Skip to main content
SpringerLink
Log in

Structural links between the renal stem/progenitor cell niche and the organ capsule

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

A special feature of the renal stem/progenitor cell niche is its always close neighborhood to the capsule during organ development. To explore this link, neonatal kidney was investigated by histochemistry and transmission electron microscopy. For adequate contrasting, fixation of specimens was performed by glutaraldehyde including tannic acid. The immunohistochemical data illustrate that renal stem/progenitor cells are not distributed randomly but are positioned specially to the capsule. Epithelial stem/progenitor cells are found to be enclosed by the basal lamina at a collecting duct (CD) ampulla tip. Only few layers of mesenchymal cells are detected between epithelial cells and the capsule. Most impressive, numerous microfibers reacting with soybean agglutinin, anti-collagen I and III originate from the basal lamina at a CD ampulla tip and line between mesenchymal stem/progenitor cells to the inner side of the capsule. This specific arrangement holds together both types of stem/progenitor cells in a cage and fastens the niche as a whole at the capsule. Electron microscopy further illustrates that the stem/progenitor cell niche is in contact with a tunnel system widely spreading between atypical smooth muscle cells at the inner side of the capsule. It seems probable that stem/progenitor cells are supplied here by interstitial fluid.

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

  • Axelrod DA (2013) Economic and financial outcomes in transplantation: whose dome is it anyway? Curr Opin Organ Transplant 18:222–228

    Article  PubMed  Google Scholar 

  • Brizzi MF, Tarone G, Defilippi P (2012) Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Curr Opin Cell Biol 24:1–7

    Article  Google Scholar 

  • Bulger RE (1973) Rat renal capsule: presence of layers of unique squamous cells. Anat Rec 177:393–407

    Article  CAS  PubMed  Google Scholar 

  • Burst V, Pütsch F, Kubacki T, Völker LA, Bartram MP, Müller RU et al (2013) Survival and distribution of injected haematopoietic stem cells in acute kidney injury. Nephrol Dial Transplant 28:1131–1139

    Article  PubMed  Google Scholar 

  • Caldas HC, Hayashi AP, Abbud-Filho M (2011) Repairing the chronic damaged kidney: the role of regenerative medicine. Transplant Proc 43:3573–3576

    Article  CAS  PubMed  Google Scholar 

  • Carroll TJ, Das A (2013) Defining the signals that constitute the nephron progenitor niche. J Am Soc Nephrol 24:873–876

    Article  CAS  PubMed  Google Scholar 

  • Chai OH, Song CH, Park SK, Kim W, Cho ES (2013) Molecular regulation of kidney development. Anat Cell Biol 46:19–31

    Article  PubMed Central  PubMed  Google Scholar 

  • Faa G, Gerosa C, Fanni D, Monga G, Zaffanello M, van Eyken P, Fanos V (2012) Morphogenesis and molecular mechanisms involved in human kidney development. J Cell Physiol 227:1257–1268

    Article  CAS  PubMed  Google Scholar 

  • Fanni D, Gerosa C, Nemola S, Mocci C, Pichiri G, Coni P et al (2012) “Physiological” renal regenerating medicine in VLBW preterm infants: could a dream come true? J Matern Fetal Neonatal Med 25:41–48

    Article  PubMed  Google Scholar 

  • Hammersen F, Staubesand J (1961) Über die Stromwege in der Nierenkapsel von Mensch und Hund; zugleich ein Beitrag zum Begriff der arterio-venösen Anatomosen. Zeitschrift Anatomie und Entwicklungsgeschichte 122:363–381

    Article  CAS  Google Scholar 

  • Hanein D, Horwitz AR (2012) The structure of cell-matrix adhesions: the new frontier. Curr Opin Cell Biol 24:134–140

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hasko JA, Richardson GP (1988) The ultrastructural organization and properties of the mouse tectorial membrane matrix. Hear Res 35:21–38

    Article  CAS  PubMed  Google Scholar 

  • Iino N, Gejyo F, Arakawa M, Ushiki T (2001) Three-dimensional analysis of nephrogenesis in the neonatal rat kidney: light and scanning electron microscopic studies. Arch Histol Cytol 64:179–190

    Article  CAS  PubMed  Google Scholar 

  • Iwatani H, Imai E (2013) Kidney repair using stem cells: myth or reality as therapeutic option. J Nephrol 23:143–146

    Google Scholar 

  • Kloth S, Aigner J, Schmidbauer A, Minuth WW (1994) Interrelationship of renal vascular development and nephrogenesis. Cell Tissue Res 277:247–257

    Article  CAS  PubMed  Google Scholar 

  • Kloth S, Ebenbeck C, Monzer J, de Vries U, Minuth WW (1997) Three-dimensional organization of the developing vasculature of the kidney. Cell Tissue Res 287:193–201

    Article  CAS  PubMed  Google Scholar 

  • Knoll GA (2013) Kidney transplantation in the older adult. Am J Kidney Dis 61:790–797

    Article  PubMed  Google Scholar 

  • Kobayashi K (1978) Fine structure of the mammalian renal capsule: the atypical smooth muscle cell and it functional meaning. Cell Tissue Res 195:381–394

    Article  CAS  PubMed  Google Scholar 

  • Li PK, Burdmann EA, Mehta RL (2013) Acute kidney injury: global health alert. Transplantation 95:653–657

    Article  CAS  PubMed  Google Scholar 

  • Little MH (2011) Renal organogenesis: what can it tell us about renal repair and regeneration? Organogenesis 7:229–241

    Article  PubMed Central  PubMed  Google Scholar 

  • Little MH, McMahon A (2012) Mammalian kidney development: principles, progress, and projections. Cold Spring Harb Perspect Biol 4:a008300

    Article  PubMed  Google Scholar 

  • McCampbell KK, Wingert RA (2012) Renal stem cells: fact or science fiction? Biochem J 444:153–168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Minuth WW, Denk L (2012a) Illustration of extensive extracellular matrix at the epithelial-mesenchymal interface within the renal stem/progenitor cell niche. BMC Clin Pathol 12:16

    Article  PubMed Central  PubMed  Google Scholar 

  • Minuth WW, Denk L (2012b) Cell projections and extracellular matrix cross the interstitial interface within the renal stem/progenitor cell niche: accidental, structural or functional cues? Nephron Exp Nephrol 122:131–140

    Article  CAS  PubMed  Google Scholar 

  • Minuth WW, Denk L (2013) The interstitial interface within the renal stem/progenitor cell niche exhibits an unique microheterogeneous composition. Int J Mol Sci 14:13657–13669

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Minuth WW, Denk L, Miess C, Glashauser A (2011) Peculiarities of the extracellular matrix in the interstitium of the renal stem/progenitor cell niche. Histochem Cell Biol 136:321–334

    Article  CAS  PubMed  Google Scholar 

  • Minuth WW, Denk L, Gruber M (2013) Search for chemically defined culture medium to assist initial regeneration of diseased renal parenchyma after stem/progenitor cell implantation. Int J Stem Cell Res Transplant 1:202

    Google Scholar 

  • Möllendorf W (1930) Harn- und Geschlechtsapparat. In: Handbuch der Mikroskopischen Anatomie des Menschen, Band VII. pp 140–143

  • O’Brien L, McMahon A (2013) Progenitor programming in mammalian nephrogenesis. Nephrology 18:177–179

    Article  PubMed  Google Scholar 

  • Park HC, Yasudo K, Kuo MC, Ni J, Ratliff B, Chander P, Goligorsky MS (2010) Renal capsule as a stem cell niche. Am J Renal Physiol 298:F1254–F1262

    Article  CAS  Google Scholar 

  • Pasquier J, Rafii A (2013) Role of microenvironment in ovarian cancer stem cell maintenance. Biomed Res Int: 630782. doi:10.1155/2013/630782

  • Piludu M, Fanos V, Congiu T, Piras M, Gerosa C, Mocci C, Fanni D, Nemolato S, Muntoni S, Iacovidou N, Faa G (2012) The pine-cone body: an intermediate structure between the cap mesenchyme and the renal vesicle in the developing nod mouse kidney revealed by an ultrastructural study. J Mater Fetal Neonatal Med 25:72–75

    Article  Google Scholar 

  • Rak-Raszewska A, Wilm B, Edgar D, Kenny S, Woolf AS, Murray P (2012) Development of embryonic stem cells in recombinant kidneys. Organogenesis 8:125–136

    Article  PubMed Central  PubMed  Google Scholar 

  • Rothenburger M, Völker W, Vischer P, Glasmacher B, Scheld HH, Deiwick M (2002) Ultrastructure of proteoglycans in tissue-engineered cardiovascular structures. Tissue Eng 8:1049–1056

    Article  CAS  PubMed  Google Scholar 

  • Schumacher K, Strehl R, Minuth WW (2002a) Detection of glycosylated sites in embryonic rabbit kidney by lectin histochemistry. Histochem Cell Biol 118:79–87

    CAS  PubMed  Google Scholar 

  • Schumacher K, Strehl R, de Vries U, Groene HJ, Minuth WW (2002b) SBA-positive fibers between the CD ampulla, mesenchyme, and renal capsule. J Am Soc Nephrol 13:2446–2453

    Article  CAS  PubMed  Google Scholar 

  • Schumacher K, Strehl R, Minuth WW (2003) Characterization of micro-fibers at the interface between the renal collecting duct ampulla and the cap condensate. Nephron Exp Nephrol 95:e43–e54

    Article  CAS  PubMed  Google Scholar 

  • Schumacher K, Klar J, Wagner C, Minuth WW (2005) Temporal-spatial co-localisation of tissue transglutaminase-9 (MMP-9) with SBA-positive micro-fibers in the embryonic kidney cortex. Cell Tissue Res 319:491–500

    Article  CAS  PubMed  Google Scholar 

  • Sedrakyan S, Angelow S, DeFilippo RE, Perin L (2012) Stem cells as a therapeutic approach to chronic kidney diseases. Curr Urol Rep 13:47–54

    Article  PubMed  Google Scholar 

  • Strehl R, Minuth WW (2001) Partial identification of the mab (CD)Amp 1 antigen at the epithelial-mesenchymal interface of the developing kidney. Histochem Cell Biol 116:389–396

    Article  CAS  PubMed  Google Scholar 

  • Strehl R, Kloth S, Aigner J, Steiner P, Minuth WW (1997) PCDAmp1, a new antigen at the interface of the embryonic collecting duct epithelium and the nephrogenic mesenchyme. Kidney Int 52:1469–1477

    Article  CAS  PubMed  Google Scholar 

  • Strehl R, Trautner V, Kloth S, Minuth WW (1999) Existence of a dense reticular meshwork surrounding the nephron inducer in neonatal rabbit kidney. Cell Tissue Res 298:539–548

    Article  CAS  PubMed  Google Scholar 

  • Wagers AJ (2012) The stem cell niche in regenerative medicine. Cell Stem Cell 10:362–369

    Article  CAS  PubMed  Google Scholar 

  • Watson AR, Hayes WN, Vondrak K, Ariceta G, Schmitt CP, Ekim M et al (2013) Factors influencing choice of renal replacement therapy in European Paediatrics Nephrology Units. Pediatr Nephrol 28:2361–2368

    Article  PubMed  Google Scholar 

  • Yokote S, Yokoo T (2012) Stem cells in kidney regeneration. Curr Med Chem 19:6009–6017

    Article  CAS  PubMed  Google Scholar 

  • Yokote S, Yokoo T (2013) Organogenesis for kidney regeneration. Curr Opin Organ Transplant 18:186–190

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular and Cellular Anatomy, University of Regensburg, University Street 31, 93053, Regensburg, Germany

    Will W. Minuth & Lucia Denk

Authors
  1. Will W. Minuth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lucia Denk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Will W. Minuth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Minuth, W.W., Denk, L. Structural links between the renal stem/progenitor cell niche and the organ capsule. Histochem Cell Biol 141, 459–471 (2014). https://doi.org/10.1007/s00418-014-1179-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-014-1179-0

Keywords

Search

Navigation