HOXA9 promotes homotypic and heterotypic cell interactions that facilitate ovarian cancer dissemination via its induction of P-cadherin

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Ko, Song Y ^a   Naora, Honami ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cell adhesion; Homeobox gene; Metastasis; Ovarian cancer; P cadherin

Indexed keywords

P CADHERIN; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR HOXA9; CADHERIN; HOMEODOMAIN PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOIKIS; ARTICLE; CANCER SURVIVAL; CDH3 GENE; CELL ADHESION; CELL AGGREGATION; CELL DEATH; CELL INTERACTION; CELL INVASION; CELL MIGRATION; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENOME; HISTOPATHOLOGY; HOXA9 GENE; IN VITRO STUDY; METASTASIS; MICROSCOPY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; OVARY CARCINOMA; PERITONEAL CAVITY; PERITONEUM CELL; PROMOTER REGION; PROTEIN INDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL; SUSPENSION CELL CULTURE; TUMOR CELL INOCULATION; WESTERN BLOTTING; ANIMAL; CELL COMMUNICATION; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; OVARY TUMOR; PATHOLOGY; PERITONEUM TUMOR; SECONDARY;

MUS;

ANIMALS; CADHERINS; CELL COMMUNICATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICE; NEOPLASM METASTASIS; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904082239     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-170     Document Type: Article

References (51)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013, 63:11-30.
2. Naora H, Montell DJ. Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat Rev Cancer 2005, 5:355-366.
3. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol 2010, 177:1053-1064.
4. Sodek KL, Murphy KJ, Brown TJ, Ringuette MJ. Cell-cell and cell-matrix dynamics in intraperitoneal cancer metastasis. Cancer Metastasis Rev 2012, 31:397-414.
5. Burleson KM, Casey RC, Skubitz KM, Pambuccian SE, Oegema TR, Skubitz AP. Ovarian carcinoma ascites spheroids adhere to extracellular matrix components and mesothelial cell monolayers. Gynecol Oncol 2004, 93:170-181.
6. Abate-Shen C. Deregulated homeobox gene expression in cancer: cause or consequence?. Nat Rev Cancer 2002, 2:777-785.
7. Samuel S, Naora H. Homeobox gene expression in cancer: insights from developmental regulation and deregulation. Eur J Cancer 2005, 41:2428-2437.
8. Pearson JC, Lemons D, McGinnis W. Modulating Hox gene functions during animal body patterning. Nat Rev Genet 2005, 6:893-904.
9. Taylor HS, Vanden Heuvel GB, Igarashi P. A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes. Biol Reprod 1997, 57:1338-1345.
10. Ko SY, Barengo N, Ladanyi A, Lee JS, Marini F, Lengyel E, Naora H. HOXA9 promotes ovarian cancer growth by stimulating cancer-associated fibroblasts. J Clin Invest 2012, 122:3603-3617.
11. Patel IS, Madan P, Getsios S, Bertrand MA, MacCalman CD. Cadherin switching in ovarian cancer progression. Int J Cancer 2003, 106:172-177.
12. Quattrocchi L, Green AR, Martin S, Durrant L, Deen S. The cadherin switch in ovarian high-grade serous carcinoma is associated with disease progression. Virchows Arch 2011, 459:21-29.
13. Cheung LW, Leung PC, Wong AS. Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene 2010, 29:2427-2440.
14. Usui A, Ko SY, Barengo N, Naora H. P-cadherin promotes ovarian cancer dissemination through tumor cell aggregation and tumor-peritoneum tnteractions. Mol Cancer Res 2014, 12:504-513.
15. 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, 53:891-898.
16. Pasca di Magliano M, Hebrok M. Hedgehog signalling in cancer formation and maintenance. Nat Rev Cancer 2003, 3:903-911.
17. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008, 8:387-398.
18. Ranganathan P, Weaver KL, Capobianco AJ. Notch signalling in solid tumours: a little bit of everything but not all the time. Nat Rev Cancer 2011, 11:338-351.
19. Care A, Silvani A, Meccia E, Mattia G, Stoppacciaro A, Parmiani G, Peschle C, Colombo MP. HOXB7 constitutively activates basic fibroblast growth factor in melanomas. Mol Cell Biol 1996, 16:4842-4851.
20. Coletta RD, Christensen K, Reichenberger KJ, Lamb J, Micomonaco D, Huang L, Wolf DM, Muller-Tidow C, Golub TR, Kawakami K, Ford HL. The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1. Proc Natl Acad Sci U S A 2004, 101:6478-6483.
21. Trinh BQ, Barengo N, Naora H. Homeodomain protein DLX4 counteracts key transcriptional control mechanisms of the TGF-beta cytostatic program and blocks the antiproliferative effect of TGF-beta. Oncogene 2011, 30:2718-2729.
22. Micalizzi DS, Wang CA, Farabaugh SM, Schiemann WP, Ford HL. Homeoprotein Six1 increases TGF-beta type I receptor and converts TGF-beta signaling from suppressive to supportive for tumor growth. Cancer Res 2010, 70:10371-10380.
23. Yu Y, Davicioni E, Triche TJ, Merlino G. The homeoprotein six1 transcriptionally activates multiple protumorigenic genes but requires ezrin to promote metastasis. Cancer Res 2006, 66:1982-1989.
24. Daftary GS, Troy PJ, Bagot CN, Young SL, Taylor HS. Direct regulation of beta3-integrin subunit gene expression by HOXA10 in endometrial cells. Mol Endocrinol 2002, 16:571-579.
25. Zhu R, Wong KF, Lee NP, Lee KF, Luk JM. HNF1alpha and CDX2 transcriptional factors bind to cadherin-17 (CDH17) gene promoter and modulate its expression in hepatocellular carcinoma. J Cell Biochem 2010, 111:618-626.
26. Gumbiner BM. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 2005, 6:622-634.
27. Halbleib JM, Nelson WJ. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 2006, 20:3199-3214.
28. Sivertsen S, Berner A, Michael CW, Bedrossian C, Davidson B. Cadherin expression in ovarian carcinoma and malignant mesothelioma cell effusions. Acta Cytol 2006, 50:603-607.
29. Veatch AL, Carson LF, Ramakrishnan S. Differential expression of the cell-cell adhesion molecule E-cadherin in ascites and solid human ovarian tumor cells. Int J Cancer 1994, 58:393-399.
30. Davidson B, Berner A, Nesland JM, Risberg B, Berner HS, Trope CG, Kristensen GB, Bryne M, Florenes AV. E-cadherin and alpha-, beta-, and gamma-catenin protein expression is up-regulated in ovarian carcinoma cells in serous effusions. J Pathol 2000, 192:460-469.
31. Kang HG, Jenabi JM, Zhang J, Keshelava N, Shimada H, May WA, Ng T, Reynolds CP, Triche TJ, Sorensen PH. E-cadherin cell-cell adhesion in ewing tumor cells mediates suppression of anoikis through activation of the ErbB4 tyrosine kinase. Cancer Res 2007, 67:3094-3105.
32. Kumar S, Park SH, Cieply B, Schupp J, Killiam E, Zhang F, Rimm DL, Frisch SM. A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol Cell Biol 2011, 31:4036-4051.
33. Taniuchi K, Nakagawa H, Hosokawa M, Nakamura T, Eguchi H, Ohigashi H, Ishikawa O, Katagiri T, Nakamura Y. Overexpressed P-cadherin/CDH3 promotes motility of pancreatic cancer cells by interacting with p120ctn and activating rho-family GTPases. Cancer Res 2005, 65:3092-3099.
34. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
35. Shi X, Bai S, Li L, Cao X. Hoxa-9 represses transforming growth factor-beta-induced osteopontin gene transcription. J Biol Chem 2001, 276:850-855.
36. Lessan K, Aguiar DJ, Oegema T, Siebenson L, Skubitz AP. CD44 and beta1 integrin mediate ovarian carcinoma cell adhesion to peritoneal mesothelial cells. Am J Pathol 1999, 154:1525-1537.
37. Heyman L, Kellouche S, Fernandes J, Dutoit S, Poulain L, Carreiras F. Vitronectin and its receptors partly mediate adhesion of ovarian cancer cells to peritoneal mesothelium in vitro. Tumour Biol 2008, 29:231-244.
38. Ko SY, Lengyel E, Naora H. The Mullerian HOXA10 gene promotes growth of ovarian surface epithelial cells by stimulating epithelial-stromal interactions. Mol Cell Endocrinol 2010, 317:112-119.
39. Chen GT, Tai CT, Yeh LS, Yang TC, Tsai HD. Identification of the cadherin subtypes present in the human peritoneum and endometriotic lesions: potential role for P-cadherin in the development of endometriosis. Mol Reprod Dev 2002, 62:289-294.
40. Van Marck V, Stove C, Van Den Bossche K, Stove V, Paredes J, Vander Haeghen Y, Bracke M. P-cadherin promotes cell-cell adhesion and counteracts invasion in human melanoma. Cancer Res 2005, 65:8774-8783.
41. Bauer K, Dowejko A, Bosserhoff AK, Reichert TE, Bauer RJ. P-cadherin induces an epithelial-like phenotype in oral squamous cell carcinoma by GSK-3beta-mediated Snail phosphorylation. Carcinogenesis 2009, 30:1781-1788.
42. Mandeville JA, Silva Neto B, Vanni AJ, Smith GL, Rieger-Christ KM, Zeheb R, Loda M, Libertino JA, Summerhayes IC. P-cadherin as a prognostic indicator and a modulator of migratory behaviour in bladder carcinoma cells. BJU Int 2008, 102:1707-1714.
43. Rowlands TM, Symonds JM, Farookhi R, Blaschuk OW. Cadherins: crucial regulators of structure and function in reproductive tissues. Rev Reprod 2000, 5:53-61.
44. Lawrence HJ, Helgason CD, Sauvageau G, Fong S, Izon DJ, Humphries RK, Largman C. Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood 1997, 89:1922-1930.
45. Radice GL, Ferreira-Cornwell MC, Robinson SD, Rayburn H, Chodosh LA, Takeichi M, Hynes RO. Precocious mammary gland development in P-cadherin-deficient mice. J Cell Biol 1997, 139:1025-1032.
46. Wu Q, Lothe RA, Ahlquist T, Silins I, Trope CG, Micci F, Nesland JM, Suo Z, Lind GE. DNA methylation profiling of ovarian carcinomas and their in vitro models identifies HOXA9, HOXB5, SCGB3A1, and CRABP1 as novel targets. Mol Cancer 2007, 6:45.
47. Soshnikova N, Duboule D. Epigenetic regulation of vertebrate Hox genes: a dynamic equilibrium. Epigenetics 2009, 4:537-540.
48. Cha TL, Zhou BP, Xia W, Wu Y, Yang CC, Chen CT, Ping B, Otte AP, Hung MC. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 2005, 310:306-310.
49. Yuan ZQ, Sun M, Feldman RI, Wang G, Ma X, Jiang C, Coppola D, Nicosia SV, Cheng JQ. Frequent activation of AKT2 and induction of apoptosis by inhibition of phosphoinositide-3-OH kinase/Akt pathway in human ovarian cancer. Oncogene 2000, 19:2324-2330.
50. Zhang CC, Yan Z, Zhang Q, Kuszpit K, Zasadny K, Qiu M, Painter CL, Wong A, Kraynov E, Arango ME, Mehta PP, Popoff I, Casperson GF, Los G, Bender S, Anderes K, Christensen JG, VanArsdale T. PF-03732010: a fully human monoclonal antibody against P-cadherin with antitumor and antimetastatic activity. Clin Cancer Res 2010, 16:5177-5188.
51. Kenny HA, Krausz T, Yamada SD, Lengyel E. Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra-cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum. Int J Cancer 2007, 121:1463-1472.