Parkin deficiency contributes to pancreatic tumorigenesis by inducing spindle multipolarity and misorientation

Cell Cycle

Volumn 12, Issue 7, 2013, Pages 1133-1141

  Sun, Xiaodong ^a   Liu, Min ^b   Hao, Jihui ^c   Li, Dengwen ^a   Luo, Youguang ^a   Wang, Xiuchao ^c   Yang, Yunfan ^a   Li, Fang ^a   Shui, Wenqing ^a   Chen, Quan ^a   Zhou, Jun ^a  

^a NANKAI UNIVERSITY   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c KEY LABORATORY OF CANCER PREVENTION AND THERAPY   (China)

Author keywords

Cell proliferation; Pancreatic cancer; Parkin; Spindle misorientation; Spindle multipolarity

Indexed keywords

MESSENGER RNA; PARKIN;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL CYCLE PHASE; CELL FUNCTION; CELL POLARITY; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DEPLETION; DOWN REGULATION; ENZYME DEFICIENCY; GENE DOSAGE; GENE EXPRESSION; GENE SILENCING; GENERAL PATHOLOGICAL PARAMETERS; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; PANCREAS CANCER; SPINDLE CELL;

EID: 84875909195     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24215     Document Type: Article

References (45)

1. Shimura H, Hattori N, Kubo Si, Mizuno Y, Asakawa S, Minoshima S, et al. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 2000; 25:302-5; PMID:10888878; http://dx.doi.org/10.1038/77060
2. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998; 392:605-8; PMID:9560156; http://dx.doi.org/10.1038/ 33416
3. Debatisse M, Le Tallec B, Letessier A, Dutrillaux B, Brison O. Common fragile sites: mechanisms of instability revisited. Trends Genet 2012; 28:22- 32; PMID:22094264; http://dx.doi.org/10.1016/j. tig.2011.10.003
4. Tanaka K, Suzuki T, Hattori N, Mizuno Y. Ubiquitin, proteasome and parkin. Biochim Biophys Acta 2004; 1695:235-47; PMID:15571819; http://dx.doi. org/10.1016/j.bbamcr.2004.09.026
5. Kuroda Y, Mitsui T, Kunishige M, Shono M, Akaike M, Azuma H, et al. Parkin enhances mitochondrial biogenesis in proliferating cells. Hum Mol Genet 2006; 15:883-95; PMID:16449237; http://dx.doi. org/10.1093/hmg/ddl006
6. Rothfuss O, Fischer H, Hasegawa T, Maisel M, Leitner P, Miesel F, et al. Parkin protects mitochondrial genome integrity and supports mitochondrial DNA repair. Hum Mol Genet 2009; 18:3832-50; PMID:19617636; http://dx.doi.org/10. 1093/hmg/ddp327
7. Geisler S, Holmström KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, et al. PINK1/Parkinmediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12:119-31; PMID:20098416; http://dx.doi.org/10.1038/ncb2012
8. Yang F, Jiang Q, Zhao J, Ren Y, Sutton MD, Feng J. Parkin stabilizes microtubules through strong binding mediated by three independent domains. J Biol Chem 2005; 280:17154-62; PMID:15737990; http://dx.doi. org/10.1074/jbc. M500843200
9. Cesari R, Martin ES, Calin GA, Pentimalli F, Bichi R, McAdams H, et al. Parkin, a gene implicated in autosomal recessive juvenile parkinsonism, is a candidate tumor suppressor gene on chromosome 6q25-q27. Proc Natl Acad Sci USA 2003; 100:5956- 61; PMID:12719539; http://dx.doi.org/10.1073/pnas.0931262100
10. Denison SR, Wang F, Becker NA, Schüle B, Kock N, Phillips LA, et al. Alterations in the common fragile site gene Parkin in ovarian and other cancers. Oncogene 2003; 22:8370-8; PMID:14614460; http://dx.doi. org/10.1038/sj.onc.1207072
11. Wang F, Denison S, Lai JP, Philips LA, Montoya D, Kock N, et al. Parkin gene alterations in hepatocellular carcinoma. Genes Chromosomes Cancer 2004; 40:85- 96; PMID:15101042; http://dx.doi.org/10.1002/gcc.20020
12. Picchio MC, Martin ES, Cesari R, Calin GA, Yendamuri S, Kuroki T, et al. Alterations of the tumor suppressor gene Parkin in non-small cell lung cancer. Clin Cancer Res 2004; 10:2720-4; PMID:15102676; http://dx.doi.org/10.1158/1078- 0432.CCR-03-0086
13. Poulogiannis G, McIntyre RE, Dimitriadi M, Apps JR, Wilson CH, Ichimura K, et al. PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proc Natl Acad Sci USA 2010; 107:15145-50; PMID:20696900; http://dx.doi.org/10.1073/pnas.1009941107
14. Veeriah S, Taylor BS, Meng S, Fang F, Yilmaz E, Vivanco I, et al. Somatic mutations of the Parkinson's disease-associated gene PARK2 in glioblastoma and other human malignancies. Nat Genet 2010; 42:77-82; PMID:19946270; http://dx.doi.org/10.1038/ng.491
15. Letessier A, Garrido-Urbani S, Ginestier C, Fournier G, Esterni B, Monville F, et al. Correlated break at PARK2/FRA6E and loss of AF-6/Afadin protein expression are associated with poor outcome in breast cancer. Oncogene 2007; 26:298-307; PMID:16819513; http://dx.doi.org/10.1038/sj.onc.1209772
16. Fujiwara M, Marusawa H, Wang HQ, Iwai A, Ikeuchi K, Imai Y, et al. Parkin as a tumor suppressor gene for hepatocellular carcinoma. Oncogene 2008; 27:6002- 11; PMID:18574468; http://dx.doi.org/10.1038/onc.2008.199
17. Agirre X, Román-Gómez J, Vázquez I, Jiménez-Velasco A, Garate L, Montiel-Duarte C, et al. Abnormal methylation of the common PARK2 and PACRG promoter is associated with downregulation of gene expression in acute lymphoblastic leukemia and chronic myeloid leukemia. Int J Cancer 2006; 118:1945- 53; PMID:16287063; http://dx.doi.org/10.1002/ijc.21584
18. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012; 62:10-29; PMID:22237781; http://dx.doi.org/10.3322/caac.20138
19. Koorstra JB, Hustinx SR, Offerhaus GJ, Maitra A. Pancreatic carcinogenesis. Pancreatology 2008; 8:110-25; PMID:18382097; http://dx.doi. org/10.1159/000123838
20. Campbell PJ, Yachida S, Mudie LJ, Stephens PJ, Pleasance ED, Stebbings LA, et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010; 467:1109-13; PMID:20981101; http://dx.doi.org/ 10.1038/nature09460
21. Iacobuzio-Donahue CA. Genetic evolution of pancreatic cancer: lessons learnt from the pancreatic cancer genome sequencing project. Gut 2012; 61:1085- 94; PMID:21749982; http://dx.doi.org/10.1136/gut.2010.236026
22. Goonetilleke KS, Siriwardena AK. Systematic review of carbohydrate antigen (CA 19-9) as a biochemical marker in the diagnosis of pancreatic cancer. Eur J Surg Oncol 2007; 33:266-70; PMID:17097848; http://dx.doi.org/10.1016/j. ejso.2006.10.004
23. Ghaneh P, Costello E, Neoptolemos JP. Biology and management of pancreatic cancer. Gut 2007; 56:1134- 52; PMID:17625148
24. Hezel AF, Kimmelman AC, Stanger BZ, Bardeesy N, Depinho RA. Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev 2006; 20:1218- 49; PMID:16702400; http://dx.doi.org/10.1101/gad.1415606
25. Chen Y, Fang ST, Yeh PC, Yang HH, Chen SY, Chang CJ, et al. The C-terminus of PARK2 is required for its self-interaction, solubility and role in the spindle assembly checkpoint. Biochim Biophys Acta 2012; 1822:573-80; PMID:22200450; http://dx.doi. org/10.1016/j.bbadis.2011.12.007
26. Zhao J, Ren Y, Jiang Q, Feng J. Parkin is recruited to the centrosome in response to inhibition of proteasomes. J Cell Sci 2003; 116:4011-9; PMID:12928331; http://dx.doi.org/10.1242/jcs.00700
27. Kapitein LC, Peterman EJ, Kwok BH, Kim JH, Kapoor TM, Schmidt CF. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 2005; 435:114-8; PMID:15875026; http://dx.doi. org/10.1038/nature03503
28. Liu M, Aneja R, Sun X, Xie S, Wang H, Wu X, et al. Parkin regulates Eg5 expression by Hsp70 ubiquitination-dependent inactivation of c-Jun NH2- terminal kinase. J Biol Chem 2008; 283:35783-8; PMID:18845538; http://dx.doi.org/10. 1074/jbc. M806860200
29. Liu M, Wang X, Yang Y, Li D, Ren H, Zhu Q, et al. Ectopic expression of the microtubule-dependent motor protein Eg5 promotes pancreatic tumourigenesis. J Pathol 2010; 221:221-8; PMID:20455257; http://dx.doi.org/10.1002/path.2706
30. Castillo A, Morse HC 3rd, Godfrey VL, Naeem R, Justice MJ. Overexpression of Eg5 causes genomic instability and tumor formation in mice. Cancer Res 2007; 67:10138-47; PMID:17974955; http://dx.doi. org/10.1158/0008-5472.CAN-07-0326
31. Saunders W. Centrosomal amplification and spindle multipolarity in cancer cells. Semin Cancer Biol 2005; 15:25-32; PMID:15613285; http://dx.doi. org/10.1016/j.semcancer.2004.09.003
32. Ganem NJ, Godinho SA, Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009; 460:278-82; PMID:19506557; http://dx.doi.org/10.1038/nature08136
33. Holland AJ, Cleveland DW. Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 2009; 10:478-87; PMID:19546858; http://dx.doi.org/10.1038/nrm2718
34. Morin X, Bellaïche Y. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev Cell 2011; 21:102-19; PMID:21763612; http://dx.doi.org/10.1016/j.devcel. 2011.06.012
35. Pease JC, Tirnauer JS. Mitotic spindle misorientation in cancer-out of alignment and into the fire. J Cell Sci 2011; 124:1007-16; PMID:21402874; http://dx.doi. org/10.1242/jcs.081406
36. Yamashita YM, Jones DL, Fuller MT. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 2003; 301:1547- 50; PMID:12970569; http://dx.doi.org/10.1126/science. 1087795
37. den Elzen N, Buttery CV, Maddugoda MP, Ren G, Yap AS. Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Mol Biol Cell 2009; 20:3740- 50; PMID:19553471; http://dx.doi.org/ 10.1091/mbc. E09-01-0023
38. Thoma CR, Toso A, Gutbrodt KL, Reggi SP, Frew IJ, Schraml P, et al. VHL loss causes spindle misorientation and chromosome instability. Nat Cell Biol 2009; 11:994-1001; PMID:19620968; http://dx.doi. org/10.1038/ncb1912
39. Joch M, Ase AR, Chen CX, MacDonald PA, Kontogiannea M, Corera AT, et al. Parkin-mediated monoubiquitination of the PDZ protein PICK1 regulates the activity of acid-sensing ion channels. Mol Biol Cell 2007; 18:3105-18; PMID:17553932; http://dx.doi.org/10.1091/mbc.E05-11-1027
40. Moore DJ, West AB, Dikeman DA, Dawson VL, Dawson TM. Parkin mediates the degradation-independent ubiquitination of Hsp70. J Neurochem 2008; 105:1806-19; PMID:18248624; http://dx.doi. org/10.1111/j.1471-4159.2008.05261.x
41. Chew KC, Matsuda N, Saisho K, Lim GG, Chai C, Tan HM, et al. Parkin mediates apparent E2-independent monoubiquitination in vitro and contains an intrinsic activity that catalyzes polyubiquitination. PLoS ONE 2011; 6:e19720; PMID:21625422; http://dx.doi. org/10.1371/journal.pone.0019720
42. Hansen GM, Justice MJ. Activation of Hex and mEg5 by retroviral insertion may contribute to mouse B-cell leukemia. Oncogene 1999; 18:6531- 9; PMID:10597256; http://dx.doi.org/10.1038/sj.onc.1203023
43. Sun X, Shi X, Liu M, Li D, Zhang L, Liu X, et al. Mdp3 is a novel microtubule-binding protein that regulates microtubule assembly and stability. Cell Cycle 2011; 10:3929-37; PMID:22142902; http://dx.doi. org/10.4161/cc.10.22. 18106
44. Wang H, Liu B, Zhang C, Peng G, Liu M, Li D, et al. Parkin regulates paclitaxel sensitivity in breast cancer via a microtubule-dependent mechanism. J Pathol 2009; 218:76-85; PMID:19214989; http://dx.doi. org/10.1002/path.2512
45. Shi X, Liu M, Li D, Wang J, Aneja R, Zhou J. Cep70 contributes to angiogenesis by modulating microtubule rearrangement and stimulating cell polarization and migration. Cell Cycle 2012; 11:1554-63; PMID:22437770; http://dx.doi.org/10.4161/cc.19954