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PLOS ONE  2011 

An In Vitro Model of the Glomerular Capillary Wall Using Electrospun Collagen Nanofibres in a Bioartificial Composite Basement Membrane

DOI: 10.1371/journal.pone.0020802

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Abstract:

The filtering unit of the kidney, the glomerulus, contains capillaries whose walls function as a biological sieve, the glomerular filtration barrier. This comprises layers of two specialised cells, glomerular endothelial cells (GEnC) and podocytes, separated by a basement membrane. Glomerular filtration barrier function, and dysfunction in disease, remains incompletely understood, partly due to difficulties in studying the relevant cell types in vitro. We have addressed this by generation of unique conditionally immortalised human GEnC and podocytes. However, because the glomerular filtration barrier functions as a whole, it is necessary to develop three dimensional co-culture models to maximise the benefit of the availability of these cells. Here we have developed the first two tri-layer models of the glomerular capillary wall. The first is based on tissue culture inserts and provides evidence of cell-cell interaction via soluble mediators. In the second model the synthetic support of the tissue culture insert is replaced with a novel composite bioartificial membrane. This consists of a nanofibre membrane containing collagen I, electrospun directly onto a micro-photoelectroformed fine nickel supporting mesh. GEnC and podocytes grew in monolayers on either side of the insert support or the novel membrane to form a tri-layer model recapitulating the human glomerular capillary in vitro. These models will advance the study of both the physiology of normal glomerular filtration and of its disruption in glomerular disease.

References

[1]  Kefalides NA (1973) Structure and biosynthesis of basement membranes. Int Rev Connect Tissue Res 6: 63–104.
[2]  Durbeej M, Fecker L, Hjalt T, Zhang HY, Salmivirta K, et al. (1996) Expression of laminin alpha 1, alpha 5 and beta 2 chains during embryogenesis of the kidney and vasculature. Matrix Biol 15: 397–413.
[3]  Haraldsson B, Nystrom J, Deen WM (2008) Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88: 451–487.
[4]  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.
[5]  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.
[6]  Foster RR, Slater SC, Seckley J, Kerjaschki D, Bates DO, et al. (2008) Vascular endothelial growth factor-C, a potential paracrine regulator of glomerular permeability, increases glomerular endothelial cell monolayer integrity and intracellular calcium. Am J Pathol 173: 938–948.
[7]  Satchell SC, Anderson KL, Mathieson PW (2004) Angiopoietin 1 and vascular endothelial growth factor modulate human glomerular endothelial cell barrier properties. J Am Soc Nephrol 15: 566–574.
[8]  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.
[9]  Davis B, Dei Cas A, Long DA, White KE, Hayward A, et al. (2007) Podocyte-specific expression of angiopoietin-2 causes proteinuria and apoptosis of glomerular endothelia. J Am Soc Nephrol 18: 2320–2329.
[10]  Hall V (1957) The protoplasmic basis of glomerular filtration. Am Heart J 54: 1.
[11]  Saleem MA, O'Hare MJ, Reiser J, Coward RJ, Inward CD, et al. (2002) A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol 13: 630–638.
[12]  Satchell SC, Tasman CH, Singh A, Ni L, Geelen J, et al. (2006) Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF. Kidney Int 69: 1633–1640.
[13]  Ma SH, Lepak LA, Hussain RJ, Shain W, Shuler ML (2005) An endothelial and astrocyte co-culture model of the blood-brain barrier utilizing an ultra-thin, nanofabricated silicon nitride membrane. Lab Chip 5: 74–85.
[14]  Dai NT, Yeh MK, Liu DD, Adams EF, Chiang CH, et al. (2005) A co-cultured skin model based on cell support membranes. Biochem Biophys Res Commun 329: 905–908.
[15]  Hermanns MI, Unger RE, Kehe K, Peters K, Kirkpatrick CJ (2004) Lung epithelial cell lines in coculture with human pulmonary microvascular endothelial cells: development of an alveolo-capillary barrier in vitro. Lab Invest 84: 736–752.
[16]  Biegel D, Pachter JS (1994) Growth of brain microvessel endothelial cells on collagen gels: applications to the study of blood-brain barrier physiology and CNS inflammation. In Vitro Cell Dev Biol Anim 30A: 581–588.
[17]  Hirschberg R, Wang S, Mitu GM (2008) Functional symbiosis between endothelium and epithelial cells in glomeruli. Cell Tissue Res 331: 485–493.
[18]  Daley WP, Peters SB, Larsen M (2008) Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci 121: 255–264.
[19]  Abbott NJ, Hughes CC, Revest PA, Greenwood J (1992) Development and characterisation of a rat brain capillary endothelial culture: towards an in vitro blood-brain barrier. J Cell Sci 103(Pt 1): 23–37.
[20]  Wang S, Nagrath D, Chen PC, Berthiaume F, Yarmush ML (2008) Three-dimensional primary hepatocyte culture in synthetic self-assembling peptide hydrogel. Tissue Eng Part A 14: 227–236.
[21]  Bakunts K, Gillum N, Karabekian Z, Sarvazyan N (2008) Formation of cardiac fibers in Matrigel matrix. Biotechniques 44: 341–348.
[22]  Matthews JA, Wnek GE, Simpson DG, Bowlin GL (2002) Electrospinning of collagen nanofibers. Biomacromolecules 3: 232–238.
[23]  Barnes CP, Sell SA, Boland ED, Simpson DG, Bowlin GL (2007) Nanofiber technology: designing the next generation of tissue engineering scaffolds. Adv Drug Deliv Rev 59: 1413–1433.
[24]  Zhang Y, Venugopal JR, El-Turki A, Ramakrishna S, Su B, et al. (2008) Electrospun biomimetic nanocomposite nanofibers of hydroxyapatite/chitosan for bone tissue engineering. Biomaterials 29: 4314–4322.
[25]  He W, Yong T, Teo WE, Ma Z, Ramakrishna S (2005) Fabrication and endothelialization of collagen-blended biodegradable polymer nanofibers: potential vascular graft for blood vessel tissue engineering. Tissue Eng 11: 1574–1588.
[26]  Zhong S, Teo WE, Zhu X, Beuerman R, Ramakrishna S, et al. (2005) Formation of collagen-glycosaminoglycan blended nanofibrous scaffolds and their biological properties. Biomacromolecules 6: 2998–3004.
[27]  Rho KS, Jeong L, Lee G, Seo BM, Park YJ, et al. (2006) Electrospinning of collagen nanofibers: effects on the behavior of normal human keratinocytes and early-stage wound healing. Biomaterials 27: 1452–1461.
[28]  Williamson MR, Black R, Kielty C (2006) PCL-PU composite vascular scaffold production for vascular tissue engineering: attachment, proliferation and bioactivity of human vascular endothelial cells. Biomaterials 27: 3608–3616.
[29]  Saeki T, Morioka T, Arakawa M, Shimizu F, Oite T (1991) Modulation of mesangial cell proliferation by endothelial cells in coculture. Am J Pathol 139: 949–957.
[30]  Wang PC, Takezawa T (2005) Reconstruction of renal glomerular tissue using collagen vitrigel scaffold. J Biosci Bioeng 99: 529–540.
[31]  Kitahara T, Hiromura K, Ikeuchi H, Yamashita S, Kobayashi S, et al. (2005) Mesangial cells stimulate differentiation of endothelial cells to form capillary-like networks in a three-dimensional culture system. Nephrol Dial Transplant 20: 42–49.
[32]  Satchell SC, Buchatska O, Khan SB, Bhangal G, Tasman CH, et al. (2007) Interferon-beta Reduces Proteinuria in Experimental Glomerulonephritis. J Am Soc Nephrol 18: 2875–2884.
[33]  Cui TG, Foster RR, Saleem M, Mathieson PW, Gillatt DA, et al. (2004) Differentiated human podocytes endogenously express an inhibitory isoform of vascular endothelial growth factor (VEGF165b) mRNA and protein. Am J Physiol Renal Physiol 286: F767–773.
[34]  Bevan HS, van den Akker NM, Qiu Y, Polman JA, Foster RR, et al. (2008) The alternatively spliced anti-angiogenic family of VEGF isoforms VEGFxxxb in human kidney development. Nephron Physiol 110: p57–67.
[35]  Macarak EJ, Howard PS (1983) Adhesion of endothelial cells to extracellular matrix proteins. J Cell Physiol 116: 76–86.
[36]  Tillman BW, Yazdani SK, Lee SJ, Geary RL, Atala A, et al. (2009) The in vivo stability of electrospun polycaprolactone-collagen scaffolds in vascular reconstruction. Biomaterials 30: 583–588.
[37]  Lopez-Heredia MA, Sohier J, Gaillard C, Quillard S, Dorget M, et al. (2008) Rapid prototyped porous titanium coated with calcium phosphate as a scaffold for bone tissue engineering. Biomaterials 29: 2608–2615.

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