Development of kidney glomerular endothelial cells and their role in basement membrane assembly

Organogenesis

Volumn 5, Issue 1, 2009, Pages 1-13

  Abrahamson, Dale R ^a  

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

Author keywords

Glomerular basement membrane; Laminin; Podocytes; Type IV collagen; Vascular endothelial growth factor

Indexed keywords

COLLAGEN TYPE 4; LAMININ; TRANSCRIPTION FACTOR; VASCULOTROPIN;

ANGIOGENESIS; CELL DIFFERENTIATION; CELL MATURATION; EPITHELIUM CELL; GLOMERULUS; GLOMERULUS BASEMENT MEMBRANE; GLOMERULUS CAPILLARY; HUMAN; INTROSPECTION; KIDNEY DEVELOPMENT; KIDNEY EPITHELIUM; NONHUMAN; REGULATORY MECHANISM; REVIEW;

EID: 65949118275     PISSN: 15476278     EISSN: 15558592     Source Type: Journal    
DOI: 10.4161/org.7577     Document Type: Review

References (119)

1. Farquhar MG, Wissig SL and Palade GE. Glomerular permeability I. ferritin transfer across the normal glomerular capillary wall. J Exp Med 1961; 113:47-87.
2. Jeansson M, Haraldsson B. Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am J Physiol Renal Physiol 2006; 290:111-116
3. Kerjaschki D. Caught flat-footed: Podocyte damage and the molecular bases of focal glomerulosclerosis. J Clin Invest 2001; 108:1583-1587 (Pubitemid 33144868)
4. Miner JH. Focusing on the glomerular slit diaphragm. Podocin enters the picture. Am J Pathol 2002; 160:3-5. (Pubitemid 34052258)
5. Somlo S, Mundel P. Getting a foothold in nephrotic syndrome. Nat Genet 2000; 24:333-335 (Pubitemid 30187426)
6. Mundel P, Reiser J, Zuniga Mejia Borja A, Pavenstadt H, et al. Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines. Exp Cell Res 1997; 236:248-258 (Pubitemid 27452369)
7. Shankland SJ, Pippin JW, Reiser J, Mundel P. Podocytes in culture: past, present and future. Kidney Int 2007; 72:26-36. (Pubitemid 47014453)
8. Ruotsalainen V, Ljungberg P, Wartiovaara J, Lenkkeri U, Kestila M, Jalanko H, et al. Nephrin is specifically located at the slit diaphragm of glomerular podocytes. Proc Natl Acad Sci USA 1999; 96:7962-7967 (Pubitemid 29328390)
9. Holzman LB, St. John PL, Kovarila A, Verma R, Holthofer H, Abrahamson DR. Nephrin localizes to the slit pore of the glomerular epithelial cell. Kidney Int 1999; 56:1481-1491
10. Holthofer H, Ahola H, Solin ML, Wang S, Palmern T, Luimula P, et al. Nephrin localizes at the podocyte filtration slit area and is characteristically spliced in the human kidney. Am J Pathol 1999; 155:1681-1687
11. Kawachi H, Koike H, Kurihara H, Yaoita E, Orikasa M, Shia MA, Sakai T, Yamamoto T, Salant DJ. Cloning of rat nephrin: Expression in developing glomeruli and in proteinuric states. Kidney Int 2000; 57:1949-1961. (Pubitemid 30252286)
12. Schwarz K, Simons K, Reiser J, Kriz W, Holzman LB, Shaw AS, Mundel P. Podocin is a raft-associated component of the glomerular slit diaphragm that interacts with CD2AP and nephrin. J Am Soc Nephrol 2001; 12:60.
13. Roselli S, Gribouval O, Boute N, Sich M, Benessy F, Attie T, et al. Podocin localizes in the kidney to the slit diaphragm area. Am J Pathol 2002; 160:131-139
14. Inoue T, Yaoita E, Kurihara H, Shimuzu F, Sakai T, Koboyashi T, et al. FAT is a component of glomerular slit diaphragms. Kidney Int 2001; 59:1003-1012
15. Simons M, Schwarz K, Kriz W, Miettinen A, Reiser J, Mundel P, Holthofer H. Involvement of lipid rafts in nephrin phosphorylation and organization of the glomerular slit diaphragm. Am J Pathol 2001; 159:1069-1077 (Pubitemid 32847197)
16. Shih NY, Li J, Karpitskii V, Nguyen A, Dustin ML, Kanagawa O, et al. Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 1999; 286:312-315
17. Kaplan JM, Kim SH, North KN, Rennke H, Correia LA, Tong HQ, et al. Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 2000; 24:251-256
18. Reiser J, Kriz W, Kretzler M, Mundel P. The glomerular slit diaphragm is a modified adherens junction. J Am Soc Nephrol 2000; 11:1-8. (Pubitemid 30020420)
19. Schnabel E, Anderson JM, Farquhar MG. The tight junction protein ZO-1 is concentrated along slit diaphragms of the glomerular epithelium. J Cell Biol 1990; 111:1255-1263 (Pubitemid 20263804)
20. Kashtan CE. Familial hematuria due to type IV collagen mutations: Alport syndrome and thin basement membrane nephropathy. Curr Opin Pediatr 2004; 16:177-181
21. Kashtan CE. Familial hematurias: What we know and what we don't. Pediatr Nephrol 2005; 20:1027-1035
22. Heikkila P, Tryggvason K, Thorner P. Animal models of Alport syndrome: Advancing the prospects for effective gene therapy. Exp Nephrol 2000; 8:1-7.
23. Miner JH, Li C. Defective glomerulogenesis in the absence of laminin alpha5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev Biol 2000; 217:278-289 (Pubitemid 30060876)
24. Noakes PG, Miner JH, Gautam M, Cunningham JM, Sanes JR, Merlie JP. The renal glomerulus of mice lacking s-laminin/laminin β2: Nephrosis despite molecular compensation by laminin β1. Nat Genet 1995; 10:400-406
25. Cosgrove D, Meehan DT, Grunkemeyer JA, Kornak JM, Sayers R, Hunter WJ, et al. Collagen COL4A3 knockout: A mouse model for autosomal Alport syndrome. Genes Dev 1996; 10:2981-2992
26. Miner JH, Sanes JR. Molecular and functional defects in kidneys of mice lacking collagen alpha3(IV): Implications for Alport syndrome. J Cell Biol 1996; 135:1403-1413
27. Lu W, Phillips CL, Killen PD, Hlaing T, Harrison WR, Elder FF, et al. Insertional mutation of the collagen genes Col4a3 and Col4a4 in a mouse model of Alport syndrome. Genomics 1999; 61:113-124
28. Kreidberg JA, Donovan MJ, Goldstein SL, Rennke H, Shepherd K, Jones RC, Jaenisch R. Alpha3 beta1 integrin has a crucial role in kidney and lung organogenesis. Development 1996; 122:3537-3547 (Pubitemid 26395995)
29. Bissell MJ, Hall HG, Parry G. How does the extracellular matrix direct gene expression? J Theor Biol 1982; 99:31-68.
30. Sage H. Collagens of basement membranes. J Invest Dermatol 1982; 79:51-59 (Pubitemid 12080824)
31. Miner JH, Abrahamson DR. Molecular and cellular mechanisms of glomerular capillary development. In: Alpern RJ, Hebert SC, eds, Seldin and Giebisch's The Kidney. 4th edition. Burlington, MA: Academic Press 1988; 691-706.
32. Quaggin SE, Kreidberg JA. Development of the renal glomerulus: good neighbors and good fences. Development 2008; 135:609-620
33. Khoshnoodi J, Pedchenko V, Hudson BG. Mammalian collagen IV. Microsc Res Tech 2008; 71:357-370
34. Gubler MC. Inherited diseases of the glomerular basement membrane. Nat Clin Pract Nephrol 2008; 4:24-37. (Pubitemid 350308222)
35. Saxen L. Organogenesis of Kidney. Cambridge: Cambridge University Press 1987; 1-173.
36. Abrahamson DR. Glomerulogenesis in the developing kidney. Semin Nephrol 1991; 11:375-389
37. Woolf AS. The life of the human kidney before birth: Its secrets unfold. Pediatr Res 2001; 49:8-10.
38. Abrahamson DR. Structure and development of the glomerular capillary wall and basement membrane. Am J Physiol 1987; 253:783-794
39. Ekblom P. Formation of basement membranes in the embryonic kidney: an immunohistological study. J Cell Biol 1981; 91:1-10. (Pubitemid 12252759)
40. Lelongt B, Makino H, Kanwar YS. Maturation of the developing renal glomerulus with respect to basement membrane proteoglycans. Kidney Int 1987; 32:498-506. (Pubitemid 17154739)
41. Reeves WH, Kanwar YS, Farquhar MG. Assembly of the glomerular filtration surface. Differentiation of anionic sites in glomerular capillaries of newborn rat kidney. J Cell Biol 1980; 85:735-753
42. Haroldsson B, Nystrom J, Deen WM. Properties of the glomerular basement barrier and mechanisms of proteinuria. Physiol Rev 2008; 88:451-487
43. Abrahamson DR. Origin of the glomerular basement membrane visualized after in vivo labeling of laminin in newborn rat kidneys. J Cell Biol 1985; 100:1988-2000.
44. Kanwar YS, Jakubowski ML, Rosenzweig LJ, Gibbons JT. De novo cellular synthesis of sulfated proteoglycans of the developing renal glomerulus in vivo. Proc Natl Acad Sci USA 1984; 81:7108-7111 (Pubitemid 15216706)
45. Sariola H, Timpl R, von der Mark K, Mayne R, Fitch JM, Linsenmayer TF, et al. Dual origin of the glomerular basement membrane. Dev Biol 1984; 101:86-96.
46. Abrahamson DR, Perry EW. Evidence for splicing new basement membrane into old during glomerular development in newborn rat kidneys. J Cell Biol 1986; 103:2489-2498 (Pubitemid 17216673)
47. Hyink DP, Abrahamson DR. Origin of the glomerular vasculature in the developing kidney. Semin Nephrol 1995; 15:300-314.
48. Sariola H, Ekblom P, Lehtonen E, Saxen L. Differentiation and vascularization of the metanephric kidney grafted on the chorioallantoic membrane. Dev Biol 1983; 96:427-435
49. Hyink DP, Tucker DC, St. John PL, et al. Endogenous origin of glomerular endothelial and mesangial cells in grafts of embryonic kidneys. Am J Physiol 1996; 270:886-899
50. Robert B, St. John PL, Hyink DP, Abrahamson DR. Evidence that embryonic kidney cells expressing flk-1 are intrinsic, vasculogenic angioblasts. Am J Physiol Renal Physiol 1996; 271:744-753 (Pubitemid 126757695)
51. Robert B, St. John PL, Abrahamson DR. Direct visualization of renal vascular morphogenesis in Flk1 heterozygous mutant mice. Am J Physiol Renal Physiol 1998; 275:164-172 (Pubitemid 28376347)
52. Tufro A, Norwood VF, Carey RM, Gomez RA. Vascular endothelial growth factor induces nephrogenesis and vasculogenesis. J Am Soc Nephrol 1999; 10:2125-2134 (Pubitemid 29453490)
53. Loughna S, Hardman P, Landels E, et al. A molecular and genetic analysis of renal glomerular capillary development. Angiogenesis 1997; 1:84-101.
54. Sequeira Lopez ML, Pentz ES, Robert B, et al. Embryonic origin and lineage of juxtaglomerular cells. Am J Physiol Renal Physiol 2001; 281:345-356
55. Daniel TO, Abrahamson DR. Endothelial signal integration in vascular assembly. Annu Rev Physiol 2000; 62:649-671 (Pubitemid 30618278)
56. Robert B, Abrahamson DR. Control of glomerular capillary development by growth factor/receptor kinases. Pediatr Nephrol 2001; 16:294-301. (Pubitemid 32229853)
57. Carmeliet P, Ferreira V, Breier G, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380:435-439
58. Ferrara N, Carver-Moore K, Chen H, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996; 380:439-442
59. Shalaby F, Rossant J, Yamaguchi TP, Gertsenestein M, Wu XF, Breitman ML, et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995; 376:62-66
60. Fong G-H, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor kinase in regulating the assembly of vascular endothelium. Nature 1995; 376:66-70.
61. Simon M, Grone HJ, Johren O, et al. Expression of vascular endothelial growth factor and its receptors in human renal ontogenesis and in adult kidney. Am J Physiol 1995; 268:240-250
62. Tufro A. VEGF spatially directs angiogenesis during metanephric development in vitro. Dev Biol 2000; 227:558-566
63. Esser S, Wolburg K, Wolburg H, Breier G, Kurzchalia T, Risau W. Vascular endothelial growth factor induces endothelial fenestrations in vitro. J Cell Biol 1998; 140:947-959 (Pubitemid 28141231)
64. Kitamoto Y, Tokunaga H, Tomita K. Vascular endothelial growth factor is an essential molecule for mouse kidney development: glomerulogenesis and nephrogenesis. J Clin Invest 1997; 99:2351-2357 (Pubitemid 27227711)
65. Eremina V, Cui S, Gerber H, et al. Vascular endothelial growth factor-A signaling in the podocyte-endothelial compartment is required for mesangial cell migration and survival. J Am Soc Nephrol 2006; 17:724-735
66. Eremina V, Sood M, Haigh J, et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 2003; 111:701-716
67. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005; 306:12.
68. Maxwell PH, Ratcliffe PJ. Oxygen sensors and angiogenesis. Semin Cell Dev Biol 2002; 13:29-37. (Pubitemid 35418312)
69. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, et al. VEGF is required for growth and survival in neonatal mice. Development 1999; 126:149-159
70. Abedi H, Zachary I. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J Biol Chem 1997; 272:15442-15451 (Pubitemid 27255570)
71. Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the anti-apoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem 1998; 273:13313-13316 (Pubitemid 28246905)
72. Bernhardt WM, Schmitt R, Rosenberger C, et al. Expression of hypoxia-inducible transcription factors in developing human and rat kidneys. Kidney Int 2006; 69:114-122
73. Freeburg PB, Robert B, St. John PL, Abrahamson DR. Podocyte expression of hypoxiainducible factor (HIF)-1 and HIF-2 during glomerular development. J Am Soc Nephrol 2003; 14:927-938 (Pubitemid 36359275)
74. Freeburg PB, Abrahamson DR. Divergent expression patterns for hypoxia-inducible factor-1beta and aryl hydrocarbon receptor nuclear transporter-2 in developing kidney. J Am Soc Nephrol 2004; 15:2569-2578 (Pubitemid 41103363)
75. Freeburg PB, Abrahamson DR. Hypoxia-inducible factors and kidney vascular development. J Am Soc Nephrol 2003; 14:2723-2730 (Pubitemid 37305634)
76. Steenhard BM, Freeburg PB, Isom K, Stroganova L, Borza DB, Hudson BG, et al. Kidney development and gene expression in the HIF2α knockout mouse. Dev Dyn 2007; 236:1115-1125
77. Tian H, Hammer RE, Matsumoto AM, Russell DW, McKnight SL. The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev 1998; 12:3320-3324 (Pubitemid 28520979)
78. Haase VH. The VHL/HIF oxygen sensing pathway and its rele3vance to kidney disease. Kidney Int 2006; 69:1302-1307
79. Haase VH. Hypoxia-inducible factors in the kidney. Am J Physiol Renal Physiol 2006; 291:271-281
80. Kaelin WG. The von Hippel-Lindau tumor suppressor gene and kidney cancer. Clin Can Res 2004; 10:6290-6295
81. Steenhard B, Isom K, Stroganova L, St. John P, Freeburg P, Holzman L, et al. Podocyte-selective deletion of von Hippel-Lindau (VHL) protein causes albuminuria. J Am Soc Nephrol 2005; 16:667.
82. Ding M, Cui S, Li C, Jothy S, Haase V, Steer BM, et al. Loss of the tumor suppressor Vhlh leads to upregulation of Cxcr4 and rapidly progressive glomerulonephritis in mice. Nat Med 2006; 12:1081-1087
83. 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; 293:1397-1407 (Pubitemid 47583976)
84. Woolf AS, Yuan HT. Angiopoietin growth factors and Tie receptor tyrosine kinases in renal vascular development. Pediatr Nephrol 2001; 16:177-184 (Pubitemid 32125170)
85. Ulleras E, Wilcock A, Miller SJ, Franklin GC. The sequential activation and repression of the human PDGF-B gene during chronic hypoxia reveals antagonistic roles for the depletion of oxygen and glucose. Growth Factors 2001; 19:233-245 (Pubitemid 34071670)
86. Alpers CE, Seifert RA, Hedkins KL, Johnson RJ, Bowen-Pope DR. Developmental patterns of PDGF B-chain, PDGF-receptor and β-actin expression in human glomerulogenesis. Kidney Int 1992; 42:390-399
87. Eichmann A, Makinen T, Alitalo K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev 2005; 19:1013-1021 (Pubitemid 40632446)
88. Klagsbrun M, Eichmann A. A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Fact Rev 2005; 16:535-548 (Pubitemid 41022016)
89. Robert B, Zhao X, Abrahamson DR. Coexpression of neuropilin-1, Flk1 and VEGF(164) in developing and mature mouse kidney glomeruli. Am J Physiol Renal Physiol 2000; 279:275-282
90. Villegas G, Tufro A. Ontogeny of semaphorins 3A and 3F and their receptors neuropilins 1 and 2 in the kidney. Mech Dev 2002; 119:149-153 (Pubitemid 36356030)
91. Harper SJ, Xing CY, Whittle C, et al. Expression of neuropilin-1 by human glomerular epithelial cells in vitro and in vivo. Clin Sci 2001; 101:439-446
92. Guan F, Villegas G, Teichman J, et al. Autocrine VEGF system in podocytes regulates podocin and its interaction with CD2AP. Am J Physiol Renal Physiol 2006; 291:422-428
93. Daniel TO, Stein E, Cerretti DP, St. John PL, Robert B, Abrahamson DR. ELK and LERK-2 in developing kidney and microvascular endothelial assembly. Kidney Int 1996; 50:73-81. (Pubitemid 26418475)
94. Aumailley M, Bruckner-Tuderman L, Carter WG, et al. A simplified laminin nomenclature. Matrix Biol 2005; 24:326-332
95. Miner JH, Yurchenco PD. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 2004; 20:255-284 (Pubitemid 39488639)
96. Colognato H, Yurchenco PD. Form and function: the laminin family of heterotrimers. Dev Dyn 2000; 218:213-234 (Pubitemid 30349637)
97. Miner JH. Renal basement membrane components. Kidney Int 1999; 56:2016-2024 (Pubitemid 30004730)
98. Miner JH. Developmental biology of glomerular basement membrane components. Curr Opin Nephrol Hypertens 1998; 7:13-19 (Pubitemid 28037515)
99. St. John PL, Abrahamson DR. Glomerular endothelial cells and podocytes jointly synthesize laminin-1 and -11 chains. Kidney Int 2001; 60:1037-1046 (Pubitemid 34205803)
100. Miner JH, Li C. Defective glomerulogenesis in the absence of laminin a5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev Biol 2000; 217:278-289 (Pubitemid 30060876)
101. Abrahamson DR, St. John PL, Isom K, Robert B, Miner JH. Partial rescue of glomerular laminin α5 mutation by wildtype endothelial cells produce hybrid glomeruli. J Am Soc Nephrol 2007; 18:2285-2297 (Pubitemid 47203844)
102. Miner JH, Go G, Cunningham J, Patton BL, Jarad G. Transgenic isolation of skeletal muscle and kidney defects in laminin beta2 mutant mice: implications for Pierson syndrome. Development 2006; 133:967-975
103. Hudson BG. The molecular basis of Goodpasture and Alport syndromes: beacons for the discovery of the collagen IV family. J Am Soc Nephrol 2004; 15:2514-2527 (Pubitemid 41103358)
104. Hudson BG, Tryggvason K, Sundaramoorthy M, Neilson EG. Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N Engl J Med 2003; 348:2543-2556 (Pubitemid 36706542)
105. Desjardins M, Bendayan M. Ontogenesis of glomerular basement membrane: Structural and functional properties. J Cell Biol 1991; 113:689-700.
106. Ninomiya Y, Kagawa M, Iyama K, et al. Differential expression of two basement membrane collagen genes, COL4A6 and COL4A5, demonstrated by immunofluorescence staining using peptide-specific monoclonal antibodies. J Cell Biol 1995; 130:1219-1229
107. Butkowski RJ, Langeveld JPM, Wieslander J, Hamilton J, Hudson BG. Localization of the Goodpasture epitope to a novel chain of basement membrane collagen. J Biol Chem 1987; 262:7874-7877
108. Tryggvason K, Zhou J, Hostikka SL, Shows TB. Molecular genetics of Alport syndrome. Kidney Int 1993; 43:38-44. (Pubitemid 23167443)
109. Kashtan CE. Alport syndrome and thin glomerular basement membrane disease. J Am Soc Nephrol 1998; 9:1736-1750 (Pubitemid 28405082)
110. Kashtan CE. Alport syndrome. An inherited disorder of renal, ocular and cochlear basement membranes. Medicine 1999; 78:338-360
111. Kalluri R, Shield CF, Todd P, Hudson BG, Neilson EG. 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 1997; 99:2470-2478 (Pubitemid 27227726)
112. Gunwar S, Ballester F, Noelken ME, Sado Y, Ninomiya Y, Hudson BG. Glomerular basement membrane. Identification of a novel disulfide-cross-linked network of alpha3, alpha4 and alpha5 chains of type IV collagen and its implications for the pathogenesis of Alport syndrome. J Biol Chem 1998; 273:8767-8775
113. 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; 10:2981-2992
114. Miner JH, Sanes JR. Molecular and functional defects in kidneys of mice lacking collagen alpha3(IV): Implications for Alport syndrome. J Cell Biol 1996; 135:1403-1413
115. Lu W, Phillips CL, Killen PD, Hlaing T, Harrison WR, Elder FF, et al. Insertional mutation of the collagen genes Col4a3 and Col4a4 in a mouse model of Alport syndrome. Genomics 1999; 61:113-124
116. Abrahamson DR, Prettyman AC, Robert B, St. John PL. Laminin-1 reexpression in Alport mouse glomerular basement membranes. Kidney Int 2003; 63:826-834 (Pubitemid 36315560)
117. Cosgrove D, Rodgers K, Meehan D, Miller C, Bovard K, Gilroy A, et al. Integrin alpha-1beta1 and transforming growth factor-beta1 play distinct roles in Alport glomerular pathogenesis and serve as dual targets for metabolic therapy. Am J Pathol 2000; 157:1649-1659
118. Abrahamson DR, Hudson BG, Stroganova L, St. Borza DB, John PL. Cellular origins of glomerular basement membrane type IV collagen networks. J Am Soc Nephrol 2009; in press.
119. Morello R, Zhou G, Dreyer SD, Harvey SJ, Ninomiya Y, Thorner PS, et al. Regulation of glomerular basement membrane collagen expression by LMX1B contributes to renal disease in nail patella syndrome. Nat Genet 2001; 27:205-208