Skip to main content
SpringerLink
Log in

Sex different cytochrome-c uptake in the proximal tubule of the rat kidney

  • Published:
Histochemistry Aims and scope Submit manuscript

Summary

The present study deals with the dose- and time-dependent uptake of cytochrome c (CYT c) in the proximal tubule of the rat kidney, and shows that there are segment and sex differences in the reabsorption of CYT c. Rats of both sexes were intravenously injected with different doses of CYT c (0.75–9.0 mg per 100 g body weight), and the kidneys were investigated by light and electron microscopy at different times (3 min, 10 min, and 2 h) after the injection. After 3 and 10 min, CYT c was demonstrated in apical vacuoles of different sizes and in some lysosomes of the S1 and S2 semgents, whereas after 2 h, CYT c was found only in lysosomes of all three segments of the proximal tubule. At these times, the S1 segment contained more CYT c than the S2 and S3 segments. However, 2 h after the injection of 6 or 9 mg CYT c, the differences between the S1 and S2 segments disapeared almost completely, due to a strong lysosomal accumulation of CYT c in the S2 segment. At all studied times and CYT-c doses, the S3 segment contained less CYT c than the S1 and S2 segments. On the whole, different levels of CYT-c reabsorption were found in the different segments of the proximal tubule, which was saturable with increasing CYT-c doses, i.e. firstly in the proximal and then in the distal parts of the proximal tubule. Two hours after the injection of CYT c, a difference between males and females was observed, with the lysosomes of the S1 and S2 segments of females containing more CYT c than those of males. Thus, more CYT c was reabsorbed in the proximal tubule of females than in that of males.

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

  • Baumann K, Cojocel C (1981) Microperfusion and clearance studies on renal protein reabsorption. Contrib Nephrol 24:8–17

    Google Scholar 

  • Baumann K, Cojocel C, Franzen-Sieveking M (1979) Inhibition of endocytic lysozym uptake by cationic proteins in microperfused proximal tubule of rat kidney. Pflügers Arch (Suppl) 379:R12

    Google Scholar 

  • Baumann K, Bode F, Ottosen PD, Madsen KM, Maunsbach AB (1980) Quantitative analysis of protein absorption in microperfused proximal tubules of the rat kidney. In: Maunsbach AB, Olson TS, Christensen EI (eds) Functional ultrastructure of the kidney. Academic Press, London New York, pp 291–301

    Google Scholar 

  • Bode F, Pockrandt-Helmstedt H, Baumann K, Kinne R (1974) Analysis of the pinocytic process in the rat kidney. I. Isolation of the pinocytic vesicles from rat kidney cortex. J Cell Biol 63:998–1008

    Google Scholar 

  • Bode F, Baumann K, Kinne R (1975) Biochemical aspects of pinocytosis in kidney. Contrib Nephrol 1:21–27

    Google Scholar 

  • Bode F, Baumann K, Kinne R (1976) Analysis of the pinocytic process in rat kidney. Biochim Biophys Acta 433:294–310

    Google Scholar 

  • Bode F, Ottosen PD, Madsen KM, Maunsbach AB (1980) Does transtubular transport of intact protein occur in kidney? In: Maunsbach AB, Olson TS, Christensen EI (eds) Functional ultrastructure of the kidney. Academic Press, London New York, pp 385–395

    Google Scholar 

  • Bourdeau JE, Carone FA (1974) Protein handling by the renal tubule. Nephron 13:22–34

    Google Scholar 

  • Bourdeau JE, Carone FA, Ganote CE (1972) Serum albumin uptake in isolated perfused renal tubules. J Cell Biol 54:382–398

    Google Scholar 

  • Carone FA, Peterson DR, Oparil S, Pullman TN (1979) Renal tubular transport and catabolism of proteins and peptides. Kidney Int 16:271–278

    Google Scholar 

  • Christensen EI (1976) Rapid protein uptake and digestion in proximal tubule lysosomes. Kidney Int 10:301–310

    Google Scholar 

  • Christensen EI, Maunsbach AB (1974) Intralysosomal digestion of lysozym in renal proximal tubule cells. Kidney Int 6:396–407

    Google Scholar 

  • Christensen EI, Carone FA, Rennke HG (1981) Effect of molecular charge on endocytic uptake of ferritin in renal proximal tubule cells. Lab Invest 44:351–358

    Google Scholar 

  • Christensen EI, Rennke HG, Carone FA (1983) Renal tubular uptake of protein: effect of molecular charge. Am J Physiol 244:F436–441

    Google Scholar 

  • Cojocel C, Franzen-Sieveking M, Beckmann G, Baumann K (1981) Inhibition of renal accumulation of lysozym (basic low molecular weight protein) by basic proteins and other basic substances. Pflügers Arch 390:211–215

    Google Scholar 

  • Conway TP, Poulik MD (1977) Catabolism of rat β2-microglobulin in the rat. J Lab Clin Med 89:1208–1214

    Google Scholar 

  • Cortney MA, Sawin LL, Weiss DD (1970) Renal tubular protein absorption in the rat. J Clin Invest 49:1–4

    Google Scholar 

  • Daigeler R (1981) Sex dependent changes in the rat kidney after hypophysectomy. Cell Tissue Res 216:423–443

    Google Scholar 

  • Davidson SJ, Hughes WL, Barnwell A (1971) Renal protein absorption into sub-cellular particles: I. Studies with intact kidneys and fractionated homogenates. Exp Cell Res 67:171–187

    Google Scholar 

  • Ericsson JLE (1965) Transport and digestion of hemoglobin in the proximal tubule. II. Electron microscopy. Lab Invest 14:16–39

    Google Scholar 

  • Falk N (1984) Nachweis exogener Meerrettichperoxidase im Hauptstück der Niere männlicher und weiblicher Ratten. Z mikrosk-anat Forsch 98:451–464

    Google Scholar 

  • Flatmark T (1965) Studies on the peroxidase effect of cytochrome c. IV. The influence of pH and certain anions on the overall reaction. Act Chem Scand 19:2059–2074

    Google Scholar 

  • Fröhlich H, Kulger P, Schiebler TH (1984) Geschlechtsdifferentes Proteinmuster im Harn von Ratten nach Kastration. Z mikrosk-anat Forsch 98:86–106

    Google Scholar 

  • Galaske RG, Van Liew JB, Feld LG (1979) Filtration and reabsorption of endogeneous low-molecular-weight protein in rat kidney. Kidney Int 16:394–403

    Google Scholar 

  • Graham RC, Karnovsky MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: Ultrastructure cytochemistry by a new technique. J Histochem Cytochem 14:291–302

    Google Scholar 

  • Grinnell F, Tobleman MQ, Hackenbrock CR (1975) The distribution and mobility of anionic sites on the surfaces of baby hamster kidney cells. J Cell Biol 66:470–479

    Google Scholar 

  • Herbert M (1983) Elektronenmikroskopisch-morphometrische Untersuchungen am Nierenhauptstück männlicher und weiblicher Ratten nach Kastration und Testosteronsubstitution. Z mikrosk-anat Forsch 97:189–239

    Google Scholar 

  • Jacobson HR (1981) Functional segmentation of the mammalian nephron. Am J Physiol 241:F203–218

    Google Scholar 

  • Jedrzejewski K, Kugler P (1982) Peptidases in the kidney and urine of rats after castration. Histochemistry 74:63–84

    Google Scholar 

  • Karnovsky MJ, Rice DF (1969) Exogenous cytochrome c as an ultrastructural tracer. J Histochem Cytochem 17:751–573

    Google Scholar 

  • Kato M, Kato K, Goodman DS (1984) Immunocytochemical studies on the localization of plasma and cellular retinol binding proteins and of transhyretin (prealbumin) in rat liver and kidney. J Cell Biol 98:1696–1704

    Google Scholar 

  • Kerjaschki D, Noronha-Blob L, Sacktor B, Farquhar MG (1984) Microdomains of distinctive glycoprotein composition in the kidney proximal tubule brush border. J Cell Biol 98:1505–1513

    Google Scholar 

  • Kiesewetter F, Kugler P (1985) Geschlechtsdifferenter lysosomaler Abbau von exogenem Cytochrom c im Nierenhauptstück der Ratte. Z mikrosk-anat Forsch (in press)

  • Kugler P (1982a) On angiotensin-degrading aminopeptidases in the rat kidney. Adv Anat Embryol Cell Biol, Vol 76. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Kugler P (1982b) Quantitative histochemistry of the lysosomal dipeptidylaminopeptidase II in the proximal tubule of rat kidney. Histochemistry 76:557–566

    Google Scholar 

  • Kugler P, Vornberger G (1985) Renal cathepsin B activities in rats after estration and treatment with sex hormones. (in preparation).

  • Liew JB van, Buentig W, Stolte H, Boylan JW (1970) Protein excretion, micropuncture study of capsular and proximal tubule fluid. Am J Physiol 219:F299–305

    Google Scholar 

  • Lojda Z, Gossrau R, Schiebler TH (1979) Enzyme histochemistry. A labratory manual. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Maack T, Sumpio B (1982) Renal accumulation and catabolism of cytochrome c (CYT C) in the isolated perfused rat kidney. Kidney Int 21:254

    Google Scholar 

  • Maack T, Johnson V, Kau ST, Figueiredo J, Sigulem D (1979) Renal filtration, transport, and metabolism of low molecular-weight proteins. Kidney Int 16:251–270

    Google Scholar 

  • Madsen KM, Christensen EI (1978) Effects of mercury on lysosomal protein digestion in the kidney proximal tubule. Lab Invest 38:165–174

    Google Scholar 

  • Maunsbach AB (1966a) Observations on the segmentation of the proximal tubule in the rat kidney. J Ultrastruct Res 16:239–258

    Google Scholar 

  • Maunsbach AB (1966b) Absorption of I125-labeled homologous albumin by rat kidney proximal tubule cells. J Ultrastruct Res 15:197–241

    Google Scholar 

  • Maunsbach AB, Christensen EI (1974) Lysosomal accumulation and digestion of β2-microglobulin in rat kidney tubules. Int Res Commun Sys 2:1737–1746

    Google Scholar 

  • Nolte A, Ohkuma M (1969) Elektronenmikroskopisch-histochemische Untersuchungen zur Darstellung saurer Mucopolysaccharide und sialinsäurehaltiger Glycoproteine in Nierenrinde und innerem Nierenmark der Ratte. Histochemie 17:170–180

    Google Scholar 

  • Ottosen PD, Bode F, Madsen KM, Maunsbach AB (1979) Renal handling of lysozyme in the rat. Kidney Int 15:246–254

    Google Scholar 

  • Pape W, Baumann K (1981) Proteinreabsorption (Cytochrome c) in microperfused proximal tubules of rat kidney. Pflügers Arch (Suppl) 391:R23

    Google Scholar 

  • Pesce AJ, Clyne DH, Pollak VE, Kant SK (1980) Renal tubular interactions of proteins. Clin Biochem 13:209–215

    Google Scholar 

  • Plattner H, Wachter E, Gröbner P (1977) A heme-nonapeptide tracer for electron microscopy. Preparations, characterization and comparison with other heme-tracer. Histochemistry 53:223–242

    Google Scholar 

  • Rambourg A, Leblond CP (1967) Electron microscopic observations on the carbohydrate rich cell coat present at the surface of cells in the rat. J Cell Biol 32:27–53

    Google Scholar 

  • Schiebler TH, Danner KG (1978) The effect of sex hormones on the proximal tubules in the rat kidney. Cell Tissue Res 192:527–549

    Google Scholar 

  • Sellers AL, Goodman HC, Mormorston J, Smith M (1950) Sex difference in proteinuria in the rat. Am J Physiol 163:662–667

    Google Scholar 

  • Seno S, Tsujii T, Ono T, Ukita S (1983) Cationic cacodylate iron colloid for detection of anionic sites on cell surface and the histochemical stain of acid mucopolysaccharides. Histochemistry 78:27–31

    Google Scholar 

  • Silverstein SC, Steinman RM, Cohn ZA (1977) Endocytosis. Annu Rev Biochem 46:669–722

    Google Scholar 

  • Stacy BD, Wallace ALC, Grinnell RT, Wilson BW (1976) Absorption of 125J-labelled sheep growth hormone in single proximal tubules of rat kidney. J Endocrinol 68:21–30

    Google Scholar 

  • Steinman RM, Mellman IS, Muller WA, Cohn ZA (1983) Endocytosis and the recycling of plasma membrane. J Cell Biol 96:1–27

    Google Scholar 

  • Straus W (1964) Occurence of phagosomes and phagolysosomes in different segments of the nephron in relation to the reabsorption, transport, digestion, and extrusion of intravenously injected horseradish peroxidase. J Cell Biol 21:295–308

    Google Scholar 

  • Straus W (1967) Changes in intracellular location of small phagosomes (micropinocytic vesicles) in kidney and liver cells in relation to time after injection and dose of horseradish peroxidase. J Histochem Cytochem 15:381–393

    Google Scholar 

  • Sumpio BE, Maack T (1982) Kinetics, competition, and selectivity of tubular absorption of proteins. Am J Physiol 243:F379–392

    Google Scholar 

  • Sumpio BE, Tate SS, Maack T (1981) Effects of iodoacetate and lysine on tubular absorption of β2-microglobulin (β2M) and cytochrome c (CYT C) in the isolated perfused rat kidney (IPRK). Kidney Int 19:259

    Google Scholar 

  • Thoenes W, Langer KH (1969) Die Endocytose-Phase der Eiweiß-resorption im proximalen Nierentubules. Virchows Ach Abt B Cellpathol 2:361–379

    Google Scholar 

  • Winckler J (1970) Zum Einfrieren von Gewebe in Stickstoffgekühltem Propan. Histochemie 23:44–50

    Google Scholar 

  • Zabel M, Schiebler TH (1980) Histochemical, autoradiographic and electron microscopic investigations of the renal proximal tubule of male and female rats after castration. Histochemistry 69:255–276

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Anatomical Institute, University of Würzburg, Koellikerstraße 6, D-8700, Würzburg, Federal Republic of Germany

    F. Kiesewetter & P. Kugler

Authors
  1. F. Kiesewetter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Kugler
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dedicated to Prof. Dr. E. Lindner, Department of Anatomy, University of Regensburg, on the occasion of his 65th birthday

Supported by the Deutsche Forschungsgemeinschaft (SFB 105)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kiesewetter, F., Kugler, P. Sex different cytochrome-c uptake in the proximal tubule of the rat kidney. Histochemistry 82, 557–564 (1985). https://doi.org/10.1007/BF00489977

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00489977

Keywords

Search

Navigation