Central European Journal of Medicine

, Volume 9, Issue 3, pp 500–504 | Cite as

Quiescent satellite glial cells of the adult trigeminal ganglion

  • Mugurel C. Rusu
  • Valentina M. Mănoiu
  • Nicolae Mirancea
  • Gheorghe Nini
Research Article


Sensory ganglia comprise functional units built up by neurons and satellite glial cells (SGCs). In animal species there was proven the presence of neuronoglial progenitor cells in adult samples. Such neural crest-derived progenitors were found in immunohistochemistry (IHC). These findings were not previously documented in transmission electron microscopy (TEM). It was thus aimed to assess in TEM if cells of the human adult trigeminal ganglion indeed have ultrastructural features to qualify for a progenitor, or quiescent phenotype. Trigeminal ganglia were obtained from fifteen adult donor cadavers. In TEM, cells with heterochromatic nuclei, a pancytoplasmic content of free ribosomes, few perinuclear mitochondria, poor developed endoplasmic reticulum, lack of Golgi complexes and membrane trafficking specializations, were found included in the neuronal envelopes built-up by SGCs. The ultrastructural pattern was strongly suggestive for these cells being quiescent progenitors. However, further experiments should correlate the morphologic and immune phenotypes of such cells.


Sensory ganglion Transmission electron microscopy Satellite glial cells Progenitor cells Human trigeminal ganglion 


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  1. [1]
    Lazarov N. E., Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus, Prog Neurobiol, 2002, 66, 19–59PubMedCrossRefGoogle Scholar
  2. [2]
    van Velzen M., Laman J. D., Kleinjan A., Poot A., Osterhaus A. D., Verjans G. M., Neuron-interacting satellite glial cells in human trigeminal ganglia have an APC phenotype, J Immunol, 2009, 183, 2456–2461PubMedCrossRefGoogle Scholar
  3. [3]
    Durham P. L., Garrett F. G., Development of functional units within trigeminal ganglia correlates with increased expression of proteins involved in neuron-glia interactions, Neuron Glia Biol, 2010, doi:10.1017/S1740925X100002321-11Google Scholar
  4. [4]
    Damodaram S., Thalakoti S., Freeman S. E., Garrett F. G., Durham P. L., Tonabersat inhibits trigeminal ganglion neuronal-satellite glial cell signaling, Headache, 2009, 49, 5–20PubMedCentralPubMedCrossRefGoogle Scholar
  5. [5]
    Levy Bde F., Cunha Jdo C., Chadi G., Cellular analysis of S100Beta and fibroblast growth factor-2 in the dorsal root ganglia and sciatic nerve of rodents. focus on paracrine actions of activated satellite cells after axotomy, Int J Neurosci, 2007, 117, 1481–1503PubMedCrossRefGoogle Scholar
  6. [6]
    Capuano A., De Corato A., Lisi L., Tringali G., Navarra P., Dello Russo C., Proinflammatoryactivated trigeminal satellite cells promote neuronal sensitization: relevance for migraine pathology, Mol Pain, 2009, 5, 43PubMedCentralPubMedCrossRefGoogle Scholar
  7. [7]
    Takeda M., Takahashi M., Matsumoto S., Contribution of the activation of satellite glia in sensory ganglia to pathological pain, Neurosci Biobehav Rev, 2009, 33, 784–792PubMedCrossRefGoogle Scholar
  8. [8]
    Rusu M. C., Pop F., Hostiuc S., Dermengiu D., Lala A. I., Ion D. A., Manoiu V. S., Mirancea N., The human trigeminal ganglion: c-kit positive neurons and interstitial cells, Ann Anat, 2011, 193, 403–411PubMedCrossRefGoogle Scholar
  9. [9]
    Lagares A., Li H. Y., Zhou X. F., Avendano C., Primary sensory neuron addition in the adult rat trigeminal ganglion: evidence for neural crest glioneuronal precursor maturation, J Neurosci, 2007, 27, 7939–7953PubMedCrossRefGoogle Scholar
  10. [10]
    Li H. Y., Say E. H., Zhou X. F., Isolation and characterization of neural crest progenitors from adult dorsal root ganglia, Stem Cells, 2007, 25, 2053–2065PubMedCrossRefGoogle Scholar
  11. [11]
    Singh R. P., Cheng Y. H., Nelson P., Zhou F. C., Retentive multipotency of adult dorsal root ganglia stem cells, Cell Transplant, 2009, 18, 55–68PubMedCentralPubMedCrossRefGoogle Scholar
  12. [12]
    Yu L., Ding Y., Spencer A., Ma J., Lu R., Rudkin B. B., Yuan C., Dorsal root ganglion progenitors differentiate to gamma-aminobutyric acid- and choline acetyltransferase-positive neurons, Neural Regen Res, 2012, 7, 485–491Google Scholar
  13. [13]
    Vukojevic K., Skobic H., Saraga-Babic M., Proliferation and differentiation of glial and neuronal progenitors in the development of human spinal ganglia, Differentiation, 2009, 78, 91–98PubMedCrossRefGoogle Scholar
  14. [14]
    Aihara Y., Hayashi Y., Hirata M., Ariki N., Shibata S., Nagoshi N., Nakanishi M., Ohnuma K., Warashina M., Michiue T., Uchiyama H., Okano H., Asashima M., Furue M. K., Induction of neural crest cells from mouse embryonic stem cells in a serum-free monolayer culture, Int J Dev Biol, 2010, 54, 1287–1294PubMedCrossRefGoogle Scholar
  15. [15]
    Vukojevic K., Petrovic D., Saraga-Babic M., Nestin expression in glial and neuronal progenitors of the developing human spinal ganglia, Gene Expr Patterns, 2010, 10, 144–151PubMedCrossRefGoogle Scholar
  16. [16]
    Calderone A., Nestin+ cells and healing the infarcted heart, Am J Physiol Heart Circ Physiol, 2012, 302, H1–9PubMedCrossRefGoogle Scholar
  17. [17]
    Rusu M. C., Hostiuc S., Loreto C., Paduraru D., Nestin immune labeling in human adult trigeminal ganglia, Acta Histochem, 2013, 115, 86–88PubMedCrossRefGoogle Scholar
  18. [18]
    Wiese C., Rolletschek A., Kania G., Blyszczuk P., Tarasov K. V., Tarasova Y., Wersto R. P., Boheler K. R., Wobus A. M., Nestin expression-a property of multi-lineage progenitor cells?, Cell Mol Life Sci, 2004, 61, 2510–2522PubMedCrossRefGoogle Scholar
  19. [19]
    Gherghiceanu M., Popescu L. M., Cardiomyocyte precursors and telocytes in epicardial stem cell niche: electron microscope images, J Cell Mol Med, 2010, 14, 871–877PubMedCrossRefGoogle Scholar
  20. [20]
    Popescu L. M., Manole C. G., Gherghiceanu M., Ardelean A., Nicolescu M. I., Hinescu M. E., Kostin S., Telocytes in human epicardium, J Cell Mol Med, 2010, 14, 2085–2093PubMedCrossRefGoogle Scholar
  21. [21]
    Brohl D., Vasyutina E., Czajkowski M. T., Griger J., Rassek C., Rahn H. P., Purfurst B., Wende H., Birchmeier C., Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals, Dev Cell, 2012, 23, 469–481PubMedCrossRefGoogle Scholar
  22. [22]
    Didilescu A. C., Rusu M. C., Nini G., Dental pulp as a stem cell reservoir, Rom J Morphol Embryol, 2013, 54, 473–478PubMedGoogle Scholar
  23. [23]
    Rusu M. C., Dermengiu D., Loreto C., Motoc A. G., Pop E., Astrocitary niches in human adult medulla oblongata, Acta Histochem, 2013, 115, 296–300PubMedCrossRefGoogle Scholar
  24. [24]
    Zammit P. S., Partridge T. A., Yablonka-Reuveni Z., The skeletal muscle satellite cell: the stem cell that came in from the cold, J Histochem Cytochem, 2006, 54, 1177–1191PubMedCrossRefGoogle Scholar
  25. [25]
    Rusu M. C., Pop F., Hostiuc S., Dermengiu D., Lala A. I., Ion D. A., Manoiu V. S., Mirancea N., The human trigeminal ganglion: c-kit positive neurons and interstitial cells, Ann Anat, 2011, 193, 403–411PubMedCrossRefGoogle Scholar
  26. [26]
    Shi X., Garry D. J., Muscle stem cells in development, regeneration, and disease, Genes Dev, 2006, 20, 1692–1708PubMedCrossRefGoogle Scholar
  27. [27]
    Matsuura S., Shimizu K., Shinoda M., Ohara K., Ogiso B., Honda K., Katagiri A., Sessle B. J., Urata K., Iwata K., Mechanisms underlying ectopic persistent tooth-pulp pain following pulpal inflammation, PLoS One, 2013, 8, e52840PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Mugurel C. Rusu
    • 1
    • 2
    • 3
  • Valentina M. Mănoiu
    • 4
  • Nicolae Mirancea
    • 3
  • Gheorghe Nini
    • 5
  1. 1.„Carol Davila” University of Medicine and PharmacyBucharestRomania
  2. 2.MEDCENTER — Center of Excellence in Laboratory Medicine and PathologyBucharestRomania
  3. 3.Institute of Biology of Bucharest — The Romanian AcademyBucharestRomania
  4. 4.Faculty of GeographyUniversity of BucharestBucharestRomania
  5. 5.Faculty of Medicine, Pharmacy and Dental Medicine“Vasile Goldiş” Western UniversityAradRomania

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