Skip to main content

The Steno Hypothesis and Glomerular Basement Membrane Biochemistry in Diabetic Nephropathy

  • Chapter
The Kidney and Hypertension in Diabetes Mellitus

Abstract

So far, at the biochemical level, the pathogenesis of diabetic nephropathy is unresolved. Not surprisingly perhaps since even our understanding of the biochemical fundaments of normal glomerular function remains incomplete. In addition, when exploring the pathogenesis of diabetic nephropathy, we are likely to witness the composite course of succeeding stages, each of which may have its own pathogenetic trait.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Deckert T, Feldt-Rasmussen B, Borch-Johnsen K, Jensen T, Kofoed-Enevoldsen A. Albuminuria reflects widespread vascular damage. Diabetologia 1989; 32:219–26.

    Article  PubMed  CAS  Google Scholar 

  2. Mathiesen ER. Prevention of diabetic nephropathy: Microalbuminuria and perspectives for intervention in insulin-dependent diabetes. Dan Med Bull 1993; 40:273–285.

    PubMed  CAS  Google Scholar 

  3. Kanwar YS. Biophysiology of glomerular filtration and proteinuria. Lab Invest 1984; 51: 7–21.

    PubMed  CAS  Google Scholar 

  4. Deen WM, Satvat B. Determinants of the glomerular filtration of proteins. Am J Physiol 1981; 241: F162–F170.

    Google Scholar 

  5. Viberti GC, Mackintosh D, Keen H. Determinants of the penetration of proteins through the glomerular barrier in IDDM Diabetes 1983; 32: Suppl. 2: 92–95.

    PubMed  Google Scholar 

  6. Deckert T, Kofoed-Enevoldsen A, Vidal P, Nørgaard K, Andreasen HB, Feldt-Rasmussen B. Size- and charge selectivity of glomerular filtration in IDDM patients with and without albuminuria. Diabetologia 1993; 36: 244–251.

    Article  PubMed  CAS  Google Scholar 

  7. Bangstad H-J, Kofoed-Enevoldsen A, Dahl-Jørgensen K, Hanssen KF. Glomerular charge selectivity and the influence of improved blood glucose control. Diabetologia 1992; 35: 1165–1169.

    Article  PubMed  CAS  Google Scholar 

  8. Myers BD, Winetz JA, Chui F, Michaels AS. Mechanisms of proteinuria in diabetic nephropathy — A study of glomerular barrier function. Kidney Int 1982; 21: 633–641.

    Article  PubMed  CAS  Google Scholar 

  9. Deen WM, Bridges CR, Brenner BM, Myers BD. Heterosporous model of glomerular size selectivity, application to normal and nephrotic humans. Am J Physiol 1985; 249: F374-F389.

    Google Scholar 

  10. Kofoed-Enevoldsen A. Heparan sulphate in the metabolism of diabetic nephropathy. Diabetes/Metabolism Reviews 1995; 11: 137–160.

    Article  PubMed  CAS  Google Scholar 

  11. Vernier RL, Steffes MW, Sisson-Ross S, Mauer SM. Heparan sulfate proteoglycan in the glomerular basement membrane in type 1 diabetes mellitus. Kidney Int 1992; 41:1070–1080.

    Article  PubMed  CAS  Google Scholar 

  12. Rosenzweig LJ, Kanwar Y. Removal of sulfated (heparan sulfate) or nonsulfated (hyaluronic acid) glycosaminoglycans results in increased permeability of the glomerular basement membrane to 125I-bovine serum albumin. Lab Invest 1982; 47: 177–184.

    PubMed  CAS  Google Scholar 

  13. Van Den Bom J, Van Den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assmann KJM, Berden JHM. A monoclonal antibody against GBM heparan sulfate induces an acute selective proteinuria in rats. Kidney Int 1992; 41: 115–123.

    Article  Google Scholar 

  14. Tamsma JT, van den Born J, Bruijn JA, Assmann KJM, Weening JJ, Berden JHM, Wieslander J, Schrama E, Hermans J, Veerkamp JH, Lemkes HHPJ, van der Woude FJ. Expression of glomerular extracellular matrix components in human diabetic nephropathy — decrease of heparan sulphate in the glomerular basement membrane. Diabetologia 1994; 37: 313–320.

    Article  PubMed  CAS  Google Scholar 

  15. Riser BL, Cortes P, Zhao X, Bernstein J, Dumler F, Narins RG, Hassett CC, Sury-Sastry KS, Atherton J, Holcomb MA. Intraglomerular pressure and mesangial stretching stimulate extracellular matrix formation in the rat. J Clin Invest 1992; 90: 1932–1943.

    Article  PubMed  CAS  Google Scholar 

  16. Shimomura H, Spiro RG. Studies on macromolecular components of human glomerular basement membrane and alterations in diabetes. Diabetes 1987; 36: 374–381.

    Article  PubMed  CAS  Google Scholar 

  17. Parthasarathy N, Spiro RG. Effect of diabetes on the glycosaminoglycan component of the human glomerular basement membrane. Diabetes 1982; 31: 738–741.

    Article  PubMed  CAS  Google Scholar 

  18. Nerlich A, Schleicher E. Immunohistochemical localization of extracellular matrix components in human diabetic glomerular lesions. Am J Pathol 1991; 139: 889–899.

    PubMed  CAS  Google Scholar 

  19. Van Den Born J, Van Den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assmann KJM, Weening JJ, Berden JHM. The distribution of GBM heparan sulfate proteoglycan core protein and side chains in human glomerular diseases by monoclonal antibodies. Kidney Int 1993; 43: 454–463.

    Article  PubMed  CAS  Google Scholar 

  20. Reddi AS, Ramamurthi R, Miller M, Dhuper S, Lasker N. Enalapril improves albuminuria by preventing glomerular loss of heparan sulfate in diabetic rats. Biochem Med Metab Biol 1991; 45:119–131.

    Article  PubMed  CAS  Google Scholar 

  21. Klein DJ, Brown DM, Oegema TR. Glomerular proteoglycans in diabetes. Diabetes 1986; 35: 1130–1142.

    Article  PubMed  CAS  Google Scholar 

  22. Kanwar YS, Rosenzweig LJ, Linker A, Jakubowski ML. Decreased de novo synthesis of glomerular proteoglycans in diabetes. ProcNatl Acad Sci USA 1983; 80: 2272–2275.

    Article  CAS  Google Scholar 

  23. Cohen MP, Surma ML. Effect of diabetes on in vivo metabolism of 35S-labelled glomerular basement membrane. Diabetes 1984; 33: 8–12.

    Article  PubMed  CAS  Google Scholar 

  24. Klein DJ, Oegema TR, Brown DM. Release of glomerular heparan-35SO4 proteoglycan by heparin from glomeruli of streptozotocin-induced diabetic rats. Diabetes 1989; 38: 130–139.

    Article  PubMed  CAS  Google Scholar 

  25. Wu V-Y, Wilson B, Cohen MP. Disturbances in glomerular basement membrane glycosaminoglycans in experimental diabetes. Diabetes 1987; 36: 679–683.

    Article  PubMed  CAS  Google Scholar 

  26. Templeton DM. Retention of glomerular basement membrane proteoglycans accompanying loss of anionic site staining in experimental diabetes. Lab Invest 1989; 61: 202–211.

    PubMed  CAS  Google Scholar 

  27. Cohen MP, Klepser H, Wu V-Y. Undersulfation of glomerular basement membrane heparan sulfate in experimental diabetes and lack of correction with aldose reductase inhibition. Diabetes 1988; 37: 1324–1327.

    Article  PubMed  CAS  Google Scholar 

  28. Fukui M, Nakamura T, Ebihara I, Shirato I, Tomino Y, Koide H. ECM gene expression and its modulation by insulin in diabetic rats. Diabetes 1992; 41: 1520–1527.

    Article  PubMed  CAS  Google Scholar 

  29. Kofoed-Enevoldsen A, Noonan D, Deckert T. Diabetes mellitus induced inhibition of glucosaminyl N-deacetylase — effect of short-term blood glucose control. Diabetologia 1993; 36: 310–315.

    Article  PubMed  CAS  Google Scholar 

  30. Kashihara N, Watanabe Y, Makino H, Wallner EI, Kanwar Y. Selective decreased de novo synthesis of glomerular proteoglycans under the influence of reactive oxygen species. Proc Natl Acad Sci USA 1992; 89: 6309–6313.

    Article  PubMed  CAS  Google Scholar 

  31. Olgemöller B, Schwaabe S, Gerbitz KD, Schleicher ED. Elevated glucose decreases the content of a basement membrane associated heparan sulphate proteoglycan in proliferating cultured porcine mesangial cells. Diabetologia 1992; 35: 183–186.

    Article  PubMed  Google Scholar 

  32. Doi T, Vlassara H, Kirstein M, Yamada Y, Striker GE, Striker LJ. Receptor-specific increase in extracellular matrix production in mouse mesangial cells by advanced glysosylation end products is mediated via platelet-derived growth factor. Proc Natl Acad Sci USA 1992; 89: 2873–2877.

    Article  PubMed  CAS  Google Scholar 

  33. Cagliero E, Roth T, Roy S, Lorenzi M. Characteristics and mechanisms of high-glucose-induced overexpression of basement membrane components in cultures human endothelial cells. Diabetes 1991;40:102–110.

    Article  PubMed  CAS  Google Scholar 

  34. Ziyadeh FN, Snipes ER, Watanabe M, Alvarez RJ, Goldfarb S, Haverty TP. High glucose induces cell hypertrophy and stimulates collagen gene transcription in proximal tubule. Am J Physiol 1990; 259: F704–F714.

    Google Scholar 

  35. Shankland SJ, Scholey JW. Expression of transforming growth factor-ßl during diabetic renal hypertrophy. Kidney Int 1994; 46: 430–442.

    Article  PubMed  CAS  Google Scholar 

  36. Border WA, Noble NA, Yamamoto T, Harper JR, Yamaguchi Y, Pierschbacher MD, Ruoslahti. Natural inhibitor of transforming growth factor-ß protects against scarring in experimental kidney disease. Nature 1992; 360:361–364.

    Article  PubMed  CAS  Google Scholar 

  37. Mulder M, Lombardi P, Jansen H, van Berkel TJC, Frants RR, Havekes LM Heparan sulphate proteoglycans are involved in the lipoprotein lipase-mediated enhancement of the cellular binding of very low density and low density lipoproteins. Biochem Biophys Res Commun 1992; 185: 582–587.

    Article  PubMed  CAS  Google Scholar 

  38. Sudhalter J, Folkman J, Svahn CM, Bergendal K, D’Amore PA Importance of size, sulfatation and anticoagulant activity in the potentiation of acidic fibroblast growth factor by heparin. J Biol Chem 1989; 264: 6892–6897.

    PubMed  Google Scholar 

  39. Turnbull JE, Fernig DG, Ke Y, Wilkinson MC, Gallagher JT. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J Biol Chem 1992; 267: 10337–10341.

    PubMed  CAS  Google Scholar 

  40. Deckert T, Jensen T, Feldt-Rasmussen B, Kofoed-Enevoldsen A, Borch-Johnsen K, Stender S. Albuminuria a risk marker of atherosclerosis in insulin dependent diabetes mellitus. Cardiovasc Risk Factors 1991; 1: 347–360.

    Google Scholar 

  41. Deckert T, Kofoed-Enevoldsen A, Nørgaard K, Borch-Johnsen K, Feldt-Rasmussen B, Jensen T. Microalbuminuria — implications for micro and macrovascular disease. Diabetes Care 1992; 15: 1181–1191.

    Article  PubMed  CAS  Google Scholar 

  42. Gruden G, Cavallo-Perin P, Bazzan M, Stella S, Bruno A, Pagano G. Haemostatic alterations in microalbuminuric insulin-dependent diabetic patients (Abstract). Diabetologia 1993; 36: Suppl. 1:A215.

    Google Scholar 

  43. Myrup B, Rossing P, Jensen T, Gram J, Kluft C, Jespersen J. Prothrombin fragment 1+2, a marker of thrombin formation, is related to transcapillary escape rate of albumin in insulin-dependent diabetic patients (Abstract). Diabetologia 1993; 36: Suppl. 1: A71.

    Google Scholar 

  44. Kofoed-Enevoldsen A, Bent-Hansen L, Deckert T. Transcapillary filtration of plasma protein in long-term type 1 (insulin-dependent) diabetic patients. Scand J Clin Lab Invest 1992; 52: 591–597.

    Article  PubMed  CAS  Google Scholar 

  45. Bent-Hansen L, Feldt-Rasmussen B, Kvemeland A, Deckert T. Plasma disappearance of glycated and non-glycated albumin in type 1 (insulin-dependent) diabetes mellitus — evidence for charge dependent alterations of the plasma to lymph pathway. Diabetologia 1993; 36: 361–363.

    Article  PubMed  CAS  Google Scholar 

  46. Kjellén L, Bielefeld D, Höök M. Reduced sulfatation of liver heparan sulfate in experimentally diabetic rats. Diabetes 1983; 32: 337–342.

    Article  PubMed  Google Scholar 

  47. Unger E, Pettersson I, Eriksson UJ, Lindahl U, Kjellén L. Decreased activity of the heparan sulfate modifying enzyme glucosaminyl N-deacatylase in hepatocytes from streptozotocin-diabetic rats. J Biol Chem 1991; 266: 8671–8674.

    PubMed  CAS  Google Scholar 

  48. Kofoed-Enevoldsen A, Eriksson UJ. Inhibition of N-acetylheparosan deacetylase in diabetic rats. Diabetes 1991; 40: 1449–1452.

    Article  PubMed  CAS  Google Scholar 

  49. Kofoed-Enevoldsen A. Inhibition of glomerular glucosaminyl N-deacetylase in diabetic rats. Kidney Int 1992; 41: 763–767.

    Article  PubMed  CAS  Google Scholar 

  50. Kofoed-Enevoldsen A, Kotinis A, Deckert T. Poor metabolic control decreases n-deacetylase activity type-1 diabetic-patients (Abstract). Diabetologia 1994; 37: Suppl. 1: A3.

    Article  Google Scholar 

  51. Kofoed-Enevoldsen A, Petersen JS, Deckert T. Glucosaminyl N-deacetylase in cultured fibroblasts — comparison of patients with and without diabetic nephropathy, and identification of a possible mechanism for diabetes-induced N-deacetylase inhibition. Diabetologia 1993; 36: 536–540.

    Article  PubMed  CAS  Google Scholar 

  52. Walkenbach RJ, Hazen R, Lamer J. Reversible inhibition of cyclic AMP-dependent protein kinase by insulin. Mol Cell Biochem 1978; 19: 31–41.

    Article  PubMed  CAS  Google Scholar 

  53. Kida Y, Nyomba BL, Bogardus C, Mott DM. Defective insulin response of cyclic adenosine monophosphate-dependent protein kinase in insulin resistant humans. J Clin Invest 1991; 87: 673–679.

    Article  PubMed  CAS  Google Scholar 

  54. Trevisan R, Nosadini R, Fioretto P, Semplicini A, Donadon V, Doria A et al. Clustering of risk factors in hypertensive insulin-dependent diabetics with high sodium-lithium countertransport. Kidney Int 1992; 41: 855–861.

    Article  PubMed  CAS  Google Scholar 

  55. Myrup B, Hansen PM, Jensen T, Kofoed-Enevoldsen A, Feldt-Rasmussen B, Gram J, Kluft C, Jespersen J, Deckert T. Effect of low-dose heparin on urinary albumin excretion in insulin-dependent diabetes mellitus. Lancet 1995; 345: 421–422.

    Article  PubMed  CAS  Google Scholar 

  56. Tamsma JT, van der Woude FJ, Lemkes HH. Effect of sulphated glycosaminoglycans on albuminuria in patients with overt diabetic (type 1) nephropathy Nephrol Dial Transplant 1996; 11(1): 182–185.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Kofoed-Enevoldsen, A. (1998). The Steno Hypothesis and Glomerular Basement Membrane Biochemistry in Diabetic Nephropathy. In: Mogensen, C.E. (eds) The Kidney and Hypertension in Diabetes Mellitus. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-6752-0_30

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-6752-0_30

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-6754-4

  • Online ISBN: 978-1-4757-6752-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics