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Telocytes of the human adult trigeminal ganglion

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Abstract

Telocytes (TCs) are typically defined as cells with telopodes by their ultrastructural features. Their presence was reported in various organs, however little is known about their presence in human trigeminal ganglion. To address this issue, samples of trigeminal ganglia were tested by immunocytochemistry for CD34 and examined by transmission electron microscopy (TEM). We found that TCs are CD34 positive and form networks within the ganglion in close vicinity to microvessels and nerve fibers around the neuronal–glial units (NGUs). TEM examination confirmed the existence of spindle-shaped and bipolar TCs with one or two telopodes measuring between 15 to 53 μm. We propose that TCs are cells with stemness capacity which might contribute in regeneration and repair processes by: modulation of the stem cell activity or by acting as progenitors of other cells present in the normal tissue. In addition, further studies are needed to establish if they might influence the neuronal circuits.

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References

  • Albulescu R, Tanase C, Codrici E, Popescu DI, Cretoiu SM, Popescu LM. The secretome of myocardial telocytes modulates the activity of cardiac stem cells. J Cell Mol Med. 2015;19:1783–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bei Y, Wang F, Yang C, Xiao J. Telocytes in regenerative medicine. J Cell Mol Med. 2015a;19:1441–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bei Y, Zhou Q, Fu S, Lv D, Chen P, Chen Y, et al. Cardiac telocytes and fibroblasts in primary culture: different morphologies and immunophenotypes. PLoS One. 2015b;10:e0115991.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bei Y, Wang F, Yang C, Xiao J. Telocytes in regenerative medicine. J Cell Mol Med. 2015a.

  • Campeanu RA, Radu BM, Cretoiu SM, Banciu DD, Banciu A, Cretoiu D, et al. Near-infrared low-level laser stimulation of telocytes from human myometrium. Lasers Med Sci. 2014;29:1867–74.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cantarero I, Luesma MJ, Junquera C. The primary cilium of telocytes in the vasculature: electron microscope imaging. J Cell Mol Med. 2011;15:2594–600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chotinantakul K, Leeanansaksiri W. Hematopoietic stem cell development, niches, and signaling pathways. Bone Marrow Res. 2012;2012:270425.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cismasiu VB, Popescu LM. Telocytes transfer extracellular vesicles loaded with microRNAs to stem cells. J Cell Mol Med. 2015;19:351–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cismasiu VB, Radu E, Popescu LM. miR-193 expression differentiates telocytes from other stromal cells. J Cell Mol Med. 2011;15:1071–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cretoiu D, Cretoiu SM. Telocytes in the reproductive organs: current understanding and future challenges. Semin Cell Dev Biol. 2016.

  • Cretoiu SM, Popescu LM. Telocytes revisited. Biomolecular Concepts. 2014;5:353–69.

    Article  CAS  PubMed  Google Scholar 

  • Cretoiu D, Cretoiu SM, Simionescu AA, Popescu LM. Telocytes, a distinct type of cell among the stromal cells present in the lamina propria of jejunum. Histol Histopathol. 2012;27:1067–78.

    CAS  PubMed  Google Scholar 

  • Cretoiu SM, Cretoiu D, Marin A, Radu BM, Popescu LM. Telocytes: ultrastructural, immunohistochemical and electrophysiological characteristics in human myometrium. Reproduction. 2013;145:357–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cretoiu D, Hummel E, Zimmermann H, Gherghiceanu M, Popescu LM. Human cardiac telocytes: 3D imaging by FIB-SEM tomography. J Cell Mol Med. 2014;18:2157–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cretoiu D, Gherghiceanu M, Hummel E, Zimmermann H, Simionescu O, Popescu LM. FIB-SEM tomography of human skin telocytes and their extracellular vesicles. J Cell Mol Med. 2015a;19:714–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cretoiu SM, Radu BM, Banciu A, Banciu DD, Cretoiu D, Ceafalan LC, et al. Isolated human uterine telocytes: immunocytochemistry and electrophysiology of T-type calcium channels. Histochem Cell Biol. 2015b;143:83–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz-Flores L, Gutierrez R, Saez FJ, Diaz-Flores Jr L, Madrid JF. Telocytes in neuromuscular spindles. J Cell Mol Med. 2013;17:457–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz-Flores L, Gutierrez R, Garcia MP, Saez FJ, Diaz-Flores Jr L, Valladares F, et al. CD34+ stromal cells/fibroblasts/fibrocytes/telocytes as a tissue reserve and a principal source of mesenchymal cells. Location, morphology, function and role in pathology. Histol Histopathol. 2014;29:831–70.

    CAS  PubMed  Google Scholar 

  • Diaz-Flores L, Gutierrez R, Garcia MP, Gonzalez M, Saez FJ, Aparicio F, et al. Human resident CD34+ stromal cells/telocytes have progenitor capacity and are a source of alphaSMA+ cells during repair. Histol Histopathol. 2015a;30:615–27.

    CAS  PubMed  Google Scholar 

  • Diaz-Flores L, Gutierrez R, Garcia MP, Gonzalez M, Diaz-Flores L Jr, Madrid JF. Telocytes as a source of progenitor cells in regeneration and repair through granulation tissue. Curr Stem Cell Res Ther. 2015a

  • Diaz-Flores L, Gutierrez R, Diaz-Flores L, Gomez MG Jr, Saez FJ, Madrid JF. Behaviour of telocytes during physiopathological activation. Semin Cell Dev Biol. 2016.

  • Fertig ET, Gherghiceanu M, Popescu LM. Extracellular vesicles release by cardiac telocytes: electron microscopy and electron tomography. J Cell Mol Med. 2014;18:1938–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gherghiceanu M, Popescu LM. Cardiac telocytes—their junctions and functional implications. Cell Tissue Res. 2012;348:265–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haslene-Hox H, Tenstad O, Wiig H. Interstitial fluid-a reflection of the tumor cell microenvironment and secretome. Biochim Biophys Acta. 2013;1834:2336–46.

    Article  CAS  PubMed  Google Scholar 

  • Ibba-Manneschi L, Rosa I, Manetti M. Telocyte implications in human pathology: an overview. Semin Cell Dev Biol. 2016

  • Kai-Kai MA. Cytochemistry of the trigeminal and dorsal root ganglia and spinal cord of the rat. Comp Biochem Physiol A Comp Physiol. 1989;93:183–93.

    Article  CAS  PubMed  Google Scholar 

  • Manetti M, Guiducci S, Ruffo M, Rosa I, Faussone-Pellegrini MS, Matucci-Cerinic M, et al. Evidence for progressive reduction and loss of telocytes in the dermal cellular network of systemic sclerosis. J Cell Mol Med. 2013;17:482–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manetti M, Rosa I, Messerini L, Guiducci S, Matucci-Cerinic M, Ibba-Manneschi L. A loss of telocytes accompanies fibrosis of multiple organs in systemic sclerosis. J Cell Mol Med. 2014;18:253–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manetti M, Rosa I, Messerini L, Ibba-Manneschi L. Telocytes are reduced during fibrotic remodelling of the colonic wall in ulcerative colitis. J Cell Mol Med. 2015;19:62–73.

    Article  PubMed  PubMed Central  Google Scholar 

  • Manole CG, Gherghiceanu M, Simionescu O. Telocyte dynamics in psoriasis. J Cell Mol Med. 2015

  • Maxwell DS. Fine structure of the normal trigeminal ganglion in the cat and monkey. J Neurosurg. 1967;26:127–31.

    Article  PubMed  Google Scholar 

  • Milia AF, Ruffo M, Manetti M, Rosa I, Conte D, Fazi M, et al. Telocytes in Crohn’s disease. J Cell Mol Med. 2013;17:1525–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Old EA, Clark AK, Malcangio M. The role of glia in the spinal cord in neuropathic and inflammatory pain. Handb Exp Pharmacol. 2015;227:145–70.

    Article  PubMed  Google Scholar 

  • Popescu LM, Faussone-Pellegrini MS. Telocytes—a case of serendipity: the winding way from interstitial cells of Cajal (ICC), via interstitial Cajal-like cells (ICLC) to telocytes. J Cell Mol Med. 2010;14:729–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popescu LM, Fertig ET, Gherghiceanu M. Reaching out: junctions between cardiac telocytes and cardiac stem cells in culture. J Cell Mol Med. 2015.

  • Richter M, Kostin S. The failing human heart is characterized by decreased numbers of telocytes as result of apoptosis and altered extracellular matrix composition. J Cell Mol Med. 2015;19:2597–606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roatesi I, Radu BM, Cretoiu D, Cretoiu SM. Uterine telocytes: a review of current knowledge. Biol Reprod. 2015;93:10.

    Article  PubMed  Google Scholar 

  • Rusu MC. Skin telopodes. Romanian J Morphol Embryol = Rev Roum Morphol Embryol. 2014;55:723–4.

    Google Scholar 

  • Rusu MC, Pop F, Hostiuc S, Dermengiu D, Lala AI, Ion DA, et al. The human trigeminal ganglion: c-kit positive neurons and interstitial cells. Ann Anat = Anat Anz: Off Organ Anat Ges. 2011;193:403–11.

    Article  CAS  Google Scholar 

  • Rusu MC, Jianu AM, Mirancea N, Didilescu AC, Manoiu VS, Paduraru D. Tracheal telocytes. J Cell Mol Med. 2012a;16:401–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rusu MC, Jianu AM, Pop F, Hostiuc S, Leonardi R, Curca GC. Immunolocalization of 200 kDa neurofilaments in human cardiac endothelial cells. Acta Histochem. 2012b;114:842–5.

    Article  CAS  PubMed  Google Scholar 

  • Rusu MC, Nicolescu MI, Jianu AM, Lighezan R, Manoiu VS, Paduraru D. Esophageal telocytes and hybrid morphologies. Cell Biol Int. 2012c;36:1079–88.

    Article  PubMed  Google Scholar 

  • Rusu MC, Pop F, Hostiuc S, Curca GC, Jianu AM, Paduraru D. Telocytes form networks in normal cardiac tissues. Histol Histopathol. 2012d;27:807–16.

    CAS  PubMed  Google Scholar 

  • Rusu MC, Hostiuc S, Loreto C, Paduraru D. Nestin immune labeling in human adult trigeminal ganglia. Acta Histochem. 2013;115:86–8.

    Article  CAS  PubMed  Google Scholar 

  • Rusu MC, Folescu R, Manoiu VS, Didilescu AC. Suburothelial interstitial cells. Cells Tissues Organs. 2014a;199:59–72.

    Article  CAS  PubMed  Google Scholar 

  • Rusu MC, Loreto C, Manoiu VS. Network of telocytes in the temporomandibular joint disc of rats. Acta Histochem. 2014b;116:663–8.

    Article  PubMed  Google Scholar 

  • Rusu MC, Mănoiu VM, Mirancea N, Nini G. Quiescent satellite glial cells of the adult trigeminal ganglion. Cent Eur J Med. 2014c;9:500–4.

    Google Scholar 

  • Sasai N, Briscoe J. Primary cilia and graded Sonic Hedgehog signaling. Wiley Interdiscip Rev Dev Biol. 2012;1:753–72.

    Article  CAS  PubMed  Google Scholar 

  • Song D, Cretoiu D, Zheng M, Qian M, Zhang M, Cretoiu SM, et al. Comparison of Chromosome 4 gene expression profile between lung telocytes and other local cell types. J Cell Mol Med. 2015

  • Sun X, Zheng M, Zhang M, Qian M, Zheng Y, Li M, et al. Differences in the expression of chromosome 1 genes between lung telocytes and other cells: mesenchymal stem cells, fibroblasts, alveolar type II cells, airway epithelial cells and lymphocytes. J Cell Mol Med. 2014;18:801–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thalakoti S, Patil VV, Damodaram S, Vause CV, Langford LE, Freeman SE, et al. Neuron-glia signaling in trigeminal ganglion: implications for migraine pathology. Headache. 2007;47:1008–23. discussion 1024-1005.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vannucchi MG, Traini C, Manetti M, Ibba-Manneschi L, Faussone-Pellegrini MS. Telocytes express PDGFRalpha in the human gastrointestinal tract. J Cell Mol Med. 2013;17:1099–108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vannucchi MG, Bani D, Faussone-Pellegrini M-S. Telocytes contribute as cell progenitors and differentiation inductors in tissue regeneration. Curr Stem Cell Res Ther. 2015

  • Wallingford JB, Mitchell B. Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes Dev. 2011;25:201–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Ye L, Jin M, Wang X. Global analyses of chromosome 17 and 18 genes of lung telocytes compared with mesenchymal stem cells, fibroblasts, alveolar type II cells, airway epithelial cells, and lymphocytes. Biol Direct. 2015;10:9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang J, Chi C, Liu Z, Yang G, Shen ZJ, Yang XJ. Ultrastructure damage of oviduct telocytes in rat model of acute salpingitis. J Cell Mol Med. 2015

  • Zhang HQ, Lu SS, Xu T, Feng YL, Li H, Ge JB. Morphological evidence of telocytes in mice aorta. Chin Med J. 2015;128:348–52.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng M, Sun X, Zhang M, Qian M, Zheng Y, Li M, et al. Variations of chromosomes 2 and 3 gene expression profiles among pulmonary telocytes, pneumocytes, airway cells, mesenchymal stem cells and lymphocytes. J Cell Mol Med. 2014;18:2044–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Wei L, Zhong C, Fu S, Bei Y, Huica RI, et al. Cardiac telocytes are double positive for CD34/PDGFR-alpha. J Cell Mol Med. 2015;19:2036–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Zheng M, Song D, Ye L, Wang X. Global comparison of chromosome X genes of pulmonary telocytes with mesenchymal stem cells, fibroblasts, alveolar type II cells, airway epithelial cells, and lymphocytes. J Transl Med. 2015;13:318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was partially supported by grants of the Romanian National Authority for Scientific Research, CNCS—UEFISCDI, project numbers 82/2012 and 194/2014.

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Authors and Affiliations

  1. Division of Anatomy, Faculty of Dental Medicine, Carol Davila University of Medicine and Pharmacy, Bucharest, Romania

    Mugurel Constantin Rusu & Alexandra Diana Vrapciu

  2. International Society of Regenerative Medicine and Surgery (ISRMS), Bucharest, Romania

    Mugurel Constantin Rusu

  3. MEDCENTER – Center of Excellence in Laboratory Medicine and Pathology, Bucharest, Romania

    Mugurel Constantin Rusu

  4. Division of Cellular and Molecular Biology and Histology, Department 2 Morphological Sciences, Faculty of Medicine, Carol Davila University of Medicine and Pharmacy, Bucharest, Romania

    Dragos Cretoiu & Sanda Maria Cretoiu

  5. Victor Babes National Institute of Pathology, Bucharest, Romania

    Dragos Cretoiu & Sanda Maria Cretoiu

  6. Division of Legal Medicine and Bioethics, Department 2 Morphological Sciences, Faculty of Medicine, Carol Davila University of Medicine and Pharmacy, Bucharest, Romania

    Sorin Hostiuc & Dan Dermengiu

  7. Department of Forensic Pathology, National Institute of Legal Medicine, Bucharest, Romania

    Dan Dermengiu

  8. Department of Cellular and Molecular Biology, National Institute of Research and Development for Biological Sciences, Bucharest, Romania

    Vasile Sorin Manoiu

  9. Institute of Biology of Bucharest, The Romanian Academy, Bucharest, Romania

    Nicolae Mirancea

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  1. Mugurel Constantin Rusu
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  2. Dragos Cretoiu
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  3. Alexandra Diana Vrapciu
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  4. Sorin Hostiuc
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  5. Dan Dermengiu
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  6. Vasile Sorin Manoiu
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  7. Sanda Maria Cretoiu
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Correspondence to Sanda Maria Cretoiu or Nicolae Mirancea.

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Mugurel Constantin Rusu and Dragos Cretoiu contributed equally to this work.

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Rusu, M.C., Cretoiu, D., Vrapciu, A.D. et al. Telocytes of the human adult trigeminal ganglion. Cell Biol Toxicol 32, 199–207 (2016). https://doi.org/10.1007/s10565-016-9328-y

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  • DOI: https://doi.org/10.1007/s10565-016-9328-y

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