Characterization of LMX-1A as a metastasis suppressor in cervical cancer

Journal of Pathology

Volumn 219, Issue 2, 2009, Pages 222-231

  Liu, Chin Yu ^a,b   Chao, Tai Kuang ^b   Su, Po Hsuan ^a   Lee, Hsin Yi ^b   Shih, Yu Lueng ^b   Su, Her Young ^b   Chu, Tang Yuan ^c   Yu, Mu Hsien ^b   Lin, Ya Wen ^a   Lai, Hung Cheng ^a,b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^c TZU CHI UNIVERSITY   (Taiwan)

Author keywords

Cancer; Cervical cancer; Cervix; Epigenetic; Epigenetics; Epithelial mesenchymal transition; LIM homeobox; LMX 1A; Metastasis; Methylation

Indexed keywords

HOMEOBOX PROTEIN LMX 1A; HOMEODOMAIN PROTEIN; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL CYCLE; CELL INVASION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DISEASE SEVERITY; DISTANT METASTASIS; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC TRAIT; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TUMOR SUPPRESSOR GENE; UTERINE CERVIX; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU; XENOGRAFT;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; PHENOTYPE; PRECANCEROUS CONDITIONS; SIGNAL TRANSDUCTION; TRANSPLANTATION, HETEROLOGOUS; UTERINE CERVICAL NEOPLASMS;

EID: 70349120416     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2589     Document Type: Article

References (54)

1. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-19. (Pubitemid 29406813)
2. zur Hausen H. Cervical carcinoma and human papillomavirus: on the road to preventing a major human cancer. J Natl Cancer Inst 2001;93:252-253. (Pubitemid 32219803)
3. Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 2007;7:11-22. (Pubitemid 46020844)
4. Atkin NB, Baker MC. DNA ploidy of cervical intraepithelial neoplasia (CIN). Cancer Genet Cytogenet 1997;94:151-152.
5. Kersemaekers AM, Hermans J, Fleuren GJ, van de Vijver MJ. Loss of heterozygosity for defined regions on chromosomes 3, 11 and 17 in carcinomas of the uterine cervix. Br J Cancer 1998;77:192-200. (Pubitemid 28029534)
6. Mitra AB. Genetic deletion and human papillomavirus infection in cervical cancer: loss of heterozygosity sites at 3p and 5p are important genetic events. Int J Cancer 1999;82:322-324.
7. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004;4:143-153.
8. Sampath TK, Maliakal JC, Hauschka PV, Jones WK, Sasak H, Tucker RF, et al. Recombinant human osteogenic protein-1 (hOP-1) induces new bone formation in vivo with a specific activity comparable with natural bovine osteogenic protein and stimulates osteoblast proliferation and differentiation in vitro. J Biol Chem 1992;267:20352-20362.
9. Laird PW. The power and the promise of DNA methylation markers. Nat Rev Cancer 2003;3:253-266.
10. Baylin SB, Herman JG. DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 2000;16:168-174.
11. Narayan G, Arias-Pulido H, Koul S, Vargas H, Zhang FF, Villella J, et al. Frequent promoter methylation of CDH1, DAPK, RARB, and HIC1 genes in carcinoma of cervix uteri: its relationship to clinical outcome. Mol Cancer 2003;2:24. (Pubitemid 38751473)
12. Steenbergen RD, Kramer D, Braakhuis BJ, Stern PL, Verheijen RH, Meijer CJ, et al. TSLC1 gene silencing in cervical cancer cell lines and cervical neoplasia. J Natl Cancer Inst 2004;96:294-305. (Pubitemid 38256274)
13. Sova P, Feng Q, Geiss G, Wood T, Strauss R, Rudolf V, et al. Discovery of novel methylation biomarkers in cervical carcinoma by global demethylation and microarray analysis. Cancer Epidemiol Biomarkers Prev 2006;15:114-123.
14. Lai HC, Lin YW, Huang TH, Yan P, Huang RL, Wang HC, et al. Identification of novel DNA methylation markers in cervical cancer. Int J Cancer 2008;123:161-167. (Pubitemid 351705204)
15. Hobert O, Westphal H. Functions of LIM-homeobox genes. Trends Genet 2000;16:75-83.
16. Chung MT, Lai HC, Sytwu HK, Yan MD, Shih YL, Chang CC, et al. SFRP1 and SFRP2 suppress the transformation and invasion abilities of cervical cancer cells through Wnt signal pathway. Gynecol Oncol 2009;112:646-653.
17. Zi X, Guo Y, Simoneau AR, Hope C, Xie J, Holcombe RF, et al. Expression of Frzb/secreted Frizzled-related protein 3, a secreted Wnt antagonist, in human androgen-independent prostate cancer PC-3 cells suppresses tumor growth and cellular invasiveness. Cancer Res 2005;65:9762-9770. (Pubitemid 41541453)
18. Seo HS, Liu DD, Bekele BN, Kim MK, Pisters K, Lippman SM, et al. Cyclic AMP response element-binding protein overexpression: a feature associated with negative prognosis in never smokers with non-small cell lung cancer. Cancer Res 2008;68:6065-6073.
19. Arafa M, Boniver J, Delvenne P. Detection of HPV-induced cervical (pre)neoplastic lesions: a tissue microarray (TMA) study. Appl Immunohistochem Mol Morphol 2008;16:422-432.
20. Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 2003;15:740-746.
21. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol 2006;7:131-142.
22. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-454.
23. Lee MY, Chou CY, Tang MJ, Shen MR. Epithelial-mesenchymal transition in cervical cancer: correlation with tumor progression, epidermal growth factor receptor over-expression, and snail upregulation. Clin Cancer Res 2008;14:4743-4750.
24. Geiger T, Sabanay H, Kravchenko-Balasha N, Geiger B, Levitzki A. Anomalous features of EMT during keratinocyte transformation. PLoS ONE 2008;3:e1574. (Pubitemid 351836824)
25. Kartenbeck J, Haselmann U, Gassler N. Synthesis of junctional proteins in metastasizing colon cancer cells. Eur J Cell Biol 2005;84:417-430. (Pubitemid 40353079)
26. Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006;66:8319-8326. (Pubitemid 44449137)
27. Rodriguez-Sastre MA, Gonzalez-Maya L, Delgado R, Lizano M, Tsubaki G, Mohar A, et al. Abnormal distribution of E-cadherin and β-catenin in different histologic types of cancer of the uterine cervix. Gynecol Oncol 2005;97:330-336. (Pubitemid 40614872)
28. Murakami A, Nakagawa T, Fukushima C, Torii M, Sueoka K, Nawata S, et al. Relationship between decreased expression of squamous cell carcinoma antigen 2 and E-cadherin in primary cervical cancer lesions and lymph node metastasis. Oncol Rep 2008;19:99-104. (Pubitemid 351176136)
29. Vogel A, Rodriguez C, Warnken W, Izpisua Belmonte JC. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 1995;378:716-720. (Pubitemid 26001942)
30. Failli V, Bachy I, Retaux S. Expression of the LIM-homeodomain gene Lmx1a (Dreher) during development of the mouse nervous system. Mech Dev 2002;118:225-228. (Pubitemid 35292143)
31. Millonig JH, Millen KJ, Hatten ME. The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 2000;403:764-769.
32. Paz MF, Wei S, Cigudosa JC, Rodriguez-Perales S, Peinado MA, Huang TH, et al. Genetic unmasking of epigenetically silenced tumor suppressor genes in colon cancer cells deficient in DNA methyltransferases. Hum Mol Genet 2003;12:2209-2219. (Pubitemid 37107311)
33. Xu J, Lamouille S, Derynck R. TGF-β-induced epithelial to mesenchymal transition. Cell Res 2009;19:156-172.
34. Millen KJ, Millonig JH, Hatten ME. Roof plate and dorsal spinal cord dl1 interneuron development in the Dreher mutant mouse. Dev Biol 2004;270:382-392.
35. Chizhikov VV, Millen KJ. Control of roof plate formation by Lmx1a in the developing spinal cord. Development 2004;131:2693-2705. (Pubitemid 38877901)
36. Kishigami S, Mishina Y. BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev 2005;16:265-278. (Pubitemid 40910316)
37. Miyazono K, Miyazawa K. Id: a target of BMP signaling. Sci STKE 2002;2002:PE40.
38. Kang Y, Chen CR, Massague J. A self-enabling TGFβ response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell 2003;11:915-926. (Pubitemid 36566314)
39. Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-β superfamily signalling. Genes Cells 2002;7:1191-1204. (Pubitemid 36024597)
40. Massague J. TGFβ in Cancer. Cell 2008;134:215-230.
41. Rothhammer T, Poser I, Soncin F, Bataille F, Moser M, Bosserhoff AK. Bone morphogenic proteins are over-expressed in malignant melanoma and promote cell invasion and migration. Cancer Res 2005;65:448-456.
42. Deng H, Makizumi R, Ravikumar TS, Dong H, Yang W, Yang WL. Bone morphogenetic protein-4 is overexpressed in colonic adenocarcinomas and promotes migration and invasion of HCT116 cells. Exp Cell Res 2007;313:1033-1044. (Pubitemid 46273448)
43. Theriault BL, Shepherd TG, Mujoomdar ML, Nachtigal MW. BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis 2007;28:1153-1162.
44. Nishanian TG, Kim JS, Foxworth A, Waldman T. Suppression of tumorigenesis and activation of Wnt signaling by bone morphogenetic protein 4 in human cancer cells. Cancer Biol Ther 2004;3:667-675. (Pubitemid 41351107)
45. Buckley S, Shi W, Driscoll B, Ferrario A, Anderson K, Warburton D. BMP4 signaling induces senescence and modulates the oncogenic phenotype of A549 lung adenocarcinoma cells. Am J Physiol Lung Cell Mol Physiol 2004;286:L81-86. (Pubitemid 38055861)
46. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006;444:761-765. (Pubitemid 44949605)
47. Hamdy FC, Autzen P, Robinson MC, Horne CH, Neal DE, Robson CN. Immunolocalization and messenger RNA expression of bone morphogenetic protein-6 in human benign and malignant prostatic tissue. Cancer Res 1997;57:4427-4431. (Pubitemid 27413455)
48. Haudenschild DR, Palmer SM, Moseley TA, You Z, Reddi AH. Bone morphogenetic protein (BMP)-6 signaling and BMP antagonist noggin in prostate cancer. Cancer Res 2004;64:8276-8284. (Pubitemid 39491765)
49. Yang S, Du J, Wang Z, Yuan W, Qiao Y, Zhang M, et al. BMP-6 promotes E-cadherin expression through repressing ΔEF1 in breast cancer cells. BMC Cancer 2007;7:211. (Pubitemid 351188972)
50. Takiguchi T, Kobayashi M, Suzuki R, Yamaguchi A, Isatsu K, Nishihara T, et al. Recombinant human bone morphogenetic protein-2 stimulates osteoblast differentiation and suppresses matrix metalloproteinase-1 production in human bone cells isolated from mandibulae. J Periodontal Res 1998;33:476-485. (Pubitemid 128527350)
51. Otto TC, Bowers RR, Lane MD. BMP-4 treatment of C3H10T1/2 stem cells blocks expression of MMP-3 and MMP-13. Biochem Biophys Res Commun 2007;353:1097-1104.
52. Kumagai T, Shimizu T, Takeda K. Bone morphogenetic protein-2 suppresses invasiveness of TSU-Pr1 cells with the inhibition of MMP-9 secretion. Anticancer Res 2006;26:293-298. (Pubitemid 43206089)
53. Darby S, Cross SS, Brown NJ, Hamdy FC, Robson CN. BMP-6 over-expression in prostate cancer is associated with increased Id-1 protein and a more invasive phenotype. J Pathol 2008;214:394-404. (Pubitemid 351212395)
54. Su HY, Lai HC, Lin YW, Chou YC, Liu CY, Yu MH. An epigenetic marker panel for screening and prognostic prediction of ovarian cancer. Int J Cancer 2008;124:387-393.