Bluet-Pajot MT, Zizzari P, Tillet Y, Epelbaum J: Pulsatile cerebrospinal fluid and plasma ghrelin in relation to growth hormone secretion and food intake in the sheep. J Neuroendocrinol 2008; 20: 1138-1146.
25. Banks WA, Burney BO, Robinson SM: Effects of triglycerides, obesity, and starvation on ghrelin transport across the blood-brain barrier. Peptides 2008; 29: 2061-2065.
26. Ciofi P, Garret M, Lapirot O, Lafon P, Loyens A, Prevot V, Levine JE: Brain-endocrine interactions: a microvascular route in the mediobasal hypothalamus. Endocrinology 2009; 150: 5509-5519.
27. Rehfeld JF: Cholecystokinin. Best Pract Res Clin Endocrinol Metab 2004; 18: 569-586. (Pubitemid 39481233)
28. Moran TH, Baldessarini AR, Salorio CF, Lowery T, Schwartz GJ: Vagal afferent and efferent contributions to the inhibition of food intake by cholecystokinin. Am J Physiol Regul Integr Comp Physiol 1997; 272:R1245-R1251.
29. Wank SA: Cholecystokinin receptors. Am J Physiol Gastrointest Liver Physiol 1995; 269:G628-G646. (Pubitemid 3005920)
30. Bi S, Ladenheim EE, Schwartz GJ, Moran TH: A role for NPY overexpression in the dorsomedial hypothalamus in hyperphagia and obesity of OLETF rats. Am J Physiol Regul Integr Comp Physiol 2001; 281: R254-R260.
31. Meereis-Schwanke K, Klonowski-Stumpe H, Herberg L, Niederau C: Long-term effects of CCK-agonist and -antagonist on food intake and body weight in Zucker lean and obese rats. Peptides 1998; 19: 291-299. (Pubitemid 28097928)
32. Adrian TE, Long RG, Fuessl HS, Bloom SR: Plasma peptide YY (PYY) in dumping syndrome. Dig Dis Sci 1985;30:1145-1148. (Pubitemid 16132373)
33. Gelegen C, Chandarana K, Choudhury AI, Al-Qassab H, Evans IM, Irvine EE, Hyde CB, Claret M, Andreelli F, Sloan SE, Leiter AB, Withers DJ, Batterham RL: Regulation of hindbrain PYY expression by acute food deprivation, prolonged caloric restriction, and weight loss surgery in mice. Am J Physiol Endocrinol Metab 2012; 303:E659-E668.
34. Karra E, Chandarana K, Batterham RL: The role of peptide YY in appetite regulation and obesity. J Physiol 2009; 587: 19-25.
35. Ueno H, Yamaguchi H, Mizuta M, Nakazato M: The role of PYY in feeding regulation. Regul Pept 2008; 145: 12-16.
36. Nonaka N, Shioda S, Niehoff ML, Banks WA: Characterization of blood-brain barrier permeability to PYY3-36 in the mouse. J Pharmacol Exp Ther 2003; 306: 948-953. (Pubitemid 37025300)
37. Batterham RL, Heffron H, Kapoor S, Chivers JE, Chandarana K, Herzog H, Le Roux CW, Thomas EL, Bell JD, Withers DJ: Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metab 2006; 4: 223-233. (Pubitemid 44307976)
38. Field BCT, Chaudhri OB, Bloom SR: Bowels control brain: gut hormones and obesity. Nat Rev Endocrinol 2010; 6: 444-453.
39. Ekblad E, Sundler F: Distribution of pancreatic polypeptide and peptide YY. Peptides 2002; 23: 251-261. (Pubitemid 34127963)
40. Tasan RO, Lin S, Hetzenauer A, Singewald N, Herzog H, Sperk G: Increased novelty-induced motor activity and reduced depression-like behavior in neuropeptide Y (NPY)-Y4 receptor knockout mice. Neuroscience 2009; 158: 1717-1730.
41. Edelsbrunner ME, Painsipp E, Herzog H, Holzer P: Evidence from knockout mice for distinct implications of neuropeptide-Y Y2 and Y4 receptors in the circadian control of locomotion, exploration, water and food intake. Neuropeptides 2009; 43: 491-497.
42. Banks WA, Kastin AJ, Jaspan JB: Regional variation in transport of pancreatic-polypeptide across the blood-brain barrier of mice. Pharmacol Biochem Behav 1995; 51: 139-147.
43. Asakawa A, Inui A, Yuzuriha H, Ueno N, Katsuura G, Fujimiya M, Fujino MA, Niijima A, Meguid MM, Kasuga M: Characterization of the effects of pancreatic polypeptide in the regulation of energy balance. Gastroenterology 2003; 124: 1325-1336. (Pubitemid 36531807)
44. Kieffer TJ, Habener JL: The glucagon-like peptides. Endocr Rev 1999; 20: 876-913. (Pubitemid 30647076)
45. Holst JJ: The physiology of glucagon-like peptide 1. Physiol Rev 2007; 87: 1409-1439. (Pubitemid 350041474)
46. Habib AM, Richards P, Cairns LS, Rogers GJ, Bannon CAM, Parker HE, Morley TCE, Yeo GSH, Reimann F, Gribble FM: Overlap of endocrine hormone expression in the mouse intestine revealed by transcriptional profiling and flow cytometry. Endocrinology 2012; 153: 3054-3065.
47. Du XB, Kosinski JR, Lao JL, Shen XL, Petrov A, Chicchi GG, Eiermann GJ, Pocai A: Differential effects of oxyntomodulin and GLP-1 on glucose metabolism. Am J Physiol Endocrinol Metabol 2012; 303:E265- E271.
48. Dakin CL, Small CJ, Batterham RL, Neary NM, Cohen MA, Patterson M, Ghatei MA, Bloom SR: Peripheral oxyntomodulin reduces food intake and body weight gain in rats. Endocrinology 2004; 145: 2687-2695. (Pubitemid 38686215)
49. Pocai A, Carrington PE, Adams JR, Wright M, Eiermann G, Zhu L, Du XB, Petrov A, Lassman ME, Jiang GQ, Liu F, Miller C, Tota LM, Zhou GC, Zhang XP, Sountis MM, Santoprete A, Capito E, Chicchi GG, Thornberry N, Bianchi E, Pessi A, Marsh DJ, SinhaRoy R: Glucagon-like peptide 1/glucagon receptor dual agonism reverses obesity in mice. Diabetes 2009; 58: 2258-2266.
50. Meeran K, O'Shea D, Edwards CMB, Turton MD, Heath MM, Gunn I, Abusnana S, Rossi M, Small CJ, Goldstone AP, Taylor GM, Sunter D, Steere J, Choi SJ, Ghatei MA, Bloom SR: Repeated intracerebroventricular administration of glucagon-like peptide- 1(7-36) amide or exendin(9-39) alters body weight in the rat. Endocrinology 1999; 140: 244-250. (Pubitemid 29011165)
51. Scrocchi LA, Brown TJ, MacLusky N, Brubaker PL, Auerbach AB, Joyner AL, Drucker DJ: Glucose intolerance but normal satiety in mice with a null mutation in the glucagon-like peptide 1 receptor gene. Nat Med 1996; 2: 1254-1258. (Pubitemid 26375413)
52. Parker HE, Wallis K, le Roux CW, Wong KY, Reimann F, Gribble FM: Molecular mechanisms underlying bile acid-stimulated glucagon-like peptide-1 secretion. Brh J Pharmacol 2012; 165: 414-423.
53. Drucker DJ, Nauck MA: The incretin system: glucagon- like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006; 368: 1696-1705. (Pubitemid 46048557)
54. Sandoval DA, Bagnol D, Woods SC, D'Alessio DA, Seeley RJ: Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 2008; 57: 2046-2054.
55. Hisadome K, Reimann F, Gribble FM, Trapp S: Leptin directly depolarizes preproglucagon neurons in the nucleus tractus solitarius electrical properties of glucagon-like peptide-1 neurons. Diabetes 2010; 59: 1890-1898.
56. Tang-Christensen M, Vrang N, Larsen PJ: Glucagon- like peptide 1(7-36) amide's central inhibition of feeding and peripheral inhibition of drinking are abolished by neonatal monosodium glutamate treatment. Diabetes 1998; 47: 530-537. (Pubitemid 28160441)
57. Choudhury AI, Heffron H, Smith MA, Al-Qassab H, Xu AW, Selman C, Simmgen M, Clements M, Claret M, MacColl G, Bedford DC, Hisadome K, Diakonov I, Moosajee V, Bell JD, Speakman JR, Batterham RL, Barsh GS, Ashford MLJ, Withers DJ: The role of insulin receptor substrate 2 in hypothalamic and β-cell function. J Clin Invest 2005; 115: 940-950. (Pubitemid 40489398)
58. Corp ES, Woods SC, Porte D, Dorsa DM, Figlewicz DP, Baskin DG: Localization of I-125 insulin binding sites in the rat hypothalamus by quantitative autoradiography. Neurosci Lett 1986; 70: 17-22. (Pubitemid 16023232)
59. Zlokovic BV, Jovanovic S, Miao W, Samara S, Verma S, Farrell CL: Differential regulation of leptin transport by the choroid plexus and blood-brain barrier and high affinity transport systems for entry into hypothalamus and across the blood-cerebrospinal fluid barrier. Endocrinology 2000; 141: 1434-1441. (Pubitemid 32269111)
60. Lakhi S, Snow W, Fry M: Insulin modulates the electrical activity of subfornical organ neurons. Neuroreport 2013; 24: 329-334.
61. Tartaglia LA: The leptin receptor. J Biol Chem 1997; 272: 6093-6096. (Pubitemid 27118072)
62. Munzberg H: Leptin-signaling pathways and leptin resistance. Forum Nutr 2010; 63: 123-132.
63. Banks WA: Leptin transport across the blood-brain barrier: Implications for the cause and treatment of obesity. Curr Pharm Des 2001; 7: 125-133. (Pubitemid 32409711)
64. Ladyman SR, Grattan DR: Region-specific reduction in leptin-induced phosphorylation of signal transducer and activator of transcription-3 (STAT3) in the rat hypothalamus is associated with leptin resistance during pregnancy. Endocrinology 2004; 145: 3704-3711. (Pubitemid 39037556)
65. Farooqi IS, O'Rahilly S: Genetics of obesity in humans. Endocr Rev 2006; 27: 710-718. (Pubitemid 44936054)
66. Caro JF, Kolaczynski JW, Nyce MR, Ohannesian JP, Opentanova I, Goldman WH, Lynn RB, Zhang PL, Sinha MK, Considine RV: Decreased cerebrospinalfluid/ serum leptin ratio in obesity: a possible mechanism for leptin resistance. Lancet 1996; 348: 159-161. (Pubitemid 26238099)
67. Abbatecola AM, Ferrucci L, Grella R, Bandinelli S, Bonafe M, Barbieri M, Corsi AM, Lauretani F, Franceschi C, Paolisso G: Diverse effect of inflammatory markers on insulin resistance and insulin-resistance syndrome in the elderly. J Am Geriatr Soc 2004; 52: 399-404. (Pubitemid 38339521)
68. King GL, Johnson SM: Receptor-mediated transport of insulin across endothelial cells. Science 1985; 227: 1583-1586. (Pubitemid 15119466)
69. Banks WA: The blood-brain barrier as a regulatory interface in the gut-brain axes. Physiol Behav 2006; 89: 472-476. (Pubitemid 44634576)
70. Wolburg H, Lippoldt A: Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 2002; 38: 323-337. (Pubitemid 36398254)
71. Abbott NJ, Ronnback L, Hansson E: Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7: 41-53. (Pubitemid 41828930)
72. Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He LQ, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C: Pericytes regulate the blood-brain barrier. Nature 2010; 468: 557-561.
73. Banks WA, Kastin AJ: Peptides and the blood-brain barrier - lipophilicity as a predictor of permeability. Brain Res Bull 1985; 15: 287-292. (Pubitemid 16229709)
74. Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ: Structure and function of the bloodbrain barrier. Neurobiol Dis 2010; 37: 13-25.
75. Banks WA: Blood-brain barrier and energy balance. Obesity (Silver Spring) 2006; 14(suppl 5): 234S-237S.
76. Skipor J, Thiery JC: The choroid plexus - cerebrospinal fluid system: undervaluated pathway of neuroendocrine signaling into the brain. Acta Neurobiol Exp 2008; 68: 414-428.
77. Medeiros N, Dai L, Ferguson AV: Glucose-responsive neurons in the subfornical organ of the rat - a novel site for direct CNS monitoring of circulating glucose. Neuroscience 2012; 201: 157-165.
78. Bearer EL, Orci L: Endothelial fenestral diaphragms: a quick-freeze, deep-etch study. J Cell Biol 1985; 100: 418-428. (Pubitemid 15173247)
79. Burguera B, Couce ME, Curran GL, Jensen MD, Lloyd RV, Cleary MP, Poduslo JF: Obesity is associated with a decreased leptin transport across the blood-brain barrier in rats. Diabetes 2000; 49: 1219-1223. (Pubitemid 30439098)
80. Mullier A, Bouret SG, Prevot V, Dehouck B: Differential distribution of tight junction proteins suggests a role for tanycytes in blood-hypothalamus barrier regulation in the adult mouse brain. J Comp Neurol 2010; 518: 943-962.
81. Langlet F, Mullier A, Bouret SG, Prevot V, Dehouck B: Tanycyte-like cells form a blood-cerebrospinal fluid barrier in the circumventricular organs of the mouse brain. J Comp Neurol 2013; 521: 3389-3405.
82. Cheunsuang O, Stewart AL, Morris R: Differential uptake of molecules from the circulation and CSF reveals regional and cellular specialisation in CNS detection of homeostatic signals. Cell Tissue Res 2006; 325: 397-402. (Pubitemid 44050802)
83. Langlet F, Levin BE, Luquet S, Mazzone M, Messina A, Dunn-Meynell AA, Balland E, Lacombe A, Mazur D, Carmeliet P, Bouret SG, Prevot V, Dehouck B: Tanycytic VEGF-A boosts blood-hypothalamus barrier plasticity and access of metabolic signals to the arcuate nucleus in response to fasting. Cell Metab 2013;17: 607-617.
84. Banks WA, Coon AB, Robinson SM, Moinuddin A, Shultz JM, Nakaoke R, Morley JE: Triglycerides induce leptin resistance at the blood-brain barrier. Diabetes 2004; 53: 1253-1260. (Pubitemid 38569011)
85. Daubert DL, Chung MY, Brooks VL: Insulin resistance and impaired baroreflex gain during pregnancy. Am J Physiol Regul Integr Comp Physiol 2007; 292: R2188-R2195. (Pubitemid 47080678)
86. Halaas JL, Boozer C, Blair-West J, Fidahusein N, Denton DA, Friedman JM: Physiological response to long-term peripheral and central leptin infusion in lean and obese mice. Proc Natl Acad Sci USA 1997; 94: 8878-8883. (Pubitemid 27335133)
87. Baura GD, Foster DM, Kaiyala K, Porte D, Kahn SE, Schwartz MW: Insulin transport from plasma into the central nervous system is inhibited by dexamethasone in dogs. Diabetes 1996; 45: 86-90. (Pubitemid 26010428)
88. Reger MA, Watson GS, Green PS, Wilkinson CW, Baker LD, Cholerton B, Fishel MA, Plymate SR, Breitner JCS, DeGroodt W, Mehta P, Craft S: Intranasal insulin improves cognition and modulates β-amyloid in early ad. Neurology 2008; 70: 440-448.
89. Kastin AJ, Akerstrom V: Glucose and insulin increase the transport of leptin through the bloodbrain barrier in normal mice but not in streptozotocin- diabetic mice. Neuroendocrinology 2001; 73: 237-242. (Pubitemid 32424517)
90. Pardridge WM, Eisenberg J, Yang J: Human bloodbrain barrier insulin-receptor. J Neurochem 1985; 44: 1771-1778.
91. Bello NT, Liang NC: The use of serotonergic drugs to treat obesity - is there any hope? Drug Des Devel Ther 2011; 5: 95-109.
92. Spranger J, Verma S, Gohring I, Bobbert T, Seifert J, Sindler AL, Pfeiffer A, Hileman SM, Tschöp M, Banks WA: Adiponectin does not cross the bloodbrain barrier but modifies cytokine expression of brain endothelial cells. Diabetes 2006; 55: 141-147. (Pubitemid 43343309)