Underexpression of LATS1 TSG in colorectal cancer is associated with promoter hypermethylation

World Journal of Gastroenterology

Volumn 19, Issue 27, 2013, Pages 4363-4373

  Wierzbicki, Piotr M ^a   Adrych, Krystian ^a   Kartanowicz, Dorota ^a   Stanislawowski, Marcin ^a   Kowalczyk, Anna ^b   Godlewski, Janusz ^b   Skwierz Bogdanska, Iwona ^c   Celinski, Krzysztof ^d   Gach, Tomasz ^e   Kulig, Jan ^e   Korybalski, Bartlomiej ^f   Kmiec, Zbigniew ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

^b UNIVERSITY OF WARMIA AND MAZURY IN OLSZTYN   (Poland)

^c Hospital of the Ministry of Internal Affairs   (Poland)

^d MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^e JAGIELLONIAN UNIVERSITY   (Poland)

^f ST ADALBERT HOSPITAL   (Poland)

Author keywords

Colorectal cancer; Large tumor suppressor 1; Microsatellite instability; Promoter hypermethylation; Quantitative polymerase chain reaction; Reduced expression; Salvador Warts Hippo pathway

Indexed keywords

GENOMIC DNA;

ADULT; AGED; ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA METHYLATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LATS1 GENE; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; PROMOTER REGION; REVERSE TRANSCRIPTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TUMOR SUPPRESSOR GENE;

EID: 84880439674     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v19.i27.4363     Document Type: Article

References (56)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010; 127: 2893-2917 [PMID: 21351269 DOI: 10.1002/ijc.25516]
2. Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, Feuer EJ, Thun MJ. Cancer statistics, 2005. CA Cancer J Clin 2005; 55: 10-30 [PMID: 15661684]
3. Walsh JM, Terdiman JP. Colorectal cancer screening: scientific review. JAMA 2003; 289: 1288-1296 [PMID: 12633191]
4. St John MA, Tao W, Fei X, Fukumoto R, Carcangiu ML, Brownstein DG, Parlow AF, McGrath J, Xu T. Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat Genet 1999; 21: 182-186 [PMID: 9988269 DOI: 10.1038/5965]
5. Xu T, Wang W, Zhang S, Stewart RA, Yu W. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 1995; 121: 1053-1063 [PMID: 7743921]
6. Iida S, Hirota T, Morisaki T, Marumoto T, Hara T, Kuninaka S, Honda S, Kosai K, Kawasuji M, Pallas DC, Saya H. Tumor suppressor WARTS ensures genomic integrity by regulating both mitotic progression and G1 tetraploidy checkpoint function. Oncogene 2004; 23: 5266-5274 [PMID: 15122335 DOI: 10.1038/sj.onc.1207623]
7. Tao W, Zhang S, Turenchalk GS, Stewart RA, St John MA, Chen W, Xu T. Human homologue of the Drosophila melanogaster lats tumour suppressor modulates CDC2 activity. Nat Genet 1999; 21: 177-181 [PMID: 9988268 DOI: 10.1038/5960]
8. Bothos J, Tuttle RL, Ottey M, Luca FC, Halazonetis TD. Human LATS1 is a mitotic exit network kinase. Cancer Res 2005; 65: 6568-6575 [PMID: 16061636]
9. Yang X, Yu K, Hao Y, Li DM, Stewart R, Insogna KL, Xu T. LATS1 tumour suppressor affects cytokinesis by inhibiting LIMK1. Nat Cell Biol 2004; 6: 609-617 [PMID: 15220930 DOI: 10.1038/ncb1140]
10. Hergovich A, Hemmings BA. Mammalian NDR/LATS protein kinases in hippo tumor suppressor signaling. Biofactors 2009; 35: 338-345 [PMID: 19484742 DOI: 10.1002/biof.47]
11. Liu AM, Wong KF, Jiang X, Qiao Y, Luk JM. Regulators of mammalian Hippo pathway in cancer. Biochim Biophys Acta 2012; 1826: 357-364 [PMID: 22683405]
12. Grusche FA, Degoutin JL, Richardson HE, Harvey KF. The Salvador/Warts/Hippo pathway controls regenerative tissue growth in Drosophila melanogaster. Dev Biol 2011; 350: 255-266 [PMID: 21111727]
13. Zhang X, Milton CC, Humbert PO, Harvey KF. Transcriptional output of the Salvador/warts/hippo pathway is controlled in distinct fashions in Drosophila melanogaster and mammalian cell lines. Cancer Res 2009; 69: 6033-6041 [PMID: 19584286]
14. Harvey K, Tapon N. The Salvador-Warts-Hippo pathway-an emerging tumour-suppressor network. Nat Rev Cancer 2007; 7: 182-191 [PMID: 17318211]
15. Zeng Q, Hong W. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 2008; 13: 188-192 [PMID: 18328423]
16. Moleirinho S, Chang N, Sims AH, Tilston-Lünel AM, Angus L, Steele A, Boswell V, Barnett SC, Ormandy C, Faratian D, Gunn-Moore FJ, Reynolds PA. KIBRA exhibits MSTindependent functional regulation of the Hippo signaling pathway in mammals. Oncogene 2013; 32: 1821-1830 [PMID: 22614006 DOI: 10.1038/onc.2012.196]
17. Hao Y, Chun A, Cheung K, Rashidi B, Yang X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 2008; 283: 5496-5509 [PMID: 18158288]
18. Matallanas D, Romano D, Yee K, Meissl K, Kucerova L, Piazzolla D, Baccarini M, Vass JK, Kolch W, O'neill E. RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol Cell 2007; 27: 962-975 [PMID: 17889669]
19. Yang X, Li DM, Chen W, Xu T. Human homologue of Drosophila lats, LATS1, negatively regulate growth by inducing G(2)/M arrest or apoptosis. Oncogene 2001; 20: 6516-6523 [PMID: 11641775 DOI: 10.1038/sj.onc.1204817]
20. Hisaoka M, Tanaka A, Hashimoto H. Molecular alterations of h-warts/LATS1 tumor suppressor in human soft tissue sarcoma. Lab Invest 2002; 82: 1427-1435 [PMID: 12379777]
21. Jiang Z, Li X, Hu J, Zhou W, Jiang Y, Li G, Lu D. Promoter hypermethylation-mediated down-regulation of LATS1 and LATS2 in human astrocytoma. Neurosci Res 2006; 56: 450-458 [PMID: 17049657]
22. Takahashi Y, Miyoshi Y, Takahata C, Irahara N, Taguchi T, Tamaki Y, Noguchi S. Down-regulation of LATS1 and LATS2 mRNA expression by promoter hypermethylation and its association with biologically aggressive phenotype in human breast cancers. Clin Cancer Res 2005; 11: 1380-1385 [PMID: 15746036]
23. Siam R, Harada R, Cadieux C, Battat R, Vadnais C, Nepveu A. Transcriptional activation of the Lats1 tumor suppressor gene in tumors of CUX1 transgenic mice. Mol Cancer 2009; 8: 60 [PMID: 19656388]
24. Steinmann K, Sandner A, Schagdarsurengin U, Dammann RH. Frequent promoter hypermethylation of tumor-related genes in head and neck squamous cell carcinoma. Oncol Rep 2009; 22: 1519-1526 [PMID: 19885608]
25. Xu ZP, Zhu JS, Zhang Q, Wang XY. A breakdown of the Hippo pathway in gastric cancer. Hepatogastroenterology 2011; 58: 1611-1617 [PMID: 21940329 DOI: 10.5754/hge10669]
26. Bianchini M, Levy E, Zucchini C, Pinski V, Macagno C, De Sanctis P, Valvassori L, Carinci P, Mordoh J. Comparative study of gene expression by cDNA microarray in human colorectal cancer tissues and normal mucosa. Int J Oncol 2006; 29: 83-94 [PMID: 16773188]
27. Demokan S, Dalay N. Role of DNA methylation in head and neck cancer. Clin Epigenetics 2011; 2: 123-150 [PMID: 22704334 DOI: 10.1007/s13148-011-0045-3]
28. Dumitrescu RG. Epigenetic markers of early tumor development. Methods Mol Biol 2012; 863: 3-14 [PMID: 22359284 DOI: 10.1007/978-1-61779-612-8_1]
29. Draht MX, Riedl RR, Niessen H, Carvalho B, Meijer GA, Herman JG, van Engeland M, Melotte V, Smits KM. Promoter CpG island methylation markers in colorectal cancer: the road ahead. Epigenomics 2012; 4: 179-194 [PMID: 22449189 DOI: 10.2217/epi.12.9]
30. Khare S, Verma M. Epigenetics of colon cancer. Methods Mol Biol 2012; 863: 177-185 [PMID: 22359293 DOI: 10.1007/978-1-61779-612-8_10]
31. Morinaga N, Shitara Y, Yanagita Y, Koida T, Kimura M, Asao T, Kimijima I, Takenoshita S, Hirota T, Saya H, Kuwano H. Molecular analysis of the h-warts/LATS1 gene in human breast cancer. Int J Oncol 2000; 17: 1125-1129 [PMID: 11078797]
32. Wierzbicki PM, Dubowska J, Adrych K, Kartanowicz D, Dobrowolski S, Stanislawowski M, Chybicki J, Korybalski B, Godlewski J, Mazurek A, Kotwas M, Wronska A, Kmiec Z. Promoter hypermethylation and underexpression of PLAGL1 and LATS1 tumor suppressor genes in colorectal cancer. Imaging of cell dynamics. Gdansk: Folia Histochem Cytobiol, 2008: 78.
33. Cavalieri D, Dolara P, Mini E, Luceri C, Castagnini C, Toti S, Maciag K, De Filippo C, Nobili S, Morganti M, Napoli C, Tonini G, Baccini M, Biggeri A, Tonelli F, Valanzano R, Orlando C, Gelmini S, Cianchi F, Messerini L, Luzzatto L. Analysis of gene expression profiles reveals novel correlations with the clinical course of colorectal cancer. Oncol Res 2007; 16: 535-548 [PMID: 18306933]
34. McLendon R, Friedman A, Bigner D, Van Meir EG, Brat DJ, Mastrogianakis GM, Olson JJ, Mikkelsen T, Lehman N, Aldape K, Yung WK, Bogler O, Weinstein JN, VandenBerg S, Berger M, Prados M, Muzny D, Morgan M, Scherer S, Sabo A, Nazareth L, Lewis L, Hall O, Zhu Y, Ren Y, Alvi O, Yao J, Hawes A, Jhangiani S, Fowler G, San L.A, Kovar C, Cree A, Dinh H, Santibanez J, Joshi V, Gonzalez-Garay ML, Miller CA, Milosavljevic A, Donehower L, Wheeler DA, Gibbs RA, Cibulskis K, Sougnez C, Fennell T, Mahan S, Wilkinson J, Ziaugra L, Onofrio R, Bloom T, Nicol R, Ardlie K, Baldwin J, Gabriel S, Lander ES, Ding L, Fulton RS, McLellan MD, Wallis J, Larson DE, Shi X, Abbott R, Fulton L, Chen K, Koboldt DC, Wendl MC, Meyer R, Tang Y, Lin L, Osborne JR, Dunford-Shore BH, Miner TL, Delehaunty K, Markovic C, Swift G, Courtney W, Pohl C, Abbott S, Hawkins A, Leong S, Haipek C, Schmidt H, Wiechert M, Vickery T, Scott S, Dooling DJ, Chinwalla A, Weinstock GM, Mardis ER, Wilson RK, Getz G, Winckler W, Verhaak RG, Lawrence MS, O'Kelly M, Robinson J, Alexe G, Beroukhim R, Carter S, Chiang D, Gould J, Gupta S, Korn J, Mermel C, Mesirov J, Monti S, Nguyen H, Parkin M, Reich M, Stransky N, Weir BA, Garraway L, Golub T, Meyerson M, Chin L, Protopopov A, Zhang J, Perna I, Aronson S, Sathiamoorthy N, Ren G, Yao J, Wiedemeyer WR, Kim H, Kong SW, Xiao Y, Kohane IS, Seidman J, Park PJ, Kucherlapati R, Laird PW, Cope L, Herman JG, Weisenberger DJ, Pan F, Van den Berg D, Van Neste L, Yi JM, Schuebel KE, Baylin SB, Absher DM, Li JZ, Southwick A, Brady S, Aggarwal A, Chung T, Sherlock G, Brooks JD, Myers RM, Spellman PT, Purdom E, Jakkula LR, Lapuk AV, Marr H, Dorton S, Choi YG, Han J, Ray A, Wang V, Durinck S, Robinson M, Wang NJ, Vranizan K, Peng V, Van Name E, Fontenay GV, Ngai J, Conboy JG, Parvin B, Feiler HS, Speed TP, Gray JW, Brennan C, Socci ND, Olshen A, Taylor BS, Lash A, Schultz N, Reva B, Antipin Y, Stukalov A, Gross B, Cerami E, Wang WQ, Qin LX, Seshan VE, Villafania L, Cavatore M, Borsu L, Viale A, Gerald W, Sander C, Ladanyi M, Perou CM, Hayes DN, Topal MD, Hoadley KA, Qi Y, Balu S, Shi Y, Wu J, Penny R, Bittner M, Shelton T, Lenkiewicz E, Morris S, Beasley D, Sanders S, Kahn A, Sfeir R, Chen J, Nassau D, Feng L, Hickey E, Barker A, Gerhard DS, Vockley J, Compton C, Vaught J, Fielding P, Ferguson ML, Schaefer C, Zhang J, Madhavan S, Buetow KH, Collins F, Good P, Guyer M, Ozenberger B, Peterson J, Thomson E; Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455: 1061-1068 [PMID: 18772890 DOI: 10.1038/Nature07385]
35. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3: 1101-1108 [PMID: 18546601]
36. Wierzbicki PM, Adrych K, Kartanowicz D, Dobrowolski S, Stanislawowski M, Chybicki J, Godlewski J, Korybalski B, Smoczynski M, Kmiec Z. Fragile histidine triad (FHIT) gene is overexpressed in colorectal cancer. J Physiol Pharmacol 2009; 60 Suppl 4: 63-70 [PMID: 20083853]
37. Wierzbicki PM, Adrych K, Kartanowicz D, Wypych J, Stan-islawowski M, Zwolinska-Wcislo M, Celinski K, Skrodzka D, Godlewski J, Korybalski B, Smoczynski M, Kmiec Z. Overexpression of the fragile histidine triad (FHIT) gene in inflammatory bowel disease. J Physiol Pharmacol 2009; 60 Suppl 4: 57-62 [PMID: 20083852]
38. Rubie C, Kempf K, Hans J, Su T, Tilton B, Georg T, Brittner B, Ludwig B, Schilling M. Housekeeping gene variability in normal and cancerous colorectal, pancreatic, esophageal, gastric and hepatic tissues. Mol Cell Probes 2005; 19: 101-109 [PMID: 15680211]
39. Niu Y, Yeh S, Miyamoto H, Li G, Altuwaijri S, Yuan J, Han R, Ma T, Kuo HC, Chang C. Tissue prostate-specific antigen facilitates refractory prostate tumor progression via enhancing ARA70-regulated androgen receptor transactivation. Cancer Res 2008; 68: 7110-7119 [PMID: 18757426]
40. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, Burt RW, Meltzer SJ, Rodriguez-Bigas MA, Fodde R, Ranzani GN, Srivastava S. A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res 1998; 58: 5248-5257 [PMID: 9823339]
41. Wierzbicki PM, Adrych K, Kartanowicz D, Wypych J, Stanislawowski M, Dobrowolski S, Chybicki J, Zwolinska-Wcislo M, celinski K, Korybalski B, Smoczynski M, Sledzinski Z, Kmiec Z. Microsatellite instability status in inflammatory bowel disease and colorectal cancer. Ann Acad Med Gedan 2009; 39: 163-171.
42. Wittekind C, Compton CC, Greene FL, Sobin LH. TNM residual tumor classification revisited. Cancer 2002; 94: 2511-2516 [PMID: 12015777 DOI: 10.1002/cncr.10492]
43. Samee A, Selvasekar CR. Current trends in staging rectal cancer. World J Gastroenterol 2011; 17: 828-834 [PMID: 21412492 DOI: 10.3748/wjg.v17.i7.828]
44. Avruch J, Zhou D, Bardeesy N. YAP oncogene overexpression supercharges colon cancer proliferation. Cell Cycle 2012; 11: 1090-1096 [PMID: 22356765 DOI: 10.4161/cc.11.6.19453]
45. Wu WK, Wang XJ, Cheng AS, Luo MX, Ng SS, To KF, Chan FK, Cho CH, Sung JJ, Yu J. Dysregulation and crosstalk of cellular signaling pathways in colon carcinogenesis. Crit Rev Oncol Hematol 2013; 86: 251-277 [PMID: 23287077]
46. Matallanas D, Romano D, Al-Mulla F, O'Neill E, Al-Ali W, Crespo P, Doyle B, Nixon C, Sansom O, Drosten M, Barbacid M, Kolch W. Mutant K-Ras activation of the proapoptotic MST2 pathway is antagonized by wild-type K-Ras. Mol Cell 2011; 44: 893-906 [PMID: 22195963 DOI: 10.1016/ j.molcel.2011.10.016]
47. Ji T, Liu D, Shao W, Yang W, Wu H, Bian X. Decreased expression of LATS1 is correlated with the progression and prognosis of glioma. J Exp Clin Cancer Res 2012; 31: 67 [PMID: 22909338 DOI: 10.1186/1756-9966-31-67]
48. Laghi L, Malesci A. Microsatellite instability and therapeutic consequences in colorectal cancer. Dig Dis 2012; 30: 304-309 [PMID: 22722556 DOI: 10.1159/000337003]
49. Manne U, Shanmugam C, Katkoori VR, Bumpers HL, Grizzle WE. Development and progression of colorectal neoplasia. Cancer Biomark 2010; 9: 235-265 [PMID: 22112479 DOI: 10.3233/CBM-2011-0160]
50. Smigiel R, Stembalska A, Stal A, Jonkisz A, Trusewicz A, Dobosz T, Grzebieniak Z, Sasiadek M. The Microsatellite Instability in Patients with Colon Cancer Treated in Lower Silesia. Adv Clin Exp Med 2006; 15: 29-36.
51. Birkenkamp-Demtroder K, Mansilla F, Sørensen FB, Kruhøffer M, Cabezón T, Christensen LL, Aaltonen LA, Verspaget HW, Ørntoft TF. Phosphoprotein Keratin 23 accumulates in MSS but not MSI colon cancers in vivo and impacts viability and proliferation in vitro. Mol Oncol 2007; 1: 181-195 [PMID: 19383294 DOI: 10.1016/j.molonc.2007.05.005]
52. Mizoguchi M, Kuga D, Guan Y, Hata N, Nakamizo A, Yoshimoto K, Sasaki T. Loss of heterozygosity analysis in malignant gliomas. Brain Tumor Pathol 2011; 28: 191-196 [PMID: 21629980 DOI: 10.1007/s10014-011-0038-0]
53. Beaty MW, Quezado M, Sobel ME, Duray P, Merino MJ. Loss of heterozygosity on chromosome 1 and 9 and hormone receptor analysis of metastatic malignant melanoma presenting in breast. Int J Surg Pathol 2005; 13: 9-18 [PMID: 15735850]
54. Armaghany T, Wilson JD, Chu Q, Mills G. Genetic alterations in colorectal cancer. Gastrointest Cancer Res 2012; 5: 19-27 [PMID: 22574233]
55. Ashktorab H, Schäffer AA, Daremipouran M, Smoot DT, Lee E, Brim H. Distinct genetic alterations in colorectal cancer. PLoS One 2010; 5: e8879 [PMID: 20126641 DOI: 10.1371/ journal.pone.0008879]
56. Matsuura K, Nakada C, Mashio M, Narimatsu T, Yoshimoto T, Tanigawa M, Tsukamoto Y, Hijiya N, Takeuchi I, Nomura T, Sato F, Mimata H, Seto M, Moriyama M. Downregulation of SAV1 plays a role in pathogenesis of highgrade clear cell renal cell carcinoma. BMC Cancer 2011; 11: 523 [PMID: 22185343 DOI: 10.1186/1471-2407-11-523]