Human olfactory mesenchymal stromal cells co-expressing horizontal basal and ensheathing cell proteins in culture

Carlos Ayala-Grosso, Rosalinda Pieruzzini, Leslie Vargas-Saturno, José E. Cardier, .

Keywords: Olfactory mucosa, homeostasis, mesenchymal stem cells

Abstract

Introduction: The olfactory neuro-epithelium has an intrinsic capability of renewal during lifetime provided by the existence of globose and horizontal olfactory precursor cells. Additionally, mesenchymal stromal olfactory cells also support the homeostasis of the olfactory mucosa cell population. Under in vitro culture conditions with Dulbecco modified eagle/F12 medium supplemented with 10% fetal bovine serum, tissue biopsies from upper turbinate have generated an adherent population of cells expressing mainly mesenchymal stromal phenotypic markers. A closer examination of these cells has also found co-expression of olfactory precursors and ensheathing cell phenotypic markers. These results were suggestive of a unique property of olfactory mesenchymal stromal cells as potentially olfactory progenitor cells.
Objective: To study whether the expression of these proteins in mesenchymal stromal cells is modulated upon neuronal differentiation.
Materials and methods: We observed the phenotype of olfactory stromal cells under DMEM/F12 plus 10% fetal bovine serum in comparison to cells from spheres induced by serum-free medium plus growth factors inducers of neural progenitors.
Results: The expression of mesenchymal stromal (CD29+, CD73+, CD90+, CD45-), horizontal basal (ICAM-1/CD54+, p63+, p75NGFr+), and ensheathing progenitor cell (nestin+, GFAP+) proteins was determined in the cultured population by flow cytometry. The determination of Oct 3/4, Sox-2, and Mash-1 transcription factors, as well as the neurotrophins BDNF, NT3, and NT4 by RT-PCR in cells, was indicative of functional heterogeneity of the olfactory mucosa tissue sample.
Conclusions: Mesenchymal and olfactory precursor proteins were downregulated by serum-free medium and promoted differentiation of mesenchymal stromal cells into neurons and astroglial cells.

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  • Carlos Ayala-Grosso Unidad de Terapia Celular, Laboratorio de Patología Celular y Molecular, Centro de Medicina Experimental, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela
  • Rosalinda Pieruzzini Servicio de Neurorinología, Departamento de Otorrinolaringología, Hospital Militar Dr. Carlos Arvelo, Caracas, Venezuela
  • Leslie Vargas-Saturno Unidad de Terapia Celular, Laboratorio de Patología Celular y Molecular, Centro de Medicina Experimental, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela
  • José E. Cardier Unidad de Terapia Celular, Laboratorio de Patología Celular y Molecular, Centro de Medicina Experimental, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela

References

Schwob JE, Jang W, Holbrook EH, Holbrook EH, Lin B, Herrick DB, et al. Stem and progenitor cells of the mammalian olfactory epithelium: Taking poietic license. J Comp Neurol. 2017;525:1034-54. https://doi.org/10.1002/cne.24105

Schwob JE, Jang W, Holbrook EH. Stem cells of the olfactory epithelium. In: Rao MS, editor. Neural development and stem cells. 3rd edition. New York: Springer Science Business Media; 2012. p. 201-22.

Graziadei PP. Cell dynamics in the olfactory mucosa. Tissue Cell. 1973;5:113-31.

Jang W, Youngentob SL, Schwob JE. Globose basal cells required for reconstitution of olfactory epithelium after methyl bromide lesion. J Comp Neurol 2003;460:123-40. https://doi.org/10.1002/cne.10642

Carter LA, MacDonald JL, Roskams AJ. Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci. 2004;24:5670-83. https://doi.org/10.1523/JNEUROSCI.0330-04.2004

Fletcher RB, Prasol MS, Estrada J, Baudhuin A, Vranizan K, Choi YG, et al. p63 regulates olfactory stem cell self-renewal and differentiation. Neuron. 2011;72:748-59. https://doi.org/10.1016/j.neuron.2011.09.009

Holbrook EH, Wu E, Curry WT, Lin DT, Schwob JE. Immunohistochemical characterization of human olfactory tissue. Laryngoscope. 2011;121:1687-701. https://doi.org/10.1002/lary.21856

Deng J, Petersen BE, Steindler DA, Jorgensen ML, Laywell ED. Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells. 2006;24:1054-64. https://doi.org/10.1634/stemcells.2005-0370

Chase LG, Lakshmipathy U, Solchaga LA, Rao MS, Vemuri MC. A novel medium for the expansion of human mesenchymal stem cells. Stem Cell Res Ther. 2010;1:8. https://doi.org/10.1186/scrt8

Delorme B, Nivet E, Gaillard J, Häupl T, Ringe J, Devèze A, et al. The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev. 2010;19:853-66. https://doi.org/10.1089/scd.2009.0267

Lindsay SL, Riddell JS, Barnett SC. Olfactory mucosa for transplant-mediated repair: A complex tissue for a complex injury? Glia. 2010;58:125-34. https://doi.org/10.1002/glia.20917

Lindsay SL, Johnstone SA, Mountford JC, Sheikh S, Allan DB, Clark L, et al. Human mesenchymal stem cells isolated from olfactory biopsies but not bone enhance CNS myelination in vitro. Glia. 2013;61:368-82. https://doi.org/10.1002/glia.22440

Fernández VB, Romaniuk MA, Choi H, Labovsky V, Otaegui J, Chasseing NA. Mesenchymal stem cells and their use in therapy: What has been achieved? Differentiation. 2013;85:1-10. https://doi.org/10.1016/j.diff.2012.08.004

Lindsay SL, Toft A, Griffin J, M M Emraja A, Barnett SC, Riddell JS. Human olfactory mesenchymal stromal cell transplants promote remyelination and earlier improvement in gait co-ordination after spinal cord injury. Glia. 2017;65:639-56. https://doi.org/10.1002/glia.23117

Girard SD, Devéze A, Nivet E, Gepner B, Roman FS, Féron F. Isolating nasal olfactory stem cells from rodents or humans. J Vis Exp. 2011;54:1-5. https://doi.org/10.3791/2762

Hahn CG, Han LY, Rawson NE, Mirza N, Borgmann-Winter K, Lenox RH, et al. In vivo and in vitro neurogenesis in human olfactory epithelium. J Comp Neurol. 2005;483:154-63. https://doi.org/10.1002/cne.20424

Heng BC, Cao T, Stanton LW, Robson P, Olsen B. Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro. J Bone Miner Res 2004;19:1379-94. https://doi.org/10.1359/JBMR.040714

Hess DC, Borlongan CV. Stem cells and neurological diseases. Cell Prolif. 2007;41(Suppl.1):94-114. https://doi.org/10.1111/j.1365-2184.2008.00486.x

Marshall CT, Lu C, Winstead W, Zhang X, Winstead W, Zhang X, et al. The therapeutic potential of human olfactory-derived stem cells. Histol Histopathol. 2006;21:633-43. https://doi.org/10.14670/HH-21.633

Leung CT, Coulombe PA, Reed RR. Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci. 2007;10:720-6. https://doi.org/10.1038/nn1882

Nivet E, Vignes M, Girard SD, Pierrisnard C, Baril N, Devèze A, et al. Engraftment of human nasal olfactory stem cells restores neuroplasticity in mice with hippocampal lesions. J Clin Invest. 2011;121:2808-20. https://doi.org/10.1172/JCI44489

Ramón-Cueto A, Cordero MI, Santos-Benito FF, Ávila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron. 2000;25:425-35. https://doi.org/10.1016/S0896-6273(00)80905-8

Ayala-Grosso CA, Pieruzzini R, Diaz-Solano D, Wittig O, Abrante L, Vargas L, et al. Amyloid-aβ peptide in olfactory mucosa and mesenchymal stromal cells of mild cognitive impairment and Alzheimer’s disease patients. Brain Pathol. 2015;25:136-45. https://doi.org/10.1111/bpa.12169

Solís-Chagoyán H, Flores-Soto E, Reyes-García J, Valdés-Tovar M, Calixto E, Montaño LM, et al. Voltage-activated calcium channels as functional markers of mature neurons in human olfactory neuroepithelial cells: Implications for the study of neurodevelopment in neuropsychiatric disorders. Int J Mol Sci. 2016;17. https://doi.org/10.3390/ijms17060941

Cercós MG, Galván-Arrieta T, Valdés-Tovar M, Solís-Chagoyán H, Argueta J, Benítez-King G, et al. Abnormally increased secretion in olfactory neuronal precursors from a case of schizophrenia is modulated by melatonin: A pilot study. Int J Mol Sci. 2017;18. https://doi.org/10.3390/ijms18071439

Galván-Arrieta T, Trueta C, Cercós MG, Valdés-Tovar M, Alarcón S, Oikawa J, et al. The role of melatonin in the neurodevelopmental etiology of schizophrenia: A study in human olfactory neuronal precursors. J Pineal Res. 2017;63. https://doi.org/10.1111/jpi.12421

Lavoie J, Gassó Astorga P, Segal-Gavish H, Wu YC, Chung Y, Cascella NG, et al. The olfactory neural epithelium as a tool in neuroscience. Trends Mol Med. 2017;23:100-3. https://doi.org/10.1016/j.molmed.2016.12.010

Masurkar AV, Devanand DP. Olfactory dysfunction in the elderly: Basic circuitry and alterations with normal aging and Alzheimer’s disease. Curr Geriatr Rep. 2014;3:91-100. https://doi.org/10.1007/s13670-014-0080-y

Jiménez-Vaca AL, Benítez-King G, Ruiz V, Ramírez-Rodríguez GB, Hernández-de la Cruz B, Salamanca-Gómez FA, et al. Exfoliated human olfactory neuroepithelium: A source of neural progenitor cells. Mol Neurobiol. 2018;55:2516-23. https://doi.org/10.1007/s12035-017-0500-z

Doty RL. Olfactory dysfunction in Parkinson disease. Nat Rev Neurol. 2012;8:329-39. https://doi.org/10.1038/nrneurol.2012.80

Murrell W, Féron F, Wetzig A, Cameron N, Splatt K, Bellette B, et al. Multipotent stem cells from adult olfactory mucosa. Dev Dyn. 2005;233:496-515. https://doi.org/10.1002/dvdy.20360

Zhang X, Klueber KM, Guo Z, Lu C, Roisen FJ. Adult human olfactory neural progenitors cultured in defined medium. Exp Neurol. 2004;186:112-23. https://doi.org/10.1016/j.expneurol.2003.10.022

Lovell MA, Jafek BW, Moran DT, Rowley JC 3rd. Biopsy of human olfactory mucosa. An instrument and a technique. Arch Otolaryngol. 1982;108:247-9.

Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem.1997;64:295-312.

Murdoch B, Roskams AJ. Olfactory epithelium progenitors: Insights from transgenic mice and in vitro biology. J Mol Histol. 2007;38:581-99. https://doi.org/10.1007/s10735-007-9141-2

Wislet-Gendebien S, Bruyère F, Hans G, Leprince P, Moonen G, Rogister B. Nestin-positive mesenchymal stem cells favour the astroglial lineage in neural progenitors and stem cells by releasing active BMP4. BMC Neurosci. 2004;5:33. https://doi.org/10.1186/1471-2202-5-33

Wislet-Gendebien S, Leprince P, Moonen G, Rogister B. Regulation of neural markers nestin and GFAP expression by cultivated bone marrow stromal cells. J Cell Sci. 2003;116:3295-302. https://doi.org/10.1242/jcs.00639

Mark P, Kleinsorge M, Gaebel R, Lux CA, Toelk A, Pittermann E, et al. Human mesenchymal stem cells display reduced expression of CD105 after culture in medium. Stem Cells Int. 2013;2013:698076. https://doi.org/10.1155/2013/698076

Othman M, Lu C, Klueber K, Winstead W, Roisen F. Clonal analysis of adult human olfactory neurosphere forming cells. Biotech Histochem. 2005;80:189-200. https://doi.org/10.1080/10520290500469777

Krolewski RC, Jang W, Schwob JE. The generation of olfactory epithelial neurospheres in vitro predicts engraftment capacity following transplantation in vivo. Exp Neurol. 2011;229:308-23. https://doi.org/10.1016/j.expneurol.2011.02.014

How to Cite
1.
Ayala-Grosso C, Pieruzzini R, Vargas-Saturno L, Cardier JE. Human olfactory mesenchymal stromal cells co-expressing horizontal basal and ensheathing cell proteins in culture. biomedica [Internet]. 2020 Mar. 1 [cited 2024 May 18];40(1):72-88. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/4762
Published
2020-03-01
Section
Original articles

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