Spindle poisons and cell fate: A tale of two pathways

Molecular Interventions

Volumn 11, Issue 2, 2011, Pages 141-150

  Matson, Daniel R ^a   Stukenberg, P Todd ^a  

^a UNIVERSITY OF VIRGINIA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; ANTIMITOTIC AGENT; ANTINEOPLASTIC AGENT; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; BUB1 RELATED PROTEIN; BUB3 PROTEIN; CASEIN KINASE II; CELL CYCLE PROTEIN 20; CYCLIN B; CYCLIN DEPENDENT KINASE 1; DOCETAXEL; MITOGEN ACTIVATED PROTEIN KINASE P38; MULTIPROTEIN COMPLEX; OKADAIC ACID; PACLITAXEL; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEASOME; PROTEIN FBW7; PROTEIN MAD1; PROTEIN MAD2; PROTEIN MCL 1; PROTEIN SERINE THREONINE KINASE; PROTEIN USP9X; REGULATOR PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; VINBLASTINE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL DEATH; CELL FATE; CELLULAR STRESS RESPONSE; CHROMOSOME SEGREGATION; DRUG MECHANISM; DRUG TARGETING; HUMAN; MANTLE CELL LYMPHOMA; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS SPINDLE; MULTIPLE MYELOMA; PROTEIN PROTEIN INTERACTION; REVIEW; SPINDLE ASSEMBLY CHECKPOINT; TREATMENT RESPONSE; TUMOR CELL; UNSPECIFIED SIDE EFFECT;

ANTIMITOTIC AGENTS; APOPTOSIS; HUMANS; MITOSIS; MITOTIC SPINDLE APPARATUS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 79955679067     PISSN: 15340384     EISSN: 15432548     Source Type: Journal    
DOI: 10.1124/mi.11.2.12     Document Type: Review

References (78)

1. Wood KW, Cornwell WD, and Jackson JR (2001) Past and future of the mitotic spindle as an oncology target. Curr Opin Pharmacol 1:370-377. (Pubitemid 33585986)
2. Pellegrini F and Budman DR (2005) Review: Tubulin function, action of antitubulin drugs, and new drug development. Cancer Invest 23:264-273. (Pubitemid 40770744)
3. Hadfield JA, Ducki S, Hirst N, and McGown AT (2003) Tubulin and microtubules as targets for anticancer drugs. Prog Cell Cycle Res 5:309-325.
4. Montero A, Fossella F, Hortobagyi G, and Valero V (2005) Docetaxel for treatment of solid tumours: A systematic review of clinical data. Lancet Oncol 6:229-239. (Pubitemid 40450714)
5. Duflos A, Kruczynski A, and Barret JM (2002) Novel aspects of natural and modified vinca alkaloids. Curr Med Chem Anticancer Agents 2:55-70. (Pubitemid 34649868)
6. Jordan MA and Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253-265. (Pubitemid 38525281)
7. Longley DB and Johnston PG (2005) Molecular mechanisms of drug resistance. J Pathol 205:275-292. (Pubitemid 40227997)
8. Kavallaris M (2010) Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer 10:194-204. This review details the many mechanisms by which cancer cells gain resistance to spindle poison therapeutics.
9. (Pubitemid 27085170)
10. Shah JV and Cleveland DW (2000) Waiting for anaphase: Mad2 and the spindle assembly checkpoint. Cell 103:997-1000. (Pubitemid 32037387)
11. Bharadwaj R and Yu H (2004) The spindle checkpoint, aneuploidy, and cancer. Oncogene 23:2016-2027. (Pubitemid 38496731)
12. Kastan MB and Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432:316-323. (Pubitemid 39551659)
13. Vermeulen K, Van Bockstaele DR, and Berneman ZN (2003) The cell cycle: A review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 36:131-149. (Pubitemid 36808270)
14. Santaguida S and Musacchio A (2009) The life and miracles of kinetochores. EMBO J. 28:2511-2531. This review serves as an excellent introduction to the structure and functions of the kinetochore.
15. Chan GK, Liu ST, and Yen TJ (2005) Kinetochore structure and function. Trends Cell Biol 15:589-598. (Pubitemid 41619423)
16. Cheeseman IM and Desai A (2008) Molecular architecture of the kinetochore- microtubule interface. Nat Rev Mol Cell Biol 9:33-46. This review details the nature of the microtubule binding site at the kinetochore.
17. Cleveland DW, Mao Y, and Sullivan KF (2003) Centromeres and kinetochores: From epigenetics to mitotic checkpoint signaling. Cell 112:407-421. (Pubitemid 36263076)
18. Lew DJ and Burke DJ (2003) The spindle assembly and spindle position checkpoints. Annu.Rev.Genet. 37:251-282. (Pubitemid 38041427)
19. Millband DN, Campbell L, and Hardwick KG (2002) The awesome power of multiple model systems: Interpreting the complex nature of spindle checkpoint signaling. Trends Cell Biol 12:205-209. (Pubitemid 34327605)
20. Kops GJ (2008) The kinetochore and spindle checkpoint in mammals. Front Biosci 13:3606-3620. (Pubitemid 351594646)
21. Clute P and Pines J (1999) Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1:82-87. (Pubitemid 129501948)
22. Peters JM (2006) The anaphase promoting complex/cyclosome: A machine designed to destroy. Nat Rev Mol Cell Biol 7:644-656. This excellent review of the APC/C E3 ubiquitin ligase is still quite relevant.
23. Brito DA and Rieder CL (2006) Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr Biol 16: 1194-1200. This article demonstrated that cells can exit mitosis in the presence of spindle poisons through an APC/Cmediated phenomenon known as mitotic slippage. (Pubitemid 43867292)
24. Li R and Murray AW (1991) Feedback control of mitosis in budding yeast. Cell 66:519-531. This article is one of two seminal, independent screens in yeast that identified the first bona fide checkpoint proteins in the SAC. (Pubitemid 121001388)
25. Hoyt MA, Totis L, and Roberts BT (1991) S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66:507- 517. This article is the second of two independent yeast screens that identified the first bona fide checkpoint proteins in the SAC. (Pubitemid 121001387)
26. Gassmann R, Holland AJ, Varma D, Wan X, Civril F, Cleveland DW, Oegema K, Salmon ED, and Desai A (2010) Removal of Spindly from microtubule-attached kinetochores controls spindle checkpoint silencing in human cells. Genes Dev 24:957-971.
27. Maia AF, Feijao T, Vromans MJ, Sunkel CE, and Lens SM (2010) Aurora B kinase cooperates with CENP-E to promote timely anaphase onset. Chromosoma 119:405-413.
28. Liu ST, Hittle JC, Jablonski SA, Campbell MS, Yoda K, and Yen TJ (2003) Human CENP-I specifies localization of CENP-F, MAD1 and MAD2 to kinetochores and is essential for mitosis. Nat Cell Biol 5:341-345. (Pubitemid 36432299)
29. Wan X, O'Quinn RP, Pierce HL, Joglekar AP, Gall WE, DeLuca JG, Carroll CW, Liu ST, Yen TJ, McEwen BF, et al. (2009) Protein architecture of the human kinetochore microtubule attachment site. Cell 137:672-684.
30. Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR 3rd, and Cleveland DW (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8: 458-469.
31. Hori T, Amano M, Suzuki A, Backer CB, Welburn JP, Dong Y, McEwen BF, Shang WH, Suzuki E, Okawa K, et al. (2008) CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135:1039-1052.
32. Gascoigne KE and Taylor SS (2009) How do anti-mitotic drugs kill cancer cells? J Cell Sci 122:2579-2585. This recent review highlights the degree of variation in the cellular response to spindle poisons and summarizes the results of high-throughput imaging experiments.
33. Rieder CL and Maiato H (2004) Stuck in division or passing through: What happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell 7:637-651. (Pubitemid 39462685)
34. Weaver BA and Cleveland DW (2005) Decoding the links between mitosis, cancer, and chemotherapy: The mitotic checkpoint, adaptation, and cell death. Cancer Cell 8:7-12. This review remains an excellent introduction to the role of the mitotic checkpoint in cancer therapy. (Pubitemid 40991810)
35. Yusuf RZ, Duan Z, Lamendola DE, Penson RT, and Seiden MV (2003) Paclitaxel resistance: Molecular mechanisms and pharmacologic manipulation. Curr Cancer Drug Targets 3:1-19. (Pubitemid 36119417)
36. McGrogan BT, Gilmartin B, Carney DN, and McCann A (2008) Taxanes, microtubules and chemoresistant breast cancer. Biochim Biophys Acta 1785:96-132.
37. Gascoigne KE and Taylor SS (2008) Cancer cells display profound intraand interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 14:111-122. This article utilized high-throughput single cell imaging to measure variation in response to spindle poisons.
38. Orth JD, Tang Y, Shi J, Loy CT, Amendt C, Wilm C, Zenke FT, and Mitchison TJ (2008) Quantitative live imaging of cancer and normal cells treated with Kinesin-5 inhibitors indicates significant differences in phenotypic responses and cell fate. Mol Cancer Ther 7:3480-3489.
39. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770-776.
40. Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3:614-620. (Pubitemid 27264969)
41. Huang HC, Shi J, Orth JD, and Mitchison TJ (2010) Cell death when the SAC is out of commission. Cell.Cycle 9:
42. Wertz IE, Kusam S, Lam C, Okamoto T, Sandoval W, Anderson DJ, Helgason E, Ernst JA, Eby M, Liu J, et al. (2011) Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 471:110- 114. The results of this article demonstrated that Mcl1 can sensitize cells to spindle poison treatment by regulating the induction of apoptosis.
43. Youle RJ and Strasser A (2008) The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59.
44. Michels J, Johnson PW, and Packham G (2005) Mcl-1. Int J Biochem Cell Biol 37:267-271. This review is becoming a bit dated but remains the best general introduction to Mcl1. (Pubitemid 39330187)
45. Craig RW (2002) MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumorigenesis. Leukemia 16:444-454. (Pubitemid 34449724)
46. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J, et al. (2010) Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463:103-107.
47. Krajewska M, Krajewski S, Epstein JI, Shabaik A, Sauvageot J, Song K, Kitada S, and Reed JC (1996) Immunohistochemical analysis of bcl- 2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol 148:1567-1576. (Pubitemid 26135897)
48. Kaufmann SH, Karp JE, Svingen PA, Krajewski S, Burke PJ, Gore SD, and Reed JC (1998) Elevated expression of the apoptotic regulator Mcl-1 at the time of leukemic relapse. Blood 91:991-1000. (Pubitemid 28078303)
49. Khoury JD, Medeiros LJ, Rassidakis GZ, McDonnell TJ, Abruzzo LV, and Lai R (2003) Expression of Mcl-1 in mantle cell lymphoma is associated with high-grade morphology, a high proliferative state, and p53 overexpression. J Pathol 199:90-97. (Pubitemid 36054733)
50. Nilsson J, Yekezare M, Minshull J, and Pines J (2008) The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat Cell Biol 10:1411-1420.
51. Huang J, Sheung J, Dong G, Coquilla C, Daniel-Issakani S, and Payan DG (2005) High-throughput screening for inhibitors of the e3 ubiquitin ligase APC. Methods Enzymol 399:740-754. (Pubitemid 41772765)
52. Whitehurst AW, Bodemann BO, Cardenas J, Ferguson D, Girard L, Peyton M, Minna JD, Michnoff C, Hao W, Roth MG, et al. (2007) Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature 446:815-819. (Pubitemid 46582032)
53. Banerjee D and Liefshitz A (2001) Potential of the proteasomal inhibitor MG-132 as an anticancer agent, alone and in combination. Anticancer Res 21:3941-3947. (Pubitemid 34229268)
54. Giuliano M, D'Anneo A, De Blasio A, Vento R, and Tesoriere G (2003) Apoptosis meets proteasome, an invaluable therapeutic target of anticancer drugs. Ital J Biochem 52:112-121.
55. Schenkein D (2002) Proteasome inhibitors in the treatment of B-cell malignancies. Clin Lymphoma 3:49-55.
56. Hernandez-Vargas H, von Kobbe C, Sanchez-Estevez C, Julian-Tendero M, Palacios J, and Moreno-Bueno G (2007) Inhibition of paclitaxelinduced proteasome activation influences paclitaxel cytotoxicity in breast cancer cells in a sequence-dependent manner. Cell Cycle 6:2662-2668. (Pubitemid 350224050)
57. Fujita T, Washio K, Takabatake D, Takahashi H, Yoshitomi S, Tsukuda K, Ishibe Y, Ogasawara Y, Doihara H, and Shimizu N (2005) Proteasome inhibitors can alter the signaling pathways and attenuate the P-glycoprotein-mediated multidrug resistance. Int J Cancer 117:670-682. (Pubitemid 41504558)
58. Kane RC, Dagher R, Farrell A, Ko CW, Sridhara R, Justice R, and Pazdur R (2007) Bortezomib for the treatment of mantle cell lymphoma. Clin Cancer Res 13:5291-5294. (Pubitemid 47510352)
59. Einsele H (2010) Bortezomib. Recent Results Cancer Res. 184:173-187.
60. Bae SH, Ryoo HM, Kim MK, Lee KH, Sin JI, and Hyun MS (2008) Effects of the proteasome inhibitor bortezomib alone and in combination with chemotherapeutic agents in gastric cancer cell lines. Oncol Rep 19:1027-1032. (Pubitemid 351802676)
61. Wagenblast J, Hambek M, Baghi M, Gstöttner W, Strebhardt K, Ackermann H, and Knecht R (2008) Antiproliferative activity of bortezomib alone and in combination with cisplatin or docetaxel in head and neck squamous cell carcinoma cell lines. J Cancer Res Clin Oncol 134:323-330. (Pubitemid 351170053)
62. Inoshita S, Takeda K, Hatai T, Terada Y, Sano M, Hata J, Umezawa A, and Ichijo H (2002) Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J Biol Chem 277:43730-43734. (Pubitemid 36157790)
63. Trembley JH, Chen Z, Unger G, Slaton J, Kren BT, Van Waes C, and Ahmed K (2010) Emergence of protein kinase CK2 as a key target in cancer therapy. Biofactors 36:187-195. A good recent review article describing CK2 and the rationale for targeting this kinase in therapy.
64. Karin M and Gallagher E (2005) From JNK to pay dirt: Jun kinases, their biochemistry, physiology and clinical importance. IUBMB Life 57:283-295. (Pubitemid 40904256)
65. Bogoyevitch MA, Ngoei KR, Zhao TT, Yeap YY, and Ng DC (2010) c-Jun N-terminal kinase (JNK) signaling: Recent advances and challenges. Biochim Biophys Acta 1804:463-475. This article describes the many functions of JNK, its biochemistry, and challenges in targeting this kinase for therapy.
66. Kumar S, Boehm J, and Lee JC (2003) p38 MAP kinases: Key signalling molecules as therapeutic targets for inflammatory diseases. Nat Rev Drug Discov 2:717-726. (Pubitemid 37361787)
67. St-Denis NA and Litchfield DW (2009) Protein kinase CK2 in health and disease: From birth to death: The role of protein kinase CK2 in the regulation of cell proliferation and survival. Cell Mol Life Sci 66:1817-1829.
68. Wagner EF and Nebreda AR (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9:537-549.
69. Genovese MC (2009) Inhibition of p38: Has the fat lady sung? Arthritis Rheum 60:317-320.
70. Manning AM and Davis RJ (2003) Targeting JNK for therapeutic benefit: From junk to gold? Nat Rev Drug Discov 2:554-565. (Pubitemid 37361747)
71. Duncan JS and Litchfield DW (2008) Too much of a good thing: The role of protein kinase CK2 in tumorigenesis and prospects for therapeutic inhibition of CK2. Biochim Biophys Acta 1784:33-47.
72. Ahmad KA, Wang G, Unger G, Slaton J, and Ahmed K (2008) Protein kinase CK2-a key suppressor of apoptosis. Adv Enzyme Regul 48:179-187.
73. C, Marani M, Pardo O, Warne PH, Kelly G, Sahai E, Elustondo F, Chang J, Temple J, Ahmed AA, et al. (2007) Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell. 11:498-512. This article identified genes that regulated cell sensitivity to paclitaxel through a high-throughput RNA interference screen. (Pubitemid 46856907)
74. Dounay AB and Forsyth CJ (2002) Okadaic acid: The archetypal serine/ threonine protein phosphatase inhibitor. Curr Med Chem 9:1939-1980. (Pubitemid 35256499)
75. Deng X, Ito T, Carr B, Mumby M, and May WS Jr (1998) Reversible phosphorylation of Bcl2 following interleukin 3 or bryostatin 1 is mediated by direct interaction with protein phosphatase 2A. J Biol Chem 273:34157-34163. (Pubitemid 29008888)
76. Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L, Adorno M, Martello G, Stinchfield MJ, Soligo S, Morsut L, et al. (2009) FAM/ USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 136:123-135.
77. Théard D, Labarrade F, Partisani M, Milanini J, Sakagami H, Fon EA, Wood SA, Franco M, and Luton F (2010) USP9x-mediated deubiquitination of EFA6 regulates de novo tight junction assembly. EMBO J 29:1499-1509.
78. Reed SI (2003) Ratchets and clocks: The cell cycle, ubiquitylation and protein turnover. Nat Rev Mol Cell Biol 4:855-864. (Pubitemid 37411724)