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BioMed Research International
Volume 2014 (2014), Article ID 328348, 7 pages
http://dx.doi.org/10.1155/2014/328348
Research Article

New Insights into c-Ret Signalling Pathway in the Enteric Nervous System and Its Relationship with ALS

1Department of Human Anatomy and Histology, Faculty of Medicine, University of Zaragoza, Domingo Miral, s/n, 50009 Zaragoza, Spain
2Aragon Health Sciences Institute (I+CS), Zaragoza, Spain
3Department of Cellular Biology, Physiology and Immunology, Faculty of Medicine, University of Córdoba, Spain
4Maimonides Institute for Biomedical Research of Cordoba (IMIBIC), Spain
5Department of Obstetrics, Gynaecology and Surgery, University of Zaragoza, Spain
6Department Pharmacology and Physiology, Faculty of Medicine, University of Zaragoza, Spain

Received 23 January 2014; Accepted 7 April 2014; Published 28 April 2014

Academic Editor: Ana Cristina Calvo

Copyright © 2014 M. J. Luesma 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. D. R. Rosen, T. Siddique, D. Patterson et al., “Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis,” Nature, vol. 362, no. 6415, pp. 59–62, 1993. View at Publisher · View at Google Scholar · View at Scopus
  2. D. W. Cleveland and J. D. Rothstein, “From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS,” Nature Reviews Neuroscience, vol. 2, no. 11, pp. 806–819, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. L. P. Rowland and N. A. Shneider, “Amyotrophic lateral sclerosis,” The New England Journal of Medicine, vol. 344, no. 22, pp. 1688–1700, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. M. D. Weiss, P. Weydt, and G. T. Carter, “Current pharmacological management of amyotropic lateral sclerosis and a role for rational polypharmacy,” Expert Opinion on Pharmacotherapy, vol. 5, no. 4, pp. 735–746, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Ryu, G. S. Jeon, N. R. Cashman, N. W. Kowall, and J. Lee, “Differential expression of c-Ret in motor neurons versus non-neuronal cells is linked to the pathogenesis of ALS,” Laboratory Investigation, vol. 91, no. 3, pp. 342–352, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Mitsuma, M. Yamamoto, M. Li et al., “Expression of GDNF receptor (RET and GDNFR-α) mRNAs in the spinal cord of patients with amyotrophic lateral sclerosis,” Brain Research, vol. 820, no. 1-2, pp. 77–85, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Yamamoto, M. Li, N. Mitsuma et al., “Preserved phosphorylation of RET receptor protein in spinal motor neurons of patients with amyotrophic lateral sclerosis: an immunohistochemical study by a phosphorylation-specific antibody at tyrosine 1062,” Brain Research, vol. 912, no. 1, pp. 89–94, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. GFRa Nomenclature Committee, “Nomenclature of GPI-linked receptors for the GDNF ligand family,” Neuron, vol. 19, no. 3, p. 485, 1997. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Takahashi and G. M. Cooper, “Ret transforming gene encodes a fusion protein homologous to tyrosine kinases,” Molecular and Cellular Biology, vol. 7, no. 4, pp. 1378–1385, 1987. View at Google Scholar · View at Scopus
  10. M. Takahashi, J. Ritz, and G. M. Cooper, “Activation of a novel human transforming gene, ret, by DNA rearrangement,” Cell, vol. 42, no. 2, pp. 581–588, 1985. View at Google Scholar · View at Scopus
  11. J. J. S. Treanor, L. Goodman, F. De Sauvage et al., “Characterization of a multicomponent receptor for GDNF,” Nature, vol. 382, no. 6586, pp. 80–83, 1996. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Trupp, E. Arenas, M. Fainzilber et al., “Functional receptor for GDNF encoded by the c-ret proto-oncogene,” Nature, vol. 381, no. 6585, pp. 785–789, 1996. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Ito, M. Yamamoto, M. Li et al., “Differential temporal expression of mRNAs for ciliary neurotrophic factor (CNTF), leukemia inhibitory factor (LIF), interleukin-6 (IL-6), and their receptors (CNTFR α, LIFRβ, IL-6R α and gp130) in injured peripheral nerves,” Brain Research, vol. 793, no. 1-2, pp. 321–327, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. V. Pachnis, B. Mankoo, and F. Costantini, “Expression of the c-ret proto-oncogene during mouse embryogenesis,” Development, vol. 119, no. 4, pp. 1005–1017, 1993. View at Google Scholar · View at Scopus
  15. T. Tsuzuki, M. Takahashi, N. Asai, T. Iwashita, M. Matsuyama, and J. Asai, “Spatial and temporal expression of the ret proto-oncongene product in embryonic, infant and adult rat tissues,” Oncogene, vol. 10, no. 1, pp. 191–198, 1995. View at Google Scholar · View at Scopus
  16. P. L. Durbec, L. B. Larsson-Blomberg, A. Schuchardt, F. Costantini, and V. Pachnis, “Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts,” Development, vol. 122, no. 1, pp. 349–358, 1996. View at Google Scholar · View at Scopus
  17. M. Trupp, E. Arenas, M. Fainzilber et al., “Functional receptor for GDNF encoded by the c-ret proto-oncogene,” Nature, vol. 381, no. 6585, pp. 785–789, 1996. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Watanabe, T. Harada, T. Ito et al., “Ret proto-oncogene product is a useful marker of lineage determination in the development of the enteric nervous system in rats,” Journal of Pediatric Surgery, vol. 32, no. 1, pp. 28–33, 1997. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Lucinia, L. D. ’Angeloa, M. Patrunob, F. Mascarellob, P. de Girolamoa, and L. Castaldoa, “GDNF family ligand RET receptor in the brain of adult zebrafish,” Neuroscience Letters, vol. 502, pp. 214–218, 2011. View at Google Scholar
  20. M. D. Gershon, A. L. Kirchgessner, and P. R. Wade, “Functional anatomy of the enteric nervous system,” in Physiology of the Gastrointestinal Tract, L. R. Johnson, Ed., pp. 381–422, Raven Press, New York, NY, USA, 3rd edition, 1994. View at Google Scholar
  21. M. D. Gershon, “Genes and lineages in the formation of the enteric nervous system,” Current Opinion in Neurobiology, vol. 7, no. 1, pp. 101–109, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Natale, L. Pasquali, A. Paparelli, and F. Fornai, “Parallel manifestations of neuropathologies in the enteric and central nervous systems,” Neurogastroenterology and Motility, vol. 23, no. 12, pp. 1056–1065, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. P. Sanchez, I. Silos-Santiago, J. Frisen, B. He, S. A. Lira, and M. Barbacid, “Renal agenesis and the absence of enteric neurons in mice lacking GDNF,” Nature, vol. 382, no. 6586, pp. 70–73, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Guoa, Q. Wanga, K. Zhanga et al., “HO-1 induction in motor cortex and intestinal dysfunction in TDP-43 A315T transgenic mice,” Brain Research, vol. 1460, pp. 214–218, 2012. View at Google Scholar
  25. D. J. Anderson, “Cellular and molecular biology of neural crest cell lineage determination,” Trends in Genetics, vol. 13, no. 7, pp. 276–280, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Bronner-Fraser, “Origins and developmental potential of the neural crest,” Experimental Cell Research, vol. 218, no. 2, pp. 405–417, 1995. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Ito and M. Sieber-Blum, “Pluripotent and developmentally restricted neural-crest-derived cells in posterior visceral arches,” Developmental Biology, vol. 156, no. 1, pp. 191–200, 1993. View at Publisher · View at Google Scholar · View at Scopus
  28. S. J. Morrison, P. M. White, C. Zock, and D. J. Anderson, “Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells,” Cell, vol. 96, no. 5, pp. 737–749, 1999. View at Google Scholar · View at Scopus
  29. S. E. Fraser and M. Bronner-Fraser, “Migrating neural crest cells in the trunk of the avian embryo are multipotent,” Development, vol. 112, no. 4, pp. 913–920, 1991. View at Google Scholar · View at Scopus
  30. L. Lo and D. J. Anderson, “Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities,” Neuron, vol. 15, no. 3, pp. 527–539, 1995. View at Publisher · View at Google Scholar · View at Scopus
  31. T. P. Rothman, N. M. Le Douarin, J. C. Fontaine-Perus, and M. D. Gershon, “Developmental potential of neural crest-derived cells migrating from segments of developing quail bowel back-grafted into younger chick host embryos,” Development, vol. 109, no. 2, pp. 411–423, 1990. View at Google Scholar · View at Scopus
  32. T. P. Rothman, D. Goldowitz, and M. D. Gershon, “Inhibition of migration of neural crest-derived cells by the abnormal mesenchyme of the presumptive aganglionic bowel of ls/ls mice: analysis with aggregation and interspecies chimeras,” Developmental Biology, vol. 159, no. 2, pp. 559–573, 1993. View at Publisher · View at Google Scholar · View at Scopus
  33. H. M. Young, A. J. Bergner, and T. Müller, “Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine,” Journal of Comparative Neurology, vol. 456, no. 1, pp. 1–11, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Patel, N. Harker, L. Moreira-Santos et al., “Differential RET signaling pathways drive development of the enteric lymphoid and nervous systems,” Science Signaling, vol. 5, no. 235, article ra55, 2012. View at Publisher · View at Google Scholar
  35. M. A. Parisi and R. P. Kapur, “Genetics of Hirschsprung disease,” Current Opinion in Pediatrics, vol. 12, no. 6, pp. 610–617, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Manié, M. Santoro, A. Fusco, and M. Billaud, “The RET receptor: function in development and dysfunction in congenital malformation,” Trends in Genetics, vol. 17, no. 10, pp. 580–589, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Ishii, T. Doi, K. Inoue et al., “Correlation between multiple RET mutations and severity of Hirschsprung’s disease,” Pediatric Surgery International, vol. 29, pp. 157–163, 2013. View at Google Scholar
  38. D. M. Rodrigues, A. Y. Li, D. G. Nair, and M. G. Blennerhassett, “Glial cell line-derived neurotrophic factor is a key neurotrophin in the postnatal enteric nervous system,” Neurogastroenterology and Motility, vol. 23, no. 2, pp. e44–e56, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. A. J. Porter, D. A. Wattchow, S. J. H. Brookes, and M. Costa, “The neurochemical coding and projections of circular muscle motor neurons in the human colon,” Gastroenterology, vol. 113, no. 6, pp. 1916–1923, 1997. View at Google Scholar · View at Scopus
  40. D. A. Wattchow, A. J. Porter, S. J. H. Brookes, and M. Costa, “The polarity of neurochemically defined myenteric neurons in the human colon,” Gastroenterology, vol. 113, no. 2, pp. 497–506, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Hens, J.-M. Vanderwinden, M.-H. De Laet, D. W. Scheuermann, and J.-P. Timmermans, “Morphological and neurochemical identification of enteric neurones with mucosal projections in the human small intestine,” Journal of Neurochemistry, vol. 76, no. 2, pp. 464–471, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. M. M. Hao and H. M. Young, “Development of enteric neuron diversity,” Journal of Cellular and Molecular Medicine, vol. 13, no. 7, pp. 1193–1210, 2009. View at Google Scholar
  43. B. Facello, L. Castaldo, L. De Martino, and C. Lucini, “Glial cell line-derived neurotrophic factor in Purkinje cells of adult zebrafish: an autocrine mode of action?” Neuroscience Letters, vol. 465, no. 2, pp. 133–137, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. K. A. Sharkey and E. J. Parr, “The enteric nervous system in intestinal inflammation,” Canadian Journal of Gastroenterology, vol. 10, no. 5, pp. 335–341, 1996. View at Google Scholar · View at Scopus
  45. M. Hanani, O. Ledder, V. Yutkin et al., “Regeneration of myenteric plexus in the mouse colon after experimental denervation with benzalkonium chloride,” Journal of Comparative Neurology, vol. 462, no. 3, pp. 315–327, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. F. S. Ramalho, G. C. Santos, L. N. Z. Ramalho, J. K. Kajiwara, and S. Zucoloto, “Myenteric neuron number after acute and chronic denervation of the proximal jejunum induced by benzalkonium chloride,” Neuroscience Letters, vol. 163, no. 1, pp. 74–76, 1993. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Filogamo and C. Cracco, “Models of neuronal plasticity and repair in the enteric nervous system: a review,” Italian Journal of Anatomy and Embryology, vol. 100, pp. 185–195, 1995. View at Google Scholar · View at Scopus
  48. M.-T. Liu, Y.-H. Kuan, J. Wang, R. Hen, and M. D. Gershon, “5-HT4 receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice,” Journal of Neuroscience, vol. 29, no. 31, pp. 9683–9699, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. D. L. Stemple and D. J. Anderson, “Isolation of a stem cell for neurons and glia from the mammalian neural crest,” Cell, vol. 71, no. 6, pp. 973–985, 1992. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Geuna, P. Borrione, and G. Filogamo, “Postnatal histogenesis in the peripheral nervous system,” International Journal of Developmental Neuroscience, vol. 20, no. 6, pp. 475–479, 2002. View at Publisher · View at Google Scholar · View at Scopus