Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 936891, 6 pages
http://dx.doi.org/10.1155/2014/936891
Review Article

ATP Release through Lysosomal Exocytosis from Peripheral Nerves: The Effect of Lysosomal Exocytosis on Peripheral Nerve Degeneration and Regeneration after Nerve Injury

1Department of Anatomy and Neurobiology, School of Medicine, Biomedical Science Institution, Kyung Hee University, Hoegi-Dong 1, Dongdaemun-Gu, Seoul 130-701, Republic of Korea
2Department of Pediatrics, Haeundae Paik Hospital, Inje University, 875 Haeun-daero, Haeundae-gu, Busan 612-896, Republic of Korea
3Department of Anatomy and Cell Biology, College of Medicine, Dong-A University, Busan 602-714, Republic of Korea

Received 13 April 2014; Revised 29 May 2014; Accepted 16 June 2014; Published 30 June 2014

Academic Editor: W. David Arnold

Copyright © 2014 Junyang Jung et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Holtzman, Lysosomes, Plenum Press, New York, NY, USA, 1989.
  2. C. de Duve, “The lysosome concept,” in Proceedings of the Ciba Foundation Symposium on Lysosomes, A. V. S. de Reuck and M. P. Cameron, Eds., pp. 1–35, J. & A. Churchill, London, UK, 1963. View at Google Scholar
  3. S. Kornfeld and I. Mellman, “The biogenesis of lysosomes,” Annual Review of Cell Biology, vol. 5, pp. 483–525, 1989. View at Publisher · View at Google Scholar · View at Scopus
  4. E. J. Blott and G. M. Griffiths, “Secretory lysosomes,” Nature Reviews Molecular Cell Biology, vol. 3, no. 2, pp. 122–131, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. N. W. Andrews, “Regulated secretion of conventional lysosomes,” Trends in Cell Biology, vol. 10, no. 8, pp. 316–321, 2000. View at Publisher · View at Google Scholar
  6. R. Sundler, “Lysosomal and cytosolic pH as regulators of exocytosis in mouse macrophages,” Acta Physiologica Scandinavica, vol. 161, no. 4, pp. 553–556, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Reddy, E. V. Caler, and N. W. Andrews, “Plasma membrane repair is mediated by Ca2+-regulated exocytosis of lysosomes,” Cell, vol. 106, no. 2, pp. 157–169, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. R. A. Steinhardt, G. Bi, and J. M. Alderton, “Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release,” Science, vol. 263, no. 5145, pp. 390–393, 1994. View at Publisher · View at Google Scholar · View at Scopus
  9. R. M. E. Arantes and N. W. Andrews, “A role for synaptotagmin VII-regulated exocytosis of lysosomes in neurite outgrowth from primary sympathetic neurons,” The Journal of Neuroscience, vol. 26, no. 17, pp. 4630–4637, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Chakrabarti, K. S. Kobayashi, R. A. Flavell et al., “Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice,” The Journal of Cell Biology, vol. 162, no. 4, pp. 543–549, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Pankratov, U. Lalo, A. Verkhratsky, and R. A. North, “Vesicular release of ATP at central synapses,” Pflügers Archiv, vol. 452, no. 5, pp. 589–597, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Zhang, H. K. Wang, C. Q. Ye et al., “ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression,” Neuron, vol. 40, no. 5, pp. 971–982, 2003. View at Google Scholar
  13. S. J. Robertson and F. A. Edwards, “ATP and glutamate are released from separate neurones in the rat medial habenula nucleus: frequency dependence and adenosine-mediated inhibition of release,” The Journal of Physiology, vol. 508, part 3, pp. 691–701, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. H. Jo and L. W. Role, “Coordinate release of ATP and GABA at in vitro synapses of lateral hypothalamic neurons,” The Journal of Neuroscience, vol. 22, no. 12, pp. 4794–4804, 2002. View at Google Scholar
  15. U. Lalo, N. Voitenko, and P. Kostyuk, “Iono- and metabotropically induced purinergic calcium signalling in rat neocortical neurons,” Brain Research, vol. 799, no. 2, pp. 285–291, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. M. P. Abbracchio, G. Burnstock, A. Verkhratsky, and H. Zimmermann, “Purinergic signalling in the nervous system : an overview,” Trends in Neurosciences, vol. 32, no. 1, pp. 19–29, 2009. View at Google Scholar
  17. H. Campwala and S. J. Fountain, “Constitutive and agonist stimulated ATP secretion in leukocytes,” Communicative & Integrative Biology, vol. 6, no. 3, Article ID e23631, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Bianco, M. Fumagalli, E. Pravettoni et al., “Pathophysiological roles of extracellular nucleotides in glial cells: differential expression of purinergic receptors in resting and activated microglia,” Brain Research Reviews, vol. 48, no. 2, pp. 144–156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Koizumi, Y. Shigemoto-Mogami, K. Nasu-Tada et al., “UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis,” Nature, vol. 446, no. 7139, pp. 1091–1095, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Iijima, “Quinacrine-induced degeneration of non-adrenergic, non-cholinergic autonomic nerves in the rat anococcygeus muscle,” Cell and Tissue Research, vol. 230, no. 3, pp. 639–648, 1983. View at Publisher · View at Google Scholar · View at Scopus
  21. Z. Zhang, G. Chen, W. Zhou et al., “Regulated ATP release from astrocytes through lysosome exocytosis,” Nature Cell Biology, vol. 9, no. 8, pp. 945–953, 2007. View at Publisher · View at Google Scholar
  22. E. Pryazhnikov and L. Khiroug, “Sub-micromolar increase in [Ca2+]i triggers delayed exocytosis of ATP in cultured astrocytes,” GLIA, vol. 56, no. 1, pp. 38–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Oya, T. Kitaguchi, Y. Yanagihara et al., “Vesicular nucleotide transporter is involved in ATP storage of secretory lysosomes in astrocytes,” Biochemical and Biophysical Research Communications, vol. 438, no. 1, pp. 145–151, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Dou, H. J. Wu, H. Q. Li et al., “Microglial migration mediated by ATP-induced ATP release from lysosomes,” Cell Research, vol. 22, no. 6, pp. 1022–1033, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Imura, Y. Morizawa, R. Komatsu et al., “Microglia release ATP by exocytosis,” Glia, vol. 61, no. 8, pp. 1320–1330, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Ralevic and G. Burnstock, “Receptors for purines and pyrimidines,” Pharmacological Reviews, vol. 50, no. 3, pp. 413–492, 1998. View at Google Scholar · View at Scopus
  27. G. Vrbova, N. Mehra, H. Shanmuganathan, N. Tyreman, M. Schachner, and T. Gordon, “Chemical communication between regenerating motor axons and Schwann cells in the growth pathway,” European Journal of Neuroscience, vol. 30, no. 3, pp. 366–375, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. B. Stevens and R. D. Fields, “Response of Schwann cells to action potentials in development,” Science, vol. 287, no. 5461, pp. 2267–2271, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. S. D. Jeftinija and K. V. Jeftinija, “ATP stimulates release of excitatory amino acids from cultured Schwann cells,” Neuroscience, vol. 82, no. 3, pp. 927–934, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. A. D. Ansselin, D. F. Davey, and D. G. Allen, “Extracellular ATP increases intracellular calcium in cultured adult Schwann cells,” Neuroscience, vol. 76, no. 3, pp. 947–955, 1996. View at Publisher · View at Google Scholar · View at Scopus
  31. G. J. Liu, E. L. Werry, and M. R. Bennett, “Secretion of ATP from Schwann cells in response to uridine triphosphate,” The European Journal of Neuroscience, vol. 21, no. 1, pp. 151–160, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. G. J. Liu and M. R. Bennett, “ATP secretion from nerve trunks and Schwann cells mediated by glutamate,” Neuroreport, vol. 14, no. 16, pp. 2079–2083, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. H. Shin, S. J. Lee, and J. Jung, “Secretion of ATP from Schwann cells through lysosomal exocytosis during Wallerian degeneration,” Biochemical and Biophysical Research Communications, vol. 429, no. 3-4, pp. 163–167, 2012. View at Google Scholar
  34. S. Martinez-Arca, P. Alberts, A. Zahraoui, D. Louvard, and T. Galli, “Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth,” Journal of Cell Biology, vol. 149, no. 4, pp. 889–899, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Craxton and M. Goedert, “Alternative splicing of synaptotagmins involving transmembrane exon skipping,” FEBS Letters, vol. 460, no. 3, pp. 417–422, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Sawada, N. Echigo, N. Juge et al., “Identification of a vesicular nucleotide transporter,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 15, pp. 5683–5686, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Holton, “The liberation of adenosine triphosphate on antidromic stimulation of sensory nerves,” The Journal of Physiology, vol. 157, no. 3, pp. 494–504, 1959. View at Google Scholar
  38. Y. Matsuka, T. Ono, H. Iwase et al., “Altered ATP release and metabolism in dorsal root ganglia of neuropathic rats,” Molecular Pain, vol. 4, p. 66, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. C. F. Stevens, “Neurotransmitter release at central synapses,” Neuron, vol. 40, no. 2, pp. 381–388, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Burnstock, “Physiology and pathophysiology of purinergic neurotransmission,” Physiological Reviews, vol. 87, no. 2, pp. 659–797, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Pankratov, U. Lalo, A. Verkhratsky, and R. A. North, “Vesicular release of ATP at central synapses,” Pflugers Archiv European Journal of Physiology, vol. 452, no. 5, pp. 589–597, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. P. Bodin and G. Burnstock, “Purinergic signalling: ATP release,” Neurochemical Research, vol. 26, no. 8-9, pp. 959–969, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Soeda, H. Tatsumi, and Y. Katayama, “Neurotransmitter release from growth cones of rat dorsal root ganglion neurons in culture,” Neuroscience, vol. 77, no. 4, pp. 1187–1199, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. X. Zhang, Y. Chen, C. Wang, and L.-Y. M. Huang, “Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 23, pp. 9864–9869, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Jung, Y. H. Shin, H. Konishi, S. J. Lee, and H. Kiyama, “Possible lysosomal primary sensory neurons,” Biochemical and Biophysical Research Communications, vol. 430, no. 2, pp. 488–493, 2013. View at Google Scholar
  46. M. Tsuda, Y. Shigemoto-Mogami, S. Koizumi et al., “P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury,” Nature, vol. 424, no. 6950, pp. 778–783, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. M. N. Ghabriel and G. Allt, “The role of Schmidt-Lanterman incisures in Wallerian degeneration. I. A quantitative teased fibre study,” Acta Neuropathologica, vol. 48, no. 2, p. 93, 1979. View at Google Scholar · View at Scopus
  48. M. N. Ghabriel and G. Allt, “The role of Schmidt-Lanterman incisures in Wallerian degeneration. II: an electron microscopic study,” Acta Neuropathologica, vol. 48, no. 2, pp. 95–103, 1979. View at Publisher · View at Google Scholar · View at Scopus
  49. H. F. Webster, “The relationship between Schmidt-Lantermann incisures and myelin segmentation during wallerian degeneration,” Annals of the New York Academy of Sciences, vol. 122, pp. 29–38, 1965. View at Google Scholar · View at Scopus
  50. J. Jung, W. Cai, S. Y. Jang et al., “Transient lysosomal activation is essential for p75 nerve growth factor receptor expression in myelinated Schwann cells during Wallerian degeneration,” Anatomy and Cell Biology, vol. 44, no. 1, pp. 41–49, 2011. View at Publisher · View at Google Scholar
  51. H. K. Lee, Y. K. Shin, J. Jung, S. Y. Seo, S. Y. Baek, and H. T. Park, “Proteasome inhibition suppresses schwann cell dedifferentiation in vitro and in vivo,” Glia, vol. 57, no. 16, pp. 1825–1834, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. H. Shin, H. J. Chung, C. Park et al., “Adenosine 5′-triphosphate (ATP) inhibits schwann cell demyelination during Wallerian degeneration,” Cellular and Molecular Neurobiology, vol. 34, no. 3, pp. 361–368, 2014. View at Publisher · View at Google Scholar
  53. P. Dubový, “Wallerian degeneration and peripheral nerve conditions for both axonal regeneration and neuropathic pain induction,” Annals of Anatomy, vol. 193, no. 4, pp. 267–275, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Rotshenker, “Wallerian degeneration: the innate-immune response to traumatic nerve injury,” Journal of Neuroinflammation, vol. 8, article 109, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. W. G. Junger, “Immune cell regulation by autocrine purinergic signalling,” Nature Reviews Immunology, vol. 11, no. 3, pp. 201–212, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. G. Burnstock, “Purinergic signalling: its unpopular beginning, its acceptance and its exciting future,” BioEssays, vol. 34, no. 3, pp. 218–225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. G. Chen, Z. Zhang, Z. Wei et al., “Lysosomal exocytosis in Schwann cells contributes to axon remyelination,” Glia, vol. 60, no. 2, pp. 295–305, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. M. C. Harrisingh, E. Perez-Nadales, D. B. Parkinson, D. S. Malcolm, A. W. Mudge, and A. C. Lloyd, “The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation,” The EMBO Journal, vol. 23, no. 15, pp. 3061–3071, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. D. B. Parkinson, A. Bhaskaran, P. Arthur-Farraj et al., “c-Jun is a negative regulator of myelination,” The Journal of Cell Biology, vol. 181, no. 4, pp. 625–637, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. D. P. Yang, J. Kim, N. Syed et al., “p38 MAPK activation promotes denervated schwann cell phenotype and functions as a negative regulator of schwann cell differentiation and myelination,” Journal of Neuroscience, vol. 32, no. 21, pp. 7158–7168, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. K. R. Jessen and R. Mirsky, “Negative regulation of myelination: relevance for development, injury, and demyelinating disease,” GLIA, vol. 56, no. 14, pp. 1552–1565, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Taniuchi, H. B. Clark, J. B. Schweitzer, and E. M. Johnson Jr., “Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties,” Journal of Neuroscience, vol. 8, no. 2, pp. 664–681, 1988. View at Google Scholar · View at Scopus
  63. Y. H. Shin, S. J. Lee, and J. Jung, “Extracellular ATP inhibits Schwann cell dedifferentiation and proliferation in an ex vivo model of Wallerian degeneration,” Biochemical and Biophysical Research Communications, vol. 430, no. 2, pp. 852–857, 2013. View at Google Scholar
  64. R. D. Fields and B. Stevens, “ATP: an extracellular signaling molecule between neurons and glia,” Trends in Neurosciences, vol. 23, no. 12, pp. 625–633, 2000. View at Publisher · View at Google Scholar · View at Scopus
  65. H. Zimmermann, N. Braun, B. Kegel, and P. Heine, “New insights into molecular structure and function of ecto-nucleotidases in the nervous system,” Neurochemistry International, vol. 32, no. 5-6, pp. 421–425, 1998. View at Publisher · View at Google Scholar · View at Scopus