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BioMed Research International
Volume 2015, Article ID 134050, 21 pages
http://dx.doi.org/10.1155/2015/134050
Research Article

Identification of Glioblastoma Phosphotyrosine-Containing Proteins with Two-Dimensional Western Blotting and Tandem Mass Spectrometry

Tianyao Guo,1,2,3 Xiaowei Wang,1,2,3 Maoyu Li,1,2,3 Haiyan Yang,1,2,3 Ling Li,1 Fang Peng,1,2,3 and Xianquan Zhan1,2,3,4

1Key Laboratory of Cancer Proteomics of Chinese Ministry of Health, Xiangya Hospital, Central South University, 87 Xiangya Road, Changsha, Hunan 410008, China
2Hunan Engineering Laboratory for Structural Biology and Drug Design, Xiangya Hospital, Central South University, 87 Xiangya Road, Changsha, Hunan 410008, China
3State Local Joint Engineering Laboratory for Anticancer Drugs, Xiangya Hospital, Central South University, 87 Xiangya Road, Changsha, Hunan 410008, China
4The State Key Laboratory of Medical Genetics, Central South University, 88 Xiangya Road, Changsha, Hunan 410008, China

Received 11 June 2014; Revised 25 August 2014; Accepted 25 August 2014

Academic Editor: Fa-Yun Che

Copyright © 2015 Tianyao Guo 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. X. Zhang, K. Højlund, M. Luo, C. Meyer, T. Geetha, and Z. Yi, “Novel tyrosine phosphorylation sites in rat skeletal muscle revealed by phosphopeptide enrichment and HPLC-ESI-MS/MS,” Journal of Proteomics, vol. 75, no. 13, pp. 4017–4026, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Zheng, P. Hu, D. F. Quinn, and Y. K. Wang, “Phosphotyrosine proteomic study of interferon α signaling pathway using a combination of immunoprecipitation and immobilized metal affinity chromatography,” Molecular and Cellular Proteomics, vol. 4, no. 6, pp. 721–730, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Tunter, “Tyrosine phosphorylation: thirty years and counting,” Current Opinion in Cell Biology, vol. 21, no. 2, pp. 40–46, 2009. View at Google Scholar
  4. S. Lamprianou and S. Harroch, “Receptor protein tyrosine phosphatase from stem cells to mature glial cells of the central nervous system,” Journal of Molecular Neuroscience, vol. 29, no. 3, pp. 241–255, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Hunter, “Synthetic peptide substrates for a tyrosine protein kinase,” The Journal of Biological Chemistry, vol. 257, no. 9, pp. 4843–4848, 1982. View at Google Scholar · View at Scopus
  6. J. A. Cooper, F. S. Esch, S. S. Taylor, and T. Hunter, “Phosphorylation sites in enolase and lactate dehydrogenase utilized by tyrosine protein kinase in vivo and in vitro,” The Journal of Biological Chemistry, vol. 259, no. 12, pp. 7835–7841, 1984. View at Google Scholar · View at Scopus
  7. T. Patschinsky, T. Hunter, F. S. Esch, J. A. Cooper, and B. M. Sefton, “Analysis of the sequence of amino acids surrounding sites of tyrosine phosphorylation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 4, pp. 973–977, 1982. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Manning, D. B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam, “The protein kinase complement of the human genome,” Science, vol. 298, no. 5600, pp. 1912–1934, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Blume-Jensen and T. Hunter, “Oncogenic kinase signalling,” Nature, vol. 411, no. 6835, pp. 355–365, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Johnson and F. M. White, “Toward quantitative phosphotyrosine profiling in vivo,” Seminars in Cell & Developmental Biology, vol. 23, no. 8, pp. 854–862, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. A. D. Zoumaro-Djayoon, A. J. R. Heck, and J. Muñoz, “Targeted analysis of tyrosine phosphorylation by immuno-affinity enrichment of tyrosine phosphorylated peptides prior to mass spectrometric analysis,” Methods, vol. 56, no. 2, pp. 268–274, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. P. A. Futreal, A. Kasprzyk, E. Birney, J. C. Mullikin, R. Wooster, and M. R. Stratton, “Cancer and genomics,” Nature, vol. 409, no. 6822, pp. 850–852, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Hunter and B. M. Sefton, “Transforming gene product of Rous sarcoma virus phosphorylates tyrosine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 3, pp. 1311–1315, 1980. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Amit, R. Wides, and Y. Yarden, “Evolvable signaling networks of receptor tyrosine kinases: relevance of robustness to malignancy and to cancer therapy,” Molecular Systems Biology, vol. 3, article 151, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. U. Andersson, D. Johansson, P. Behnam-Motlagh, M. Johansson, and B. Malmer, “Treatment schedule is of importance when gefitinib is combined with irradiation of glioma and endothelial cells in vitro,” Acta Oncologica, vol. 46, no. 7, pp. 951–960, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Traxler, P. R. Allegrini, R. Brandt et al., “AEE788: a dual family epidermal growth factor receptor/ErbB2 and vascular endothelial growth factor receptor tyrosine kinase inhibitor with antitumor and antiangiogenic activity,” Cancer Research, vol. 64, no. 14, pp. 4931–4941, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. A. C. Navis, A. Bourgonje, P. Wesseling et al., “Effects of dual targeting of tumor cells and stroma in human glioblastoma xenografts with a tyrosine kinase inhibitor against c-MET and VEGFR2,” PLoS ONE, vol. 8, no. 3, Article ID e58262, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Wu, C. Huang, X. Li et al., “LRRC4 inhibits glioblastoma cell proliferation, migration, and angiogenesis by downregulating pleiotropic cytokine expression and responses,” Journal of Cellular Physiology, vol. 214, no. 1, pp. 65–74, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. H. K. Gan, M. Lappas, D. X. Cao, A. Cvrljevdic, A. M. Scott, and T. G. Johns, “Targeting a unique EGFR epitope with monoclonal antibody 806 activates NF-κB and initiates tumour vascular normalization,” Journal of Cellular and Molecular Medicine, vol. 13, no. 9, pp. 3993–4001, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Ye, Q. Gao, T. Xu et al., “Upregulation of LRIG1 suppresses malignant glioma cell growth by attenuating EGFR activity,” Journal of Neuro-Oncology, vol. 94, no. 2, pp. 183–194, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. A. H. Sikkema, E. S. J. M. de Bont, G. Molema et al., “Vascular endothelial growth factor receptor 2 (VEGFR-2) signalling activity in paediatric pilocytic astrocytoma is restricted to tumour endothelial cells,” Neuropathology and Applied Neurobiology, vol. 37, no. 5, pp. 538–548, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. I. Sancho-Martinez and A. Martin-Villalba, “Tyrosine phosphorylation and CD95: a FAScinating switch,” Cell Cycle, vol. 8, no. 6, pp. 838–842, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. B. C. Merk, J. L. Owens, M.-B. S. Lopes, C. M. Silva, and I. M. Hussaini, “STAT6 expression in glioblastoma promotes invasive growth,” BMC Cancer, vol. 11, article 184, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Nakada, J. A. Niska, N. L. Tran, W. S. McDonough, and M. E. Berens, “EphB2/R-ras signaling regulates glioma cell adhesion, growth, and invasion,” The American Journal of Pathology, vol. 167, no. 2, pp. 565–576, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Wang, G. Moncayo, P. Morin et al., “Mer receptor tyrosine kinase promotes invasion and survival in glioblastoma multiforme,” Oncogene, vol. 32, no. 7, pp. 872–882, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Takino, M. Nakada, H. Miyamori, J. Yamashita, K. M. Yamada, and H. Sato, “CrkI adapter protein modulates cell migration and invasion in glioblastoma,” Cancer Research, vol. 63, no. 9, pp. 2335–2337, 2003. View at Google Scholar · View at Scopus
  27. C. A. Lipinski, N. L. Tran, C. Bay et al., “Differential role of proline-rich tyrosine kinase 2 and focal adhesion kinase in determining glioblastoma migration and proliferation,” Molecular Cancer Research, vol. 1, no. 5, pp. 323–332, 2003. View at Google Scholar · View at Scopus
  28. K. Kubo, T. Shimizu, S.-I. Ohyama et al., “Novel potent orally active selective VEGFR-2 tyrosine kinase inhibitors: Synthesis, structure-activity relationships, and antitumor activities of N-phenyl-N′-{4-(4-quinolyloxy)phenyl}ureas,” Journal of Medicinal Chemistry, vol. 48, no. 5, pp. 1359–1366, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Guo, B. Hu, W. Gu et al., “Platelet-derived growth factor-B enhances glioma angiogenesis by stimulating vascular endothelial growth factor expression in tumor endothelia and by promoting pericyte recruitment,” The American Journal of Pathology, vol. 162, no. 4, pp. 1083–1093, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. M. E. Hegi, A.-C. Diserens, P. Bady et al., “Pathway analysis of glioblastoma tissue after preoperative treatment with the EGFR tyrosine kinase inhibitor gefitinib—a phase II trial,” Molecular Cancer Therapeutics, vol. 10, no. 6, pp. 1102–1112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. D. A. Haas-Kogan, M. D. Prados, T. Tihan et al., “Epidermal growth factor receptor, protein kinase B/Akt, and glioma response to erlotinib,” Journal of the National Cancer Institute, vol. 97, no. 12, pp. 880–887, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Abulrob, S. Giuseppin, M. F. Andrade, A. McDermid, M. Moreno, and D. Stanimirovic, “Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae,” Oncogene, vol. 23, no. 41, pp. 6967–6979, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. N. A. Lokker, C. M. Sullivan, S. J. Hollenbach, M. A. Israel, and N. A. Giese, “Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors,” Cancer Research, vol. 62, no. 13, pp. 3729–3735, 2002. View at Google Scholar · View at Scopus
  34. H. Raghu, A. K. Nalla, C. S. Gondi, M. Gujrati, D. H. Dinh, and J. S. Rao, “uPA and uPAR shRNA inhibit angiogenesis via enhanced secretion of SVEGFR1 independent of GM-CSF but dependent on TIMP-1 in endothelial and glioblastoma cells,” Molecular Oncology, vol. 6, no. 1, pp. 33–47, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Massa, F. Barbieri, C. Aiello et al., “The phosphotyrosine phosphatase η mediates somatostatin inhibition of glioma proliferation via the dephosphorylation of ERK1/2,” Annals of the New York Academy of Sciences, vol. 1030, pp. 264–274, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Liu, Y. Yang, C. Wang et al., “The effect of epidermal growth factor receptor variant III on glioma cell migration by stimulating ERK phosphorylation through the focal adhesion kinase signaling pathway,” Archives of Biochemistry and Biophysics, vol. 502, no. 2, pp. 89–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. M.-J. Park, M.-S. Kim, I.-C. Park et al., “PTEN suppresses hyaluronic acid-induced matrix metalloproteinase-9 expression in U87MG glioblastoma cells through focal adhesion kinase dephosphorylation,” Cancer Research, vol. 62, no. 21, pp. 6318–6322, 2002. View at Google Scholar · View at Scopus
  38. J. N. Contessa, M. S. Bhojani, H. H. Freeze, A. Rehemtulla, and T. S. Lawrence, “Inhibition of N-linked glycosylation disrupts receptor tyrosine kinase signaling in tumor cells,” Cancer Research, vol. 68, no. 10, pp. 3803–3809, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Pal, A. Glekas, M. Doubrovin et al., “Molecular imaging of EGFR kinase activity in tumors with 124I-Labeled small molecular tracer and positron emission tomography,” Molecular Imaging and Biology, vol. 8, no. 5, pp. 262–277, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Puputti, O. Tynninen, P. Pernilä et al., “Expression of KIT receptor tyrosine kinase in endothelial cells of juvenile brain tumors,” Brain Pathology, vol. 20, no. 4, pp. 763–770, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. M. R. Stettner, W. Wang, L. B. Nabors et al., “Lyn kinase activity is the predominant cellular Src kinase activity in glioblastoma tumor cells,” Cancer Research, vol. 65, no. 13, pp. 5535–5543, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Zagzag, B. Shiff, G. I. Jallo et al., “Tenascin-C promotes microvascular cell migration and phosphorylation of focal adhesion kinase,” Cancer Research, vol. 62, no. 9, pp. 2660–2668, 2002. View at Google Scholar · View at Scopus
  43. W.-J. Park, Y. Y. Lim, N. S. Kwon, K. J. Baek, D.-S. Kim, and H.-Y. Yun, “Leucine-rich glioma inactivated 3 induces neurite outgrowth through akt and focal adhesion kinase,” Neurochemical Research, vol. 35, no. 5, pp. 789–796, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Sciaccaluga, G. L. Gianfranceschi, S. Rocco et al., “Constitutive phosphorylation of Janus kinase 2 in the GL15 glioblastoma derived human cell line,” Oncology Reports, vol. 17, no. 1, pp. 17–23, 2007. View at Google Scholar · View at Scopus
  45. A. Shimizu, A. Mammoto, J. E. Italiano Jr. et al., “ABL2/ARG tyrosine kinase mediates SEMA3F-induced RhoA inactivation and cytoskeleton collapse in human glioma cells,” The Journal of Biological Chemistry, vol. 283, no. 40, pp. 27230–27238, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Fukai, H. Yokote, R. Yamanaka, T. Arao, K. Nishio, and T. Itakura, “EphA4 promotes cell proliferation and migration through a novel EphA4-FGFR1 signaling pathway in the human glioma U251 cell line,” Molecular Cancer Therapeutics, vol. 7, no. 9, pp. 2768–2778, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. D.-P. Liu, Y. Wang, H. P. Koeffler, and D. Xie, “Ephrin-A1 is a negative regulator in glioma through down-reguation of EphA2 and FAK,” International Journal of Oncology, vol. 30, no. 4, pp. 865–871, 2007. View at Google Scholar · View at Scopus
  48. X. Zhou, L. Hua, W. Zhang et al., “FRK controls migration and invasion of human glioma cells by regulating JNK/c-Jun signaling,” Journal of Neuro-Oncology, vol. 110, no. 1, pp. 9–19, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. E. C. Brantley, L. B. Nabors, G. Y. Gillespie et al., “Loss of protein inhibitors of activated STAT-3 expression in glioblastoma multiforme tumors: implications for STAT-3 activation and gene expression,” Clinical Cancer Research, vol. 14, no. 15, pp. 4694–4704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. P. J. Boersema, L. Y. Foong, V. M. Y. Ding et al., “In-depth qualitative and quantitative profiling of tyrosine phosphorylation using a combination of phosphopeptide immunoaffinity purification and stable isotope dimethyl labeling,” Molecular and Cellular Proteomics, vol. 9, no. 1, pp. 84–99, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. X. Zhan and D. M. Desiderio, “A reference map of a human pituitary adenoma proteome,” Proteomics, vol. 3, no. 5, pp. 699–713, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. X. Zhan and D. M. Desiderio, “Spot volume vs. amount of protein loaded onto a gel: a detailed, statistical comparison of two gel electrophoresis systems,” Electrophoresis, vol. 24, no. 11, pp. 1818–1833, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Martínez-Ruiz, L. Villanueva, C. G. de Orduña et al., “S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 24, pp. 8525–8530, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. H. L. Forsythe, J. L. Jarvis, J. W. Turner, L. W. Elmore, and S. E. Holt, “Stable association of HSP90 and p23, but not HSP70, with active human telomerase,” The Journal of Biological Chemistry, vol. 276, no. 19, pp. 15571–15574, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Yang, S. M. Roe, M. J. Cliff et al., “Molecular basis for TPR domain-mediated regulation of protein phosphatase 5,” The EMBO Journal, vol. 24, no. 1, pp. 1–10, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Chadli, J. D. Graham, M. G. Abel et al., “GCUNC-45 is a novel regulator for the progesterone receptor/hsp90 chaperoning pathway,” Molecular & Cellular Biology, vol. 26, no. 5, pp. 1722–1730, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Retzlaff, M. Stahl, H. C. Eberl et al., “Hsp90 is regulated by a switch point in the C-terminal domain,” EMBO Reports, vol. 10, no. 10, pp. 1147–1153, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Sciacovelli, G. Guzzo, V. Morello et al., “The mitochondrial chaperone TRAP1 promotes neoplastic growth by inhibiting succinate dehydrogenase,” Cell Metabolism, vol. 17, no. 6, pp. 988–999, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. L. Zhang, P. Karsten, S. Hamm et al., “TRAP1 rescues PINK1 loss-of-function phenotypes,” Human Molecular Genetics, vol. 22, no. 14, Article ID ddt132, pp. 2829–2841, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Yoshida, S. Tsutsumi, G. Muhlebach et al., “Molecular chaperone TRAP1 regulates a metabolic switch between mitochondrial respiration and aerobic glycolysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 17, pp. E1604–E1612, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. M. H. Baumann, T. Wisniewski, E. Levy, G. T. Plant, and J. Ghiso, “C-terminal fragments of α-and β-tubulin form amyloid fibrils in vitro and associate with amyloid deposits of familial cerebral amyloid angiopathy, British type,” Biochemical and Biophysical Research Communications, vol. 219, no. 1, pp. 238–242, 1996. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Rogowski, F. Juge, J. van Dijk et al., “Stable association of HSP90 and p23, but not HSP70, with active human telomerase,” Cell, vol. 137, no. 6, pp. 1076–1087, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. K.-W. Chang, P.-Y. Yang, H.-Y. Lai, T.-S. Yeh, T.-C. Chen, and C.-T. Yeh, “Identification of a novel actin isoform in hepatocellular carcinoma,” Hepatology Research, vol. 36, no. 1, pp. 33–39, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Kosako, M. Amano, M. Yanagida et al., “Phosphorylation of glial fibrillary, acidic protein at the same sites by cleavage furrow kinase and Rho-associated kinase,” The Journal of Biological Chemistry, vol. 272, no. 16, pp. 10333–10336, 1997. View at Publisher · View at Google Scholar · View at Scopus
  65. J. A. Read, V. J. Winter, C. M. Eszes, R. B. Sessions, and R. L. Brady, “Structural basis for altered activity of M- and H-isozyme forms of human lactate dehydrogenase,” Proteins, vol. 43, no. 2, pp. 175–185, 2001. View at Google Scholar
  66. Y. M. Gu, Y. H. Jin, J. K. Choi, K. H. Baek, C. Y. Yeo, and K. Y. Lee, “Protein kinase A phosphorylates and regulates dimerization of 14-3-3 epsilon,” FEBS Letters, vol. 580, no. 1, pp. 305–310, 2006. View at Google Scholar
  67. N. Bogdanova, J. Horst, M. Chlystun et al., “A common haplotype of the annexin A5 (ANXA5) gene promoter is associated with recurrent pregnancy loss,” Human Molecular Genetics, vol. 16, no. 5, pp. 573–578, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Ritter, C. Buechler, A. Boettcher et al., “Cloning and characterization of a novel apolipoprotein A-I binding protein, AI-BP, secreted by cells of the kidney proximal tubules in response to HDL or apoA-I,” Genomics, vol. 79, no. 5, pp. 693–702, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Rush, A. Moritz, K. A. Lee et al., “Immunoaffinity profiling of tyrosine phosphorylation in cancer cells,” Nature Biotechnology, vol. 23, no. 1, pp. 94–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. V. Pancholi, “Multifunctional α-enolase: its role in diseases,” Cellular and Molecular Life Sciences, vol. 58, no. 7, pp. 902–920, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Serra-Pagès, Q. G. Medley, M. Tang, A. Hart, and M. Streuli, “Liptins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins,” The Journal of Biological Chemistry, vol. 273, no. 25, pp. 15611–15620, 1998. View at Publisher · View at Google Scholar · View at Scopus
  72. K. Miura, K. M. Jacques, S. Stauffer et al., “ARAP1: a point of convergence for arf and rho signaling,” Molecular Cell, vol. 9, no. 1, pp. 109–119, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. S. C. Moser, D. Bensaddek, B. Ortmann et al., “PHD1 links cell-cycle progression to oxygen sensing through hydroxylation of the centrosomal protein Cep192,” Developmental Cell, vol. 26, no. 4, pp. 381–392, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Sakurai, J. Gavard, Y. Annas-Linhares et al., “Semaphorin 3E initiates antiangiogenic signaling through plexin D1 by regulating Arf6 and R-Ras,” Molecular and Cellular Biology, vol. 30, no. 12, pp. 3086–3098, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. H. Daub, J. V. Olsen, M. Bairlein et al., “Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle,” Molecular Cell, vol. 31, no. 3, pp. 438–448, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. X. Huang, W. Yuan, W. Huang et al., “ZNF569, a novel KRAB-containing zinc finger protein, suppresses MAPK signaling pathway,” Biochemical and Biophysical Research Communications, vol. 346, no. 3, pp. 621–628, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. L. Peleg, F. Meltzer, M. Karpati, and B. Goldman, “GM2 gangliosidosis B1 variant: biochemical and molecular characterization of hexosaminidase A,” Biochemical and Molecular Medicine, vol. 54, no. 2, pp. 126–132, 1995. View at Publisher · View at Google Scholar · View at Scopus
  78. M. A. Tischfield, T. M. Bosley, M. A. M. Salih et al., “Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development,” Nature Genetics, vol. 37, no. 10, pp. 1035–1037, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. H. Le Hir, M. J. Moore, and L. E. Maquat, “Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions,” Genes and Development, vol. 14, no. 9, pp. 1098–1108, 2000. View at Google Scholar · View at Scopus