Cancer: The kinase activity of the Ser/Thr kinase BUB1 promotes TGF-β signaling

Science Signaling

Volumn 8, Issue 358, 2015, Pages

  Nyati, Shyam ^a   Schinske Sebolt, Katrina ^a   Pitchiaya, Sethuramasundaram ^a   Chekhovskiy, Katerina ^a   Chator, Areeb ^a   Chaudhry, Nauman ^a   Dosch, Joseph ^b   Van Dort, Marcian E ^b   Varambally, Sooryanarayana ^b   Kumar Sinha, Chandan ^b,c   Nyati, Mukesh Kumar ^a   Ray, Dipankar ^a   Walter, Nils G ^a   Yu, Hongtao ^d,e   Ross, Brian Dale ^a,b   Rehemtulla, Alnawaz ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2OH BNPP1; BUDDING UNINHIBITED BY BENZIMIDAZOLE 1; ENZYME INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOTRANSFERASE; PROTEIN KINASE B; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; UNCLASSIFIED DRUG; BUB1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; RECEPTOR REGULATED SMAD PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL ADHESION; CELL CYCLE REGULATION; CELL INVASION; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LUNG CARCINOMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; DIMERIZATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; GENETICS; HIGH THROUGHPUT SCREENING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; WESTERN BLOTTING;

MUS;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; DIMERIZATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD PROTEINS, RECEPTOR-REGULATED; TRANSFORMING GROWTH FACTOR BETA;

EID: 84920960690     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005379     Document Type: Article

References (61)

1. Y. Drabsch, P. ten Dijke, TGF-β signalling and its role in cancer progression and metastasis. Cancer Metastasis Rev. 31, 553-568 (2012).
2. J. Xu, S. Lamouille, R. Derynck, TGF-β-induced epithelial to mesenchymal transition. Cell Res. 19, 156-172 (2009).
3. R. Derynck, R. J. Akhurst, A. Balmain, TGF-β signaling in tumor suppression and cancer progression. Nat. Genet. 29, 117-129 (2001).
4. S. Nyati, K. Schinske, D. Ray, M. Nyati, B. D. Ross, A. Rehemtulla, Molecular imaging of TGFβ-induced Smad2/3 phosphorylation reveals a role for receptor tyrosine kinases in modulating TGFβ signaling. Clin. Cancer Res. 17, 7424-7439 (2011).
5. A. Zieba, K. Pardali, O. Söderberg, L. Lindbom, E. Nyström, A. Moustakas, C. H. Heldin, U. Landegren, Intercellular variation in signaling through the TGF-β pathway and its relation to cell density and cell cycle phase. Mol. Cell. Proteomics 11, M111.013482 (2012).
6. L. Zawel, J. L. Dai, P. Buckhaults, S. B. Zhou, K. W. Kinzler, B. Vogelstein, S. E. Kern, Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell 1, 611-617 (1998).
7. V. L. Johnson, M. I. F. Scott, S. V. Holt, D. Hussein, S. S. Taylor, Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression. J. Cell Sci. 117, 1577-1589 (2004).
8. H. Yu, Z. Tang, Bub1 multitasking in mitosis. Cell Cycle 4, 262-265 (2005).
9. J. S. Kang, M. J. Yang, B. Li, W. Qi, C. Zhang, K. M. Shokat, D. R. Tomchick, M. Machius, H. T. Yu, Structure and substrate recruitment of the human spindle checkpoint kinase Bub1. Mol. Cell 32, 394-405 (2008).
10. S. Lawler, X. H. Feng, R. H. Chen, E. M. Maruoka, C. W. Turck, I. Griswold-Prenner, R. Derynck, The type II transforming growth factor-β receptor autophosphorylates not only on serine and threonine but also on tyrosine residues. J. Biol. Chem. 272, 14850-14859 (1997).
11. S. Souchelnytskyi, P. ten Dijke, K. Miyazono, C. H. Heldin, Phosphorylation of Ser165 in TGF-beta type I receptor modulates TGF-beta1-induced cellular responses. EMBO J. 15, 6231-6240 (1996).
12. A. J. Galliher, W. P. Schiemann, Src phosphorylates Tyr284 in TGF-β type II receptor and regulates TGF-β stimulation of p38 MAPK during breast cancer cell proliferation and invasion. Cancer Res. 67, 3752-3758 (2007).
13. P. Kavsak, R. K. Rasmussen, C. G. Causing, S. Bonni, H. Zhu, G. H. Thomsen, J. L. Wrana, Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGFβ receptor for degradation. Mol. Cell 6, 1365-1375 (2000).
14. J. S. Kang, E. F. Saunier, R. J. Akhurst, R. Derynck, The type I TGF-β receptor is covalently modified and regulated by sumoylation. Nat. Cell Biol. 10, 654-664 (2008).
15. W. Shi, C. Sun, B. He, W. Xiong, X. Shi, D. Yao, X. Cao, GADD34-PP1c recruited by Smad7 dephosphorylates TGFβ type I receptor. J. Cell Biol. 164, 291-300 (2004).
16. F. Huang, Y. G. Chen, Regulation of TGF-β receptor activity. Cell Biosci. 2, 9 (2012).
17. J. S. Kang, C. Liu, R. Derynck, New regulatory mechanisms of TGF-β receptor function. Trends Cell Biol. 19, 385-394 (2009).
18. C. Le Roy, J. L. Wrana, Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell Biol. 6, 112-126 (2005).
19. H. Mitchell, A. Choudhury, R. E. Pagano, E. B. Leof, Ligand-dependent and -independent transforming growth factor-β receptor recycling regulated by clathrin-mediated endocytosis and Rab11. Mol. Biol. Cell 15, 4166-4178 (2004).
20. X. H. D. Zhang, X. T. C. Yang, N. J. Chung, A. Gates, E. Stec, P. Kunapuli, D. J. Holder, M. Ferrer, A. S. Espeseth, Robust statistical methods for hit selection in RNA interference high-throughput screening experiments. Pharmacogenomics 7, 299-309 (2006).
21. M. M. Martin, J. A. Buckenberger, J. Jiang, G. E. Malana, D. L. Knoell, D. S. Feldman, T. S. Elton, TGF-β1 stimulates human AT1 receptor expression in lung fibroblasts by cross talk between the Smad, p38 MAPK, JNK, and PI3K signaling pathways. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L790-L799 (2007).
22. J. Y. Yi, I. Shin, C. L. Arteaga, Type I transforming growth factor β receptor binds to and activates phosphatidylinositol 3-kinase. J. Biol. Chem. 280, 10870-10876 (2005).
23. J. P. Thiery, J. P. Sleeman, Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142 (2006).
24. E. Meulmeester, P. Ten Dijke, The dynamic roles of TGF-β in cancer. J. Pathol. 223, 205-218 (2011).
25. H. Kasai, J. T. Allen, R. M. Mason, T. Kamimura, Z. Zhang, TGF-β 1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir. Res. 6, 56 (2005).
26. J. H. Kim, Y. S. Jang, K. S. Eom, Y. I. Hwang, H. R. Kang, S. H. Jang, C. H. Kim, Y. B. Park, M. G. Lee, I. G. Hyun, K. S. Jung, D. G. Kim, Transforming growth factor β1 induces epithelial-to-mesenchymal transition of A549 cells. J. Korean Med. Sci. 22, 898-904 (2007).
27. W. Qi, H. T. Yu, KEN-box-dependent degradation of the Bub1 spindle checkpoint kinase by the anaphase-promoting complex/cyclosome. J. Biol. Chem. 282, 3672-3679 (2007).
28. G. J. Inman, F. J. Nicolás, J. F. Callahan, J. D. Harling, L. M. Gaster, A. D. Reith, N. J. Laping, C. S. Hill, SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65-74 (2002).
29. D. Perera, V. Tilston, J. A. Hopwood, M. Barchi, R. P. Boot-Handford, S. S. Taylor, Bub1 maintains centromeric cohesion by activation of the spindle checkpoint. Dev. Cell 13, 566-579 (2007).
30. S. Pitchiaya, J. R. Androsavich, N. G. Walter, Intracellular single molecule microscopy reveals two kinetically distinct pathways for microRNA assembly. EMBO Rep. 13, 709-715 (2012).
31. M. Kawabata, A. Chytil, H. L. Moses, Cloning of a novel type II serine/threonine kinase receptor through interaction with the type I transforming growth factor-β receptor. J. Biol. Chem. 270, 5625-5630 (1995).
32. T. Tsukazaki, T. A. Chiang, A. F. Davison, L. Attisano, J. L. Wrana, SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell 95, 779-791 (1998).
33. Y. Wan, X. Liu, M. W. Kirschner, The anaphase-promoting complex mediates TGF-β signaling by targeting SnoN for destruction. Mol. Cell 8, 1027-1039 (2001).
34. P. Cherukuri, A. J. DeCastro, A. L. Balboni, S. L. Downey, J. Y. Liu, J. A. Hutchinson, J. DiRenzo, Phosphorylation of ΔNp63α via a novel TGFβ/ALK5 signaling mechanism mediates the anti-clonogenic effects of TGFβ. PLOS One 7, e50066 (2012).
35. D. J. de Gorter, M. van Dinther, O. Korchynskyi, P. ten Dijke, Biphasic effects of transforming growth factor β on bone morphogenetic protein-induced osteoblast differentiation. J. Bone Miner. Res. 26, 1178-1187 (2011).
36. S. Dupont, A. Mamidi, M. Cordenonsi, M. Montagner, L. Zacchigna, M. Adorno, G. Martello, M. J. Stinchfield, S. Soligo, L. Morsut, M. Inui, S. Moro, N. Modena, F. Argenton, S. J. Newfeld, S. Piccolo, FAM/USP9x, a deubiquitinating enzyme essential for TGFβ signaling, controls Smad4 monoubiquitination. Cell 136, 123-135 (2009).
37. J. Izrailit, H. K. Berman, A. Datti, J. L. Wrana, M. Reedijk, High throughput kinase inhibitor screens reveal TRB3 and MAPK-ERK/TGFβ pathways as fundamental Notch regulators in breast cancer. Proc. Natl. Acad. Sci. U.S.A. 110, 1714-1719 (2013).
38. J. Mullenders, A. W. Fabius, M. M. van Dongen, H. J. Kuiken, R. L. Beijersbergen, R. Bernards, Interleukin-1R-associated kinase 2 is a novel modulator of the transforming growth factor β signaling cascade. Mol. Cancer Res. 8, 592-603 (2010).
39. H. Yu, M. Königshoff, A. Jayachandran, D. Handley, W. Seeger, N. Kaminski, O. Eickelberg, Transgelin is a direct target of TGF-β/Smad3-dependent epithelial cell migration in lung fibrosis. FASEB J. 22, 1778-1789 (2008).
40. L. Zhang, F. F. Zhou, Y. Drabsch, R. Gao, B. E. Snaar-Jagalska, C. Mickanin, H. Z. Huang, K. A. Sheppard, J. A. Porter, C. X. Lu, P. ten Dijke, USP4 is regulated by AKT phosphorylation and directly deubiquitylates TGF-β type I receptor. Nat. Cell Biol. 14, 717-726 (2012).
41. N. Schultz, D. R. Marenstein, D. A. De Angelis, W. Q. Wang, S. Nelander, A. Jacobsen, D. S. Marks, J. Massagué, C. Sander, Off-target effects dominate a large-scale RNAi screen for modulators of the TGF-β pathway and reveal microRNA regulation of TGFBR2. Silence 2, 3 (2011).
42. H. Ikushima, K. Miyazono, Cellular context-dependent "colors" of transforming growth factor-β signaling. Cancer Sci. 101, 306-312 (2010).
43. S. S. Söderberg, G. Karlsson, S. Karlsson, Complex and context dependent regulation of hematopoiesis by TGF-β superfamily signaling. Ann. N. Y. Acad. Sci. 1176, 55-69 (2009).
44. C. Petritsch, H. Beug, A. Balmain, M. Oft, TGF-β inhibits p70 S6 kinase via protein phosphatase 2A to induce G1 arrest. Genes Dev. 14, 3093-3101 (2000).
45. P. ten Dijke, H. Yamashita, H. Ichijo, P. Franzén, M. Laiho, K. Miyazono, C. H. Heldin, Characterization of type I receptors for transforming growth factor-beta and activin. Science 264, 101-104 (1994).
46. M. Barrios-Rodiles, K. R. Brown, B. Ozdamar, R. Bose, Z. Liu, R. S. Donovan, F. Shinjo, Y. M. Liu, J. Dembowy, I. W. Taylor, V. Luga, N. Przulj, M. Robinson, H. Suzuki, Y. Hayashizaki, I. Jurisica, J. L. Wrana, High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307, 1621-1625 (2005).
47. C. Dees, M. Tomcik, K. Palumbo, A. Akhmetshina, A. Horn, P. Zerr, O. Distler, G. Schett, J. H. W. Distler, JAK2 mediates the stimulatory effects of transforming growth factor beta on fibroblast activation and tissue fibrosis. Arthritis Rheum. 63, S944-S945 (2011).
48. X. Wang, S. Shaw, F. Amiri, D. C. Eaton, M. B. Marrero, Inhibition of the Jak/STAT signaling pathway prevents the high glucose-induced increase in TGF-β and fibronectin synthesis in mesangial cells. Diabetes 51, 3505-3509 (2002).
49. J. Song, EMT or apoptosis: A decision for TGF-β. Cell Res. 17, 289-290 (2007).
50. T. Hirschhorn, L. Barizilay, N. I. Smorodinsky, M. Ehrlich, Differential regulation of Smad3 and of the type II transforming growth factor-β receptor in mitosis: Implications for signaling. PLOS One 7, e43459 (2012).
51. P. Meraldi, P. K. Sorger, A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J. 24, 1621-1633 (2005).
52. T. K. Kim, E. K. Mo, C. G. Yoo, C. T. Lee, S. K. Han, Y. S. Shim, Y. W. Kim, Alteration of cell growth and morphology by overexpression of transforming growth factor β type II receptor in human lung adenocarcinoma cells. Lung Cancer 31, 181-191 (2001).
53. W. S. Kim, C. Park, Y. S. Jung, H. S. Kim, J. Han, C. H. Park, K. Kim, J. Kim, Y. M. Shim, K. Park, Reduced transforming growth factor-beta type II receptor (TGF-beta RII) expression in adenocarcinoma of the lung. Anticancer Res. 19, 301-306 (1999).
54. Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, M. J. Wheelock, Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling. Am. J. Respir. Cell Mol. Biol. 38, 95-104 (2008).
55. A. Hata, R. S. Lo, D. Wotton, G. Lagna, J. Massagué, Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 388, 82-87 (1997).
56. Y. B. Kang, P. M. Siegel, W. P. Shu, M. Drobnjak, S. M. Kakonen, C. Cordón-Cardo, T. A. Guise, J. Massagué, A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (2003).
57. S. Draghici, P. Khatri, A. L. Tarca, K. Amin, A. Done, C. Voichita, C. Georgescu, R. Romero, A systems biology approach for pathway level analysis. Genome Res. 17, 1537-1545 (2007).
58. A. L. Tarca, S. Draghici, P. Khatri, S. S. Hassan, P. Mittal, J. S. Kim, C. J. Kim, J. P. Kusanovic, R. Romero, A novel signaling pathway impact analysis. Bioinformatics 25, 75-82 (2009).
59. A. I. Saeed, V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, M. Thiagarajan, A. Sturn, M. Snuffin, A. Rezantsev, D. Popov, A. Ryltsov, E. Kostukovich, I. Borisovsky, Z. Liu, A. Vinsavich, V. Trush, J. Quackenbush, TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378 (2003).
60. M. D. Abramoff, P. J. Magalhães, S. J. Ram, Image processing with ImageJ. Biophotonics Int. 11, 36-42 (2004).
61. Y. Chen, C. S. Kam, F. Q. Liu, Y. Liu, V. C. Lui, J. R. Lamb, P. K. Tam, LPS-induced upregulation of TGF-β receptor 1 is associated with TNF-α expression in human monocyte-derived macrophages. J. Leukoc. Biol. 83, 1165-1173 (2008).