Deletion of von Hippel-Lindau in glomerular podocytes results in glomerular basement membrane thickening, ectopic subepithelial deposition of collagen α1α2α1(IV), expression of neuroglobin, and proteinuria

American Journal of Pathology

Volumn 177, Issue 1, 2010, Pages 84-96

  Steenhard, Brooke M ^a   Isom, Kathryn ^a   Stroganova, Larysa ^a   St John, Patricia L ^a   Zelenchuk, Adrian ^a   Freeburg, Paul B ^a   Holzman, Lawrence B ^b   Abrahamson, Dale R ^a  

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

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; COLLAGEN TYPE 4; CRE RECOMBINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KI 67 ANTIGEN; NEUROGLOBIN; PODOCIN; VON HIPPEL LINDAU PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GLOMERULUS; GLOMERULUS BASEMENT MEMBRANE; IMMUNOELECTRON MICROSCOPY; MESANGIUM CELL; MOUSE; MUTANT; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PODOCYTE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN STABILITY; PROTEINURIA; SUBENDOTHELIUM; URINALYSIS; URINARY EXCRETION; WILD TYPE;

EID: 77954579763     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090767     Document Type: Article

References (56)

1. Haraldsson B, Nyström J, Deen WM: Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 2008, 88(2):451-487
2. Miner JH, Abrahamson DR: Molecular and cellular mechanisms of glomerular capillary development. Seldin and Giebisch's the kidney, vol 1-2, ed 4: physiology and pathophysiology. Edited by RJ Alpern, SC Hebert. Burlington, Academic Press, 2007, pp 691-706
3. St. John PL, Abrahamson DR: Glomerular endothelial cells and podocytes jointly synthesize laminin-1 and -11 chains. Kidney Int 2001, 60(3):1037-1046
4. Abrahamson DR, Hudson BG, Stroganova L, Borza DB, St John PL: Cellular origins of type IV collagen networks in developing glomeruli. J Am Soc Nephrol 2009, 20(7):1471-1479
5. Zenker M, Aigner T, Wendler O, Tralau T, Muntefering H, Fenski R, Pitz S, Schumacher V, Royer-Pokora B, Wuhl E, Cochat P, Bouvier R, Kraus C: Human laminin beta2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mol Genet 2004, 13:2625-2632
6. Wuhl E, Kogan J, Zurowska A, Matejas V, Vandervoorde RG, Aigner T, Wendler O, Lesniewska I, Bouvier R, Reis A, Cochat P, Zenker M: Neurodevelopmental deficits in Pierson (microcoria-congenital nephrosis) syndrome. Am J Med Genet A 2007, 143:311-319
7. Noakes PG, Miner JH, Gautam M, Cunningham JM, Sanes JR, Merlie JP: The renal glomerulus of mice lacking s-laminin/laminin b2: nephrosis despite molecular compensation by laminin b1. Nat Genet 1995, 10:400-406
8. Kashtan CE: Familial hematurias: what we know and what we don't. Pediatr Nephrol 2005, 20:1027-1035 (Pubitemid 41001540)
9. Cosgrove D, Meehan DT, Grunkemeyer JA, Kornak JM, Sayers R, Hunter WJ, Samuelson GC: Collagen COL4A3 knockout: a mouse model for autosomal Alport syndrome. Genes Dev 1996, 10(23):2981-2992 (Pubitemid 26412525)
10. Miner JH, Sanes JR: Molecular and functional defects in kidneys of mice lacking alpha collagen 3(IV): implications for Alport syndrome. J Cell Biol 1996, 135:1403-1413
11. Lu W, Phillips CL, Killen PD, Hlaing T, Harrison WR, Elder FF, Miner JH, Overbeek PA, Meisler MH: Insertional mutation of the collagen genes Col4a3 and Col4a4 in a mouse model of Alport syndrome. Genomics 1999, 61:113-124 (Pubitemid 29514135)
12. Abrahamson DR, Prettyman AC, Robert B, St John PL: Laminin-1 re-expression in Alport mouse glomerular basement membranes. Kidney Int 2003, 63:826-834 (Pubitemid 36315560)
13. Abrahamson DR, Isom K, Roach E, Stroganova L, Zelenchuk A, Miner JH, St John PL: Laminin compensation in collagen α3(IV) knockout (Alport) glomeruli contributes to permeability defects. J Am Soc Nephrol 2007, 18(9):2465-2472
14. Kashtan CE, Kim Y, Lees GE, Thorner PS, Virtanes I, Miner JH: Abnormal glomerular basement membrane laminins in murine, canine, and human Alport syndrome: aberrant laminin alpha2 deposition is species independent. J Am Soc Nephrol 2001, 12(2):252-260 (Pubitemid 32116367)
15. Beirowski B, Weber M, Gross O: Chronic renal failure and shortened lifespan in COL4A3+/- mice: an animal model for thin basement membrane nephropathy. J Am Soc Nephrol 2006, 17(7):1986-1994 (Pubitemid 44036183)
16. Yang Y, Zhang SY, Sich M, Béziau A, van den Heuvel LP, Gubler MC: Glomerular extracellular matrix and growth factors in diffuse mesangial sclerosis. Pediatr Nephrol 2001, 16(5):429-438 (Pubitemid 32447708)
17. Wang Z, Jiang T, Li J, Proctor G, McManaman JL, Lucia S, Chua S, Levi M: Regulation of renal lipid metabolism, lipid accumulation, and glomerulosclerosis in FVBdb/db mice with type 2 diabetes. Diabetes 2005, 54(8):2328-2335
18. Freeburg PB, Robert B, St John PL, Abrahamson DR: Podocyte expression of hypoxia-inducible factor (HIF)-1 and HIF-2 during glomerular development. J Am Soc Nephrol 2003, 14(4):927-938 (Pubitemid 36359275)
19. Heyman SN, Khamaisi M, Rosen S, Rosenberger C: Renal parenchymal hypoxia, hypoxia response and the progression of chronic kidney disease. Am J Nephrol 2008, 28(6):998-1006
20. Mole DR, Ratcliffe PJ: Cellular oxygen sensing in health and disease. Pediatr Nephrol 2008, 23(5):681-694
21. Kaelin WG Jr: The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer 2008, 8(11):865-873
22. Nyhan MJ, O'Sullivan GC, McKenna SL: Role of the VHL (von Hippel-Lindau) gene in renal cancer: a multifunctional tumour suppressor. Biochem Soc Trans 2008, 36(pt 3):472-478
23. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB: Podocyte-specific expression of cre recombinase in transgenic mice. Genesis 2003, 35(1):39-42 (Pubitemid 36150980)
24. Steenhard BM, Isom KS, Cazcarro P, Dunmore JH, Godwin AR, St John PL, Abrahamson DR: Integration of embryonic stem cells in metanephric kidney organ culture. J Am Soc Nephrol 2005, 16(6):1623-1631 (Pubitemid 41716469)
25. Haase VH, Glickman JN, Socolovsky M, Jaenisch R: Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci USA 2001, 98(4):1583-1588 (Pubitemid 32165542)
26. Biju MP, Neumann AK, Bensinger SJ, Johnson RS, Turka LA, Haase VH: Vhlh gene deletion induces Hif-1-mediated cell death in thymocytes. Mol Cell Biol 2004, 24(20):9038-9047
27. Holzman LB, St John PL, Kovari IA, Verma R, Holthofer H, Abrahamson DR: Nephrin localizes to the slit pore of the glomerular epithelial cell. Kidney Int 1999, 56(4):1481-1491
28. Abrahamson DR, St John PL: Loss of laminin epitopes during glomerular basement membrane assembly in developing mouse kidneys. J Histochem Cytochem 1992, 40(12):1943-1953
29. Jensen EB, Gundersen HJ, Osterby R: Determination of membrane thickness distribution from orthogonal intercepts. J Microsc 1979, 115(1):19-33
30. Takemoto M, Asker N, Gerhardt H, Lundkvist A, Johansson BR, Saito Y, Betsholtz C: A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 2002, 161(3):799-805 (Pubitemid 34988366)
31. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(4):402-408
32. Zhang YZ, Lee HS: Quantitative changes in the glomerular basement membrane components in human membranous nephropathy. J Pathol 1997, 183(1):8-15
33. Ding M, Cui S, Li C, Jothy S, Haase V, Steer BM, Marsden PA, Pippin J, Shankland S, Rastaldi MP, Cohen CD, Kretzler M, Quaggin SE: Loss of the tumor suppressor Vhlh leads to upregulation of Cxcr4 and rapidly progressive glomerulonephritis in mice. Nat Med 2006, 12(9):1081-1087
34. Edgar R, Domrachev M, Lash AE: Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30(1):207-210
35. Burmester T, Weich B, Reinhardt S, Hankeln T: A vertebrate globin expressed in the brain. Nature 2000, 407(6803):520-523
36. Brukamp K, Jim B, Moeller MJ, Haase VH: Hypoxia and podocyte-specific Vhlh deletion confer risk of glomerular disease. Am J Physiol Renal Physiol 2007, 293(4):F1397-F1407
37. 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(5):707-716
38. Eremina V, Cui S, Gerber H, Ferrara N, Haigh J, Nagy A, Ema M, Rossant J, Jothy S, Miner JH, Quaggin SE: Vascular endothelial growth factor a signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival. J Am Soc Nephrol 2006, 17(3):724-735
39. Ohh M, Yauch RL, Lonergan KM, Whaley JM, Stemmer-Rachamimov AO, Louis DN, Gavin BJ, Kley N, Kaelin WG Jr., Iliopoulos O: The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol Cell 1998, 1(7):959-968
40. Bluyssen HA, Lolkema MP, van Beest M, Boone M, Snijckers CM, Los M, Gebbink MF, Braam B, Holstege FC, Giles RH, Voest EE: Fibronectin is a hypoxia-independent target of the tumor suppressor VHL. FEBS Lett 2004, 556(1-3):137-142
41. Kurban G, Hudon V, Duplan E, Ohh M, Pause A: Characterization of a von Hippel Lindau pathway involved in extracellular matrix remodeling, cell invasion, and angiogenesis. Cancer Res 2006, 66(3):1313-1319 (Pubitemid 43259909)
42. Ku CH, White KE, Dei Cas A, Hayward A, Webster Z, Bilous R, Marshall S, Viberti G, Gnudi L: Inducible overexpression of sFlt-1 in podocytes ameliorates glomerulopathy in diabetic mice. Diabetes 2008, 57(10):2824-2833
43. Iglesias-de la Cruz MC, Ziyadeh FN, Isono M, Kouahou M, Han DC, Kalluri R, Mundel P, Chen S: Effects of high glucose and TGF-beta1 on the expression of collagen IV and vascular endothelial growth factor in mouse podocytes. Kidney Int 2002, 62(3):901-913 (Pubitemid 35316719)
44. Chen S, Kasama Y, Lee JS, Jim B, Marin M, Ziyadeh FN: Podocyte-derived vascular endothelial growth factor mediates the stimulation of alpha3(IV) collagen production by transforming growth factor-beta1 in mouse podocytes. Diabetes 2004, 53(11):2939-2949 (Pubitemid 39425920)
45. Grosfeld A, Stolze IP, Cockman ME, Pugh CW, Edelmann M, Kessler B, Bullock AN, Ratcliffe PJ, Masson N: Interaction of hydroxylated collagen IV with the von hippel-lindau tumor suppressor. J Biol Chem 2007, 282(18):13264-13269 (Pubitemid 47100504)
46. Kurban G, Duplan E, Ramlal N, Hudon V, Sado Y, Ninomiya Y, Pause A: Collagen matrix assembly is driven by the interaction of von Hippel-Lindau tumor suppressor protein with hydroxylated collagen IV alpha 2. Oncogene 2008, 27(7):1004-1012
47. Minamishima YA, Moslehi J, Padera RF, Bronson RT, Liao R, Kaelin WG Jr: A feedback loop involving the Phd3 prolyl hydroxylase tunes the mammalian hypoxic response in vivo. Mol Cell Biol 2009, 29(21):5729-5741
48. Lee S, Nakamura E, Yang H, Wei W, Linggi MS, Sajan MP, Farese RV, Freeman RS, Carter BD, Kaelin WG Jr., Schlisio S: Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 2005, 8(2):155-167
49. Sun Y, Jin K, Mao XO, Zhu Y, Greenberg DA: Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury. Proc Natl Acad Sci USA 2001, 98(26):15306-15311
50. Li RC, Lee SK, Pouranfar F, Brittian KR, Clair HB, Row BW, Wang Y, Gozal D: Hypoxia differentially regulates the expression of neuroglobin and cytoglobin in rat brain. Brain Res 2006, 1096(1):173-179
51. Schmidt-Kastner R, Haberkamp M, Schmitz C, Hankeln T, Burmester T: Neuroglobin mRNA expression after transient global brain ischemia and prolonged hypoxia in cell culture. Brain Res 2006, 1103(1):173-180
52. Cohen CD, Doran PP, Blattner SM, Merkle M, Wang GQ, Schmid H, Mathieson PW, Saleem MA, Henger A, Rastaldi MP, Kretzler M: Sam68-like mammalian protein 2, identified by digital differential display as expressed by podocytes, is induced in proteinuria and involved in splice site selection of vascular endothelial growth factor. J Am Soc Nephrol 2005, 16(7):1958-1965
53. Rastaldi MP, Armelloni S, Berra S, Calvaresi N, Corbelli A, Giardino LA, Li M, Wang GQ, Fornasieri A, Villa A, Heikkila E, Soliymani R, Boucherot A, Cohen CD, Kretzler M, Nitsche A, Ripamonti M, Malgaroli A, Pesaresi M, Forloni GL, Schlöndorff D, Holthofer H, D'Amico G: Glomerular podocytes contain neuron-like functional synaptic vesicles. FASEB J 2006, 20(7):976-978
54. Burmester T, Hankeln T: What is the function of neuroglobin? J Exp Biol 2009, 212:1423-1428
55. Khan AA, Wang Y, Sun Y, Mao XO, Xie L, Miles E, Graboski J, Chen S, Ellerby LM, Jin K, Greenberg DA: Neuroglobin-overexpressing transgenic mice are resistant to cerebral and myocardial ischemia. Proc Natl Acad Sci USA 2006, 103(47):17944-17948
56. Shih SC, Robinson GS, Perruzzi CA, Calvo A, Desai K, Green JE, Ali IU, Smith LE, Senger DR: Molecular profiling of angiogenesis markers. Am J Pathol 2002, 161(1):35-41