Differentiation of adipose-derived stem cells into Schwann cell phenotype induces expression of P2X receptors that control cell death

Cell Death and Disease

Volumn 4, Issue 7, 2013, Pages

  Faroni, A A ^a,b   W Rothwell, S S ^b   A Grolla, A A ^b   Terenghi, G G ^a   Magnaghi, V V ^c   Verkhratsky, A A ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Adipose derived stem cells; ATP; Cell death; Peripheral nerve regeneration; Purinergic receptors; Schwann like cells

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; PURINERGIC P2X RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR;

ADIPOSE TISSUE; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOTOXICITY TEST; IMMUNOCYTOCHEMISTRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHWANN CELL; STEM CELL; VOLTAGE CLAMP; WESTERN BLOTTING;

ADIPOCYTES; CELL DEATH; CELL DIFFERENTIATION; HUMANS; PHENOTYPE; RECEPTORS, PURINERGIC P2X; SCHWANN CELLS; STEM CELLS; SURVIVAL ANALYSIS; UP-REGULATION;

EID: 84881073015     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.268     Document Type: Article

References (61)

1. Terenghi G, Wiberg M, Kingham PJ. Chapter 21: use of stem cells for improving nerve regeneration. Int Rev Neurobiol 2009; 87: 393-403.
2. Adams AM, Arruda EM, Larkin LM. Use of adipose-derived stem cells to fabricate scaffoldless tissue-engineered neural conduits in vitro. Neuroscience 2012; 201: 349-356.
3. Zochodne DW. The challenges and beauty of peripheral nerve regrowth. J Peripher Nerv Syst 2012; 17: 1-18.
4. Wiberg M, Terenghi G. Will it be possible to produce peripheral nerves? Surg Technol Int 2003; 11: 303-310.
5. Chalfoun CT, Wirth GA, Evans GR. Tissue engineered nerve constructs: where do we stand? J Cell Mol Med 2006; 10: 309-317.
6. Mirsky R, Jessen KR. The neurobiology of Schwann cells. Brain Pathol 1999; 9: 293-311.
7. Chen ZL, Yu WM, Strickland S. Peripheral regeneration. Annu Rev Neurosci 2007; 30: 209-233.
8. Ide C. Peripheral nerve regeneration. Neurosci Res 1996; 25: 101-121.
9. Guenard V, Kleitman N, Morrissey TK, Bunge RP, Aebischer P. Syngeneic Schwann cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral nerve regeneration. J Neurosci 1992; 12: 3310-3320.
10. Mosahebi A, Fuller P, Wiberg M, Terenghi G. Effect of allogeneic Schwann cell transplantation on peripheral nerve regeneration. Exp Neurol 2002; 173: 213-223.
11. Mosahebi A, Woodward B, Wiberg M, Martin R, Terenghi G. Retroviral labeling of Schwann cells: in vitro characterization and in vivo transplantation to improve peripheral nerve regeneration. Glia 2001; 34: 8-17.
12. Tohill M, Terenghi G. Stem-cell plasticity and therapy for injuries of the peripheral nervous system. Biotechnol Appl Biochem 2004; 40(Pt 1): 17-24.
13. Jiang L, Zhu JK, Liu XL, Xiang P, Hu J, Yu WH. Differentiation of rat adipose tissue-derived stem cells into Schwann-like cells in vitro. Neuroreport 2008; 19: 1015-1019.
14. Kingham PJ, Kalbermatten DF, Mahay D, Armstrong SJ, Wiberg M, Terenghi G. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol 2007; 207: 267-274.
15. Xu Y, Liu L, Li Y, Zhou C, Xiong F, Liu Z et al. Myelin-forming ability of Schwann cell-like cells induced from rat adipose-derived stem cells in vitro. Brain Res 2008; 1239: 49-55.
16. Radtke C, Schmitz B, Spies M, Kocsis JD, Vogt PM. Peripheral glial cell differentiation from neurospheres derived from adipose mesenchymal stem cells. Int J Dev Neurosci 2009; 27: 817-823.
17. Razavi S, Ahmadi N, Kazemi M, Mardani M, Esfandiari E. Efficient transdifferentiation of human adipose-derived stem cells into Schwann-like cells: a promise for treatment of demyelinating diseases. Adv Biomed Res 2012; 1: 12.
18. Tomita K, Madura T, Sakai Y, Yano K, Terenghi G, Hosokawa K. Glial differentiation of human adipose-derived stem cells: implications for cell-based transplantation therapy. Neuroscience 2013; 236: 55-65.
19. Mantovani C, Mahay D, Kingham M, Terenghi G, Shawcross SG, Wiberg M. Bone marrow-and adipose-derived stem cells show expression of myelin mRNAs and proteins. Regen Med 2010; 5: 403-410.
20. Tomita K, Madura T, Mantovani C, Terenghi G. Differentiated adipose-derived stem cells promote myelination and enhance functional recovery in a rat model of chronic denervation. J Neurosci Res 2012; 90: 1392-1402.
21. Kaewkhaw R, Scutt AM, Haycock JW. Anatomical site influences the differentiation of adiposederived stem cells for Schwann-cell phenotype and function. Glia 2011; 59: 734-749.
22. di Summa PG, Kalbermatten DF, Pralong E, Raffoul W, Kingham PJ, Terenghi G. Long-term in vivo regeneration of peripheral nerves through bioengineered nerve grafts. Neuroscience 2011; 181: 278-291.
23. di Summa PG, Kingham PJ, Raffoul W, Wiberg M, Terenghi G, Kalbermatten DF. Adipose-derived stem cells enhance peripheral nerve regeneration. J Plast Reconstr Aesthet Surg 2010; 63: 1544-1552.
24. Sun F, Zhou K, Mi WJ, Qiu JH. Combined use of decellularized allogeneic artery conduits with autologous transdifferentiated adipose-derived stem cells for facial nerve regeneration in rats. Biomaterials 2011; 32: 8118-8128.
25. Zhang Y, Luo H, Zhang Z, Lu Y, Huang X, Yang L et al. A nerve graft constructed with xenogeneic acellular nerve matrix and autologous adipose-derived mesenchymal stem cells. Biomaterials 2010; 31: 5312-5324.
26. Erba P, Mantovani C, Kalbermatten DF, Pierer G, Terenghi G, Kingham PJ. Regeneration potential and survival of transplanted undifferentiated adipose tissue-derived stem cells in peripheral nerve conduits. J Plast Reconstr Aesthet Surg 2010; 63: e811-e817.
27. Walsh S, Midha R. Practical considerations concerning the use of stem cells for peripheral nerve repair. Neurosurg Focus 2009; 26: E2.
28. Walsh SK, Kumar R, Grochmal JK, Kemp SW, Forden J, Midha R. Fate of stem cell transplants in peripheral nerves. Stem Cell Res 2012; 8: 226-238.
29. Magnaghi V, Procacci P, Tata AM. Chapter 15: Novel pharmacological approaches to Schwann cells as neuroprotective agents for peripheral nerve regeneration. Int Rev Neurobiol 2009; 87: 295-315.
30. Verderio C, Bianco F, Blanchard MP, Bergami M, Canossa M, Scarfone E et al. Cross talk between vestibular neurons and Schwann cells mediates BDNF release and neuronal regeneration. Brain Cell Biol 2006; 35: 187-201.
31. Magnaghi V, Ballabio M, Consoli A, Lambert JJ, Roglio I, Melcangi RC. GABA receptor-mediated effects in the peripheral nervous system: a cross-interaction with neuroactive steroids. J Mol Neurosci 2006; 28: 89-102.
32. Magnaghi V, Ballabio M, Cavarretta IT, Froestl W, Lambert JJ, Zucchi I et al. GABAB receptors in Schwann cells influence proliferation and myelin protein expression. Eur J Neurosci 2004; 19: 2641-2649.
33. Fields RD, Stevens B. ATP: an extracellular signaling molecule between neurons and glia. Trends Neurosci 2000; 23: 625-633.
34. Procacci P, Ballabio M, Castelnovo LF, Mantovani C, Magnaghi V. GABA-B receptors in the PNS have a role in Schwann cells differentiation? Front Cell Neurosci 2012; 6: 68.
35. Faroni A, Terenghi G, Magnaghi V. Expression of functional gamma-aminobutyric acid type a receptors in Schwann-like adult stem cells. J Mol Neurosci 2012; 47: 619-630.
36. Faroni A, Mantovani C, Shawcross SG, Motta M, Terenghi G, Magnaghi V. Schwann-like adult stem cells derived from bone marrow and adipose tissue express gamma-aminobutyric acid type B receptors. J Neurosci Res 2011; 89: 1351-1362.
37. Faroni A, Calabrese F, Riva MA, Terenghi G, Magnaghi V. Baclofen modulates the expression and release of neurotrophins in schwann-like adipose stem cells. J Mol Neurosci 2013; 49: 233-243.
38. Zippel N, Limbach CA, Ratajski N, Urban C, Luparello C, Pansky A et al. Purinergic receptors influence the differentiation of human mesenchymal stem cells. Stem Cells Dev 2012; 21: 884-900.
39. Fields RD, Burnstock G. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 2006; 7: 423-436.
40. Verkhratsky A, Krishtal OA, Burnstock G. Purinoceptors on neuroglia. Mol Neurobiol 2009; 39: 190-208.
41. Burnstock G. Purinergic signalling: its unpopular beginning, its acceptance and its exciting future. Bioessays 2012; 34: 218-225.
42. Burnstock G, Verkhratsky A. Long-term (trophic) purinergic signalling: purinoceptors control cell proliferation, differentiation and death. Cell Death Dis 2010; 1: e9.
43. Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P et al. P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med 2004; 10: 821-827.
44. Di Virgilio F. Liaisons dangereuses: P2X(7) and the inflammasome. Trends Pharmacol Sci 2007; 28: 465-472.
45. Di Virgilio F, Chiozzi P, Falzoni S, Ferrari D, Sanz JM, Venketaraman V et al. Cytolytic P2X purinoceptors. Cell Death Differ 1998; 5: 191-199.
46. Mantovani C, Raimondo S, Haneef MS, Geuna S, Terenghi G, Shawcross SG et al. Morphological, molecular and functional differences of adult bone marrow-and adiposederived stem cells isolated from rats of different ages. Exp Cell Res 2012; 318: 2034-2048.
47. Stevens B, Fields RD. Response of Schwann cells to action potentials in development. Science 2000; 287: 2267-2271.
48. Matute C, Torre I, Perez-Cerda F, Perez-Samartin A, Alberdi E, Etxebarria E et al. P2X(7) receptor blockade prevents ATP excitotoxicity in oligodendrocytes and ameliorates experimental autoimmune encephalomyelitis. J Neurosci 2007; 27: 9525-9533.
49. Khakh BS, North RA. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006; 442: 527-532.
50. Lecca D, Ceruti S, Fumagalli M, Abbracchio MP. Purinergic trophic signalling in glial cells: functional effects and modulation of cell proliferation, differentiation, and death. Purinergic Signal 2012; 8: 539-557.
51. Shimizu S, Kitada M, Ishikawa H, Itokazu Y, Wakao S, Dezawa M. Peripheral nerve regeneration by the in vitro differentiated-human bone marrow stromal cells with Schwann cell property. Biochem Biophys Res Commun 2007; 359: 915-920.
52. McKenzie IA, Biernaskie J, Toma JG, Midha R, Miller FD. Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci 2006; 26: 6651-6660.
53. Hill CE, Hurtado A, Blits B, Bahr BA, Wood PM, Bartlett Bunge M et al. Early necrosis and apoptosis of Schwann cells transplanted into the injured rat spinal cord. Eur J Neurosci 2007; 26: 1433-1445.
54. Pearse DD, Sanchez AR, Pereira FC, Andrade CM, Puzis R, Pressman Y et al. Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: Survival, migration, axon association, and functional recovery. Glia 2007; 55: 976-1000.
55. Tse KH, Kingham PJ, Novikov LN, Wiberg M. Adipose tissue and bone marrow-derived stem cells react similarly in an ischaemia-like microenvironment. J Tissue Eng Regen Med 2012; 6: 473-485.
56. Zhu W, Chen J, Cong X, Hu S, Chen X. Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 2006; 24: 416-425.
57. Grafe P, Schaffer V, Rucker F. Kinetics of ATP release following compression injury of a peripheral nerve trunk. Purinergic Signal 2006; 2: 527-536.
58. Shin YH, Lee SJ, Jung J. Secretion of ATP from Schwann cells through lysosomal exocytosis during Wallerian degeneration. Biochem Biophys Res Commun 2012; 429: 163-167.
59. Shin YH, Lee SJ, Jung J. Extracellular ATP inhibits Schwann cell dedifferentiation and proliferation in an ex vivo model of Wallerian degeneration. Biochem Biophys Res Commun 2013; 430: 852-857.
60. Sulaiman OA, Gordon T. Role of chronic Schwann cell denervation in poor functional recovery after nerve injuries and experimental strategies to combat it. Neurosurgery 2009; 65(4 Suppl): A105-A114.
61. Shibuya I, Tanaka K, Hattori Y, Uezono Y, Harayama N, Noguchi J et al. Evidence that multiple P2X purinoceptors are functionally expressed in rat supraoptic neurones. J Physiol 1999; 514(Pt 2): 351-367.