Loss of PDGF-B activity increases hepatic vascular permeability and enhances insulin sensitivity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 301, Issue 3, 2011, Pages

  Raines, Summer M ^a   Richards, Oliver C ^a   Schneider, Lindsay R ^a   Schueler, Kathryn L ^a   Rabaglia, Mary E ^a   Oler, Angie T ^a   Stapleton, Donald S ^a   Genové, Guillem ^b   Dawson, John A ^c   Betsholtz, Christer ^b   Attie, Alan D ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Diabetes; Pericytes; Platelet derived growth factor B

Indexed keywords

INSULIN; PLATELET DERIVED GROWTH FACTOR B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; GLUCOSE HOMEOSTASIS; INSULIN BLOOD LEVEL; INSULIN CLEARANCE; INSULIN LIKE ACTIVITY; INSULIN RELEASE; INSULIN SENSITIVITY; LIVER BLOOD VESSEL; LIVER SINUSOID; MALE; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; BLOOD GLUCOSE; CAPILLARY PERMEABILITY; GLUCOSE TOLERANCE TEST; INSULIN; INSULIN RESISTANCE; LEPTIN; LIVER; MICE; MICE, TRANSGENIC; OBESITY; PERICYTES; PROTO-ONCOGENE PROTEINS C-SIS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SIGNAL TRANSDUCTION;

EID: 80052056533     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00241.2011     Document Type: Article

References (56)

1. Abramsson A, Lindblom P, Betsholtz C. Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest 112: 1142-1151, 2003.
2. Agostino N, Chinchilli VM, Lynch CJ, Koszyk-Szewczyk A, Gingrich R, Sivik J, Drabick JJ. Effect of the tyrosine kinase inhibitors (sunitinib, sorafenib, dasatinib, and imatinib) on blood glucose levels in diabetic and nondiabetic patients in general clinical practice. J Oncol Pharm Pract. In press.
3. Ahishali E, Demir K, Ahishali B, Akyuz F, Pinarbasi B, Poturoglu S, Ibrisim D, Gulluoglu M, Ozdil S, Besisik F, Kaymakoglu S, Boztas G, Cakaloglu Y, Mungan Z, Canberk Y, Okten A. Electron microscopic findings in non-alcoholic fatty liver disease: is there a difference between hepatosteatosis and steatohepatitis? J Gastroenterol Hepatol 25: 619-626, 2010.
4. Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 100: 174-190, 2007.
5. Armulik A, Genové G, Mäe M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C. Pericytes regulate the blood-brain barrier. Nature 468: 557-561, 2010.
6. Barrett EJ, Eggleston EM, Inyard AC, Wang H, Li G, Chai W, Liu Z. The vascular actions of insulin control its delivery to muscle and regulate the rate-limiting step in skeletal muscle insulin action. Diabetologia 52: 752-764, 2009.
7. Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, Zlokovic BV. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68: 409-427, 2010.
8. Bernuau D, Guillot R, Durand AM, Raoux N, Gabreau T, Passa P, Feldmann G. Ultrastructural aspects of the liver perisinusoidal space in diabetic patients with and without microangiopathy. Diabetes 31: 1061-1067, 1982.
9. Bernuau D, Guillot R, Durand-Schneider AM, Poussier P, Moreau A, Feldmann G. Liver perisinusoidal fibrosis in BB rats with or without overt diabetes. Am J Pathol 120: 38-45, 1985.
10. Biddinger SB, Almind K, Miyazaki M, Kokkotou E, Ntambi JM, Kahn CR. Effects of diet and genetic background on sterol regulatory element-binding protein-1c, stearoyl-CoA desaturase 1, and the development of the metabolic syndrome. Diabetes 54: 1314-1323, 2005.
11. Bissell DM, Roulot D, George J. Transforming growth factor beta and the liver. Hepatology 34: 859-867, 2001.
12. Breccia M, Muscaritoli M, Alimena G. Reduction of glycosylated hemoglobin with stable insulin levels in a diabetic patient with chronic myeloid leukemia responsive to imatinib. Haematologica 90, Suppl: ECR21, 2005.
13. Breccia M, Muscaritoli M, Aversa Z, Mandelli F, Alimena G. Imatinib mesylate may improve fasting blood glucose in diabetic Ph_ chronic myelogenous leukemia patients responsive to treatment. J Clin Oncol 22: 4653-4655, 2004.
14. Brissova M, Shostak A, Shiota M, Wiebe PO, Poffenberger G, Kantz J, Chen Z, Carr C, Jerome WG, Chen J, Baldwin HS, Nicholson W, Bader DM, Jetton T, Gannon M, Powers AC. Pancreatic islet production of vascular endothelial growth factor-a is essential for islet vascularization, revascularization, and function. Diabetes 55: 2974-2985, 2006.
15. Brock RW, Dorman RB. Obesity, insulin resistance and hepatic perfusion. Microcirculation 14: 339-347, 2007.
16. Cederroth CR, Vinciguerra M, Gjinovci A, Kühne F, Klein M, Cederroth M, Caille D, Suter M, Neumann D, James RW, Doerge DR, Wallimann T, Meda P, Foti M, Rohner-Jeanrenaud F, Vassalli JD, Nef S. Dietary phytoestrogens activate AMP-activated protein kinase with improvement in lipid and glucose metabolism. Diabetes 57: 1176-1185, 2008.
17. Chiu JD, Richey JM, Harrison LN, Zuniga E, Kolka CM, Kirkman E, Ellmerer M, Bergman RN. Direct administration of insulin into skeletal muscle reveals that the transport of insulin across the capillary endothelium limits the time course of insulin to activate glucose disposal. Diabetes 57: 828-835, 2008.
18. Clark MG. Impaired microvascular perfusion: a consequence of vascular dysfunction and a potential cause of insulin resistance in muscle. Am J Physiol Endocrinol Metab 295: E732-E750, 2008.
19. Clee SM, Yandell BS, Schueler KM, Rabaglia ME, Richards OC, Raines SM, Kabara EA, Klass DM, Mui ET, Stapleton DS, Gray-Keller MP, Young MB, Stoehr JP, Lan H, Boronenkov I, Raess PW, Flowers MT, Attie AD. Positional cloning of Sorcs1, a type 2 diabetes quantitative trait locus. Nat Genet 38: 688-693, 2006.
20. Czochra P, Klopcic B, Meyer E, Herkel J, Garcia-Lazaro JF, Thieringer F, Schirmacher P, Biesterfeld S, Galle PR, Lohse AW, Kanzler S. Liver fibrosis induced by hepatic overexpression of PDGF-B in transgenic mice. J Hepatol 45: 419-428, 2006.
21. Daneman R, Zhou L, Kebede AA, Barres BA. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468: 562-566, 2010.
22. Farrell GC, Teoh NC, McCuskey RS. Hepatic microcirculation in fatty liver disease. Anat Rec (Hoboken) 291: 684-692, 2008.
23. Gaengel K, Genove G, Armulik A, Betsholtz C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29: 630-638, 2009.
24. Goodarzi MO, Lehman DM, Taylor KD, Guo X, Cui J, Quinones MJ, Clee SM, Yandell BS, Blangero J, Hsueh WA, Attie AD, Stern MP, Rotter JI. SORCS1: a novel human type 2 diabetes susceptibility gene suggested by the mouse. Diabetes 56: 1922-1929, 2007.
25. Hammes HP. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res 37, Suppl 1: 39-43, 2005.
26. Han MS, Chung KW, Cheon HG, Rhee SD, Yoon CH, Lee MK, Kim KW, Lee MS. Imatinib mesylate reduces endoplasmic reticulum stress and induces remission of diabetes in db/db mice. Diabetes 58: 329-336, 2009.
27. Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153: 543-553, 2001.
28. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126: 3047-3055, 1999.
29. Hermey G, Sjøgaard SS, Petersen CM, Nykjaer A, Gliemann J. Tumour necrosis factor alpha-converting enzyme mediates ectodomain shedding of Vps10p-domain receptor family members. Biochem J 395: 285-293, 2006.
30. Jamieson HA, Cogger VC, Twigg SM, McLennan SV, Warren A, Cheluvappa R, Hilmer SN, Fraser R, de Cabo R, Le Couteur DG. Alterations in liver sinusoidal endothelium in a baboon model of type 1 diabetes. Diabetologia 50: 1969-1976, 2007.
31. Kantarjian H, Pasquini R, Hamerschlak N, Rousselot P, Holowiecki J, Jootar S, Robak T, Khoroshko N, Masszi T, Skotnicki A, Hellmann A, Zaritsky A, Golenkov A, Radich J, Hughes T, Countouriotis A, Shah N. Dasatinib or high-dose imatinib for chronic-phase chronic myeloid leukemia after failure of first-line imatinib: a randomized phase 2 trial. Blood 109: 5143-5150, 2007.
32. Lammert E, Gu G, McLaughlin M, Brown D, Brekken R, Murtaugh LC, Gerber HP, Ferrara N, Melton DA. Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 13: 1070-1074, 2003.
33. Latry P, Bioulac-Sage P, Echinard E, Gin H, Boussarie L, Grimaud JA, Balabaud C. Perisinusoidal fibrosis and basement membrane-like material in the livers of diabetic patients. Hum Pathol 18: 775-780, 1987.
34. Le Couteur DG, Fraser R, Hilmer S, Rivory LP, McLean AJ. The hepatic sinusoid in aging and cirrhosis: effects on hepatic substrate disposition and drug clearance. Clin Pharmacokinet 44: 187-200, 2005.
35. Leveen P, Pekny M, Gebre-Medhin S, Swolin B, Larsson E, Betsholtz C. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 8: 1875-1887, 1994.
36. Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277: 242-245, 1997.
37. Lindblom P, Gerhardt H, Liebner S, Abramsson A, Enge M, Hellstrom M, Backstrom G, Fredriksson S, Landegren U, Nystrom HC, Bergstrom G, Dejana E, Ostman A, Lindahl P, Betsholtz C. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 17: 1835-1840, 2003.
38. McCuskey RS, Ito Y, Robertson GR, McCuskey MK, Perry M, Farrell GC. Hepatic microvascular dysfunction during evolution of dietary steatohepatitis in mice. Hepatology 40: 386-393, 2004.
39. Miles PD, Levisetti M, Reichart D, Khoursheed M, Moossa AR, Olefsky JM. Kinetics of insulin action in vivo. Identification of ratelimiting steps. Diabetes 44: 947-953, 1995.
40. Ostman A, Andersson M, Betsholtz C, Westermark B, Heldin CH. Identification of a cell retention signal in the B-chain of platelet-derived growth factor and in the long splice version of the A-chain. Cell Regul 2: 503-512, 1991.
41. Paterson AD, Waggott D, Boright AP, Hosseini SM, Shen E, Sylvestre MP, Wong I, Bharaj B, Cleary PA, Lachin JM, Below JE, Nicolae D, Cox NJ, Canty AJ, Sun L, Bull SB. A genome-wide association study identifies a novel major locus for glycemic control in type 1 diabetes, as measured by both A1C and glucose. Diabetes 59: 539-549, 2010.
42. Rabaglia ME, Gray-Keller MP, Frey BL, Shortreed MR, Smith LM, Attie AD. -Ketoisocaproate-induced hypersecretion of insulin by islets from diabetes-susceptible mice. Am J Physiol Endocrinol Metab 289: E218-E224, 2005.
43. Raines EW, Ross R. Compartmentalization of PDGF on extracellular binding sites dependent on exon-6-encoded sequences. J Cell Biol 116: 533-543, 1992.
44. Richards OC, Raines SM, Attie AD. The role of blood vessels, endothelial cells, and vascular pericytes in insulin secretion and peripheral insulin action. Endocr Rev 31: 343-363, 2010.
45. Sato M, Suzuki S, Senoo H. Hepatic stellate cells: unique characteristics in cell biology and phenotype. Cell Struct Funct 28: 105-112, 2003.
46. Schoemaker MH, Rots MG, Beljaars L, Ypma AY, Jansen PL, Poelstra K, Moshage H, Haisma HJ. PDGF-receptor beta-targeted adenovirus redirects gene transfer from hepatocytes to activated stellate cells. Mol Pharm 5: 399-406, 2008.
47. Soriano P. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev 8: 1888-1896, 1994.
48. Steiner DF. The proinsulin C-peptide-a multirole model. Exp Diabesity Res 5: 7-14, 2004.
49. Veneri D, Franchini M, Bonora E. Imatinib and regression of type 2 diabetes. N Engl J Med 352: 1049-1050, 2005.
50. Wang H, Liu Z, Li G, Barrett EJ. The vascular endothelial cell mediates insulin transport into skeletal muscle. Am J Physiol Endocrinol Metab 291: E323-E332, 2006.
51. Wang H, Wang AX, Barrett EJ. Caveolin-1 is required for vascular endothelial insulin uptake. Am J Physiol Endocrinol Metab 300: E134-E144, 2011.
52. Whiteman EL, Chen JJ, Birnbaum MJ. Platelet-derived growth factor (PDGF) stimulates glucose transport in 3T3-L1 adipocytes overexpressing PDGF receptor by a pathway independent of insulin receptor substrates. Endocrinology 144: 3811-3820, 2003.
53. Xian X, Hakansson J, Stahlberg A, Lindblom P, Betsholtz C, Gerhardt H, Semb H. Pericytes limit tumor cell metastasis. J Clin Invest 116: 642-651, 2006.
54. Yoshiji H, Noguchi R, Kuriyama S, Ikenaka Y, Yoshii J, Yanase K, Namisaki T, Kitade M, Masaki T, Fukui H. Imatinib mesylate (STI-571) attenuates liver fibrosis development in rats. Am J Physiol Gastrointest Liver Physiol 288: G907-G913, 2005.
55. Yuasa T, Kakuhata R, Kishi K, Obata T, Shinohara Y, Bando Y, Izumi K, Kajiura F, Matsumoto M, Ebina Y. Platelet-derived growth factor stimulates glucose transport in skeletal muscles of transgenic mice specifically expressing platelet-derived growth factor receptor in the muscle, but it does not affect blood glucose levels. Diabetes 53: 2776-2786, 2004.
56. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 372: 425-432, 1994.