Expression of functional γ-aminobutyric acid type A receptors in schwann-like adult stem cells

Journal of Molecular Neuroscience

Volumn 47, Issue 3, 2012, Pages 619-630

  Faroni, Alessandro ^a   Terenghi, Giorgio ^a   Magnaghi, Valerio ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Adipose and bone marrow stem cells; GABA; Gliotransmitters; Nerve regeneration; Schwann cells; Transdifferentiation

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; 4 AMINOBUTYRIC ACID B RECEPTOR; BETA ACTIN; BETA TUBULIN; MUSCIMOL; MYELIN;

ADIPOSE TISSUE; ADULT STEM CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GLIA; HEMATOPOIETIC STEM CELL; MALE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RAT; SCHWANN CELL; UPREGULATION;

ADIPOSE TISSUE; ADULT STEM CELLS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; HEMATOPOIETIC STEM CELLS; NEUROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SCHWANN CELLS; SCIATIC NERVE;

EID: 84863868221     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-011-9698-9     Document Type: Article

References (55)

1. Anghileri E,Marconi S, Pignatelli A et al (2008) Neuronal differentiation potential of human adipose-derived mesenchymal stem cells. Stem Cells Dev 175:909-916
2. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 39:728-739
3. Bhisitkul RB, Villa JE, Kocsis JD (1987) Axonal GABA receptors are selectively present on normal and regenerated sensory fibers in rat peripheral nerve. Exp Brain Res 663:659-663 (Pubitemid 17090801)
4. Bowery NG, Smart TG (2006) Gaba and glycine as neurotransmitters: a brief history. Br J Pharmacol 147(Suppl 1):S109-S119 (Pubitemid 43077268)
5. Bowery NG, Price GW, Hudson AL et al (1984) Gaba receptor multiplicity. Visualization of different receptor types in the mammalian CNS. Neuropharmacology 232B:219-231 (Pubitemid 14197478)
6. Brohlin M, Mahay D, Novikov LN et al (2009) Characterisation of human mesenchymal stem cells following differentiation into Schwann cell-like cells. Neurosci Res 641:41-49
7. Brown DA, Marsh S (1978) Axonal GABA-receptors in mammalian peripheral nerve trunks. Brain Res 1561:187-191 (Pubitemid 9002757)
8. Brown DA, Adams PR, Higgins AJ, Marsh S (1979) Distribution of GABA-receptors and GABA-carriers in the mammalian nervous system. J Physiol (Paris) 756:667-671 (Pubitemid 10164050)
9. Caddick J, Kingham PJ, Gardiner NJ, Wiberg M, Terenghi G (2006) Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 548:840-849 (Pubitemid 44671989)
10. di Summa PG, Kingham PJ, Raffoul W et al (2009) Adipose-derived stem cells enhance peripheral nerve regeneration. J Plast Reconstr Aesthet Surg 63:1544-1552
11. di Summa PG, Kalbermatten DF, Pralong E et al (2011) Long-term in vivo regeneration of peripheral nerves through bioengineered nerve grafts. Neuroscience 181:278-291
12. Faroni A, Magnaghi V (2011) The neurosteroid allopregnanolone modulates specific functions in central and peripheral glial cells. Front Endocrin 2:103. doi:10.3389/fendo.2011.00103
13. Faroni A, Mantovani C, Shawcross SG et al (2011) Schwann-like adult stem cells derived from bone marrow and adipose tissue express gamma-aminobutyric acid type B receptors. J Neurosci Res 89:1351-1362
14. Fritschy JM, Brunig I (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 983:299-323
15. Gago N, El-Etr M, Sananes N et al (2004) 3alpha,5alpha- Tetrahydroprogesterone (allopregnanolone) and gamma-aminobutyric acid: autocrine/paracrine interactions in the control of neonatal Psa-Ncam + progenitor proliferation. J Neurosci Res 786:770-783 (Pubitemid 39657565)
16. Jessen KR, Mirsky R, Dennison ME, Burnstock G (1979) GABA may be a neurotransmitter in the vertebrate peripheral nervous system. Nature 281(5726):71-74
17. Kaewkhaw R, Scutt AM, Haycock JW (2011) Anatomical site influences the differentiation of adipose-derived stem cells for Schwann-cell phenotype and function. Glia 595:734-749
18. Kalbermatten DF, Schaakxs D, Kingham PJ, Wiberg M (2011) Neurotrophic activity of human adipose stem cells isolated from deep and superficial layers of abdominal fat. Cell Tissue Res 3442: 251-260
19. Keilhoff G, Goihl A, Langnase K, Fansa H, Wolf G (2006) Transdifferentiation of mesenchymal stem cells into Schwann cell-like myelinating cells. Eur J Cell Biol 851:11-24 (Pubitemid 43055554)
20. Kingham PJ, Kalbermatten DF, Mahay D et al (2007) Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol 2072:267-274 (Pubitemid 47432883)
21. Magnaghi V (2007) Gaba and neuroactive steroid interactions in glia: new roles for old players? Curr Neuropharmacol 51:47-64
22. Magnaghi V, Cavarretta I, Galbiati M, Martini L, Melcangi RC (2001) Neuroactive steroids and peripheral myelin proteins. Brain Res Brain Res Rev 371-3:360-371 (Pubitemid 34020744)
23. Magnaghi V, Ballabio M, Cavarretta IT et al (2004) GABAB receptors in Schwann cells influence proliferation and myelin protein expression. Eur J Neurosci 1910:2641-2649 (Pubitemid 38746381)
24. Magnaghi V, Ballabio M, Consoli A et al (2006) GABA receptor-mediated effects in the peripheral nervous system: a cross-interaction with neuroactive steroids. J Mol Neurosci 281:89-102 (Pubitemid 43780339)
25. Magnaghi V, Ballabio M, Camozzi F et al (2008) Altered peripheral myelination in mice lacking GABAB receptors. Mol Cell Neurosci 373:599-609
26. Magnaghi V, Procacci P, Tata AM (2009) Chapter 15: novel pharmacological approaches to Schwann cells as neuroprotective agents for peripheral nerve regeneration. Int Rev Neurobiol 87:295-315
27. Magnaghi V, Parducz A, Frasca A et al (2010) Gaba synthesis in Schwann cells is induced by the neuroactive steroid allopregnanolone. J Neurochem 1124:980-990
28. Mahay D, Terenghi G, Shawcross SG (2008a) Growth factors in mesenchymal stem cells following glial-cell differentiation. Biotechnol Appl Biochem 51(Pt 4):167-176
29. Mahay D, Terenghi G, Shawcross SG (2008b) Schwann cell mediated trophic effects by differentiated mesenchymal stem cells. Exp Cell Res 314(14):2692-2701
30. Mantovani C, Mahay D, Kingham M et al (2010) Bone marrow- and adipose-derived stem cells show expression of myelin mRNAs and proteins. Regen Med 53:403-410
31. Marcoli M, Candiani S, Tonachini L et al (2008) In vitro modulation of gamma amino butyric acid (GABA) receptor expression by bone marrow stromal cells. Pharmacol Res 575:374-382
32. Melcangi RC, Magnaghi V, Cavarretta I et al (1999) Progesterone derivatives are able to influence peripheral myelin protein 22 and p0 gene expression: possible mechanisms of action. J Neurosci Res 564:349-357 (Pubitemid 29226952)
33. Melcangi RC, Cavarretta IT, Ballabio M et al (2005) Peripheral nerves: a target for the action of neuroactive steroids. Brain Res Brain Res Rev 482:328-338 (Pubitemid 40585763)
34. Morris ME, Di Costanzo GA, Fox S, Werman R (1983) Depolarizing action of GABA (gamma-aminobutyric acid) on myelinated fibers of peripheral nerves. Brain Res 2781-2:117-126 (Pubitemid 14219280)
35. Novikova LN, Brohlin M, Kingham PJ, Novikov LN, Wiberg M (2011) Neuroprotective and growth-promoting effects of bone marrow stromal cells after cervical spinal cord injury in adult rats. Cytotherapy 137:873-887
36. Olsen RW, Sieghart W (2008) International Union of Pharmacology. Lxx. Subtypes of gamma-aminobutyric acid(a) receptors: classification on the basis of subunit composition, pharmacology, and function. Update. Pharmacol Rev 603:243-260
37. Olsen RW, Sieghart W (2009) GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 561:141-148
38. Olsen RW, Snowhill EW, Wamsley JK (1984) Autoradiographic localization of low affinity GABA receptors with [3 h]bicuculline methochloride. Eur J Pharmacol 992-3:247-248 (Pubitemid 14172508)
39. Pastor A, Chvatal A, Sykova E, Kettenmann H (1995) Glycine- and GABA-activated currents in identified glial cells of the developing rat spinal cord slice. Eur J Neurosci 76:1188-1198
40. Perego C, Cairano ES, Ballabio M, Magnaghi V (2011) Neurosteroid allopregnanolone regulates EAAC1-mediated glutamate uptake and triggers actin changes in Schwann cells. J Cell Physiol. doi:10.1002/jcp.22898
41. Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 2845411:143-147 (Pubitemid 29282067)
42. Reid AJ, Sun M, Wiberg M et al (2011) Nerve repair with adipose-derived stem cells protects dorsal root ganglia neurons from apoptosis. Neuroscience 199:515-522
43. Safford KM, Safford SD, Gimble JM, Shetty AK, Rice HE (2004) Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol 1872:319-328 (Pubitemid 38610278)
44. Schwirtlich M, Emri Z, Antal K et al (2010) GABA(A) and GABA(B) receptors of distinct properties affect oppositely the proliferation of mouse embryonic stem cells through synergistic elevation of intracellular Ca(2+). FASEB J 244:1218-1228
45. Shichinohe H, Kuroda S, Yano S et al (2006) Improved expression of gamma-aminobutyric acid receptor in mice with cerebral infarct and transplanted bone marrow stromal cells: an autoradiographic and histologic analysis. J Nucl Med 473:486-491 (Pubitemid 46768491)
46. Simon J, Wakimoto H, Fujita N, Lalande M, Barnard EA (2004) Analysis of the set of GABA(A) receptor genes in the human genome. J Biol Chem 27940:41422-41435 (Pubitemid 39313583)
47. Tohill M, Mantovani C, Wiberg M, Terenghi G (2004) Rat bone marrow mesenchymal stem cells express glial markers and stimulate nerve regeneration. Neurosci Lett 3623:200-203 (Pubitemid 38648941)
48. Tse KH, Kingham PJ, Novikov LN, Wiberg M (2011) Adipose tissue and bone marrow-derived stem cells react similarly in an ischaemia-like microenvironment. J Tissue Eng Regen Med. doi:10.1002/term.452
49. Varju P, Katarova Z, Madarasz E, Szabo G (2001) GABA signalling during development: new data and old questions. Cell Tissue Res 3052:239-246 (Pubitemid 32681900)
50. Velez-Fort M, Audinat E, Angulo MC (2011) Central role of GABA in neuron-glia interactions. Neuroscientist. doi:10.1177/1073858411403317
51. von Blankenfeld G, Kettenmann H (1991) Glutamate and GABA receptors in vertebrate glial cells. Mol Neurobiol 51:31-43
52. Watanabe M, Maemura K, Kanbara K, Tamayama T, Hayasaki H (2002) GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 213:1-47 (Pubitemid 34121040)
53. Xu Y, Liu L, Li Yet al (2008) Myelin-forming ability of Schwann celllike cells induced from rat adipose-derived stem cells in vitro. Brain Res 1239:49-55
54. Yano S, Kuroda S, Shichinohe H et al (2006) Bone marrow stromal cell transplantation preserves gammaaminobutyric acid receptor function in the injured spinal cord. J Neurotrauma 2311:1682-1692 (Pubitemid 44846661)
55. Zuk PA, Zhu M, Ashjian P et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 1312:4279-4295 (Pubitemid 35471185)