PRH/HHex inhibits the migration of breast and prostate epithelial cells through direct transcriptional regulation of Endoglin

Oncogene

Volumn 33, Issue 49, 2014, Pages 5592-5600

  Kershaw, R M ^a   Siddiqui, Y H ^b   Roberts, D ^a   Jayaraman, P S ^a   Gaston, K ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

breast cancer; cell migration; HHex; invasion; PRH; prostate cancer

Indexed keywords

CELL SURFACE RECEPTOR; CHROMATIN; ENG PROTEIN, HUMAN; HHEX PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; LEUKOCYTE ANTIGEN; TRANSCRIPTION FACTOR;

BREAST TUMOR; CELL LINEAGE; CELL MOTION; CHEMISTRY; CHROMATIN; CYTOLOGY; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENE VECTOR; GENETIC TRANSCRIPTION; HUMAN; MALE; METABOLISM; PHYSIOLOGY; PROMOTER REGION; PROSTATE TUMOR; TUMOR CELL LINE; TUMOR INVASION;

ANTIGENS, CD; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL LINEAGE; CELL MOVEMENT; CHROMATIN; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC VECTORS; HOMEODOMAIN PROTEINS; HUMANS; MALE; NEOPLASM INVASIVENESS; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; RECEPTORS, CELL SURFACE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84887547270     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.496     Document Type: Article

References (42)

1. Soufi A, Jayaraman PS. PRH/Hex: An oligomeric transcription factor and multifunctional regulator of cell fate. Biochem J 2008; 412: 399-413.
2. Topisirovic I, Culjkovic B, Cohen N, Perez JM, Skrabanek L, Borden KL. The prolinerich homeodomain protein, PRH, is a tissue-specific inhibitor of eIF4E-dependent cyclin D1 mRNA transport and growth. EMBO J 2003; 22: 689-703.
3. Swingler TE, Bess KL, Yao J, Stifani S, Jayaraman PS. The proline-rich homeodomain protein recruits members of the Groucho/Transducin-like enhancer of split protein family to co-repress transcription in hematopoietic cells. J Biol Chem 2004; 279: 34938-34947.
4. Guiral M, Bess K, Goodwin G, Jayaraman PS. PRH represses transcription in hematopoietic cells by at least two independent mechanisms. J Biol Chem 2001; 276: 2961-2970.
5. Denson LA, Karpen SJ, Bogue CW, Jacobs HC. Divergent homeobox gene hex regulates promoter of the Na-dependent bile acid cotransporter. Am J Physiol Gastrointest Liver Physiol 2000; 279: G347-G355.
6. George A, Morse 3rd HC, Justice MJ. The homeobox gene Hex induces T-cellderived lymphomas when overexpressed in hematopoietic precursor cells. Oncogene 2003; 22: 6764-6773.
7. McCormack MP, Young LF, Vasudevan S, De Graaf CA, Codrington R, Rabbitts TH et al. The Lmo2 oncogene initiates leukemia in mice by inducing thymocyte selfrenewal. Science 2010; 327: 879-883.
8. Oram SH, Thoms JA, Pridans C, Janes ME, Kinston SJ, Anand S et al. A previously unrecognized promoter of LMO2 forms part of a transcriptional regulatory circuit mediating LMO2 expression in a subset of T-acute lymphoblastic leukaemia patients. Oncogene 2010; 29: 5796-5808.
9. Puppin C, Puglisi F, Pellizzari L, Manfioletti G, Pestrin M, Pandolfi M et al. HEX expression and localization in normal mammary gland and breast carcinoma. BMC Cancer 2006; 6: 192.
10. D'Elia AV, Tell G, Russo D, Arturi F, Puglisi F, Manfioletti G et al. Expression and localization of the homeodomain-containing protein HEX in human thyroid tumors. J Clin Endocrinol Metab 2002; 87: 1376-1383.
11. Jankovic D, Gorello P, Liu T, Ehret S, La SR, Desjobert C et al. Leukemogenic mechanisms and targets of a NUP98/HHEX fusion in acute myeloid leukemia. Blood 2008; 111: 5672-5682.
12. Topisirovic I, Guzman ML, McConnell MJ, Licht JD, Culjkovic B, Neering SJ et al. Aberrant eukaryotic translation initiation factor 4E-dependent mRNA transport impedes hematopoietic differentiation and contributes to leukemogenesis. Mol Cell Biol 2003; 23: 8992-9002.
13. Noy P, Gaston K, Jayaraman PS. Dasatinib inhibits leukaemic cell survival by decreasing PRH/Hhex phosphorylation resulting in increased repression of VEGF signalling genes. Leuk Res 2012; 36: 1434-1437.
14. Guerrero-Esteo M, Lastres P, Letamendia A, Perez-Alvarez MJ, Langa C, Lopez La et al. Endoglin overexpression modulates cellular morphology, migration, and adhesion of mouse fibroblasts. Eur J Cell Biol 1999; 78: 614-623.
15. Quintanilla M, Ramirez JR, Perez-Gomez E, Romero D, Velasco B, Letarte M et al. Expression of the TGF-beta coreceptor endoglin in epidermal keratinocytes and its dual role in multistage mouse skin carcinogenesis. Oncogene 2003; 22: 5976-5985.
16. Bernabeu C, Conley BA, Vary CP. Novel biochemical pathways of endoglin in vascular cell physiology. J Cell Biochem 2007; 102: 1375-1388.
17. Liu Y, Jovanovic B, Pins M, Lee C, Bergan RC. Over expression of endoglin in human prostate cancer suppresses cell detachment, migration and invasion. Oncogene 2002; 21: 8272-8281.
18. Lakshman M, Huang X, Ananthanarayanan V, Jovanovic B, Liu Y, Craft CS et al. Endoglin suppresses human prostate cancer metastasis. Clin Exp Metastasis 2011; 28: 39-53.
19. Craft CS, Romero D, Vary CP, Bergan RC. Endoglin inhibits prostate cancer motility via activation of the ALK2-Smad1 pathway. Oncogene 2007; 26: 7240-7250.
20. Romero D, Terzic A, Conley BA, Craft CS, Jovanovic B, Bergan RC et al. Endoglin phosphorylation by ALK2 contributes to the regulation of prostate cancer cell migration. Carcinogenesis 2010; 31: 359-366.
21. Wong VC, Chan PL, Bernabeu C, Law S, Wang LD, Li JL et al. Identification of an invasion and tumor-suppressing gene, Endoglin (ENG), silenced by both epigenetic inactivation and allelic loss in esophageal squamous cell carcinoma. Int J Cancer 2008; 123: 2816-2823.
22. Perez-Gomez E, Villa-Morales M, Santos J, Fernandez-Piqueras J, Gamallo C, Dotor J et al. A role for endoglin as a suppressor of malignancy during mouse skin carcinogenesis. Cancer Res 2007; 67: 10268-10277.
23. Henry LA, Johnson DA, Sarrio D, Lee S, Quinlan PR, Crook T et al. Endoglin expression in breast tumor cells suppresses invasion and metastasis and correlates with improved clinical outcome. Oncogene 2011; 30: 1046-1058.
24. Nakagawa T, Abe M, Yamazaki T, Miyashita H, Niwa H, Kokubun S et al. HEX acts as a negative regulator of angiogenesis by modulating the expression of angiogenesis-related gene in endothelial cells in vitro. Arterioscler Thromb Vasc Biol 2003; 23: 231-237.
25. Berthon P, Cussenot O, Hopwood L, Leduc A, Maitland N. Functional expression of sv40 in normal human prostatic epithelial and fibroblastic cells-differentiation pattern of nontumorigenic cell-lines. Int J Oncol 1995; 6: 333-343.
26. Lang SH, Sharrard RM, Stark M, Villette JM, Maitland NJ. Prostate epithelial cell lines form spheroids with evidence of glandular differentiation in three-dimensional Matrigel cultures. Br J Cancer 2001; 85: 590-599.
27. Desjobert C, Noy P, Swingler T, Williams H, Gaston K, Jayaraman PS. The PRH/Hex repressor protein causes nuclear retention of Groucho/TLE co-repressors. Biochem J 2009; 417: 121-132.
28. Soufi A, Smith C, Clarke AR, Gaston K, Jayaraman PS. Oligomerisation of the developmental regulator proline rich homeodomain (PRH/Hex) is mediated by a novel proline-rich dimerisation domain. J Mol Biol 2006; 358: 943-962.
29. Pimanda JE, Chan WY, Donaldson IJ, Bowen M, Green AR, Gottgens B. Endoglin expression in the endothelium is regulated by Fli-1, Erg, and Elf-1 acting on the promoter and a-8-kb enhancer. Blood 2006; 107: 4737-4745.
30. Pimanda JE, Chan WY, Wilson NK, Smith AM, Kinston S, Knezevic K et al. Endoglin expression in blood and endothelium is differentially regulated by modular assembly of the Ets/Gata hemangioblast code. Blood 2008; 112: 4512-4522.
31. Noy P, Williams H, Sawasdichai A, Gaston K, Jayaraman PS. PRH/HHex controls cell survival through coordinate transcriptional regulation of VEGF signalling. Mol Cell Biol 2010; 30: 2120-2134.
32. Guo Y, Chan R, Ramsey H, Li W, Xie X, Shelley WC et al. The homeoprotein Hex is required for hemangioblast differentiation. Blood 2003; 102: 2428-2435.
33. Botella LM, Sanchez-Elsner T, Rius C, Corbi A, Bernabeu C. Identification of a critical Sp1 site within the endoglin promoter and its involvement in the transforming growth factor-beta stimulation. J Biol Chem 2001; 276: 34486-34494.
34. Sanchez-Elsner T, Botella LM, Velasco B, Langa C, Bernabeu C. Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J Biol Chem 2002; 277: 43799-43808.
35. Botella LM, Sanchez-Elsner T, Sanz-Rodriguez F, Kojima S, Shimada J, Guerrero-Esteo M et al. Transcriptional activation of endoglin and transforming growth factor-beta signaling components by cooperative interaction between Sp1 and KLF6: Their potential role in the response to vascular injury. Blood 2002; 100: 4001-4010.
36. Williams H, Jayaraman PS, Gaston K. DNA wrapping and distortion by an oligomeric homeodomain protein. J Mol Biol 2008; 383: 10-23.
37. Noy P, Sawasdichai A, Jayaraman PS, Gaston K. Protein kinase CK2 inactivates PRH/Hhex using multiple mechanisms to de-repress VEGF-signalling genes and promote cell survival. Nucleic Acids Res 2012; 40: 9008-9020.
38. Kassouf W, Ismail HR, Aprikian AG, Chevalier S. Whole-mount prostate sections reveal differential endoglin expression in stromal, epithelial, and endothelial cells with the development of prostate cancer. Prostate Cancer Prostatic Dis 2004; 7: 105-110.
39. Oxmann D, Held-Feindt J, Stark AM, Hattermann K, Yoneda T, Mentlein R. Endoglin expression in metastatic breast cancer cells enhances their invasive phenotype. Oncogene 2008; 27: 3567-3575.
40. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9: 671-675.
41. Ma C, Wang XF. In vitro assays for the extracellular matrix protein-regulated extravasation process. CSH Protocols 2008; pdb prot5034.
42. Soufi A, Noy P, Buckle M, Sawasdichai A, Gaston K, Jayaraman PS. CK2 phosphorylation of the PRH/Hex homeodomain functions as a reversible switch for DNA binding. Nucleic Acids Res 2009; 37: 3288-3300.