A model of strain-dependent glomerular basement membrane maintenance and its potential ramifications in health and disease

Journal of Biomechanical Engineering

Volumn 134, Issue 8, 2012, Pages

  Barocas, Victor H ^a   Dorfman, Kevin D ^a   Segal, Yoav ^b,c  

^a University of Minnesota   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPORT SYNDROME; BASEMENT MEMBRANE; CAPILLARY RADIUS; FINITE STRAIN; GLOMERULAR BASEMENT MEMBRANE; GLOMERULAR CAPILLARIES; GLOMERULAR FILTRATION; LINEAR RELATION; MECHANICAL ENVIRONMENT; MODEL ASSUMPTIONS; MODEL PARAMETERS; MODEL RESULTS; ONCOTIC PRESSURE; OSMOTIC PRESSURE DIFFERENCES; PER UNIT; REASONABLE VALUE; STRAIN DEPENDENCE; STRAIN-DEPENDENT; STRUCTURAL ELEMENTS;

MECHANICAL PROPERTIES; TISSUE;

PRESSURE DROP;

COLLAGEN TYPE 4;

ALLOMETRY; ALPORT SYNDROME; ARTICLE; EQUILIBRIUM CONSTANT; GLOMERULONEPHRITIS; GLOMERULUS BASEMENT MEMBRANE; GLOMERULUS CAPILLARY; GLOMERULUS FILTRATION; GLYCATION; HEALTH STATUS; HUMAN; NONHUMAN; ONCOTIC PRESSURE; OSMOTIC PRESSURE; PREDICTIVE VALUE; BIOLOGICAL MODEL; GLYCOSYLATION; HEALTH; KIDNEY DISEASE; MECHANICAL STRESS; METABOLISM; NEPHRITIS;

COLLAGEN TYPE IV; GLOMERULAR BASEMENT MEMBRANE; GLYCOSYLATION; HEALTH; HUMANS; KIDNEY DISEASES; MODELS, BIOLOGICAL; NEPHRITIS, HEREDITARY; STRESS, MECHANICAL;

EID: 84864863767     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4007098     Document Type: Article

References (78)

1. Drumond, M. C., and Deen, W. M., 1994, "Structural Determinants of Glomerular Hydraulic Permeability," Am. J. Physiol., 266(1), pp. F1-F12.
2. Deen, W. M., Lazzara, M. J., and Myers, B. D., 2001, "Structural Determinants of Glomerular Permeability," Renal Physiol., 281(4), pp. F579-F596.
3. Haraldsson, B., Nystrom, J., and Deen, W. M., 2008, "Properties of the Glomerular Barrier and Mechanisms of Proteinuria," Physiol. Rev., 88(2), pp. 451-487. (Pubitemid 351522745)
4. Mohamed, E. I., and de Lorenzo, A., 2002, "Modeling Combined Transport of Water and Test Macromolecules Across the Glomerular Capillary Barrier: Dynamics of the Permselectivity," Eur. Biophys. J., 31(3), pp. 163-171.
5. Kriz, W., Kretzler, M., and Provoost, A. P., 1996, "Stability and Leakiness: Opposing Challenges to the Glomerulus," Kidney Int., 49(6), pp. 1570-1574. (Pubitemid 26186582)
6. Singh, P., and Thomson, S. C., 2010, "Renal Homeostasis and Tubuloglomerular Feedback," Curr. Opin. Nephrol. Hyperten., 19(1), pp. 59-64.
7. Walker, F., 1973, "The Origin, Turnover and Removal of Glomerular Basement-Membrane," J. Pathol., 110(3), pp. 233-244.
8. Endlich, N., Kress, K. R., and Reiser, J., 2001, "Podocytes Respond to Mechanical Stress In Vitro," J. Am. Soc. Nephrol., 12(3), pp. 413-422. (Pubitemid 32180009)
9. Endlich, N., and Endlich, K., 2006, "Stretch, Tension and Adhesion-Adaptive Mechanisms of the Actin Cytoskeleton in Podocytes," Eur. J. Cell Biol., 85(3), pp. 229-234.
10. Petermann, A. T., Pippin, J., and Durvasula, R., 2005, "Mechanical Stretch Induces Podocyte Hypertrophy In Vitro," Kidney Int., 67(1), pp. 157-166. (Pubitemid 40019237)
11. Flynn, B. P., Bhole, A. P., and Saeidi, N., 2010, "Mechanical Strain Stabilizes Reconstituted Collagen Fibrils Against Enzymatic Degradation by Mammalian Collagenase Matrix Metalloproteinase 8 (MMP-8)," PLos ONE, 5(8), p. e12337.
12. Zareian, R., Church, K. P., and Saeidi, N., 2010, "Probing Collagen/Enzyme Mechanochemistry in Native Tissue With Dynamic, Enzyme-Induced Creep," Langmuir, 26(12), pp. 9917-9926.
13. Bhole, A. P., Flynn, B. P., and Liles, M., 2009, "Mechanical Strain Enhances Survivability of Collagen Micronetworks in the Presence of Collagenase: Implications for Load-Bearing Matrix Growth and Stability," Philos. Trans. R. Soc. London, Ser. A, 367(1902), pp. 3339-3362.
14. Kriz, W., and Endlich, K., 2005, "Hypertrophy of Podocytes: A Mechanism to Cope With Increased Glomerular Capillary Pressures?," Kidney Int., 67(1), pp. 373-374. (Pubitemid 40019262)
15. Taber, L. A., 1998, "A Model for Aortic Growth Based on Fluid Shear and Fiber Stresses," ASME J. Biomech. Eng., 120(3), pp. 348-354. (Pubitemid 28309007)
16. Renkin, E. M., and Gilmore, J. P., 1973, Handbook of Physiology: Renal Physiology, Williams and Wilkins, Washington, D.C., pp. 185-248.
17. Singer, M. A., and Morton, A. R., 2000, "Mouse to Elephant: Biological Scaling and Kt/V," Am. J. Kidney Dis., 35(2), pp. 306-309. (Pubitemid 30070854)
18. Maluf, N. S., and Gassman, J. J., 1998, "Kidneys of the Killerwhale and Significance of Reniculism," Anat. Rec., 250(1), pp. 34-44. (Pubitemid 28028600)
19. Bohle, A., Aeikens, B., and Eenboom, A., 1998, "Human Glomerular Structure Under Normal Conditions and in Isolated Glomerular Disease," Kidney Int., Suppl., 67, pp. S186-S188. (Pubitemid 28405712)
20. Marquez, B., Zouvani, I., and Karagrigoriou, A., 2003, "A Simplified Method for Measuring the Thickness of Glomerular Basement Membranes," Ultrastruct. Pathol., 27(6), pp. 409-416. (Pubitemid 38041327)
21. Osawa, G., Kimmelstiel, P., and Seiling, V., 1966, "Thickness of Glomerular Basement Membranes," Am. J. Clin. Pathol., 45(1), pp. 7.
22. Akaoka, K., White, R. H., and Raafat, F., 1995, "Glomerular Morphometry in Childhood Reflux Nephropathy, Emphasizing the Capillary Changes," Kidney Int., 47(4), pp. 1108-1114.
23. Yun, J. C. H. and Kenney, R. A., 1978, "Structural Changes After Infusion of Mannitol in the Cat Kidney," Kidney Blood Pressure Res., 1(5), pp. 283-295. (Pubitemid 10247522)
24. Marion, M. S., and Carlson, E. C., 1989, "Ultrastructural Analyses of Acellular Glomerular Basement Membranes and Mesangial Matrix in a Spontaneously Diabetic Rhesus Monkey," Acta Anat., 135(2), pp. 119-128. (Pubitemid 19146491)
25. Nyengaard, J. R., 1993, "Number and Dimensions of Rat Glomerular Capillaries in Normal Development and After Nephrectomy," Kidney Int., 43(5), pp. 1049-1057. (Pubitemid 23137089)
26. Shirato, I., Tomino, Y., and Koide, H., 1991, "Fine Structure of the Glomerular Basement Membrane of the Rat Kidney Visualized by High-Resolution Scanning Electron Microscopy," Cell Tissue Res., 266(1), pp. 1-10.
27. Shea, S. M., 1979, "Glomerular Hemodynamics and Vascular Structure. The Pattern and Dimensions of a Single Rat Glomerular Capillary Network Reconstructed From Ultrathin Sections," Microvasc. Res., 18(2), pp. 129-143. (Pubitemid 10234931)
28. Guo, M., Ricardo, S. D., and Deane, J. A., 2005, "A Stereological Study of the Renal Glomerular Vasculature in the db/db Mouse Model of Diabetic Nephropathy," J. Anat., 207(6), pp. 813-821. (Pubitemid 43019739)
29. Endo, H., Akihisa, N., and Sasaki, M., 2002, "The Renal Structure in an Asian Elephant (Elephas Maximus)," Anat. Histol. Embryol., 31(5), pp. 269-272.
30. Hudson, B. G., Tryggvason, K., and Sundaramoorthy, M., 2003, "Alport's Syndrome, Goodpasture's Syndrome, and Type IV Collagen," New Engl. J. Med., 348(25), pp. 2543-2556. (Pubitemid 36706542)
31. Foster, K., Markowitz, G. S., and D'Agati, V. D., 2005, "Pathology of Thin Basement Membrane Nephropathy," Semin. Nephrol., 25(3), pp. 149-158. (Pubitemid 40692797)
32. Rana, K., Wang, Y. Y., and Buzza, M., 2005, "The Genetics of Thin Basement Membrane Nephropathy," Semin. Nephrol., 25(3), pp. 163-170. (Pubitemid 40692799)
33. Wang, Y. Y., and Savige, J., 2005, "The Epidemiology of Thin Basement Membrane Nephropathy," Semin. Nephrol., 25(3), pp. 136-139. (Pubitemid 40692794)
34. Lees, G. E., Helman, R. G., and Kashtan, C. E., 1998, "A Model of Autosomal Recessive Alport Syndrome in English Cocker Spaniel Dogs," Kidney Int., 54(3), pp. 706-719. (Pubitemid 28397389)
35. Beirowski, B., Weber, M., and Gross, O., 2006, "Chronic Renal Failure and Shortened Lifespan in COL4A3+/ Mice: An Animal Model for Thin Basement Membrane Nephropathy," J. Am. Soc. Nephrol., 17(7), pp. 1986-1994. (Pubitemid 44036183)
36. Kashtan, C. E., 2000, "Alport Syndrome: Abnormalities of Type IV Collagen Genes and Proteins," Ren. Fail., 22(6), pp. 737-749.
37. Kashtan, C. E., and Segal, Y., 2011, "Genetic Disorders of Glomerular Basement Membranes," Nephron. Clin. Practi., 118(1), pp. c9-c18.
38. Kashtan, C. E., 1998, "Alport Syndrome and Thin Glomerular Basement Membrane Disease," J. Am. Soc. Nephrol., 9(9), pp. 1736-1750. (Pubitemid 28405082)
39. Gunwar, S., Ballester, F., and Noelken, M. E., 1998, "Identification of a Novel Disulfide-Cross-Linked Network of a3, a4, and a5 Chains of Type IV Collagen and Its Implications for the Pathogenesis of Alport Syndrome," J. Biol. Chem., 273(15), pp. 8767-8775. (Pubitemid 28176155)
40. Gunwar, S., Ballester, F., and Noelken, M. E., 1998, "Glomerular Basement Membrane-Identification of a Novel Disulfide-Cross-Linked Network of Alpha 3, Alpha 4, and Alpha 5 Chains of Type IV Collagen and Its Implications for the Pathogenesis of Alport Syndrome," J. Biol. Chem., 273(15), pp. 8767-8775. (Pubitemid 28176155)
41. Wyss, H. M., Henderson, J. M., and Byfield, F. J., 2011, "Biophysical Properties of Normal and Diseased Renal Glomeruli," Am. J. Physiol: Cell Physiol., 300(3), pp. C397-C405.
42. Meehan, D. T., Delimont, D., and Cheung, L., 2009, "Biomechanical Strain Causes Maladaptive Gene Regulation, Contributing to Alport Glomerular Disease," Kidney Int., 76(9), pp. 968-76.
43. Rayat, C. S., Joshi, K., and Dey, P., 2007, "Glomerular Morphometry in Biopsy Evaluation of Minimal Change Disease, Membranous Glomerulonephritis, Thin Basement Membrane Disease and Alport's Syndrome," Anal. Quan. Cytol. Histo., 29(3), pp. 173-182. (Pubitemid 46984592)
44. Kalluri, R., Shield, C. F., and Todd, P., 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(10), pp. 2470-2478. (Pubitemid 27227726)
45. Lewko, B. and Stepinski, J., 2009, "Hyperglycemia and Mechanical Stress: Targeting the Renal Podocyte," J. Cell. Physiol., 221(2), pp. 288-295.
46. Brownlee, M., 2001, "Biochemistry and Molecular Cell Biology of Diabetic Complications," Nature (London), 414(6865), pp. 813-820. (Pubitemid 34000785)
47. Bohlender, J. M., Franke, S., and Stein, G., 2005, "Advanced Glycation End Products and the Kidney," Ren. Physiol., 289(4), pp. F645-F59.
48. Bailey, A. J., Sims, T. J., and Avery, N. C., 1993, "Chemistry of Collagen Cross-Links: Glucose-Mediated Covalent Cross-Linking of Type-IV Collagen in Lens Capsules," Biochem. J., 296(2), pp. 489-496. (Pubitemid 23350854)
49. Mott, J. D., Khalifah, R. G., and Nagase, H., 1997, "Nonenzymatic Glycation of Type IV Collagen and Matrix Metalloproteinase Susceptibility," Kidney Int., 52(5), pp. 1302-1312. (Pubitemid 27496059)
50. Cochrane, S. M. and Robinson, G. B., 1995, "In Vitro Glycation of Glomerular Basement Membrane Alters its Permeability: A Possible Mechanism in Diabetic Complications," FEBS Lett., 375(1-2), pp. 41-44.
51. Boyd-White, J., and Williams, J. C., Jr., 1996, "Effect of Cross-Linking on Matrix Permeability. A Model for AGE-Modified Basement Membranes," Diabetes, 45(3), pp. 348-353. (Pubitemid 26069050)
52. Brownlee, M., and Spiro, R. G., 1979, "Glomerular Basement Membrane Metabolism in the Diabetic Rat. In Vivo Studies," Diabetes, 28(2), pp. 121-125. (Pubitemid 9133934)
53. Hasslacher, C., Reichenbacher, R., and Gechter, F., 1984, "Glomerular Basement Membrane Synthesis and Serum Concentration of Type IV Collagen in Streptozotocin-Diabetic Rats," Diabetologia, 26(2), pp. 150-154. (Pubitemid 14190674)
54. Cohen, M. P., Surma, M. L., and Wu, V. Y., 1982, "In Vivo Biosynthesis and Turnover of Glomerular Basement Membrane in Diabetic Rats," Am. J. Physiol., 242(4), pp. F385-F389. (Pubitemid 12099113)
55. Iglesias-de la Cruz, M. C., Ziyadeh, F. N., and Isono, M., 2002, "Effects of High Glucose and TGF-Beta1 on the Expression of Collagen IV and Vascular Endothelial Growth Factor in Mouse Podocytes," Kidney Int., 62(3), pp. 901-913. (Pubitemid 35316719)
56. Zatz, R., and Brenner, B. M., 1986, "Pathogenesis of Diabetic Microangiopathy. The Hemodynamic View," Am. J. Med., 80(3), pp. 443-453. (Pubitemid 16098781)
57. Carmines, P. K., 2010, "The Renal Vascular Response to Diabetes," Curr. Opin. Nephrol. Hypertens., 19(1), pp. 85-90.
58. Osterby, R., Bangstad, H. J., and Nyberg, G., 2001, "On Glomerular Structural Alterations in Type-1 Diabetes. Companions of Early Diabetic Glomerulopathy," Virchows Arch., 438(2), pp. 129-135. (Pubitemid 32186580)
59. O'Rourke, M. F., 2007, "Arterial Aging: Pathophysiological Principles," Vasc. Med., 12(4), pp. 329-341.
60. Cooper, M. E., Allen, T. J., and O'Brien, R. C., 1988, "Effects of Genetic Hypertension on Diabetic Nephropathy in the Rat-Functional and Structural Characteristics," J. Hypertens., 6(12), pp. 1009-1016. (Pubitemid 19041649)
61. Nielsen, B., Gronbaek, H., and Osterby, R., 1999, "Effect of the Calcium Channel Blocker Nitrendipine in Normotensive and Spontaneously Hypertensive, Diabetic Rats on Kidney Morphology and Urinary Albumin Excretion," J. Hypertens., 17(7), pp. 973-981. (Pubitemid 29322186)
62. Valentin, A. and Humphrey, J. D., 2009, "Modeling Effects of Axial Extension on Arterial Growth and Remodeling," Med. Biol. Eng. Comput., 47(9), pp. 979-987.
63. Gleason, R. L., Jr. and Humphrey, J. D., 2005, "A 2D Constrained Mixture Model for Arterial Adaptations to Large Changes in Flow, Pressure and Axial Stretch," IMA J. Math. Appl. Med. Biol., 22(4), pp. 347-369. (Pubitemid 43118445)
64. Rachev, A., Stergiopulos, N., and Meister, J. J., 1996, "Theoretical Study of Dynamics of Arterial Wall Remodeling in Response to Changes in Blood Pressure," J. Biomech., 29(5), pp. 635-642. (Pubitemid 26093289)
65. Lu, X., Pandit, A., and Kassab, G. S., 2004, "Biaxial Incremental Homeostatic Elastic Moduli of Coronary Artery: Two-Layer Model," Am. J. Physiol. Heart Circ. Physiol., 287(4), pp. H1663-H1669. (Pubitemid 39313272)
66. Jacobsen, J. C., Mulvany, M. J., and Holstein-Rathlou, N. H., 2008, "A Mechanism for Arteriolar Remodeling Based on Maintenance of Smooth Muscle Cell Activation," Am. J. Physiol. Regulatory Integrative Comp. Physiol., 294(4), pp. R1379-R1389. (Pubitemid 351490660)
67. Pries, A. R., Reglin, B., and Secomb, T. W., 2005, "Remodeling of Blood Vessels: Responses of Diameter and Wall Thickness to Hemodynamic and Metabolic Stimuli," Hypertension, 46(4), pp. 725-731. (Pubitemid 43186745)
68. Mundel, P., and Reiser, J., 2010, "Proteinuria: An Enzymatic Disease of the Podocyte?," Kidney Int., 77(7), pp. 571-580.
69. Alford, P. W., and Taber, L. A., 2008, "Computational Study of Growth and Remodelling in the Aortic Arch," Comput. Methods Biomech. Biomed. Eng., 11(5), pp. 525-538.
70. Abrahamson, D. R., Isom, K., and Roach, E., 2007, "Laminin Compensation in Collagen a3(IV) Knockout (Alport) Glomeruli Contributes to Permeability Defects," J. Am. Soc. Nephrol., 18(9), pp. 2465-2472. (Pubitemid 47378863)
71. Rumpelt, H. J., Steinke, A., and Thoenes, W., 1992, "Alport-Type Glomerulopathy: Evidence for Diminished Capillary Loop Size," Clin. Nephrol., 37(2), pp. 57-64.
72. Srinivasan, M., Uzel, S. G., and Gautieri, A., 2009, "Alport Syndrome Mutations in Type IV Tropocollagen Alter Molecular Structure and Nanomechanical Properties," J. Struct. Biol., 168(3), pp. 503-510.
73. Sander, E. A., Stylianopoulos, T., and Tranquillo, R. T., 2009, "Image-Based Multiscale Modeling Predicts Tissue-Level and Network-Level Fiber Reorganization in Stretched Cell-Compacted Collagen Gels," Proc. Natl. Acad. Sci. U.S.A., 106(42). pp. 17675-17680.
74. Hadi, M. F., Sander, E. A., and Ruberti, J. W., 2012, "Simulated Remodeling of Loaded Collagen Networks Via Strain-Dependent Enzymatic Degradation and Constant-Rate Fiber Growth," Mech. Mater., 44, pp. 72-82.
75. Welling, L.W. and Grantham, J. J., 1972, "Physical Properties of Isolated Perfused Renal Tubules and Tubular Basement Membranes," J. Clin. Invest., 51(5), pp. 1063-1075.
76. Jorgensen, F., and Bentzon, M. W., 1968, "The Ultrastructure of the Normal Human Glomerulus," Lab. Invest., 18(1), pp. 42.
77. Bolton, G. R., Deen, W. M., and Daniels, B. S., 1998, "Assessment of the Charge Selectivity of Glomerular Basement Membrane Using Ficoll Sulfate," Am. J. Physiol., 274(5), pp. F889-F896.
78. Durvasula, R. V., Petermann, A. T., and Hiromura, K., 2004, "Activation of a Local Tissue Angiotensin System in Podocytes by Mechanical Strain," Kidney Int., 65(1), pp. 30-39. (Pubitemid 38037489)