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Stem Cells International
Volume 2016, Article ID 9695827, 13 pages
http://dx.doi.org/10.1155/2016/9695827
Research Article

Comparative Microarray Analysis of Proliferating and Differentiating Murine ENS Progenitor Cells

Institute of Clinical Anatomy and Cell Analysis, University of Tübingen, Österbergstrasse 3, 72074 Tübingen, Germany

Received 15 May 2015; Accepted 12 July 2015

Academic Editor: Kodandaramireddy Nalapareddy

Copyright © 2016 Peter Helmut Neckel 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. J. B. Furness, “The enteric nervous system and neurogastroenterology,” Nature Reviews Gastroenterology & Hepatology, vol. 9, no. 5, pp. 286–294, 2012. View at Publisher · View at Google Scholar
  2. D. Natarajan, M. Grigoriou, C. V. Marcos-Gutierrez, C. Atkins, and V. Pachnis, “Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture,” Development, vol. 126, no. 1, pp. 157–168, 1999. View at Google Scholar · View at Scopus
  3. G. M. Kruger, J. T. Mosher, S. Bixby, N. Joseph, T. Iwashita, and S. J. Morrison, “Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness,” Neuron, vol. 35, no. 4, pp. 657–669, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Metzger, P. M. Bareiss, T. Danker et al., “Expansion and differentiation of neural progenitors derived from the human adult enteric nervous system,” Gastroenterology, vol. 137, no. 6, pp. 2063.e4–2073.e4, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Metzger, C. Caldwell, A. J. Barlow, A. J. Burns, and N. Thapar, “Enteric nervous system stem cells derived from human gut mucosa for the treatment of aganglionic gut disorders,” Gastroenterology, vol. 136, no. 7, pp. 2214.e3–2225.e3, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. M. J. Saffrey, “Cellular changes in the enteric nervous system during ageing,” Developmental Biology, vol. 382, no. 1, pp. 344–355, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. M. D. Gershon, “Developmental determinants of the independence and complexity of the enteric nervous system,” Trends in Neurosciences, vol. 33, no. 10, pp. 446–456, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. F. Obermayr, R. Hotta, H. Enomoto, and H. M. Young, “Development and developmental disorders of the enteric nervous system,” Nature Reviews Gastroenterology and Hepatology, vol. 10, no. 1, pp. 43–57, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. R. J. Rintala and M. P. Pakarinen, “Long-term outcomes of Hirschsprung's disease,” Seminars in Pediatric Surgery, vol. 21, no. 4, pp. 336–343, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. T. A. Heanue and V. Pachnis, “Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies,” Nature Reviews Neuroscience, vol. 8, no. 6, pp. 466–479, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Becker, J. Peterson, S. Kulkarni, and P. J. Pasricha, “Ex vivo neurogenesis within enteric ganglia occurs in a PTEN dependent manner,” PLoS ONE, vol. 8, no. 3, Article ID e59452, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Uesaka, M. Nagashimada, and H. Enomoto, “GDNF signaling levels control migration and neuronal differentiation of enteric ganglion precursors,” The Journal of Neuroscience, vol. 33, no. 41, pp. 16372–16382, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. T. A. Heanue and V. Pachnis, “Expression profiling the developing mammalian enteric nervous system identifies marker and candidate Hirschsprung disease genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 6919–6924, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. B. P. S. Vohra, K. Tsuji, M. Nagashimada et al., “Differential gene expression and functional analysis implicate novel mechanisms in enteric nervous system precursor migration and neuritogenesis,” Developmental Biology, vol. 298, no. 1, pp. 259–271, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Mohr, P. Neckel, Y. Zhang et al., “Molecular and cell biological effects of 3,5,3′-triiodothyronine on progenitor cells of the enteric nervous system in vitro,” Stem Cell Research, vol. 11, no. 3, pp. 1191–1205, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Fleige and M. W. Pfaffl, “RNA integrity and the effect on the real-time qRT-PCR performance,” Molecular Aspects of Medicine, vol. 27, no. 2-3, pp. 126–139, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. S. L. Kline, I. M. Cheeseman, T. Hori, T. Fukagawa, and A. Desai, “The human Mis12 complex is required for kinetochore assembly and proper chromosome segregation,” The Journal of Cell Biology, vol. 173, no. 1, pp. 9–17, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. E. D. Salmon, D. Cimini, L. A. Cameron, and J. G. DeLuca, “Merotelic kinetochores in mammalian tissue cells,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 360, no. 1455, pp. 553–568, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. A. A. Ye and T. J. Maresca, “Cell division: kinetochores SKAdaddle,” Current Biology, vol. 23, no. 3, pp. R122–R124, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Lu, Z. Wang, L. Ge, N. Chen, and H. Liu, “The RZZ complex and the spindle assembly checkpoint,” Cell Structure and Function, vol. 34, no. 1, pp. 31–45, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. D. G. Johnson and C. L. Walker, “Cyclins and cell cycle checkpoints,” Annual Review of Pharmacology and Toxicology, vol. 39, pp. 295–312, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Malumbres, E. Harlow, T. Hunt et al., “Cyclin-dependent kinases: a family portrait,” Nature Cell Biology, vol. 11, no. 11, pp. 1275–1276, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. V. Gómez-Gaviro, C. E. Scott, A. K. Sesay et al., “Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 4, pp. 1317–1322, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Khodosevich, Y. Watanabe, and H. Monyer, “EphA4 preserves postnatal and adult neural stem cells in an undifferentiated state in vivo,” Journal of Cell Science, vol. 124, no. 8, pp. 1268–1279, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Abranches, M. Silva, L. Pradier et al., “Neural differentiation of embryonic stem cells in vitro: a road map to neurogenesis in the embryo,” PLoS ONE, vol. 4, no. 7, Article ID e6286, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Balasubramaniyan, N. Timmer, B. Kust, E. Boddeke, and S. Copray, “Transient expression of Olig1 initiates the differentiation of neural stem cells into oligodendrocyte progenitor cells,” Stem Cells, vol. 22, no. 6, pp. 878–882, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Kolatsi-Joannou, X. Z. Li, T. Suda, H. T. Yuan, and A. S. Woolf, “In early development of the rat mRNA for the major myelin protein P0 is expressed in nonsensory areas of the embryonic inner ear, notochord, enteric nervous system, and olfactory ensheathing cells,” Developmental Dynamics, vol. 222, no. 1, pp. 40–51, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. M. I. Morris, D. B.-D. Soglio, A. Ouimet, A. Aspirot, and N. Patey, “A study of calretinin in Hirschsprung pathology, particularly in total colonic aganglionosis,” Journal of Pediatric Surgery, vol. 48, no. 5, pp. 1037–1043, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. K. R. Jessen and R. Mirsky, “Glial cells in the enteric nervous system contain glial fibrillary acidic protein,” Nature, vol. 286, no. 5774, pp. 736–737, 1980. View at Publisher · View at Google Scholar · View at Scopus
  30. T. J. Siddiqui, R. Pancaroglu, Y. Kang, A. Rooyakkers, and A. M. Craig, “LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development,” The Journal of Neuroscience, vol. 30, no. 22, pp. 7495–7506, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Chen, O. Gil, Y. Q. Ren, G. Zanazzi, J. L. Salzer, and D. E. Hillman, “Neurotrimin expression during cerebellar development suggests roles in axon fasciculation and synaptogenesis,” Journal of Neurocytology, vol. 30, no. 11, pp. 927–937, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Janz and T. C. Südhof, “SV2C is a synaptic vesicle protein with an unusually restricted localization: anatomy of a synaptic vesicle protein family,” Neuroscience, vol. 94, no. 4, pp. 1279–1290, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. B. Marquèze, F. Berton, and M. Seagar, “Synaptotagmins in membrane traffic: which vesicles do the tagmins tag?” Biochimie, vol. 82, no. 5, pp. 409–420, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. B. C. Jongbloets and R. J. Pasterkamp, “Semaphorin signalling during development,” Development, vol. 141, no. 17, pp. 3292–3297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Metzger, S. Conrad, T. Skutella, and L. Just, “RGMa inhibits neurite outgrowth of neuronal progenitors from murine enteric nervous system via the neogenin receptor in vitro,” Journal of Neurochemistry, vol. 103, no. 6, pp. 2665–2678, 2007. View at Google Scholar · View at Scopus
  36. J. M. Spin, S. Nallamshetty, R. Tabibiazar et al., “Transcriptional profiling of in vitro smooth muscle cell differentiation identifies specific patterns of gene and pathway activation,” Physiological Genomics, vol. 19, pp. 292–302, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. J. M. Baisden, Y. Qian, H. M. Zot, and D. C. Flynn, “The actin filament-associated protein AFAP-110 is an adaptor protein that modulates changes in actin filament integrity,” Oncogene, vol. 20, no. 44, pp. 6435–6447, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. L. E. Peri, K. M. Sanders, and V. N. Mutafova-Yambolieva, “Differential expression of genes related to purinergic signaling in smooth muscle cells, PDGFRα-positive cells, and interstitial cells of Cajal in the murine colon,” Neurogastroenterology & Motility, vol. 25, no. 9, pp. e609–e620, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. S. J. Winder, B. G. Allen, O. Clément-Chomienne, and M. P. Walsh, “Regulation of smooth muscle actin—myosin interaction and force by calponin,” Acta Physiologica Scandinavica, vol. 164, no. 4, pp. 415–426, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. M. L. Mancini, J. M. Verdi, B. A. Conley et al., “Endoglin is required for myogenic differentiation potential of neural crest stem cells,” Developmental Biology, vol. 308, no. 2, pp. 520–533, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. F. T. L. van der Loop, G. Schaart, E. D. J. Timmer, F. C. S. Ramaekers, and G. J. J. M. van Eys, “Smoothelin, a novel cytoskeletal protein specific for smooth muscle cells,” The Journal of Cell Biology, vol. 134, no. 2, pp. 401–411, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. M. A. D'Angelo, J. S. Gomez-Cavazos, A. Mei, D. H. Lackner, and M. W. Hetzer, “A change in nuclear pore complex composition regulates cell differentiation,” Developmental Cell, vol. 22, no. 2, pp. 446–458, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. J. J.-C. Lin, Y. Li, R. D. Eppinga, Q. Wang, and J.-P. Jin, “Chapter 1: roles of caldesmon in cell motility and actin cytoskeleton remodeling,” International Review of Cell and Molecular Biology, vol. 274, pp. 1–68, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. S. B. Marston and C. W. J. Smith, “The thin filaments of smooth muscles,” Journal of Muscle Research and Cell Motility, vol. 6, no. 6, pp. 669–708, 1985. View at Publisher · View at Google Scholar · View at Scopus
  45. K. M. Sanders and S. M. Ward, “Kit mutants and gastrointestinal physiology,” The Journal of Physiology, vol. 578, no. 1, pp. 33–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. L. S. Campos, “Neurospheres: insights into neural stem cell biology,” Journal of Neuroscience Research, vol. 78, no. 6, pp. 761–769, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Ring, Y.-M. Kim, and M. Kahn, “Wnt/catenin signaling in adult stem cell physiology and disease,” Stem Cell Reviews and Reports, vol. 10, no. 4, pp. 512–525, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. D. C. Berwick and K. Harvey, “LRRK2: an éminence grise of Wnt-mediated neurogenesis?” Frontiers in Cellular Neuroscience, vol. 7, article 82, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Kakugawa, P. F. Langton, M. Zebisch et al., “Notum deacylates Wnt proteins to suppress signalling activity,” Nature, vol. 519, no. 7542, pp. 187–192, 2015. View at Publisher · View at Google Scholar
  50. Y. Mii and M. Taira, “Secreted Wnt ‘inhibitors’ are not just inhibitors: regulation of extracellular Wnt by secreted Frizzled-related proteins,” Development Growth & Differentiation, vol. 53, no. 8, pp. 911–923, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Kawano and R. Kypta, “Secreted antagonists of the Wnt signalling pathway,” Journal of Cell Science, vol. 116, part 13, pp. 2627–2634, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Ohazama, E. B. Johnson, M. S. Ota et al., “Lrp4 modulates extracellular integration of cell signaling pathways in development,” PLoS ONE, vol. 3, no. 12, Article ID e4092, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Ding, Y. Zhang, C. Xu, Q.-H. Tao, and Y.-G. Chen, “HECT domain-containing E3 ubiquitin ligase NEDD4L negatively regulates Wnt signaling by targeting dishevelled for proteasomal degradation,” The Journal of Biological Chemistry, vol. 288, no. 12, pp. 8289–8298, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Ishikawa, S. Kitajima, Y. Takahashi et al., “Mouse Nkd1, a Wnt antagonist, exhibits oscillatory gene expression in the PSM under the control of Notch signaling,” Mechanisms of Development, vol. 121, no. 12, pp. 1443–1453, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. D. W. Chan, C.-Y. Chan, J. W. P. Yam, Y.-P. Ching, and I. O. L. Ng, “Prickle-1 negatively regulates Wnt/β-catenin pathway by promoting Dishevelled ubiquitination/degradation in liver cancer,” Gastroenterology, vol. 131, no. 4, pp. 1218–1227, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. K. Sakamoto, S. Yamaguchi, R. Ando et al., “The nephroblastoma overexpressed gene (NOV/ccn3) protein associates with Notch1 extracellular domain and inhibits myoblast differentiation via Notch signaling pathway,” The Journal of Biological Chemistry, vol. 277, no. 33, pp. 29399–29405, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Caruso, M. Motolese, L. Iacovelli et al., “Inhibition of the canonical Wnt signaling pathway by apolipoprotein E4 in PC12 cells,” Journal of Neurochemistry, vol. 98, no. 2, pp. 364–371, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. A. J. Hanson, H. A. Wallace, T. J. Freeman, R. D. Beauchamp, L. A. Lee, and E. Lee, “XIAP monoubiquitylates Groucho/TLE to promote canonical Wnt signaling,” Molecular Cell, vol. 45, no. 5, pp. 619–628, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Takai, H. Inomata, A. Arakawa, R. Yakura, M. Matsuo-Takasaki, and Y. Sasai, “Anterior neural development requires Del1, a matrix-associated protein that attenuates canonical Wnt signaling via the Ror2 pathway,” Development, vol. 137, no. 19, pp. 3293–3302, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Katoh and M. Katoh, “FGF signaling inhibitor, SPRY4, is evolutionarily conserved target of WNT signaling pathway in progenitor cells,” International Journal of Molecular Medicine, vol. 17, no. 3, pp. 529–532, 2006. View at Google Scholar · View at Scopus
  61. P. Ordóñez-Morán, A. Irmisch, A. Barbáchano et al., “SPROUTY2 is a β-catenin and FOXO3a target gene indicative of poor prognosis in colon cancer,” Oncogene, vol. 33, no. 15, pp. 1975–1985, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Taketomi, D. Yoshiga, K. Taniguchi et al., “Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia,” Nature Neuroscience, vol. 8, no. 7, pp. 855–857, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Di Liddo, T. Bertalot, A. Schuster et al., “Anti-inflammatory activity of Wnt signaling in enteric nervous system: in vitro preliminary evidences in rat primary cultures,” Journal of Neuroinflammation, vol. 12, no. 1, p. 23, 2015. View at Publisher · View at Google Scholar