Overexpression of the dynein light chain km23-1 in human ovarian carcinoma cells inhibits tumor formation in vivo and causes mitotic delay at prometaphase/metaphase

International Journal of Cancer

Volumn 129, Issue 3, 2011, Pages 553-564

  Pulipati, Nageswara R ^a   Jin, Qunyan ^a   Liu, Xin ^a   Sun, Baodong ^a   Pandey, Manoj K ^a   Huber, Jonathan P ^a   Ding, Wei ^a   Mulder, Kathleen M ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

dynein; km23 1; mitosis; ovarian cancer

Indexed keywords

BUB1 RELATED PROTEIN; CYCLIN B1; DOXYCYCLINE; DYNEIN ADENOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KM23-1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL COUNT; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CENTROMERE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METAPHASE; MITOSIS INDEX; MITOSIS INHIBITION; MOUSE; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ANIMALS; CELL DIVISION; CELL LINE, TUMOR; CYTOPLASMIC DYNEINS; DYNEINS; FEMALE; HUMANS; METAPHASE; MICE; MICE, NUDE; MITOSIS; NEOPLASM TRANSPLANTATION; OVARIAN NEOPLASMS; PROMETAPHASE; TRANSPLANTATION, HETEROLOGOUS; UP-REGULATION;

EID: 79958045452     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25954     Document Type: Article

References (50)

1. American Cancer Society. Cancer facts and figures 2010. Atlanta, GA: American Cancer Society, 2010.
2. Wood KW, Lad L, Luo L, Qian X, Knight SD, Nevins N, Brejc K, Sutton D, Gilmartin AG, Chua PR, Desai R, Schauer SP, et al. Antitumor activity of an allosteric inhibitor of centromere-associated protein-E. Proc Natl Acad Sci USA 2010; 107: 5839-44.
3. Wacker SA, Kapoor TM,. Targeting a kinetochore-associated motor protein to kill cancer cells. Proc Natl Acad Sci USA 2010; 107: 5699-700.
4. Wojcik E, Basto R, Serr M, Scaerou F, Karess R, Hays T,. Kinetochore dynein: its dynamics and role in the transport of the rough deal checkpoint protein. Nat Cell Biol 2001; 3: 1001-7. (Pubitemid 34428745)
5. Vallee RB, Varma D, Dujardin DL,. ZW10 function in mitotic checkpoint control, dynein targeting and membrane trafficking: is dynein the unifying theme? Cell Cycle 2006; 5: 2447-51. (Pubitemid 44785820)
6. Tang Q, Staub CM, Gao G, Jin Q, Wang Z, Ding W, Aurigemma RE, Mulder KM,. A novel transforming growth factor-beta receptor-interacting protein that is also a light chain of the motor protein dynein. Mol Biol Cell 2002; 13: 4484-96. (Pubitemid 35471200)
7. Jiang J, Yu L, Huang X, Chen X, Li D, Zhang Y, Tang L, Zhao S,. Identification of two novel human dynein light chain genes, DNLC2A and DNLC2B, and their expression changes in hepatocellular carcinoma tissues from 68 Chinese patients. Gene 2001; 281: 103-13. (Pubitemid 34031909)
8. Bowman AB, Patel-King RS, Benashski SE, McCaffery JM, Goldstein LS, King SM,. Drosophila roadblock and Chlamydomonas LC7: a conserved family of dynein-associated proteins involved in axonal transport, flagellar motility, and mitosis. J Cell Biol 1999; 146: 165-80.
9. Pfister KK, Fisher EM, Gibbons IR, Hays TS, Holzbaur EL, McIntosh JR, Porter ME, Schroer TA, Vaughan KT, Witman GB, King SM, Vallee RB,. Cytoplasmic dynein nomenclature. J Cell Biol 2005; 171: 411-13. (Pubitemid 41586928)
10. Jin Q, Ding W, Mulder KM,. Requirement for the dynein light chain km23-1 in a Smad2-dependent transforming growth factor-beta signaling pathway. J Biol Chem 2007; 282: 19122-32. (Pubitemid 47100189)
11. Couwenbergs C, Labbe JC, Goulding M, Marty T, Bowerman B, Gotta M,. Heterotrimeric G protein signaling functions with dynein to promote spindle positioning in C. elegans. J Cell Biol 2007; 179: 15-22. (Pubitemid 47606679)
12. Jin Q, Ding W, Staub CM, Gao G, Tang Q, Mulder KM,. Requirement of km23 for TGFbeta-mediated growth inhibition and induction of fibronectin expression. Cell Signal 2005; 17: 1363-72. (Pubitemid 41206646)
13. Ilangovan U, Ding W, Zhong Y, Wilson CL, Groppe JC, Trbovich JT, Zuniga J, Demeler B, Tang Q, Gao G, Mulder KM, Hinck AP,. Structure and dynamics of the homodimeric dynein light chain km23. J Mol Biol 2005; 352: 338-54. (Pubitemid 41207786)
14. Jin Q, Gao G, Mulder KM,. Involvement of km23 light dynein chains in TGF beta signaling. In:, Jakowlew SB, ed. Transforming growth factor-beta in cancer therapy, vol. 1. Totowa, NJ: Humana Press Inc., 2008. 169-84.
15. Baldwin RL, Tran H, Karlan BY,. Loss of c-myc repression coincides with ovarian cancer resistance to transforming growth factor beta growth arrest independent of transforming growth factor beta/Smad signaling. Cancer Res 2003; 63: 1413-19. (Pubitemid 36348725)
16. Hu W, Wu W, Nash MA, Freedman RS, Kavanagh JJ, Verschraegen CF,. Anomalies of the TGF-beta postreceptor signaling pathway in ovarian cancer cell lines. Anticancer Res 2000; 20: 729-33. (Pubitemid 30240626)
17. Strathdee CA, McLeod MR, Hall JR,. Efficient control of tetracycline-responsive gene expression from an autoregulated bi-directional expression vector. Gene 1999; 229: 21-9. (Pubitemid 29148303)
18. Jin Q, Gao G, Mulder KM,. Requirement of a dynein light chain in TGFbeta/Smad3 signaling. J Cell Physiol 2009; 221: 707-15.
19. Mulder KM, Ramey MK, Hoosein NM, Levine AE, Hinshaw XH, Brattain DE, Brattain MG,. Characterization of transforming growth factor-beta-resistant subclones isolated from a transforming growth factor-beta-sensitive human colon carcinoma cell line. Cancer Res 1988; 48: 7120-5. (Pubitemid 19013992)
20. Howell BJ, McEwen BF, Canman JC, Hoffman DB, Farrar EM, Rieder CL, Salmon ED,. Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 2001; 155: 1159-72. (Pubitemid 34286267)
21. Beltrami E, Plescia J, Wilkinson JC, Duckett CS, Altieri DC,. Acute ablation of survivin uncovers p53-dependent mitotic checkpoint functions and control of mitochondrial apoptosis. J Biol Chem 2004; 279: 2077-84. (Pubitemid 38084480)
22. Ohishi T, Hirota T, Tsuruo T, Seimiya H,. TRF1 mediates mitotic abnormalities induced by Aurora-A overexpression. Cancer Res 2010; 70: 2041-52.
23. Yu D, Wolf JK, Scanlon M, Price JE, Hung MC,. Enhanced c-erbB-2/neu expression in human ovarian cancer cells correlates with more severe malignancy that can be suppressed by E1A. Cancer Res 1993; 53: 891-8. (Pubitemid 23077880)
24. Wu SP, Theodorescu D, Kerbel RS, Willson JK, Mulder KM, Humphrey LE, Brattain MG,. TGF-beta 1 is an autocrine-negative growth regulator of human colon carcinoma FET cells in vivo as revealed by transfection of an antisense expression vector. J Cell Biol 1992; 116: 187-96.
25. Wolf F, Wandke C, Isenberg N, Geley S,. Dose-dependent effects of stable cyclin B1 on progression through mitosis in human cells. EMBO J 2006; 25: 2802-13. (Pubitemid 43980387)
26. Borysov SI, Cheng AW, Guadagno TM,. B-Raf is critical for MAPK activation during mitosis and is regulated in an M phase-dependent manner in Xenopus egg extracts. J Biol Chem 2006; 281: 22586-96.
27. Harding A, Giles N, Burgess A, Hancock JF, Gabrielli BG,. Mechanism of mitosis-specific activation of MEK1. J Biol Chem 2003; 278: 16747-54. (Pubitemid 36799541)
28. Kang J, Yu H,. Kinase signaling in the spindle checkpoint. J Biol Chem 2009; 284: 15359-63.
29. Logarinho E, Bousbaa H,. Kinetochore-microtubule interactions "in check" by Bub1, Bub3 and BubR1: the dual task of attaching and signalling. Cell Cycle 2008; 7: 1763-8. (Pubitemid 351988741)
30. Nitta M, Kobayashi O, Honda S, Hirota T, Kuninaka S, Marumoto T, Ushio Y, Saya H,. Spindle checkpoint function is required for mitotic catastrophe induced by DNA-damaging agents. Oncogene 2004; 23: 6548-58. (Pubitemid 39265518)
31. Jeffery JM, Urquhart AJ, Subramaniam VN, Parton RG, Khanna KK,. Centrobin regulates the assembly of functional mitotic spindles. Oncogene 2010; 29: 2649-58.
32. Vakifahmetoglu H, Olsson M, Zhivotovsky B,. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008; 15: 1153-62. (Pubitemid 351850968)
33. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009; 16: 3-11.
34. D'Angiolella V, Grieco D,. Attach first, then detach: a role for cyclin B-dependent kinase 1 in coordinating proteolysis with spindle assembly. Cell Cycle 2004; 3: 132-3. (Pubitemid 40268681)
35. Clute P, Pines J,. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1999; 1: 82-7. (Pubitemid 129501948)
36. Xiong B, Yu LZ, Wang Q, Ai JS, Yin S, Liu JH, OuYang YC, Hou Y, Chen DY, Zou H, Sun QY,. Regulation of intracellular MEK1/2 translocation in mouse oocytes: cytoplasmic dynein/dynactin-mediated poleward transport and cyclin B degradation-dependent release from spindle poles. Cell Cycle 2007; 6: 1521-7.
37. Sivaram MV, Wadzinski TL, Redick SD, Manna T, Doxsey SJ,. Dynein light intermediate chain 1 is required for progress through the spindle assembly checkpoint. EMBO J 2009; 28: 902-14.
38. Lo KW, Kogoy JM, Pfister KK,. The DYNLT3 light chain directly links cytoplasmic dynein to a spindle checkpoint protein, Bub3. J Biol Chem 2007; 282: 11205-12. (Pubitemid 47100802)
39. Woodard GE, Huang NN, Cho H, Miki T, Tall GG, Kehrl JH,. Ric-8A and Gi alpha recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Mol Cell Biol 2010; 30: 3519-30.
40. Griffis ER, Stuurman N, Vale RD,. Spindly, a novel protein essential for silencing the spindle assembly checkpoint, recruits dynein to the kinetochore. J Cell Biol 2007; 177: 1005-15. (Pubitemid 46955705)
41. Kardon JR, Vale RD,. Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 2009; 10: 854-65.
42. Gaetz J, Kapoor TM,. Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles. J Cell Biol 2004; 166: 465-71. (Pubitemid 39097165)
43. Varma D, Monzo P, Stehman SA, Vallee RB,. Direct role of dynein motor in stable kinetochore-microtubule attachment, orientation, and alignment. J Cell Biol 2008; 182: 1045-54.
44. Stevens JB, Liu G, Bremer SW, Ye KJ, Xu W, Xu J, Sun Y, Wu GS, Savasan S, Krawetz SA, Ye CJ, Heng HH,. Mitotic cell death by chromosome fragmentation. Cancer Res 2007; 67: 7686-94. (Pubitemid 47281361)
45. Li S, Szymborski A, Miron MJ, Marcellus R, Binda O, Lavoie JN, Branton PE,. The adenovirus E4orf4 protein induces growth arrest and mitotic catastrophe in H1299 human lung carcinoma cells. Oncogene 2009; 28: 390-400.
46. Kwong J, Kulbe H, Wong D, Chakravarty P, Balkwill F,. An antagonist of the chemokine receptor CXCR4 induces mitotic catastrophe in ovarian cancer cells. Mol Cancer Ther 2009; 8: 1893-905.
47. Janssen A, Kops GJ, Medema RH,. Elevating the frequency of chromosome mis-segregation as a strategy to kill tumor cells. Proc Natl Acad Sci USA 2009; 106: 19108-13.
48. Vogelstein B, Kinzler KW,. Achilles' heel of cancer? Nature 2001; 412: 865-6. (Pubitemid 32821714)
49. Buck E, Eyzaguirre A, Brown E, Petti F, McCormack S, Haley JD, Iwata KK, Gibson NW, Griffin G,. Rapamycin synergizes with the epidermal growth factor receptor inhibitor erlotinib in non-small-cell lung, pancreatic, colon, and breast tumors. Mol Cancer Ther 2006; 5: 2676-84. (Pubitemid 44848994)
50. Debnath J, Brugge JS,. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 2005; 5: 675-88. (Pubitemid 41486361)