Skip to main content

Advertisement

SpringerLink
Log in

Distinct differences between cultured podocytes and parietal epithelial cells of the Bowman’s capsule

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Phenotypic changes in culture hamper the identification and characterization of cultured podocytes and parietal epithelial cells of the Bowman’s capsule (PECs). We have recently established culture conditions that restore podocytes to their differentiated phenotypes. We compared podocytes and PECs cultured under the same conditions to determine the unique characteristics of the two cell types. Performing this comparison under the same conditions accentuated these differences. Podocytes behaved like non-epithelial cells by extending cell processes even at confluence. By contrast, PECs behaved like typical epithelial cells by maintaining a polygonal appearance. Other differences were identified using immunostaining and RT-PCR; podocytes expressed high levels of podocyte-specific markers while PECs expressed high levels of PEC-specific markers. However, while podocytes expressed low levels of PEC markers, PECs expressed low levels of podocyte markers. Therefore, the identification of podocytes and PECs in culture requires the evaluation of respective cell markers and the expression of markers for other cell types.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Andrews PM, Stauver M (1979) In vitro incubation and study of kidney glomerular epithelial cells. Kidney Int 15:80–87

    Article  CAS  Google Scholar 

  • Arakawa M, Tokunaga J (1977) A scanning electron microscope study of the human Bowman's epithelium. Contrib Nephrol 6:73–78

    Article  CAS  Google Scholar 

  • Chittiprol S, Chen P, Petrovic-Djergovic D, Eichler T, Ransom RF (2011) Marker expression, behaviors, and responses vary in different lines of conditionally immortalized cultured podocytes. Am J Physiol Renal Physiol 301:F660–F671

    Article  CAS  Google Scholar 

  • Guhr SS, Sachs M, Wegner A, Becker JU, Meyer TN, Kietzmann L, Schlossarek S, Carrier L, Braig M, Jat PS, Stahl RA, Meyer-Schwesinger C (2013) The expression of podocyte-specific proteins in parietal epithelial cells is regulated by protein degradation. Kidney Int 84:532–544

    Article  CAS  Google Scholar 

  • Hatta K, Okada TS, Takeichi M (1985) A monoclonal antibody disrupting calcium-dependent cell-cell adhesion of brain tissues: possible role of its target antigen in animal pattern formation. Proc Natl Acad Sci U S A 82:2789–2793

    Article  CAS  Google Scholar 

  • Ichimura K, Miyazaki N, Sadayama S, Murata K, Koike M, Nakamura K, Ohta K, Sakai T (2015) Three-dimensional architecture of podocytes revealed by block-face scanning electron microscopy. Sci Rep 5:8993. https://doi.org/10.1038/srep08993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa Y, Kitamura M (1998) Spontaneous apoptosis of podocytes in explanted glomeruli. Kidney Int 54:2008–2013

    Article  CAS  Google Scholar 

  • Kabgani N, Grigoleit T, Schulte K, Sechi A, Sauer-Lehnen S, Tag C, Boor P, Kuppe C, Warsow G, Schordan S, Mostertz J, Chilukoti RK, Homuth G, Endlich N, Tacke F, Weiskirchen R, Fuellen G, Endlich K, Floege J, Smeets B, Moeller MJ (2012) Primary cultures of glomerular parietal epithelial cells or podocytes with proven origin. PLoS One 7:e34907

    Article  CAS  Google Scholar 

  • Katsuya K, Yaoita E, Yoshida Y, Yamamoto Y, Yamamoto T (2006) An improved method for primary culture of rat podocytes. Kidney Int 69:2101–2106

    Article  CAS  Google Scholar 

  • Kuppe C, Gröne HJ, Ostendorf T, van Kuppevelt TH, Boor P, Floege J, Smeets B, Moeller MJ (2015) Common histological patterns in glomerular epithelial cells in secondary focal segmental glomerulosclerosis. Kidney Int 88:990–998

    Article  CAS  Google Scholar 

  • Kuppe C, Leuchtle K, Wagner A, Kabgani N, Saritas T, Puelles VG, Smeets B, Hakroush S, van der Vlag J, Boor P, Schiffer M, Gröne HJ, Fogo A, Floege J, Moeller MJ (2019) Novel parietal epithelial cell subpopulations contribute to focal segmental glomerulosclerosis and glomerular tip lesions. Kidney Int 96:80–93

    Article  CAS  Google Scholar 

  • Lazareth H, Henique C, Lenoir O, Puelles VG, Flamant M, Bollée G, Fligny C, Camus M, Guyonnet L, Millien C, Gaillard F, Chipont A, Robin B, Fabrega S, Dhaun N, Camerer E, Kretz O, Grahammer F, Braun F, Huber TB, Nochy D, Mandet C, Bruneval P, Mesnard L, Thervet E, Karras A, Le Naour F, Rubinstein E, Boucheix C, Alexandrou A, Moeller MJ, Bouzigues C, Tharaux PL (2019) The tetraspanin CD9 controls migration and proliferation of parietal epithelial cells and glomerular disease progression. Nat Commun 10:3303

    Article  Google Scholar 

  • Nagata M (2016) Podocyte injury and its consequences. Kidney Int 89:1221–1230

    Article  CAS  Google Scholar 

  • Nose A, Nagafuchi A, Takeichi M (1988) Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993–1001

    Article  CAS  Google Scholar 

  • Ohse T, Chang AM, Pippin JW, Jarad G, Hudkins KL, Alpers CE, Miner JH, Shankland SJ (2009) A new function for parietal epithelial cells: a second glomerular barrier. Am J Physiol Renal Physiol 297:F1566–F1574

    Article  CAS  Google Scholar 

  • Ohtaka A, Ootaka T, Sato H, Soma J, Sato T, Saito T, Ito S (2002) Significance of early phenotypic change of glomerular podocytes detected by Pax2 in primary focal segmental glomerulosclerosis. Am J Kidney Dis 39:475–485

    Article  Google Scholar 

  • Paul R, Ewing CM, Robinson JC, Marshall FF, Johnson KR, Wheelock MJ, Isaacs WB (1997) Cadherin-6, a cell adhesion molecule specifically expressed in the proximal renal tubule and renal cell carcinoma. Cancer Res 57:2741–2748

    CAS  PubMed  Google Scholar 

  • Pavenstädt H, Kriz W, Kretzler M (2003) Cell biology of the glomerular podocyte. Physiol Rev 83:253–307

    Article  Google Scholar 

  • Rodewald R, Karnovsky MJ (1974) Porous substructure of the glomerular slit diaphragm in the rat and mouse. J Cell Biol 60:423–433

    Article  CAS  Google Scholar 

  • Takemoto M, Asker N, Gerhardt H, Lundkvist A, Johansson BR, Saito Y, Betsholtz C (2002) A new method for large-scale isolation of kidney glomeruli from mice. Am J Pathol 161:799–805

    Article  Google Scholar 

  • Webber WA, Blackbourn J (1971) The permeability of the parietal layer of Bowman's capsule. Lab Investig 25:367–373

    CAS  PubMed  Google Scholar 

  • Yaoita E, Yamamoto T, Saito M, Kawasaki K, Kihara I (1991) Desmin-positive epithelial cells outgrowing from rat encapsulated glomeruli. Eur J Cell Biol 54:140–149

    CAS  PubMed  Google Scholar 

  • Yaoita E, Yamamoto T, Takashima N, Kawasaki K, Kawachi H, Shimizu F, Kihara I (1995) Visceral epithelial cells in rat glomerular cell culture. Eur J Cell Biol 67:136–144

    CAS  PubMed  Google Scholar 

  • Yaoita E, Kurihara H, Sakai T, Ohshiro K, Yamamoto T (2001) Phenotypic modulation of parietal epithelial cells of Bowman's capsule in culture. Cell Tissue Res 304:339–349

    Article  CAS  Google Scholar 

  • Yaoita E, Yoshida Y, Nameta M, Zhang Y, Fujinaka H, Magdeldin S, Xu B, Yamamoto T (2014) Heparin increasing podocyte-specific gene expressions. Nephrology (Carlton) 19:195–201

    Article  CAS  Google Scholar 

  • Yaoita E, Yoshida Y, Nameta M, Takimoto H, Fujinaka H (2018) Induction of interdigitating cell processes in podocyte culture. Kidney Int 93:519–524

    Article  Google Scholar 

Download references

Funding

This work was supported by research grants from the Japanese Ministry of Education, Culture, Sports, Science and Technology (No. 16K09606 and No. 19K08698 to EY).

Author information

Authors and Affiliations

  1. Department of Structural Pathology, Kidney Research Center, Niigata University Graduate School of Medical and Dental Sciences, 1-757 Asahimachi-dori, Chuo-ku, Niigata-shi, Niigata, 951-8510, Japan

    Tomizo Oyama, Eishin Yaoita & Yutaka Yoshida

  2. Division of Instrumental Analysis, Center for Coordination of Research Facilities, Institute for Research Promotion, Niigata University, Niigata, Japan

    Ayako Ikarashi

  3. Department of Clinical Research, Niigata National Hospital, Kashiwazaki, Japan

    Hidehiko Fujinaka

Authors
  1. Tomizo Oyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eishin Yaoita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yutaka Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ayako Ikarashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hidehiko Fujinaka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eishin Yaoita.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

All the animal experiments were conducted in compliance with the protocol, which was reviewed by the Institutional Animal Care and Use Committee of Niigata University and approved by the President of Niigata University (Permit Number: #28 Niigata Univ. Res. 345-2, Niigata Univ. Res.SA-00210).

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 1354 kb)

(AVI 93759 kb)

(AVI 91415 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oyama, T., Yaoita, E., Yoshida, Y. et al. Distinct differences between cultured podocytes and parietal epithelial cells of the Bowman’s capsule. Cell Tissue Res 380, 581–591 (2020). https://doi.org/10.1007/s00441-020-03170-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-020-03170-4

Keywords

Search

Navigation