Prox1 and FOXC2 act as regulators of lymphangiogenesis and angiogenesis in oral squamous cell carcinoma

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Sasahira, Tomonori ^a   Ueda, Nobuhiro ^a   Yamamoto, Kazuhiko ^a   Kurihara, Miyako ^a   Matsushima, Sayako ^a   Bhawal, Ujjal K ^a,b   Kirita, Tadaaki ^a   Kuniyasu, Hiroki ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

^b NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR FOXC2; VASCULOTROPIN A; VASCULOTROPIN C;

ADULT; AGED; ANGIOGENESIS; ARTICLE; BLOOD VESSEL PARAMETERS; CANCER GROWTH; CAPILLARY DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FOXC2 GENE; GENE EXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; IN VITRO STUDY; LYMPHANGIOGENESIS; LYMPHOVESSEL DENSITY; MAJOR CLINICAL STUDY; MALE; METASTASIS; MOUTH SQUAMOUS CELL CARCINOMA; PATHOGENESIS; PROX1 GENE; TUMOR INVASION; TUMOR SUPPRESSOR GENE;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HOMEODOMAIN PROTEINS; HUMANS; LYMPHANGIOGENESIS; MALE; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84898604477     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092534     Document Type: Article

References (48)

1. Argiris A, Karamouzis MV, Raben D, Ferris RL (2008) Head and neck cancer. Lancet 371: 1695-1709. (Pubitemid 351671886)
2. Sasahira T, Kirita T, Oue N, Bhawal UK, Yamamoto K, et al. (2008) High mobility group box-1-inducible melanoma inhibitory activity is associated with nodal metastasis and lymphangiogenesis in oral squamous cell carcinoma. Cancer Sci 99: 1806-1812.
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, et al. (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90.
4. Siegel R, Ward E, Brawley O, Jemal A (2011) Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 61: 212-236.
5. Sasahira T, Kirita T, Bhawal UK, Yamamoto K, Ohmori H, et al. (2007) Receptor for advanced glycation end products (RAGE) is important in the prediction of recurrence in human oral squamous cell carcinoma. Histopathology 51: 166-172. (Pubitemid 47083983)
6. Dos Reis PP, Bharadwaj RR, Machado J, Macmillan C, Pintilie M, et al. (2008) Claudin 1 overexpression increases invasion and is associated with aggressive histological features in oral squamous cell carcinoma. Cancer 113: 3169-3180.
7. Mydlarz WK, Hennessey PT, Califano JA (2010) Advances and Perspectives in the Molecular Diagnosis of Head and Neck Cancer. Expert Opin Med Diagn 4: 53-65.
8. Marsh D, Suchak K, Moutasim KA, Vallath S, Hopper C, et al. (2011) Stromal features are predictive of disease mortality in oral cancer patients. J Pathol 223: 470-481.
9. Betschinger J, Mechtler K, Knoblich JA (2006) Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 124: 1241-1253.
10. Elsir T, Qu M, Berntsson SG, Orrego A, Olofsson T, et al. (2011) PROX1 is a predictor of survival for gliomas WHO grade II. Br J Cancer 104: 1747-1754.
11. Skog M, Bono P, Lundin M, Lundin J, Louhimo J, et al. (2011) Expression and prognostic value of transcription factor PROX1 in colorectal cancer. Br J Cancer 105: 1346-1351.
12. Nagai H, Li Y, Hatano S, Toshihito O, Yuge M, et al. (2003) Mutations and aberrant DNA methylation of the PROX1 gene in hematologic malignancies. Genes, Chromosomes and Cancer 38: 13-21. (Pubitemid 36994880)
13. Yoshimoto T, Takahashi M, Nagayama S, Watanabe G, Shimada Y, et al. (2007) RNA mutations of prox1 detected in human esophageal cancer cells by the shifted termination assay. Biochem Biophys Res Commun 359: 258-262. (Pubitemid 46880500)
14. Shimoda M, Takahashi M, Yoshimoto T, Kono T, Ikai I, et al. (2006) A homeobox protein, prox1, is involved in the differentiation, proliferation, and prognosis in hepatocellular carcinoma. Clin Cancer Res 12: 6005-6011. (Pubitemid 44703761)
15. Schneider M, Buchler P, Giese N, Giese T, Wilting J, et al. (2006) Role of lymphangiogenesis and lymphangiogenic factors during pancreatic cancer progression and lymphatic spread. Int J Oncol 28: 883-890.
16. Takahashi M, Yoshimoto T, Shimoda M, Kono T, Koizumi M, et al. (2006) Loss of function of the candidate tumor suppressor prox1 by RNA mutation in human cancer cells. Neoplasia 8: 1003-1010. (Pubitemid 44936149)
17. Versmold B, Felsberg J, Mikeska T, Ehrentraut D, Kohler J, et al. (2007) Epigenetic silencing of the candidate tumor suppressor gene PROX1 in sporadic breast cancer. Int J Cancer 121: 547-554. (Pubitemid 46986487)
18. Laerm A, Helmbold P, Goldberg M, Dammann R, Holzhausen HJ, et al. (2007) Prospero-related homeobox 1 (PROX1) is frequently inactivated by genomic deletions and epigenetic silencing in carcinomas of the bilary system. J Hepatol 46: 89-97. (Pubitemid 44834428)
19. Petrova TV, Nykanen A, Norrmen C, Ivanov KI, Andersson LC, et al. (2008) Transcription factor PROX1 induces colon cancer progression by promoting the transition from benign to highly dysplastic phenotype. Cancer Cell 13: 407-419. (Pubitemid 351609440)
20. Dadras SS, Skrzypek A, Nguyen L, Shin JW, Schulz MM, et al. (2008) Prox-1 promotes invasion of kaposiform hemangioendotheliomas. J Invest Dermatol 128: 2798-2806.
21. Miettinen M, Wang ZF (2012) Prox1 transcription factor as a marker for vascular tumors-evaluation of 314 vascular endothelial and 1086 nonvascular tumors. Am J Surg Pathol 36: 351-359.
22. Elsir T, Smits A, Lindstrom MS, Nister M (2012) Transcription factor PROX1: its role in development and cancer. Cancer Metastasis Rev 31: 793-805.
23. Kume T (2010) Specification of arterial, venous, and lymphatic endothelial cells during embryonic development. Histol Histopathol 25: 637-646.
24. Kume T (2012) The Role of FoxC2 Transcription Factor in Tumor Angiogenesis. J Oncol 2012: 204593.
25. Mani SA, Yang J, Brooks M, Schwaninger G, Zhou A, et al. (2007) Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc Natl Acad Sci U S A 104: 10069-10074. (Pubitemid 47175264)
26. Sano H, Leboeuf JP, Novitskiy SV, Seo S, Zaja-Milatovic S, et al. (2010) The Foxc2 transcription factor regulates tumor angiogenesis. Biochem Biophys Res Commun 392: 201-206.
27. Nishida N, Mimori K, Yokobori T, Sudo T, Tanaka F, et al. (2011) FOXC2 is a novel prognostic factor in human esophageal squamous cell carcinoma. Ann Surg Oncol 18: 535-542.
28. Hader C, Marlier A, Cantley L (2010) Mesenchymal-epithelial transition in epithelial response to injury: the role of Foxc2. Oncogene 29: 1031-1040.
29. Sasahira T, Kirita T, Kurihara M, Yamamoto K, Bhawal UK, et al. (2010) MIA-dependent angiogenesis and lymphangiogenesis are closely associated with progression, nodal metastasis and poor prognosis in tongue squamous cell carcinoma. Eur J Cancer 46: 2285-2294.
30. Kopfstein L, Veikkola T, Djonov VG, Baeriswyl V, Schomber T, et al. (2007) Distinct roles of vascular endothelial growth factor-D in lymphangiogenesis and metastasis. Am J Pathol 170: 1348-1361. (Pubitemid 47339341)
31. Lohela M, Bry M, Tammela T, Alitalo K (2009) VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 21: 154-165.
32. Flister MJ, Wilber A, Hall KL, Iwata C, Miyazono K, et al. (2010) Inflammation induces lymphangiogenesis through up-regulation of VEGFR-3 mediated by NF-kappaB and Prox1. Blood 115: 418-429.
33. Srinivasan RS, Geng X, Yang Y, Wang Y, Mukatira S, et al. (2010) The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev 24: 696-707.
34. Wu X, Liu NF (2011) FOXC2 transcription factor: a novel regulator of lymphangiogenesis. Lymphology 44: 35-41.
35. Sabine A, Agalarov Y, Maby-El Hajjami H, Jaquet M, Hagerling R, et al. (2012) Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Developmental Cell 22: 430-445.
36. Allred DC, Harvey JM, Berardo M, Clark GM (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 11: 155-168. (Pubitemid 28144151)
37. Matsuo Y, Sawai H, Ma J, Xu D, Ochi N, et al. (2009) IL-1alpha secreted by colon cancer cells enhances angiogenesis: the relationship between IL-1alpha release and tumor cells' potential for liver metastasis. J Surg Oncol 99: 361-367.
38. Lahat G, Lazar A, Wang X, Wang WL, Zhu QS, et al. (2009) Increased vascular endothelial growth factor-C expression is insufficient to induce lymphatic metastasis in human soft-tissue sarcomas. Clin Cancer Res 15: 2637-2646.
39. Harada K, Yamazaki T, Iwata C, Yoshimatsu Y, Sase H, et al. (2009) Identification of targets of Prox1 during in vitro vascular differentiation from embryonic stem cells: functional roles of HoxD8 in lymphangiogenesis. J Cell Sci 122: 3923-3930.
40. Li C, Fan J, Song X, Zhang B, Chen Y, et al. (2013) Expression of angiopoietin-2 and vascular endothelial growth factor receptor-3 correlates with lymphangiogenesis and angiogenesis and affects survival of oral squamous cell carcinoma. PLoS ONE 8: e75388.
41. Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8: 464-478. (Pubitemid 46823443)
42. Petrova TV, Makinen T, Makela TP, Saarela J, Virtanen I, et al. (2002) Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J 21: 4593-4599. (Pubitemid 34984346)
43. Currie MJ, Hanrahan V, Gunningham SP, Morrin HR, Frampton C, et al. (2004) Expression of vascular endothelial growth factor D is associated with hypoxia inducible factor (HIF-1alpha) and the HIF-1alpha target gene DEC1, but not lymph node metastasis in primary human breast carcinomas. J Clinical Pathol 57: 829-834. (Pubitemid 39061431)
44. Nomiya T, Nemoto K, Nakata E, Takai Y, Yamada S (2006) Expression of thymidine phosphorylase and VEGF in esophageal squamous cell carcinoma. Oncol Rep 15: 1497-1501.
45. Miyahara M, Tanuma J, Sugihara K, Semba I (2007) Tumor lymphangiogenesis correlates with lymph node metastasis and clinicopathologic parameters in oral squamous cell carcinoma. Cancer 110: 1287-1294. (Pubitemid 47435600)
46. Donnem T, Al-Saad S, Al-Shibli K, Delghandi MP, Persson M, et al. (2007) Inverse prognostic impact of angiogenic marker expression in tumor cells versus stromal cells in non small cell lung cancer. Clin Cancer Res 13: 6649-6657. (Pubitemid 350206800)
47. Birner P, Obermair A, Schindl M, Kowalski H, Breitenecker G, et al. (2001) Selective immunohistochemical staining of blood and lymphatic vessels reveals independent prognostic influence of blood and lymphatic vessel invasion in early-stage cervical cancer. Clin Cancer Res 7: 93-97. (Pubitemid 32110210)
48. Franchi A, Gallo O, Massi D, Baroni G, Santucci M (2004) Tumor lymphangiogenesis in head and neck squamous cell carcinoma: a morphometric study with clinical correlations. Cancer 101: 973-978. (Pubitemid 39100431)