Mesangial cell integrin αvβ8 provides glomerular endothelial cell cytoprotection by sequestering TGF-β and regulating PECAM-1

American Journal of Pathology

Volumn 178, Issue 2, 2011, Pages 609-620

  Khan, Shenaz ^a   Lakhe Reddy, Sujata ^a   McCarty, Joseph H ^b   Sorenson, Christine M ^c   Sheibani, Nader ^c   Reichardt, Louis F ^d   Kim, Jane H ^a   Wang, Bingcheng ^a   Sedor, John R ^a   Schelling, Jeffrey R ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

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

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA5BETA8 INTEGRIN; CD31 ANTIGEN; INTEGRIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOTHELIUM CELL; GENE SILENCING; GLOMERULAR STRUCTURE; GLOMERULUS CAPILLARY; GLOMERULUS EPITHELIUM; IMMUNOREGULATION; KIDNEY FUNCTION; MESANGIUM; MESANGIUM CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; UREMIA; WEIGHT GAIN;

EID: 79951820036     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.10.031     Document Type: Article

References (77)

1. Moyle M, Napier MA, McLean JW: Cloning and expression of a divergent integrin subunit β8. J Biol Chem 1991, 266:19650-19658 (Pubitemid 21908277)
2. Cambier S, Mu DZ, O'Connell D, Boylen K, Travis W, Liu WH, Broaddus VC, Nishimura SL: A role for the integrin αvβ8 in the negative regulation of epithelial cell growth. Cancer Res 2000, 60:7084-7093 (Pubitemid 32059188)
3. Stepp MA: α9 and β8 integrin expression correlates with the merger of the developing mouse eyelids. Dev Dyn 1999, 214:216-228
4. Travis MA, Reizis B, Melton AC, Masteller E, Tang Q, Proctor JM, Wang Y, Bernstein X, Huang X, Reichardt LF, Bluestone JA, Sheppard D: Loss of integrin αvβ8 on dendritic cells causes autoimmunity and colitis in mice. Nature 2007, 449:361-365 (Pubitemid 47443473)
5. Lacy-Hulbert A, Smith AM, Tissire H, Barry M, Crowley D, Bronson RT, Roes JT, Savill JS, Hynes RO: Ulcerative colitis and autoimmunity induced by loss of myeloid αv integrins. Proc Natl Acad Sci USA 2007, 104:15823-15828 (Pubitemid 350035383)
6. Zhu JW, Motejlek K, Wang DN, Zang KL, Schmidt A, Reichardt LF: β8 integrins are required for vascular morphogenesis in mouse embryos. Development 2002, 129:2891-2903 (Pubitemid 34874268)
7. Bader BL, Rayburn H, Crowley D, Hynes RO: Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all αv integrins. Cell 1998, 95:507-519 (Pubitemid 28533307)
8. McCarty JH, Monahan-Earley RA, Brown LF, Keller M, Gerhardt H, Rubin K, Shani M, Dvorak HF, Wolburg H, Bader BL, Dvorak AM, Hynes RO: Defective associations between blood vessels and brain parenchyma lead to cerebral hemorrhage in mice lacking αv integrins. Mol Cell Biol 2002, 22:7667-7677
9. McCarty JH, Lacy-Hulbert A, Charest A, Bronson RT, Crowley D, Housman D, Savill J, Roes J, Hynes RO: Selective ablation of αv integrins in the central nervous system leads to cerebral hemorrhage, seizures, axonal degeneration and premature death. Development 2005, 132:165-176 (Pubitemid 40207976)
10. Proctor JM, Zang K, Wang D, Wang R, Reichardt LF: Vascular development of the brain requires β8 integrin expression in the neuroepithelium. J Neurosci 2005, 25:9940-9948 (Pubitemid 41528032)
11. Mobley AK, Tchaicha JH, Shin J, Hossain MG, McCarty JH: β8 integrin regulates neurogenesis and neurovascular homeostasis in the adult brain. J Cell Sci 2009, 122:1842-1851
12. Lakhe-Reddy S, Khan S, Konieczkowski M, Jarad G, Wu KL, Reichardt LF, Takai Y, Bruggeman LA, Wang B, Sedor JR, Schelling JR: β8 integrin binds Rho GDP dissociation inhibitor-1 and activates Rac1 to inhibit mesangial cell myofibroblast differentiation. J Biol Chem 2006, 281:19688-19699 (Pubitemid 44035471)
13. Bertelli E, Regoli M, Fonzi L, Occhini R, Mannucci S, Ermini L, Toti P: Nestin expression in adult and developing human kidney. J Histochem Cytochem 2007, 55:411-421 (Pubitemid 46481948)
14. Daniel C, Albrecht H, Ludke A, Hugo C: Nestin expression in repopulating mesangial cells promotes their proliferation. Lab Invest 2008, 88:387-397 (Pubitemid 351432777)
15. Kikkawa Y, Virtanen I, Miner JH: Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin α5 in the glomerular basement membrane. J Cell Biol 2003, 161:187-196 (Pubitemid 36459090)
16. Potter EL: Development of the human glomerulus. Arch Pathol 1965, 80:241-255
17. Schlondorff D, Banas B: The mesangial cell revisited: no cell is an island. J Am Soc Nephrol 2009, 20:1179-1188
18. 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 1994, 8:1875-1887 (Pubitemid 24273888)
19. Takemoto M, He L, Norlin J, Patrakka J, Xiao Z, Petrova T, Bondjers C, Asp J, Wallgard E, Sun Y, Samuelsson T, Mostad P, Lundin S, Miura N, Sado Y, Alitalo K, Quaggin SE, Tryggvason K, Betsholtz C: Large-scale identification of genes implicated in kidney glomerulus development and function. EMBO J 2006, 25:1160-1174 (Pubitemid 43372128)
20. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE: Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 2003, 111:707-716 (Pubitemid 36278589)
21. Nishimura SL, Sheppard D, Pytela R: Integrin αvβ8. Interaction with vitronectin and functional divergence of the β8 cytoplasmic domain J Biol Chem 1994, 269:28708-28715
22. Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, Sheppard D, Broaddus VC, Nishimura SL: The integrin αvβ8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-β1. J Cell Biol 2002, 157:493-507 (Pubitemid 34839812)
23. Nishimura SL: Integrin-mediated transforming growth factor-β activation, a potential therapeutic target in fibrogenic disorders. Am J Pathol 2009, 175:1362-1370
24. Turck J, Pollock AS, Lee LK, Marti HP, Lovett DH: Matrix metalloproteinase 2 (gelatinase A) regulates glomerular mesangial cell proliferation and differentiation. J Biol Chem 1996, 271:15074-15083 (Pubitemid 26194988)
25. Annes JP, Munger JS, Rifkin DB: Making sense of latent TGFβ activation. J Cell Sci 2003, 116:217-224 (Pubitemid 36163863)
26. Hynes RO: The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219
27. Gharavi AG, Bruggeman LA, Oller S, Klotman PE, Lifton RP. Genetic background modifies the development of renal disease in HIV-1 transgenic mice. J Am Soc Nephrol 1999, 10:404A
28. George M, Ayuso E, Casellas A, Costa C, Devedjian JC, Bosch F: Beta cell expression of IGF-I leads to recovery from type 1 diabetes. J Clin Invest 2002, 109:1153-1163 (Pubitemid 34496593)
29. Schelling JR, Nkemere N, Kopp JB, Cleveland RP: Fas-dependent fratricidal apoptosis is a mechanism of tubular epithelial cell deletion in chronic renal failure. Lab Invest 1998, 78:813-824 (Pubitemid 28347878)
30. Khan S, Wu KL, Sedor JR, Abu Jawdeh BG, Schelling JR: The NHE1 Na+/H+ exchanger regulates cell survival by activating and targeting ezrin to specific plasma membrane domains. Cell Mol Biol 2006, 52:115-121 (Pubitemid 46799714)
31. Akis N, Madaio MP: Isolation, culture, and characterization of endothelial cells from mouse glomeruli. Kidney Int 2004, 65:2223-2227 (Pubitemid 38670008)
32. Kondo S, Scheef EA, Sheibani N, Sorenson CM: PECAM-1 isoform-specific regulation of kidney endothelial cell migration and capillary morphogenesis. Am J Physiol Cell Physiol 2007, 292:C2070-C2083 (Pubitemid 47080533)
33. Khan S, Koepke A, Jarad G, Schlessman K, Cleveland RP, Wang BC, Konieczkowski M, Schelling JR: Apoptosis and JNK activation are differentially regulated by Fas expression level in renal tubular epithelial cells. Kidney Int 2001, 60:65-76 (Pubitemid 32587540)
34. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB: An assay for transforming growth factor-β using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 1994, 216:276-284 (Pubitemid 24076008)
35. Kerjaschki D, Miettinen A, Farquhar MG: Initial events in the formation of immune deposits in passive Heymann nephritis. gp330-anti-gp330 immune complexes form in epithelial coated pits and rapidly become attached to the glomerular basement membrane. J Exp Med 1987, 166:109-128 (Pubitemid 17101893)
36. Baleato RM, Guthrie PL, Gubler MC, Ashman LK, Roselli S: Deletion of Cd151 results in a strain-dependent glomerular disease due to severe alterations of the glomerular basement membrane. Am J Pathol 2008, 173:927-937
37. Bird IN, Taylor V, Newton JP, Spragg JH, Simmons DL, Salmon M, Buckley CD: Homophilic PECAM-1(CD31) interactions prevent endothelial cell apoptosis but do not support cell spreading or migration. J Cell Sci 1999, 112:1989-1997 (Pubitemid 29338823)
38. Mamdouh Z, Chen X, Pierini LM, Maxfield FR, Muller WA: Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature 2003, 421:748-753 (Pubitemid 36227626)
39. Scholzen T, Gerdes J: The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000, 182:311-322 (Pubitemid 30054364)
40. Hohenstein B, Renk S, Lang K, Daniel C, Freund M, Leon C, Amann KU, Gachet C, Hugo CP: P2Y1 gene deficiency protects from renal disease progression and capillary rarefaction during passive crescentic glomerulonephritis. J Am Soc Nephrol 2007, 18:494-505 (Pubitemid 46193315)
41. Duncan GS, Andrew DP, Takimoto H, Kaufman SA, Yoshida H, Spellberg J, Luis dlP, Elia A, Wakeham A, Karan-Tamir B, Muller WA, Senaldi G, Zukowski MM, Mak TW: Genetic evidence for functional redundancy of platelet/endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J Immunol 1999, 162:3022-3030 (Pubitemid 29309332)
42. Gao C, Sun W, Christofidou-Solomidou M, Sawada M, Newman DK, Bergom C, Albelda SM, Matsuyama S, Newman PJ: PECAM-1 functions as a specific and potent inhibitor of mitochondrial-dependent apoptosis. Blood 2003, 102:169-179 (Pubitemid 36759651)
43. Dimaio TA, Wang S, Huang Q, Scheef EA, Sorenson CM, Sheibani N: Attenuation of retinal vascular development and neovascularization in PECAM-1-deficient mice. Dev Biol 2008, 315:72-88
44. Osawa M, Masuda M, Kusano K, Fujiwara K: Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J Cell Biol 2002, 158:773-785 (Pubitemid 34920115)
45. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA: A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005, 437:426-431 (Pubitemid 41613506)
46. Zhang JJ, Kelm RJ, Biswas P, Kashgarian M, and Madri JA: PECAM-1 modulates thrombin-induced tissue factor expression on endothelial cells. J Cell Physiol 2007, 210:527-537 (Pubitemid 44970427)
47. Kruger T, Benke D, Eitner F, Lang A, Wirtz M, Hamilton-Williams EE, Engel D, Giese B, Muller-Newen G, Floege J, Kurts C: Identification and functional characterization of dendritic cells in the healthy murine kidney and in experimental glomerulonephritis. J Am Soc Nephrol 2004, 15:613-621 (Pubitemid 38294791)
48. Soos TJ, Sims TN, Barisoni L, Lin K, Littman DR, Dustin ML, Nelson PJ: CX3CR1+ interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int 2006, 70:591-596 (Pubitemid 44141588)
49. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, Rifkin DB, Sheppard D: The integrin αvβ6 binds and activates latent TGFβ1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1999, 96:319-328 (Pubitemid 29077586)
50. 6-mediated activation of latent TGF-β requires the latent TGF-β binding protein-1. J Cell Biol 2004, 165:723-734
51. Schelling JR, Sinha S, Konieczkowski M, Sedor JR: Myofibroblast differentiation: plasma membrane microdomains and cell phenotype. Exp Nephrol 2002, 10:313-319 (Pubitemid 36151246)
52. Tamaki K, Okuda S, Nakayama M, Yanagida T, Fujishima M: Transforming growth factor-β1 in hypertensive renal injury in Dahl saltsensitive rats. J Am Soc Nephrol 1996, 7:2578-2589 (Pubitemid 27469564)
53. Sterzel RB, Hartner A, Schlotzer-Schrehardt U, Voit S, Hausknecht B, Doliana R, Colombatti A, Gibson MA, Braghetta P, Bressan GM: Elastic fiber proteins in the glomerular mesangium in vivo and in cell culture. Kidney Int 2000, 58:1588-1602
54. McCarty JH, Cook AA, Hynes RO: An interaction between αvβ8 integrin and Band 4.1B via a highly conserved region of the Band 4.1 C-terminal domain. Proc Natl Acad Sci USA 2005, 102:13479-13483
55. Pollman MJ, Naumovski L, Gibbons GH: Vascular cell apoptosis: cell type-specific modulation by TGF-β1 in endothelial cells versus smooth muscle cells. Circulation 1999, 99:2019-2026 (Pubitemid 29183900)
56. Fierlbeck W, Liu A, Coyle R, Ballermann BJ: Endothelial cell apoptosis during glomerular capillary lumen formation in vivo. J Am Soc Nephrol 2003, 14:1349-1354 (Pubitemid 36514675)
57. Nystrom J, Fierlbeck W, Granqvist A, Kulak SC, Ballermann BJ: A human glomerular SAGE transcriptome database. BMC Nephrol 2009, 10:13
58. Aluwihare P, Mu Z, Zhao Z, Yu D, Weinreb PH, Horan GS, Violette SM, Munger JS: Mice that lack activity of αvβ6- and αvβ8- integrins reproduce the abnormalities of Tgfb1- and Tgfb3-null mice. J Cell Sci 2009, 122:227-232
59. Hauser IA, Riess R, Hausknecht B, Thuringer H, Sterzel RB: Expression of cell adhesion molecules in primary renal disease and renal allograft rejection. Nephrol Dial Transplant 1997, 12:1122-1131 (Pubitemid 27230545)
60. Sivridis E, Giatromanolaki A, Touloupidis S, Pasadakis P, Vargemezis V: Platelet endothelial cell adhesion molecule-1 and angiogenic factor expression in idiopathic membranous nephropathy. Am J Kidney Dis 2003, 41:360-365 (Pubitemid 36152454)
61. Iruela-Arispe L, Gordon K, Hugo C, Duijvestijn AM, Claffey KP, Reilly M, Couser WG, Alpers CE, Johnson RJ: Participation of glomerular endothelial cells in the capillary repair of glomerulonephritis. Am J Pathol 1995, 147:1715-1727
62. Isome M, Fujinaka H, Yaoita E, Feng L, Adhikary LP, Abe A, Tsuchida S, Kawasaki K, Suzuki H, Kihara I, Wilson CB, Yamamoto T: Involvement of endothelial cell adhesion molecules in the development of anti-Thy-1 nephritis. Exp Nephrol 2002, 10:338-347 (Pubitemid 36151249)
63. Lastres P, Almendro N, Bellon T, Lopez-Guerrero JA, Eritja R, Bernabeu C: Functional regulation of platelet/endothelial cell adhesion molecule- 1 by TGF-β1 in promonocytic U-937 cells. J Immunol 1994, 153:4206-4218
64. Cambier S, Gline S, Mu D, Collins R, Araya J, Dolganov G, Einheber S, Boudreau N, Nishimura SL: Integrin αvβ8-mediated activation of transforming growth factor-β by perivascular astrocytes: an angiogenic control switch. Am J Pathol 2005, 166:1883-1894 (Pubitemid 40734410)
65. Isermann B, Vinnikov IA, Madhusudhan T, Herzog S, Kashif M, Blautzik J, Corat MA, Zeier M, Blessing E, Oh J, Gerlitz B, Berg DT, Grinnell BW, Chavakis T, Esmon CT, Weiler H, Bierhaus A, Nawroth PP: Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat Med 2007, 13:1349-1358 (Pubitemid 350073598)
66. Armulik A, Abramsson A, Betsholtz C: Endothelial/pericyte interactions. Circ Res 2005, 97:512-523 (Pubitemid 41361741)
67. Shi YG, Massagué J: Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003, 113:685-700
68. Sharma R, Khanna A, Sharma M, Savin VJ: Transforming growth factor-β1 increases albumin permeability of isolated rat glomeruli via hydroxyl radicals. Kidney Int 2000, 58:131-136 (Pubitemid 30429857)
69. Yamamoto T, Noble NA, Miller DE, Border WA: Sustained expression of TGF-β1 underlies development of progressive kidney fibrosis. Kidney Int 1994, 45:916-927 (Pubitemid 24094509)
70. Heldin CH, Landstrom M, Moustakas A: Mechanism of TGF-β signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr Opin Cell Biol 2009, 21:166-176
71. Wu CJ, Chen Z, Ullrich A, Greene MI, O'Rourke DM: Inhibition of EGFR-mediated phosphoinositide-3-OH kinase (PI3-K) signaling and glioblastoma phenotype by signal-regulatory proteins (SIRPs). Oncogene 2000, 19:3999-4010
72. Tai LK, Zheng Q, Pan S, Jin ZG, Berk BC: Flow activates ERK1/2 and endothelial nitric oxide synthase via a pathway involving PECAM1. SHP2, and Tie2. J Biol Chem 2005, 280:29620-29624 (Pubitemid 41177037)
73. Yang W, Klaman LD, Chen B, Araki T, Harada H, Thomas SM, George EL, Neel BG: An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev Cell 2006, 10:317-327
74. Bjarnegård M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A, Takemoto M, Gustafsson E, Fässler R, Betsholtz C: Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 2004, 131:1847-1857 (Pubitemid 38559851)
75. Abrass CK, Berfield AK, Ryan MC, Carter WG, Hansen KM: Abnormal development of glomerular endothelial and mesangial cells in mice with targeted disruption of the lama3 gene. Kidney Int 2006, 70:1062-1071 (Pubitemid 44344076)
76. Sheibani N, Sorenson CM, Frazier WA: Tissue specific expression of alternatively spliced murine PECAM-1 isoforms. Dev Dyn 1999, 214: 44-54 (Pubitemid 29028902)
77. Xie Y, Muller WA: Molecular cloning and adhesive properties of murine platelet/endothelial cell adhesion molecule 1. Proc Natl Acad Sci USA 1993, 90:5569-5573 (Pubitemid 23176202)