Skip to main content
SpringerLink
Log in

The structural relationship between mesangial cells and basement membrane of the renal glomerulus

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

It has been shown by many studies that mesangial cell contraction exerts considerable influences on glonerular filtration dynamics. However, experimental findings about the geometrical changes within the glomerular tuft going along with mesangial cell contractions are lacking. This study analyzes the geometry of mesangial cells and their relationship to glomerular capillaries, especially to the glomerular basement membrane (GBM).

By applying a new staining technique of unosmicated specimens for TEM, the cellular outlines of glomerular cells (mesangial, endothelial and epithelial) and the distribution of extracellular matrices can be more easily studied than in conventionally osmicated specimens. It became obvious that mesangial cells and the GBM are extensively connected with each other, either by direct attachments or indirectly by microfibrils. These connections are especially prominent mesangial angles, i.e. at sites where the GBM deviates from its pericapillary course and covers the mesangium. Thereby, the GBM is not only coupled to the mesangium out—via mesangial cell processes—also to the GBM at the opposing mesangial angle. It seems possible that contraction of mesangial cells can bring the GBM from opposing mesangial angles closer together. Therefore we conclude that the GBM and the contractile mesangial cells together establish a biomechanical unit capable of developing wall tension in glomerular capillaries and of changing the geometry of glomerular capillaries following mesangial contraction or relaxation.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Andrews PM, Coffey AK (1983) Cytoplasmic contractile elements in glomerular cells. Fed Proc 42:3046–3052

    Google Scholar 

  • Ausiello DA, Kreisberg JJ, Roy C, Karnovsky MJ (1980) Contraction of cultured rat glomerular mesangial cells after stimulation with angiotensin II and arginine vasopressin. J Clin Invest 65:754–760

    Google Scholar 

  • Bachmann S, Kriz W, Kuhn C, Franke WW (1983) Differentiation of cell types in the mammalian kidney by immunofluorescence microscopy using antibodies to intermediate filament proteins and desmoplakins. Histochem 77:365–394

    Google Scholar 

  • Bargmann W, Hehn GV (1971) Über des Nephron der Elasmobranchier. Z Zellforsch 114:1–21

    Google Scholar 

  • Becker CG (1972) Demonstration of actomyosin in mesangial cells of the renal glomerulus. Am J Pathol 66:97–110

    Google Scholar 

  • Böck P (1983) Elastic fiber microfibrils: Filaments that anchor the epithelium of the epiglottis. Arch Histol Jpn 46:307–314

    Google Scholar 

  • Brenner BM, Dworkin LD, Ichikawa I (1986) Glomerular ultrafiltration. In: Brenner BM, Rector FC (eds) The kidney, 3rd edn. Saunders, Berlin. vol 1, pp 124–144

    Google Scholar 

  • Bretschneider HJ (1980) Myocardial protection. Thorac Cardiovasc Surg 28:295–302

    Google Scholar 

  • Burton AC (1951) On the physical equilibrium of small blood vessels. Am J Physiol 164:319–329

    Google Scholar 

  • Carlemalm E, Garavito RM, Villinger W (1982) Resin development for electron microscopy and an analysis of embedding at low temperature. J Microsc 126:123–143

    Google Scholar 

  • Cleary EG, Gibson MA (1983) Elastin-associated microfibrils and microfibrillar proteins. Int Rev Connect Tissue Res 10: 97–209

    Google Scholar 

  • Courtoy PJ, Kanwar YS, Hynes RO, Farquhar MG (1980) Fibronectin localization in the rat glomerulus. J Cell Biol 87:691–696

    Google Scholar 

  • Demmel U, Schewe U, Böck P, Gorgas K (1979) Die Feinstruktur der Muskel-, Sehnen-und Muskel-Epithelverbindungen in der Zunge des Meerschweinchens. Cytobiol 18:460–477

    Google Scholar 

  • Dworkin LD, Brenner BM (1985) Biophysical basis of glomerular filtration. In: Seldin DW, Giebisch G (eds) The kidney: physiology and pathophysiology, Raven Press, New York, pp 397–426

    Google Scholar 

  • Essner E, Gordon SR (1984) Demonstration of microfibrils in Bruch's membrane of the eye. Tissue Cell 16:779–788

    Google Scholar 

  • Farquhar MG (1981) The glomerular basement membrane—a selective macromolecular filter. In: Hay ED (ed) Cell biology of extracellular matrix. Plenum Press, New York, pp 335–378

    Google Scholar 

  • Farquhar MG, Palade GE (1962) Functional evidence for the existence of a third cell type in the renal glomerulus. Phagocytosis of filtration residues by a distinctive “third” cell. J Cell Biol 13:55–87

    Google Scholar 

  • Foidart JB, Mahieu P (1986) Glomerular mesangial cell contractility in vitro is controlled by an angiotensin-prostaglandin balance. Mol Cell Endocrinol. 47:163–173

    Google Scholar 

  • Fullmer HM, Lillie, RD (1958) The oxytalan fiber: a previously underscribed connective tissue fiber. J Histochem Cytochem 6:425–430

    Google Scholar 

  • Gibson MA, Hughes JL, Fanning JC, Cleary EG (1986) The major antigen of elastin-associated microfibrils is a 31-kDa glycoprotein. J Biol Chem 261:11429–11436

    Google Scholar 

  • Goldfischer S, Coltoff-Schiller B, Goldfisher M (1985) Microfibrils, elastic anchoring components of the extracellular matrix, are associated with fibronectin in the zonule of zinn and aorta. Tissue Cell 17:441–450

    Google Scholar 

  • Goldfischer S, Coltoff-Schiller B, Schwarz E, Blumenfeld OO (1983) Ultrastructure and staining properties of aortic microfibrils (oxytalan). J Histochem Cytochem 31:382–390

    Google Scholar 

  • Goldman RD, Chojnackl B, Yerna MJ (1979) Ultrastructure of microfilament bundles in baby hamster kidney (BHK-21) cells. J Cell Biol 80:759–766

    Google Scholar 

  • Hanak H, Böck P (1971) Die Feinstruktur der Muskel-Sehnenver-bindung von Skelett-und Herzmuskel. J Ultrastruct Res 36:68–85

    Google Scholar 

  • Helmchen UE (1980) Die Zahl der Mesangiumzellen in einem normalen Glomerulum der Rattenniere. Eine dreidimensionale elektronenoptische Analyse. Med Diss, Tübingen

  • Hsu H-C, Churg J (1979) Glomerular microfibrils in renal diseases: A comparative electron microscopic study. Kidney Int 16:497–504

    Google Scholar 

  • Inoue S, Leblond CP (1986) The microfibrils of connective tissue: I. Ultrastructure. Am J Anat 176:121–138

    Google Scholar 

  • Inoue S, Leblond CP, Grant DS, Rico P (1986) The microfibrils of connective tissue: II Immunohistochemical detection of the amyloid P component. Am J Anat 176:139–152

    Google Scholar 

  • Kaissling B, Kriz W (1982) Variability of intercellular spaces between macula densa cells: a transmission electron microscopic study in rabbits and rats. Kidney Int 22 [Suppl 12]:9–17

    Google Scholar 

  • Kallerhoff M, Blech M, Kehrer G, Kleinert H, Siekmann W, Helmchen U, Bretschneider HJ (1986) Post-ischemic renal function after kidney protection with the HTK-solution of Bretschneider. Urol Res 14:271–277

    Google Scholar 

  • Kanwar YS (1984) Biology of Disease. Biophysiology of glomerular filtration and proteinuria. Lab Invest 51:7–21

    Google Scholar 

  • Kreisberg JI (1983) Contractile properties of the glomerular mesangium. Fed Proc 42:3053–3057

    Google Scholar 

  • Kühn K, Sterzel RB, Stolte H, Reale E (1976) Mesangial cells in different vertebrate kidneys. A thin-section and freeze-fracture study. In: Sterzel RB, Thomson D, Brod J (eds) Contrib Nephrol. Karger, Basel, vol 2, pp 9–16

    Google Scholar 

  • LaFountain JR, Zobel CR, Thomas HR, Galbreath C (1977) Fixation and Staining of F-Actin and Microfilaments using tannic acid. J Ultrastruct Res 58:78–86

    Google Scholar 

  • Latta H, Maunsbach AB, Madden SC (1960) The centrolobular region of the renal glomerulus studied by electron microscopy. J Ultrastruct Res 4:455–472

    Google Scholar 

  • Laurie GW, Leblond CP, Inoue S, Martin GR, Chung (1984) Fine structure of the glomerular basement membrane and immunolocalization of five basement membrane components to the lamina densa (Basal lamina) and its extensions in both glomeruli and tubules of the rat kidney. Am J Anat 169:463–481

    Google Scholar 

  • Linder E, Miettinen A, Törnroth T (1980) Fibronectin as a marker for the glomerular mesangium in immunohistology of kidney biopsies. Lab Invest 42:70–75

    Google Scholar 

  • Madri JA, Roll FJ, Furthmayr H, Foidart JM (1980) Ultrastructural localization of fibronectin and laminin in the basement membranes of the murine kidney. J Cell Biol 86:682–687

    Google Scholar 

  • Maupin P, Pollard TD (1983) Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-glutaraldehyde-saponin fixation. J Cell Biol 96:51–62

    Google Scholar 

  • Olesnicky L, Doty SB, Bertani T, Pirani CL (1984) Tubular microfibrils in the glomeruli of membraneous nephropathy. Arch Pathol Lab Med 108:902–905

    Google Scholar 

  • Pricam C, Humbert F, Perrelet A, Orci L (1974) Gap junctions in mesangial and lacis cells. J Cell Biol 63:349–354

    Google Scholar 

  • Ross R (1973) The elastic fiber. A review. J Histochem Cytochem 21:199–208

    Google Scholar 

  • Rostagno A, Frangione B, Pearlstein E, Garcia-Pardo A (1986) Fibronectin binds to amyloid P component. Localization of the binding site to the 31,000 Dalton C-terminal domain. Biochem Biophys Res Commun 140:12–20

    Google Scholar 

  • Sakai LY, Keene DR, Engvall E (1986) Fibrillin, a new 350-kD glycoprotein is a component of extracellular microfibrils. J Cell Biol 103:2499–2509

    Google Scholar 

  • Sakai T, Sabanovic S, Hosser H, Kriz W (1986) Heterogeneity of the podocyte membrane in rat kidney as revealed by ethanol dehydration of unosmicated specimens. Cell Tissue Res 246:145–151

    Google Scholar 

  • Savin VJ (1986) In vitro effects of angiotensin II on glomerular function. Am J Physiol 251:F627-F634

    Google Scholar 

  • Schnabel PhA, Richter J, Gebhard MM, Pomykaj Th, Preusse CJ, Ulbricht LJ, Bretschneider HJ (1985) Comparison of fixation by immersion and by perfusion after cardioplegia. Verh Anat Ges 79:311–314

    Google Scholar 

  • Schwartz E, Goldfischer S, Coltoff-Schiller B, Blumenfeld OO (1985) Extracellular matrix microfibrils are composed of core proteins coated with fibronectin. J Histochem Cytochem 33:268–274

    Google Scholar 

  • Simionescu N, Simionescu M (1976) Galloylglucoses of low molecular weight as mordant in electron microscopy. I. Procedure, and evidence for mordanting effect. J Cell Biol 70:608–621

    Google Scholar 

  • Singhal PC, Scharschmidt LA, Gibbons N, Hays RM (1986) Contraction and relaxation of cultured mesangial cells on a silicone rubber surface. Kidney Int 30:862–873

    Google Scholar 

  • Singer H (1982) Association of fibronectin and vinculin with focal contacts and stress fibers in stationary hamster fibroblasts. J Cell Biol 92:398–408

    Google Scholar 

  • Skorecki KL, Ballermann BJ, Rennke HG, Brenner BM (1983) Angiotensin II receptor regulation in isolated renal glomeruli. Fed Proc 42:3064–3070

    Google Scholar 

  • Sraer JD, Sraer J, Ardaillou R, Mimoune D (1974) Evidence for renal glomerular receptors for angiotensin II. Kidney Int 6:241–246

    Google Scholar 

  • Steinhausen M, Kücherer H, Parekh N, Snoei H (1986) Microcirculation in glomerular network: Implication of hemodynamic factors in effect of angiotensin II on glomerular function. In: Popel Johnson (eds) Microvascular Networks. Experimental and Theoretical Studies. S. Karger, Basel, 1986, pp 134–141

    Google Scholar 

  • Streeten BW, Licari PA (1983) The zonules and the elastic microfibrillar system in the ciliary body. Invest Ophthalmol Vis Sci 24:667–681

    Google Scholar 

  • Takagi M, Parmley RT, Yagasaki H, Toda Y (1984) Ultrastructural cytochemistry of oxytalan fibers in the periodontal ligament and microfibrils in the aorta with the periodic acid-thiocarbohydrazide-silver proteinate method. J Oral Pathol 13:671–678

    Google Scholar 

  • Tanaka T, Fujiwara Y, Orita Y, Sasaki E, Kitamura H, Abe H (1985) The functional characteristics of cultured rat mesangial cells. Jpn Circ J 48:1017–1029

    Google Scholar 

  • Timpl R (1986) Recent advances in the biochemistry of glomerular basement membrane. Kidney Int 30:293–298

    Google Scholar 

  • Tsujii T, Naito I, Ukita S, Ono T, Seno S (1984a) The anionic barrier system in the mesonephric renal glomerulus of the arctic lamprey, Entospheus japonicus (Martens) (Cyclostomi). Cell Tissue Res 235:491–496

    Google Scholar 

  • Tsujii T, Naito I, Ukita S, Ono T, Seno S (1984b) The anionic barrier system in the mesonephric renal glomerulus of the brown hagfish, Paramyxine atami Dean (Cyclostomi). Anat Rec 208:337–347

    Google Scholar 

  • Vasmant D, Maurice M, Feldmann G (1984) Cytoskeleton ultrastructure of podocytes and glomerular endothelial cells in man and in the rat. Anat Rec 210:17–24

    Google Scholar 

  • Yoshikawa N, Cameron AH, White RHR, Standring DM (1982) Microfibrils in glomerulopathies of children: an ultrastructural study. J Pathol 136:123–131

    Google Scholar 

  • Zimmermann KW (1929) Über den Bau des Glomerulus der menschlichen Niere. Z mikr anat Forsch 18:520–552

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Faculty of Medicine, University of Tokyo, 113, Tokyo, Japan

    Fatsuo Sakai & Wilhelm Kriz

Authors
  1. Fatsuo Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wilhelm Kriz
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Fellow of the Alexander von Humboldt Foundation

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sakai, F., Kriz, W. The structural relationship between mesangial cells and basement membrane of the renal glomerulus. Anat Embryol 176, 373–386 (1987). https://doi.org/10.1007/BF00310191

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00310191

Key words

Search

Navigation