Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2019, Article ID 3947123, 9 pages
https://doi.org/10.1155/2019/3947123
Review Article

Netrin Family: Role for Protein Isoforms in Cancer

1Amsterdam UMC, University of Amsterdam, Department of Vascular Medicine, Location Meibergdreef, Amsterdam, Netherlands
2Leiden University Medical Center, Department of Internal Medicine, Einthoven Laboratory for Vascular and Regenerative Medicine, Leiden, Netherlands

Correspondence should be addressed to Janine Maria van Gils; ln.cmul@slignav.mj

Received 7 December 2018; Accepted 6 February 2019; Published 24 February 2019

Guest Editor: Vladimir Majerciak

Copyright © 2019 Caroline Suzanne Bruikman 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. H. Schlüter, R. Apweiler, H. Holzhütter, and P. R. Jungblut, “Finding one's way in proteomics: a protein species nomenclature,” Chemistry Central Journal, vol. 3, no. 1, p. 11, 2009. View at Publisher · View at Google Scholar
  2. P. J. Grabowski and D. L. Black, “Alternative RNA splicing in the nervous system,” Progress in Neurobiology, vol. 65, no. 3, pp. 289–308, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. M. A. Garcia-Blanco, A. P. Baraniak, and E. L. Lasda, “Alternative splicing in disease and therapy,” Nature Biotechnology, vol. 22, no. 5, pp. 535–546, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Aoki-Suzuki, K. Yamada, J. Meerabux et al., “A family-based association study and gene expression analyses of netrin-G1 and -G2 genes in schizophrenia,” Biological Psychiatry, vol. 57, no. 4, pp. 382–393, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Klinck, A. Bramard, L. Inkel et al., “Multiple alternative splicing markers for ovarian cancer,” Cancer Research, vol. 68, no. 3, pp. 657–663, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. J. P. Venables, R. Klinck, C. Koh et al., “Cancer-associated regulation of alternative splicing,” Nature Structural & Molecular Biology, vol. 16, no. 6, pp. 670–676, 2009. View at Publisher · View at Google Scholar
  7. H. Climente-Gonzalez, E. Porta-Pardo, A. Godzik, E. Eyras et al., “The functional impact of alternative splicing in cancer,” Cell Reports, vol. 20, no. 9, pp. 2215–2226, 2017. View at Publisher · View at Google Scholar
  8. S. C.-W. Lee and O. Abdel-Wahab, “Therapeutic targeting of splicing in cancer,” Nature Medicine, vol. 22, no. 9, pp. 976–986, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. Z.-X. Lu, Q. Huang, J. W. Park et al., “Transcriptome-wide landscape of pre-mRNA alternative splicing associated with metastatic colonization,” Molecular Cancer Research, vol. 13, no. 2, pp. 305–318, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. J. L. Trincado, E. Sebestyén, A. Pagés, and E. Eyras, “The prognostic potential of alternative transcript isoforms across human tumors,” Genome Medicine, vol. 8, no. 1, p. 85, 2016. View at Publisher · View at Google Scholar
  11. B. J. Dickson, “Molecular mechanisms of axon guidance,” Science, vol. 298, no. 5600, pp. 1959–1964, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. N. P. Ly, K. Komatsuzaki, I. P. Fraser et al., “Netrin-1 inhibits leukocyte migration in vitro and in vivo,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 102, no. 41, pp. 14729–14734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. X. Mao, H. Xing, A. Mao et al., “Netrin-1 attenuates cardiac ischemia reperfusion injury and generates alternatively activated macrophages,” Inflammation, vol. 37, no. 2, pp. 573–580, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Delloye-Bourgeois, D. Goldschneider, A. Paradisi et al., “Nucleolar localization of a netrin-1 isoform enhances tumor cell proliferation,” Science Signaling, vol. 5, no. 236, p. ra57, 2012. View at Publisher · View at Google Scholar
  15. H. Arakawa, “Netrin-1 and its receptors in tumorigenesis,” Nature Reviews Cancer, vol. 4, no. 12, pp. 978–987, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. J. M. Van Gils, B. Ramkhelawon, L. Fernandes et al., “Endothelial expression of guidance cues in vessel wall homeostasis dysregulation under proatherosclerotic conditions,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 5, pp. 911–919, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. V. Cirulli and M. Yebra, “Netrins: beyond the brain,” Nature Reviews Molecular Cell Biology, vol. 8, no. 4, pp. 296–306, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. E. M. Yimer, K. A. Zewdie, and H. Z. Hishe, “Netrin as a novel biomarker and its therapeutic implications in diabetes mellitus and diabetes-associated complications,” Journal of Diabetes Research, vol. 2018, Article ID 8250521, 2018. View at Google Scholar · View at Scopus
  19. I. Ylivinkka, J. Keski-Oja, and M. Hyytiäinen, “Netrin-1: a regulator of cancer cell motility?” European Journal of Cell Biology, vol. 95, no. 11, pp. 513–520, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Wang, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, and M. Tessier-Lavigne, “Netrin-3, a mouse homolog of human NTN2L, is highly expressed in sensory ganglia and shows differential binding to netrin receptors,” The Journal of Neuroscience, vol. 19, no. 12, pp. 4938–4947, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Nakashiba, T. Ikeda, S. Nishimura et al., “Netrin-G1: a novel glycosyl phosphatidylinositol-linked mammalian netrin that is functionally divergent from classical netrins,” The Journal of Neuroscience, vol. 20, no. 17, pp. 6540–6550, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Yamagishi, K. Yamada, M. Sawada et al., “Netrin-5 is highly expressed in neurogenic regions of the adult brain,” Frontiers in Cellular Neuroscience, vol. 9, 2015. View at Google Scholar · View at Scopus
  23. T. Serafini, T. E. Kennedy, M. J. Galko, C. Mirzayan, T. M. Jessell, and M. Tessier-Lavigne, “The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6,” Cell, vol. 78, no. 3, pp. 409–424, 1994. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Carmeliet, “Blood vessels and nerves: common signals, pathways and diseases,” Nature Reviews Genetics, vol. 4, no. 9, pp. 710–720, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. S. D. Funk and A. W. Orr, “Ephs and ephrins resurface in inflammation, immunity, and atherosclerosis,” Pharmacological Research, vol. 67, no. 1, pp. 42–52, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Mirakaj and P. Rosenberger, “Immunomodulatory functions of neuronal guidance proteins,” Trends in Immunology, vol. 38, no. 6, pp. 444–456, 2017. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Zhang, D. Vreeken, C. S. Bruikman, A. J. van Zonneveld, and J. M. van Gils, “Understanding netrins and semaphorins in mature endothelial cell biology,” Pharmacological Research, vol. 137, pp. 1–10, 2018. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Fitamant, C. Guenebeaud, M. Coissieux et al., “Netrin-1 expression confers a selective advantage for tumor cell survival in metastatic breast cancer,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 105, no. 12, pp. 4850–4855, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Delloye-Bourgeois, J. Fitamant, A. Paradisi et al., “Netrin-1 acts as a survival factor for aggressive neuroblastoma,” The Journal of Experimental Medicine, vol. 206, no. 4, pp. 833–847, 2009. View at Publisher · View at Google Scholar
  30. L. Dumartin, C. Quemener, H. Laklai et al., “Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells,” Gastroenterology, vol. 138, no. 4, pp. 1595–1606, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Kaufmann, S. Kuphal, T. Schubert, and A. K. Bosserhoff, “Functional implication of Netrin expression in malignant melanoma,” Cellular Oncology, vol. 31, no. 6, pp. 415–422, 2009. View at Google Scholar
  32. T. Tu, C. Zhang, H. Yan et al., “CD146 acts as a novel receptor for netrin-1 in promoting angiogenesis and vascular development,” Cell Research, vol. 25, no. 3, pp. 275–287, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. Q. Zeng, Z. Wu, H. Duan et al., “Impaired tumor angiogenesis and VEGF-induced pathway in endothelial CD146 knockout mice,” Protein & Cell, vol. 5, no. 6, pp. 445–456, 2014. View at Publisher · View at Google Scholar
  34. J. M. van Gils, M. C. Derby, L. R. Fernandes, B. Ramkhelawon, T. D. Ray et al., “The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques,” Nature Immunology, vol. 13, no. 2, pp. 136–143, 2012. View at Publisher · View at Google Scholar
  35. S. Aras and M. Raza Zaidi, “TAMeless traitors: macrophages in cancer progression and metastasis,” British Journal of Cancer, vol. 117, no. 11, pp. 1583–1591, 2017. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Paradisi and P. Mehlen, “Netrin-1, a missing link between chronic inflammation and tumor progression,” Cell Cycle, vol. 9, no. 7, pp. 1253–1262, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Paradisi, C. Maisse, A. Bernet et al., “NF-kappaB regulates netrin-1 expression and affects the conditional tumor suppressive activity of the netrin-1 receptors,” Gastroenterology, vol. 135, no. 4, pp. 1248–1257, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Mehlen, S. Rabizadeh, S. J. Snipas, N. Assa-Munt, G. S. Salvesen, and D. E. Bredesen, “The DCC gene product induces apoptosis by a mechanism requiring receptor proteolysis,” Nature, vol. 395, no. 6704, pp. 801–804, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Mehlen and C. Furne, “Netrin-1: when a neuronal guidance cue turns out to be a regulator of tumorigenesis,” Cellular and Molecular Life Sciences, vol. 62, no. 22, pp. 2599–2616, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. F. Llambi, F. Causeret, E. Bloch-Gallego, and P. Mehlen, “Netrin-1 acts as a survival factor via its receptors UNC5H and DCC,” EMBO Journal, vol. 20, no. 11, pp. 2715–2722, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Wang, Z. Wei, H. Jin et al., “Autoinhibition of UNC5b revealed by the cytoplasmic domain structure of the receptor,” Molecular Cell, vol. 33, no. 6, pp. 692–703, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Mazelin, A. Bernet, C. Bonod-Bidaud et al., “Netrin-1 controls colorectal tumorigenesis by regulating apoptosis,” Nature, vol. 431, no. 7004, pp. 80–84, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Tanikawa, K. Matsuda, S. Fukuda, Y. Nakamura, and H. Arakawa, “p53RDL1 regulates p53-dependent apoptosis,” Nature Cell Biology, vol. 5, no. 3, pp. 216–223, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Bernet, L. Mazelin, M.-M. Coissieux et al., “Inactivation of the UNC5C netrin-1 receptor is associated with tumor progression in colorectal malignancies,” Gastroenterology, vol. 133, no. 6, pp. 1840–1848, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. A. D. Papanastasiou, G. Pampalakis, D. Katsaros, and G. Sotiropoulou, “Netrin-1 overexpression is predictive of ovarian malignancies,” Oncotarget , vol. 2, no. 5, pp. 363–367, 2011. View at Google Scholar · View at Scopus
  46. A. Paradisi, C. Maisse, M.-M. Coissieux et al., “Netrin-1 up-regulation in inflammatory bowel diseases is required for colorectal cancer progression,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 106, no. 40, pp. 17146–17151, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. P. N. Harter, J. Zinke, A. Scholz et al., “Netrin-1 expression is an independent prognostic factor for poor patient survival in brain metastases,” PLoS ONE, vol. 9, no. 3, p. e92311, 2014. View at Publisher · View at Google Scholar
  48. G. Passacquale, A. Phinikaridou, C. Warboys et al., “Aspirin-induced histone acetylation in endothelial cells enhances synthesis of the secreted isoform of netrin-1 thus inhibiting monocyte vascular infiltration,” British Journal of Pharmacology, vol. 172, no. 14, pp. 3548–3564, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. T. UniProt Consortium, “UniProt: the universal protein knowledgebase,” Nucleic Acids Research, vol. 46, no. 5, p. 2699, 2018. View at Publisher · View at Google Scholar
  50. T. J. Van Raay, S. M. Foskett, T. D. Connors, K. W. Klinger, G. M. Landes, and T. C. Burn, “The NTN2L gene encoding a novel human netrin maps to the autosomal dominant polycystic kidney disease region on chromosome 16p13.3,” Genomics, vol. 41, no. 2, pp. 279–282, 1997. View at Publisher · View at Google Scholar · View at Scopus
  51. A. W. Püschel, “Divergent properties of mouse netrins,” Mechanisms of Development, vol. 83, no. 1-2, pp. 65–75, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. E. T. Wang, R. Sandberg, S. Luo et al., “Alternative isoform regulation in human tissue transcriptomes,” Nature, vol. 456, no. 7221, pp. 470–476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Latil, L. Chêne, B. Cochant-Priollet et al., “Quantification of expression of netrins, slits and their receptors in human prostate tumors,” International Journal of Cancer, vol. 103, no. 3, pp. 306–315, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Yin, J. R. Sanes, and J. H. Miner, “Identification and expression of mouse netrin-4,” Mechanisms of Development, vol. 96, no. 1, pp. 115–119, 2000. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Koch, J. R. Murrell, D. D. Hunter et al., “A novel member of the netrin family, beta-netrin, shares homology with the beta chain of laminin: identification, expression, and functional characterization,” The Journal of Cell Biology, vol. 151, no. 2, pp. 221–234, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Qin, L. Yu, Y. Gao, R. Zhou, and C. Zhang, “Characterization of the receptors for axon guidance factor netrin-4 and identification of the binding domains,” Molecular and Cellular Neuroscience, vol. 34, no. 2, pp. 243–250, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. F. I. Staquicini, E. Dias-Neto, J. Li et al., “Discovery of a functional protein complex of netrin-4, laminin γ1 chain, and integrin α6β1 in mouse neural stem cells,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 106, no. 8, pp. 2903–2908, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Zhang, F. Meng, C. Wang et al., “Identification of a novel alternative splicing form of human netrin-4 and analyzing the expression patterns in adult rat brain,” Molecular Brain Research, vol. 130, no. 1-2, pp. 68–80, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Hayano, K. Sasaki, N. Ohmura et al., “Netrin-4 regulates thalamocortical axon branching in an activity-dependent fashion,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 111, no. 42, pp. 15226–15231, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Enoki, T. Sato, S. Kokabu et al., “Netrin-4 promotes differentiation and migration of osteoblasts,” In Vivo, vol. 31, no. 5, pp. 793–799, 2018. View at Publisher · View at Google Scholar
  61. Y. Hu, I. Ylivinkka, P. Chen et al., “Netrin-4 promotes glioblastoma cell proliferation through integrin β4 signaling,” Neoplasia, vol. 14, no. 3, pp. 219–227, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. L. Li, Y. Hu, I. Ylivinkka et al., “Netrin-4 protects glioblastoma cells from temozolomide induced senescence,” PLoS ONE, vol. 8, no. 11, Article ID e80363, 2013. View at Publisher · View at Google Scholar
  63. Y. Yuan, M. Leszczynska, S. Konstantinovsky, C. G. Tropé, R. Reich, and B. Davidson, “Netrin-4 is upregulated in breast carcinoma effusions compared to corresponding solid tumors,” Diagnostic Cytopathology, vol. 39, no. 8, pp. 562–566, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Esseghir, A. Kennedy, P. Seedhar et al., “Identification of NTN4, TRA1, and STC2 as prognostic markers in breast cancer in a screen for signal sequence encoding proteins,” Clinical Cancer Research, vol. 13, no. 11, pp. 3164–3173, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Srivastava, B. Thakkar, K. G. Yeoh et al., “Expression of proteins associated with hypoxia and Wnt pathway activation is of prognostic significance in hepatocellular carcinoma,” Virchows Archiv, vol. 466, no. 5, pp. 541–548, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. A. D. Thakkar, H. Raj, D. Chakrabarti et al., “Identification of gene expression signature in estrogen receptor positive breast carcinoma,” Biomarkers in Cancer, vol. 2, pp. 1–15, 2010. View at Publisher · View at Google Scholar
  67. B. Lv, C. Song, L. Wu et al., “Netrin-4 as a biomarker promotes cell proliferation and invasion in gastric cancer,” Oncotarget, vol. 6, no. 12, pp. 9794–9806, 2015. View at Publisher · View at Google Scholar
  68. A. A. Villanueva, P. Falcón, N. Espinoza et al., “The Netrin-4/Neogenin-1 axis promotes neuroblastoma cell survival and migration,” Oncotarget , vol. 8, no. 6, pp. 9767–9782, 2017. View at Google Scholar · View at Scopus
  69. A. Jayachandran, P. Prithviraj, P.-H. Lo et al., “Identifying and targeting determinants of melanoma cellular invasion,” Oncotarget , vol. 7, no. 27, pp. 41186–41202, 2016. View at Google Scholar · View at Scopus
  70. F. Larrieu-Lahargue, A. L. Welm, K. R. Thomas, and D. Y. Li, “Netrin-4 induces lymphangiogenesis in vivo,” Blood, vol. 115, no. 26, pp. 5418–5426, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. E. Lejmi, L. Leconte, S. Pédron-Mazoyer et al., “Netrin-4 inhibits angiogenesis via binding to neogenin and recruitment of Unc5B,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 105, no. 34, pp. 12491–12496, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Dakouane-Giudicelli, S. Brouillet, W. Traboulsi et al., “Inhibition of human placental endothelial cell proliferation and angiogenesis by netrin-4,” Placenta, vol. 36, no. 11, pp. 1260–1265, 2015. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. N. Li, G. Pinzón-Duarte, M. Dattilo, T. Claudepierre, M. Koch, and W. J. Brunken, “The expression and function of netrin-4 in murine ocular tissues,” Experimental Eye Research, vol. 96, no. 1, pp. 24–35, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. C. Eveno, D. Broqueres-You, J. Feron et al., “Netrin-4 delays colorectal cancer carcinomatosis by inhibiting tumor angiogenesis,” The American Journal of Pathology, vol. 178, no. 4, pp. 1861–1869, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. A.-K. B. Maier, S. Klein, N. Kociok et al., “Netrin-4 mediates corneal hemangiogenesis but not lymphangiogenesis in the mouse-model of suture-induced neovascularization,” Investigative Ophthalmology & Visual Science, vol. 58, no. 3, pp. 1387–1396, 2017. View at Publisher · View at Google Scholar · View at Scopus
  76. Y. Han, Y. Shao, T. Liu et al., “Therapeutic effects of topical netrin-4 inhibits corneal neovascularization in alkali-burn rats,” PLoS ONE, vol. 10, no. 4, p. e0122951, 2015. View at Publisher · View at Google Scholar
  77. A. M. Garrett, T. J. Jucius, L. P. R. Sigaud et al., “Analysis of expression pattern and genetic deletion of Netrin5 in the developing mouse,” Frontiers in Molecular Neuroscience, vol. 9, 2016. View at Google Scholar · View at Scopus
  78. C. M. Batista, E. D. Mariano, B. J. A. P. Barbosa et al., “Adult neurogenesis and glial oncogenesis: when the process fails,” BioMed Research International, vol. 2014, Article ID 438639, 10 pages, 2014. View at Publisher · View at Google Scholar
  79. D. S. Gerhard, L. Wagner, E. A. Feingold, C. M. Shenmen, L. H. Grouse et al., “The status, quality, and expansion of the NIH full-length cDNA project: the mammalian gene collection (MGC),” Genome Research, vol. 14, no. 10b, pp. 2121–2127, 2004. View at Publisher · View at Google Scholar
  80. Y. Yin, J. H. Miner, and J. R. Sanes, “Laminets: laminin- and netrin-related genes expressed in distinct neuronal subsets,” Molecular and Cellular Neuroscience, vol. 19, no. 3, pp. 344–358, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. J. C. Lin, W.-H. Ho, A. Gurney, and A. Rosenthal, “The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons,” Nature Neuroscience, vol. 6, no. 12, pp. 1270–1276, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. H. Matsukawa, S. Akiyoshi-Nishimura, Q. Zhang et al., “Netrin-G/NGL complexes encode functional synaptic diversification,” The Journal of Neuroscience, vol. 34, no. 47, pp. 15779–15792, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Nishimura-Akiyoshi, K. Niimi, T. Nakashiba, and S. Itohara, “Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 104, no. 37, pp. 14801–14806, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. D. Orozco and D. Edbauer, “FUS-mediated alternative splicing in the nervous system: Consequences for ALS and FTLD,” Journal of Molecular Medicine, vol. 91, no. 12, pp. 1343–1354, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. J. M. A. Meerabux, H. Ohba, M. Fukasawa et al., “Human netrin-G1 isoforms show evidence of differential expression,” Genomics, vol. 86, no. 1, pp. 112–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. T. Nakashiba, S. Nishimura, T. Ikeda, and S. Itohara, “Complementary expression and neurite outgrowth activity of netrin-G subfamily members,” Mechanisms of Development, vol. 111, no. 1-2, pp. 47–60, 2002. View at Publisher · View at Google Scholar · View at Scopus
  87. G. Wei, X. Deng, S. Agarwal, S. Iwase, C. Disteche, and J. Xu, “Patient mutations of the intellectual disability gene KDM5C downregulate netrin G2 and suppress neurite growth in neuro2a cells,” Journal of Molecular Neuroscience, vol. 60, no. 1, pp. 33–45, 2016. View at Publisher · View at Google Scholar · View at Scopus
  88. W. Zhang, I. Rajan, K. V. Savelieva et al., “Netrin-G2 and netrin-G2 ligand are both required for normal auditory responsiveness,” Genes, Brain and Behavior, vol. 7, no. 4, pp. 385–392, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. N. Amira, G. Cancel-Tassin, S. Bernardini et al., “Expression in bladder transitional cell carcinoma by real-time quantitative reverse transcription polymerase chain reaction array of 65 genes at the tumor suppressor locus 9q34.1-2: identification of 5 candidates tumor suppressor genes,” International Journal of Cancer, vol. 111, no. 4, pp. 539–542, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. C. Cavard, A. Audebourg, F. Letourneur et al., “Gene expression profiling provides insights into the pathways involved in solid pseudopapillary neoplasm of the pancreas,” The Journal of Pathology, vol. 218, no. 2, pp. 201–209, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. H. F. Clark, A. L. Gurney, E. Abaya et al., “The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: a bioinformatics assessment,” Genome Research, vol. 13, pp. 2265–2270, 2003. View at Publisher · View at Google Scholar
  92. K. Miloudi, F. Binet, A. Wilson et al., “Truncated netrin-1 contributes to pathological vascular permeability in diabetic retinopathy,” The Journal of Clinical Investigation, vol. 126, no. 8, pp. 3006–3022, 2016. View at Publisher · View at Google Scholar · View at Scopus