Generation of motor neurons from human amygdala-derived neural stem-like cells

Document Type : Original Article

Authors

1 Shefa Neuroscience Research Center, Khatam Alanbia Hospital, Tehran, Iran

2 Department of Neuroscience, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran

3 Department of Neurosurgery, Westfälische Wilhelms-Universität Münster, Münster, Germany

4 Department of Neuroscience, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

5 Department of Neurology, Westfälische Wilhelms-Universität Münster, Münster, Germany

6 Epilepsy Research Center, Westfälische Wilhelms-Universität Münster, Münster, Germany

Abstract

Objective(s): Among several cell sources, adult human neural stem/progenitor cells (hNS/PCs) have been considered outstanding cells for performing mechanistic studies in in vitro and in vivo models of neurological disorders as well as for potential utility in cell-based therapeutic approaches. Previous studies addressed the isolation and culture of hNS/PCs from human neocortical and hippocampal tissues. However, little data are available on hNS/PCs obtained from the adult human amygdala.
Materials and Methods: The present study explored the capacity of the amygdala harvested from resected brain tissues of patients with medically refractory epilepsy to generate neurosphere-like bodies and motor neuron-like cells.
Results: Although the proliferation process was slow, a considerable amount of cells was obtained after the 3rd passage. In addition, the cells could generate motor neuron-like cells under appropriate culture conditions.
Conclusion: Isolation and culture of these cells enable us to improve our knowledge of the role of the amygdala in some neurological and psychological disorders and provide a novel source for therapeutic cell transplantation.

Keywords

Main Subjects

References

1. Kennea NL, Mehmet H. Neural stem cells. J Pathol 2002;197:536-550.
2. Vescovi AL, Parati EA, Gritti A, Poulin P, Ferrario M, Wanke E, Frölichsthal-Schoeller P, Cova L, Arcellana-Panlilio M, Colombo A, Galli R. Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp Neurol 1999;156:71-83.
3. Pollard SM, Conti L, Sun Y, Goffredo D, Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex 2006;16 Suppl 1:i112-120.
4. McLaren A. Ethical and social considerations of stem cell research. Nature 2001;414:129-131.
5. Delcroix GJ, Schiller PC, Benoit JP, Montero-Menei CN. Adult cell therapy for brain neuronal damages and the role of tissue engineering. Biomaterials 2010;31:2105-2120.
6. Taupin P, Gage FH. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 2002;69:745-749.
7. Aligholi H, Hassanzadeh G, Azari H, Rezayat SM, Mehr SE, Akbari M, Attari F, Khaksarian M, Gorji A. A new and safe method for stereotactically harvesting neural stem/progenitor cells from the adult rat subventricular zone. J Neurosci Methods 2014;225:81-89.
8. Aligholi H, Rezayat SM, Azari H, Ejtemaei Mehr S, Akbari M, Modarres Mousavi SM, Attari F, Alipour F, Hassanzadeh G, Gorji A. Preparing neural stem/progenitor cells in PuraMatrix hydrogel for transplantation after brain injury in rats: A comparative methodological study. Brain Res 2016;1642:197-208.
9. Kokoeva MV, Yin H, Flier JS. Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol 2007;505:209-220.
10.    Sahab Negah S, Khooei A, Samini F, Gorji A. Laminin-derived Ile-Lys-Val-ala-Val: a promising bioactive peptide in neural tissue engineering in traumatic brain injury. Cell Tissue Res 2018;371:223-236.
11.    Arsenijevic Y, Villemure JG, Brunet JF, Bloch JJ, Déglon N, Kostic C, Zurn A, Aebischer P. Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Exp Neurol 2001;170:48-62.
12.    Pagano SF, Impagnatiello F, Girelli M, Cova L, Grioni E, Onofri M, Cavallaro M, Etteri S, Vitello F, Giombini S, Solero CL, Parati EA. Isolation and characterization of neural stem cells from the adult human olfactory bulb. Stem Cells 2000;18:295-300.
13.    Sanai N, Tramontin AD, Quiñones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-García Verdugo J, Berger MS, Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004;427:740-744.
14.    Johansson CB, Svensson M, Wallstedt L, Janson AM, Frisén J. Neural stem cells in the adult human brain. Exp Cell Res 1999;253:733-736.
15.    Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, O’Brien TF, Kusakabe M, Steindler DA. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 1999;156:333-344.
16.    Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G 2nd, Jiang L, Kang J, Nedergaard M, Goldman SA. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 2003;9:439-447.
17.    Negah SS, Aligholi H, Khaksar Z, Kazemi H, Mousavi SM, Safahani M, Dowom PB, Gorji A. Survival, proliferation, and migration of human meningioma stem-like cells in a nanopeptide scaffold. Iran J Basic Med Sci 2016;19:1271-1278.
18.    Seymour B, Dolan R. Emotion, decision making, and the amygdala. Neuron 2008;58:662-671.
19.    Gloor P, Olivier A, Quesney LF, Andermann F, Horowitz S. The role of the limbic system in experiential phenomena of temporal lobe epilepsy. Ann Neurol 1982;12:129-144.
20.    Hood TW, Siegfried J, Wieser HG. The role of stereotactic amygdalotomy in the treatment of temporal lobe epilepsy associated with behavioral disorders. Appl Neurophysiol 1983;46:19-25.
21.    Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, Saphier G, Leibel R, Goland R, Wichterle H, Henderson CE, Eggan K. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008;321:1218-1221.
22.    Hester ME, Murtha MJ, Song S, Rao M, Miranda CJ, Meyer K, Tian J, Boulting G, Schaffer DV, Zhu MX, Pfaff SL, Gage FH, Kaspar BK. Rapid and efficient generation of functional motor neurons from human pluripotent stem cells using gene delivered transcription factor codes. Mol Ther 2011;19:1905-1912.
23.    Qu Q, Li D, Louis KR, Li X, Yang H, Sun Q, Crandall SR, Tsang S, Zhou J, Cox CL, Cheng J, Wang F. High-efficiency motor neuron differentiation from human pluripotent stem cells and the function of Islet-1. Nat Commun 2014;5:3462-3449.
24.    Graebenitz S, Kedo O, Speckmann EJ, Gorji A, Panneck H, Hans V, Palomero-Gallagher N, Schleicher A, Zilles K, Pape HC. Interictal-like network activity and receptor expression in the epileptic human lateral amygdala. Brain 2011;134:2929-2947.
25.    Mori H, Ninomiya K, Kino-oka M, Shofuda T, Islam MO, Yamasaki M, Okano H, Taya M, Kanemura Y. Effect of neurosphere size on the growth rate of human neural stem/progenitor cells. J Neurosci Res 2006;84:1682-1691.
26.    Muhr J, Graziano E, Wilson S, Jessell TM, Edlund T. Convergent inductive signals specify midbrain, hindbrain, and spinal cord identity in gastrula stage chick embryos. Neuron 1999;23:689-702.
27.    Faravelli I, Bucchia M, Rinchetti P, Nizzardo M, Simone C, Frattini E, Corti S. Motor neuron derivation from human embryonic and induced pluripotent stem cells: experimental approaches and clinical perspectives. Stem Cell Res Ther 2014;5:1-13.
28.    Lamas NJ, Johnson-Kerner B, Roybon L, Kim YA, Garcia-Diaz A, Wichterle H, Henderson CE. Neurotrophic requirements of human motor neurons defined using amplified and purified stem cell-derived cultures. PLoS One 2014;9:e110324.
29.    Sahab Negah S, Khaksar Z, Aligholi H, Mohammad Sadeghi S, Modarres Mousavi SM, Kazemi H, Jahanbazi Jahan-Abad A, Gorji A. Enhancement of Neural Stem Cell Survival, Proliferation, Migration, and Differentiation in a Novel Self-Assembly Peptide Nanofibber Scaffold. Mol Neurobiol 2017;54:8050-8062.
30.    Park D, Xiang AP, Mao FF, Zhang L, Di CG, Liu XM, Shao Y, Ma BF, Lee JH, Ha KS, Walton N, Lahn BT. Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 2010;28:2162-2171.
31.    Pevny LH, Nicolis SK. Sox2 roles in neural stem cells. Int J Biochem Cell Biol 2010;42:421-424.
32.    Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-716.
33.    Wichterle H, Lieberam I, Porter JA, Jessell TM. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002;110:385-397.
34.    Jaiswal MK. Therapeutic opportunities and challenges of induced pluripotent stem cells-derived motor neurons for treatment of amyotrophic lateral sclerosis and motor neuron disease. Neural Regen Res 2017;12:723-736.
35.    Laxer KD, Trinka E, Hirsch LJ, Cendes F, Langfitt J, Delanty N, Resnick T, Benbadis SR. The consequences of refractory epilepsy and its treatment. Epilepsy Behav 2014;37:59-70.
36.    Thodeson DM, Brulet R, Hsieh J. Neural stem cells and epilepsy: functional roles and disease-in-a-dish models. Cell Tissue Res 2018;371:47-54.
37.    Rao G, Mashkouri S, Aum D, Marcet P, Borlongan CV. Contemplating stem cell therapy for epilepsy-induced neuropsychiatric symptoms. Neuropsychiatr Dis Treat 2017;13:585-596.
38.    Aligholi H, Hassanzadeh G, Azari H, Rezayat SM, Mehr SE, Akbari M, Attari F, Khaksarian M, Gorji A. A new and safe method for stereotactically harvesting neural stem/progenitor cells from the adult rat subventricular zone. J Neurosci Methods 2014;225:81-89.
39.    Soliman MA, Aboharb F, Zeltner N, Studer L. Pluripotent stem cells in neuropsychiatric disorders. Mol Psychiatry 2017;22:1241-1249.
40.    Jahanbazi Jahan-Abad A, Sahab Negah S, Hosseini Ravandi H, Ghasemi S, Borhani-Haghighi M, Stummer W, Gorji A, Khaleghi Ghadiri M. Human neural stem/progenitor cells derived from epileptic human brain in a self-assembling peptide nanoscaffold improve traumatic brain injury in rats. Mol Neurobiol [Epub ahead of print] doi: 10.1007/s12035-018-1050-1058.
Iranian Journal of Basic Medical Sciences
Volume 21, Issue 11
November 2018
Pages 1155-1160

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