Acute podocyte vascular endothelial growth factor (VEGF-A) knockdown disrupts alphavbeta3 integrin signaling in the glomerulus

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Veron, de lma ^a   Villegas, Guillermo ^b   Aggarwal, Pardeep Kumar ^a   Bertuccio, Claudia ^a   Jimenez, Juan ^b   Velazquez, Heino ^a   Reidy, Kimberly ^b   Abrahamson, Dale R ^c   Moeckel, Gilbert ^a   Kashgarian, Michael ^a   Tufro, Alda ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; DOXYCYCLINE; FIBRONECTIN; MESSENGER RNA; NEUROPILIN 1; SHORT HAIRPIN RNA; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; VITRONECTIN RECEPTOR;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SWELLING; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE EXPRESSION; GENE SILENCING; GLOMERULUS; GLOMERULUS BASEMENT MEMBRANE; IN VIVO STUDY; KIDNEY CELL CULTURE; MICROANEURYSM; MOUSE; NONHUMAN; PODOCYTE; PROTEIN PROTEIN INTERACTION; PROTEINURIA; SIGNAL TRANSDUCTION;

ANIMALS; BLOOD PRESSURE; CELLS, CULTURED; DOWN-REGULATION; DOXYCYCLINE; ENDOTHELIUM; FIBRONECTINS; GENE KNOCKDOWN TECHNIQUES; INTEGRIN ALPHAVBETA3; MICE; MODELS, ANIMAL; NEUROPILIN-1; PHENOTYPE; PODOCYTES; PROTEIN BINDING; PROTEINURIA; RENAL INSUFFICIENCY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

MUS;

EID: 84863738713     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040589     Document Type: Article

References (51)

1. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, et al. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380: 439-442.
2. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, et al. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.
3. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M, (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92: 735-745.
4. Pan Q, Chathery Y, Wu Y, Rathore N, Tong RK, et al. (2007) Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J Biol Chem 282: 24049-24056.
5. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M, (1998) Flt-1 lacking the tyrosine kinas domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci U S A 95: 9349-9354.
6. Lee S, Chen TT, Barber CL, Jordan MC, Murdock J, et al. (2007) Autocrine VEGF signaling is required for vascular homeostasis. Cell 130: 691-703.
7. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, et al. (2003) Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 88: 2348-2351.
8. Maynard SE, Min JY, Merchan J, Lim KH, Li J, et al. (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111: 649-658.
9. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, et al. (2008) VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 358: 1129-1136.
10. Veron D, Reidy K, Marlier A, Bertuccio C, Villegas G, et al. (2010) Induction of podocyte VEGF164 overexpression at different stages of development causes congenital nephrosis or steroid resistant nephrotic syndrome. Am J Pathol 177: 2225-2233.
11. Veron D, Reidy K, Bertuccio C, Techman J, Villegas G, et al. (2010) Induction of podocyte VEGF-A oveexpression in adult mice causes glomerular disease. Kidney Int 77: 989-999.
12. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, et al. (2003) Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111: 707-716.
13. Ingber DE, Folkman J, (1989) Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J Cell Biol 109: 317-330.
14. Ingber DE, Folkman J, (1989) How does extracellular matrix control capillary morphogenesis? Cell 58: 803-805.
15. Hynes RO, (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25.
16. Ruoslahti E, Noble NA, Kagami S, Border WA, (1994) Integrins. Kidney Int 44: 17-22.
17. Miner JH, Yurchenco PD, (2004) Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20: 255-284.
18. Kanasaki K, Kanda Y, Palmsten K, Tanjore H, Lee SB, et al. (2008) Integrin beta1-mediated matrix assembly and signaling are critical for the normal development and function of the kidney glomerulus. R. Dev Biol 313: 584-593.
19. Kreidberg JA, Donovan MJ, Goldstein SL, Rennke H, Shepherd K, et al. (1996) Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122: 3537-3547.
20. Sachs N, Kreft M, van den Bergh Weerman MA, Beynon AJ, Peters TA, et al. (2006) Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol 175: 33-39.
21. Pozzi A, Jarad G, Moeckel GW, Coffa S, Zhang X, et al. (2008) Beta1 integrin expression by podocytes is required to maintain glomerular structural integrity. Dev Biol 316: 288-301.
22. Yoon S, Gingras D, Bendayan M, (2001) Alterations of vitronectin and its receptor alpha(v) integrin in the rat renal glomerular wall during diabetes. Am J Kidney Dis 38: 1298-1306.
23. Hafdi Z, (2000) Distribution of alphavbeta3, alphavbeta5 integrins and the integrin associated protein-IAP (CD47) in human glomerular diseases. Cell Adhes Commun 7: 441-451.
24. Hodivala-Dilke KM, (1999) Beta integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest 103: 229-238.
25. Bader BL, Rayburn H, Crowley D, Hynes RO, (1998) Extensive vasculogenesis, angiogenesis and organogenesis precede lethality in mice lacking all av integrins. Cell 95: 507-519.
26. Wei C, Möller CC, Altintas MM, Li J, Schwarz K, et al. (2008) Modification of kidney barrier function by the urokinase receptor. Nat Med 14: 55-63.
27. Wei C, El Hindi S, Li J, Fornoni A, Goes N, et al. (2011) Circulating urokinase receptor as a cause of focal segmental glomerulosclerosis. Nat Med 17: 952-960.
28. Persson M, Engström G, Björkbacka H, Hedblad B, (2012) Soluble urokinase plasminogen activator receptor in plasma is associated with incidence of CVD. Results from the Malmö Diet and Cancer Study. Atherosclerosis 220(2): 502-505.
29. Mahabeleshwar GH, (2008) Integrin affinity modulation in angiogenesis. Cell Cycle 7: 335-347.
30. Bertuccio C, Veron D, Aggarwal PK, Holzman L, Tufro A, (2011) Vascular endothelial growth factor receptor 2 direct interaction with nephrin links VEGF-A signals to actin in kidney podocytes. J Biol Chem 286: 39933-39944.
31. Ruoslahti E, (1996) Integrin signaling and matrix assembly. Tumor Biol 17: 117-124.
32. Soldi R, Mitola S, Strasly M, Defilippi P, Tarone G, et al. (1999) Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J 18: 882-892.
33. Folkman J, (2007) Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 6: 273-286.
34. Pampori N, Hato T, Stupack DG, Aidoudi S, Cheresh DA, et al. (1999) Mechanisms and consequences of affinity modulation of integrin alpha(V)beta(3) detected with a novel patch-engineered monovalent ligand. J Biol Chem 274: 21609-21616.
35. Mundel P, Reiser J, Zúñiga Mejía Borja A, Pavenstädt H, Davidson GR, et al. (1997) Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines. Exp Cell Res 236: 248-258.
36. Guan F, Villegas G, Teichman J, Mundel P, Tufro A, (2006) Autocrine VEGF-A system in podocytes regulates podocin and its interaction with CD2AP. Am J Physiol Renal Physiol 291: F422-428.
37. Izzedine H, Massard C, Spano JP, Goldwasser F, Khayat D, et al. (2010) VEGF signalling inhibition-induced proteinuria: Mechanisms, significance and management. Eur J Cancer 46: 439-448.
38. Gurevich F, Perazella MA, (2009) Renal effects of anti-angiogenesis therapy: update for the internist. Am J Med 122: 322-328.
39. Byzova TV, Goldman CK, Pampori N, Thomas KA, Bett A, et al. (2000) A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol Cell 6: 851-860.
40. Robinson SD, Reynolds LE, Kostourou V, Reynolds AR, da Silva RG, et al. (2009) Alphav beta3 integrin limits the contribution of neuropilin-1 to vascular endothelial growth factor-induced angiogenesis. J Biol Chem 284: 33966-33981.
41. Somanath PR, Malinin NL, Byzova TV, (2009) Cooperation between integrin alphavbeta3 and VEGFR2 in angiogenesis. Angiogenesis 12: 177-185.
42. Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, et al. (2002) Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat Med 8: 27-34.
43. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W, (1998) Vascular endothelial growth factor induces endothelial fenestrations in vitro. J Cell Biol 140: 947-959.
44. Behzadian MA, Windsor LJ, Ghaly N, Liou G, Tsai NT, et al. (2003) VEGF-induced paracellular permeability in cultured endothelial cells involves urokinase and its receptor. FASEB J 17(6): 752-754.
45. Persson M, Madsen J, Ostergaard S, Ploug M, Kjaer A, (2012) 68Ga-labeling and in vivo evaluation of a uPAR binding DOTA- and NODAGA-conjugated peptide for PET imaging of invasive cancers. Nucl Med Biol 39(4): 560-569.
46. Freundlieb S, Schirra-Müller C, Bujard H, (1999) A tetracycline controlled activation/repression system with increased potential for gene transfer into mammalian cells. J Gene Med 1: 4-12.
47. Shigehara T, Zaragoza C, Kitiyakara C, Takahashi H, Lu H, et al. (2003) Inducible podocyte-specific gene expression in transgenic mice. J Am Soc Nephrol 14: 1998-2003.
48. Takemoto M, Asker N, Gerhardt H, Lundkvist A, Johansson BR, et al. (2002) A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 161: 799-805.
49. Yuen PS, Dunn SR, Miyaji T, Yasuda H, Sharma K, et al. (2004) A simplified method for HPLC determination of creatinine in mouse serum. Am J Physiol Renal Physiol 286: F1116-1119.
50. Plehm R, Barbosa ME, Bader M, (2006) Animal models for hypertension/blood pressure recording. Methods Mol Med 129: 115-126.
51. Veron D, Bertuccio CA, Marlier A, Reidy K, Garcia AM, et al. (2011) Podocyte vascular endothelial growth factor (Vegf164) overexpression causes severe nodular glomerulosclerosis in a mouse model of type I diabetes. Diabetologia 54: 1227-1241.