Upregulated Expression of Integrin α1 in Mesangial Cells and Integrin α3 and Vimentin in Podocytes of Col4a3-Null (Alport) Mice

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Steenhard, Brooke M ^a,b   Vanacore, Roberto ^c   Friedman, David ^d   Zelenchuk, Adrian ^a,b   Stroganova, Larysa ^a,b   Isom, Kathryn ^a,b   St John, Patricia L ^a,b   Hudson, Billy G ^c   Abrahamson, Dale R ^a,b   Ram Singh, Shree ^e  

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

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTEGRIN; ALPHA3 INTEGRIN; COLLAGEN ALPHA1ALPHA2ALPHA1; COLLAGEN ALPHA1ALPHA4ALPHA5; COLLAGEN TYPE 4; INTEGRIN; LAMININ; TRYPSIN; UNCLASSIFIED DRUG; VIMENTIN;

ALPORT SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL FEATURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE DELETION; GENE OVEREXPRESSION; GLOMERULUS BASEMENT MEMBRANE; IMMUNOFLUORESCENCE MICROSCOPY; ISOLATED KIDNEY; KIDNEY FAILURE; MASS SPECTROMETRY; MESANGIUM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PODOCYTE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

ANIMALS; AUTOANTIGENS; COLLAGEN TYPE IV; DISEASE MODELS, ANIMAL; GLOMERULAR BASEMENT MEMBRANE; INTEGRIN ALPHA1; INTEGRIN ALPHA3; MESANGIAL CELLS; MICE; MICE, KNOCKOUT; NEPHRITIS, HEREDITARY; PODOCYTES; UP-REGULATION; VIMENTIN;

ANIMALIA; MUS;

EID: 84870879420     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050745     Document Type: Article

References (62)

1. Haraldsson B, Nystrom J, (2012) The glomerular endothelium: New insights on function and structure. Curr Opin Nephrol Hypertens 21: 258-263.
2. Patrakka J, Tryggvason K, (2010) Molecular make-up of the glomerular filtration barrier. Biochem Biophys Res Commun 396: 164-169.
3. Kashtan CE, Segal Y, (2011) Genetic disorders of glomerular basement membranes. Nephron Clin Pract 118: c9-c18.
4. Khoshnoodi J, Pedchenko V, Hudson BG, (2008) Mammalian collagen IV. Microsc Res Tech 71: 357-370.
5. Miner JH, (2011) Organogenesis of the kidney glomerulus: Focus on the glomerular basement membrane. Organogenesis 7: 75-82.
6. Miner JH, (1999) Renal basement membrane components. Kidney Int 56: 2016-2024.
7. Zenker M, Aigner T, Wendler O, Tralau T, Munterfering H, et al. (2004) Human laminin beta2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mole Genet 13: 2625-2632.
8. Cosgrove D, Meehan DT, Grunkemeyer JA, Kornak JM, Sayers R, et al. (1996) Collagen COL4A3 knockout: a mouse model for autosomal Alport syndrome. Genes Dev 10: 2981-2992.
9. Miner JH, Sanes JR, (1996) Molecular and functional defects in kidneys of mice lacking collagen alpha 3(IV): implications for Alport syndrome. J Cell Biol 135 (5) (): 1403-1413.
10. Cosgrove D, Kalluri R, Miner JH, Segal Y, Borza DB, (2007) Choosing a mouse model to study the molecular pathobiology of Alport glomerulonephritis. Kidney Int 71: 615-618.
11. Cosgrove D, Rodgers K, Meehan D, Miller C, Bovard K, et al. (2000) Integrin α1β1 and transforming growth factor-β1 play distinct roles in Alport glomerular pathogenesis and serve as dual targets for metabolic therapy. Am J Pathol 157: 1649-1659.
12. Kashtan CE, Kim Y, Lees GE, Thorner PS, Virtanen I, et al. (2001) Abnormal glomerular basement membrane laminins in murine, canine, and human Alport syndrome: aberrant laminin alpha2 deposition is species independent. J Am Soc Nephrol 12: 252-260.
13. Abrahamson DR, Prettyman AC, Robert B, St John PL, (2003) Laminin-1 reexpression in Alport mouse glomerular basement membranes. Kidney Int 63: 826-834.
14. Abrahamson DR, Hudson BG, Stroganova L, Borza DB, St John PL, (2009) Cellular origins of type IV collagen networks in developing glomeruli. J Am Soc Nephrol 20: 1471-1479.
15. Putaala H, Soininen R, Kilpeläinen P, Wartiovaara J, Tryggvason K, (2001) The murine nephrin gene is specifically expressed in kidney, brain and pancreas: inactivation of the gene leads to massive proteinuria and neonatal death. Hum Mol Genet 10: 1-8.
16. Roselli S, Heidet L, Sich M, Henger A, Kretzler M, et al. (2004) Early glomerular filtration defect and severe renal disease in podocin-deficient mice. Mol Cell Biol 24: 550-560.
17. Kalluri R, Shield CF, Todd P, Hudson BG, Neilson EG, (1997) Isoform switching of type IV collagen is developmentally arrested in X-linked Alport syndrome leading to increased susceptibility of renal basement membranes to endoproteolysis. J Clin Invest 99: 2470-2478.
18. Meehan DT, Delimont D, Cheung L, Zallocchi M, Sansom SC, et al. (2009) Biomechanical strain causes maladaptive gene regulation, contributing to Alport glomerular disease. Kidney Int 76: 968-976.
19. Zeisberg M, Khurana M, Rao VH, Cosgrove D, Rougier JP, et al. (2006) Stage-specific action of matrix metalloproteinases influences progressive hereditary kidney disease. PLoS Med 3: e100.
20. Wyss HM, Henderson JM, Byfield FJ, Bruggeman LA, Ding Y, et al. (2011) Biophysical properties of normal and diseased renal glomeruli. Am J Physiol Cell Physiol 300: C397-C405.
21. Abrahamson DR, Isom K, Roach E, Stroganova L, Zelenchuk A, et al. (2007) Laminin compensation in collagen α3(IV) knockout (Alport) glomeruli contributes to permeability defects. J Am Soc Nephrol 18: 2465-2472.
22. Drenckhahn D, Franke RP, (1988) Ultrastructural organization of contractile and cytoskeletal proteins in glomerular podocytes of chicken, rat, and man. Lab Invest 59: 673-682.
23. Yaoita E, Franke WW, Yamamoto T, Kawasaki K, Kihara I, (1999) Identification of renal podocytes in multiple species: Higher vertebrates are vimentin positive/lower vertebrates are desmin positive. Histochem Cell Biol 111: 107-115.
24. Cortes P, Méndez M, Riser BL, Guérin CJ, Rodríguez-Barbero A, et al. (2000) F-actin fiber distribution in glomerular cells: structural and functional implications. Kidney Int 58: 2452-61.
25. Wang R, St John PL, Kretzler M, Wiggins RC, Abrahamson DR, (2000) Molecular cloning, expression, and distribution of glomerular epithelial protein 1 in developing mouse kidney. Kidney Int 57: 1847-18 59.
26. Mundel P, Heid HW, Mundel TM, Kruger M, Reiser J, et al. (1997) Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol 139: 193-204.
27. Helfand BT, Chang L, Goldman RD, (2004) Intermediate filaments are dynamic and motile elements of cellular architecture. J Cell Sci 117: 133-141.
28. Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, et al. (2009) Introducing intermediate filaments: From discovery to disease. J Clin Invest 119: 1763-1771.
29. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, et al. (2008) Nuclear lamins: Major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22: 832-853.
30. Ivaska J, Pallari HM, Nevo J, Eriksson JE, (2007) Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res 313: 2050-2062.
31. Eriksson JE, He T, Trejo-Skalli AV, Harmala-Brasken AS, Hellman J, et al. (2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J Cell Sci 117: 919-932.
32. Satelli A, Shulin L, (2011) Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 68: 3033-3046.
33. Colucci-Guyon E, Portier MM, Dunia J, Paulin D, Pournin S, et al. (1994) Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79: 679-694.
34. Colucci-Guton E, Gimenez M, Ribotta Y, Maurice T, Babinet C, et al. (1999) Cerebellar defect and impaired motor coordination in mice lacking vimentin. Glia 25: 33-43.
35. Eckes B, Colluci-Guyon E, Smola H, Nodder C, Babinet C, et al. (2000) Impaired wound healing in embryonic and adult mice lacking vimentin. J Cell Sci 113: 2455-2462.
36. Nieminen M, Henttinen T, Merinen M, Marttila-Ichihara F, Eriksson JE, et al. (2006) Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol 8: 156-162.
37. Holthofer H, Miettinen A, Lehto VP, Lehtonen E, Virtanen I, (1984) Expression of vimentin and cytokeratin types of intermediate filament proteins in developing and adult human kidney. Lab Invest 50: 552-559.
38. Stamenkovic I, Skalli O, Gabbiani G, (1986) Distribution of intermediate filament proteins in normal and diseased human glomeruli. Am J Pathol 125: 465-475.
39. Zou J, Yaoita E, Watanabe Y, Yoshida Y, Nameta M, et al. (2006) Upregulation of nestin, vimentin, and desmin in rat podocytes in response to injury. Virchows Arch 448: 485-492.
40. Zou J, Chang TH, Chang H, Yaoita E, Yoshida Y, et al. (2007) Time course of expression of intermediate filament protein vimentin, nestin, and desmin in rat renal glomerular injury. Chin Med J 120: 1203-1205.
41. Shi S, Yu L, Chiu C, Sun Y, Chen J, et al. (2008) Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol 19: 2159-2169.
42. Ostalska-Nowicka D, Zachwieja J, Nowicki M, Witt M, (2004) Expression of intermediate filaments of podocytes within nephrotic syndrome glomerulopathies in children. Histochem Cell Biol 121: 109-113.
43. Perry J, Ho M, Viero S, Zheng K, Jacobs R, et al. (2007) The intermediate filament nestin is highly expressed in normal human podocytes and podocytes in disease. Pediatr Dev Pathol 10: 369-382.
44. Hynes RO, (2002) Integrins: Bidirectional, allosteric signaling machines. Cell 110: 673-687.
45. Kreis S, Schönfeld HJ, Melchior C, Steiner B, Kieffer N, (2005) The intermediate filament protein vimentin binds specifically to a recombinant integrin alpha2/beta1 cytoplasmic tail complex and co-localizes with native alpha2/beta1 in endothelial cell focal adhesions. Exp Cell Res 305 (1) (): 110-21.
46. Ivaska J, Vuoriluoto K, Huovinen T, Izawa I, Inagaki M, et al. (2005) PKCε-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J 24: 3834-3845.
47. Pozzi A, Zent R, (2011) Extracellular matrix receptors in branched organs. Curr Opin Cell Biol 23: 547-553.
48. Kuhara T, Kagami S, Kuroda Y, (1997) Expression of beta-1 integrins on activated mesangial cells in human glomerulonephritis. J Am Soc Nephrol 8: 1679-1687.
49. Shikata K, Makino H, Moriaka S, Kashitani T, Hirata K, et al. (1995) Distribution of extracellular receptors in various forms of glomerulonephritis. Am J Kidney Dis 25: 680-688.
50. Chen X, Moeckel G, Morrow JD, Cosgrove D, Harris RC, et al. (2004) Lack of integrin alpha 1 beta 1 leads to severe glomerulosclerosis after glomerular injury. Am J Pathol 165: 617-630.
51. Zent R, Yan X, Su Y, Hudson BG, Borza DB, et al. (2006) Glomerular injury is exacerbated in diabetic integrin alpha-1 null mice. Kidney Int 70: 460-470.
52. Mathew S, Chen X, Pozzi A, Zent R, (2012) Integrins in renal development. Pediatr Nephrol 27: 891-900.
53. Kreidberg JA, Donovan MJ, Goldstein SL, Renneke H, Shepherd K, et al. (1996) Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122: 3537-3547.
54. 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.
55. 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 (3) (): 799-805.
56. Franco AT, Friedman DB, Nagy TA, Romero-Gallo J, Krishna U, Kendall A, et al. (2009) Delineation of a carcinogenic Helicobacter pylori proteome. Mol Cell Proteomics 8: 1947-1958.
57. Yates JR, Eng JK, McCormack AL, Schieltz D, (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67: 1426-1436.
58. Ma ZQ, Dasari S, Chambers MC, Litton MD, Sobecki SM, et al. (2009) IDPicker 2.0: Improved protein assembly with high discrimination peptide identification filtering. J Proteome Res 8: 3872-3881.
59. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
60. Heidet L, Borza DB, Jouin M, Sich M, Mattei MG, et al. (2003) A human-mouse chimera of the α3α4α5(IV) collagen promoter rescues the renal phenotype in Col4a3-/- Alport mice. Am J Pathol 165: 1633-1644.
61. Abrahamson DR, Irwin MH, St.John PL, Perry EW, Accavitti MA, et al. (1989) Selective immunoreactivities of kidney basement membranes to monoclonal antibodies against laminin: localization of the end of the long arm and short arms to discrete microdomains. J Cell Biol 109: 3477-3491.
62. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics Int 11: 36-42.