Hypoxia-inducible factor 1-dependent expression of platelet-derived growth factor B promotes lymphatic metastasis of hypoxic breast cancer cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 40, 2012, Pages

  Schito, Luana ^a,b   Rey, Sergio ^a   Tafani, Marco ^b   Zhang, Huafeng ^a   Wong, Carmen Chak Lui ^a   Russo, Andrea ^c   Russo, Matteo A ^b,d   Semenza, Gregg L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

Lymph node; Orthotopic transplantation; Triple negative breast cancer

Indexed keywords

DIGOXIN; HYPOXIA INDUCIBLE FACTOR 1; IMATINIB; PLATELET DERIVED GROWTH FACTOR B;

ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER CELL; CANCER INHIBITION; CELL HYPOXIA; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSACTIVATION; TUMOR VOLUME;

BREAST NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DIGOXIN; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LUCIFERASES; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-SIS; PYRIMIDINES; RNA, SMALL INTERFERING; TRANSCRIPTIONAL ACTIVATION;

MUS;

EID: 84867087464     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214019109     Document Type: Article

References (39)

1. Ran S, Volk L, Hall K, Flister MJ (2010) Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology 17:229-251.
2. Mohammed RA, Ellis IO, Elsheikh S, Paish EC, Martin SG (2009) Lymphatic and angiogenic characteristics in breast cancer: Morphometric analysis and prognostic implications. Breast Cancer Res Treat 113:261-273.
3. Achen MG, McColl BK, Stacker SA (2005) Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7:121-127. (Pubitemid 40248338)
4. Tammela T, Alitalo K (2010) Lymphangiogenesis: Molecular mechanisms and future promise. Cell 140:460-476.
5. Cao Y (2005) Opinion: Emerging mechanisms of tumour lymphangiogenesis and lymphatic metastasis. Nat Rev Cancer 5:735-743.
6. Vaupel P, Mayer A, Höckel M (2004) Tumor hypoxia and malignant progression. Methods Enzymol 381:335-354. (Pubitemid 38401518)
7. Semenza GL (2012) Hypoxia-inducible factors: Mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci 33:207-214.
8. Liao D, Corle C, Seagroves TN, Johnson RS (2007) Hypoxia-inducible factor-1α is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res 67:563-572. (Pubitemid 46192193)
9. Wong CC, et al. (2011) Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci USA 108:16369-16374.
10. Zhang H, et al. (2012) HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs. Oncogene 31: 1757-1770.
11. Wong CC, et al. (2012) Inhibitors of hypoxia-inducible factor 1 block breast cancer metastatic niche formation and lung metastasis. J Mol Med (Berl) 90:803-815.
12. Schoppmann SF, et al. (2006) Hypoxia inducible factor-1α correlates with VEGF-C expression and lymphangiogenesis in breast cancer. Breast Cancer Res Treat 99: 135-141. (Pubitemid 44268261)
13. Bos R, et al. (2003) Levels of hypoxia-inducible factor-1α independently predict prognosis in patients with lymph node negative breast carcinoma. Cancer 97: 1573-1581. (Pubitemid 36297788)
14. Kurokawa T, et al. (2003) Overexpression of hypoxia-inducible-factor 1α(HIF-1α) in oesophageal squamous cell carcinoma correlates with lymph node metastasis and pathologic stage. Br J Cancer 89:1042-1047. (Pubitemid 37239209)
15. Franco M, et al. (2006) Targeted anti-vascular endothelial growth factor receptor-2 therapy leads to short-term and long-term impairment of vascular function and increase in tumor hypoxia. Cancer Res 66:3639-3648.
16. Dowlatshahi K, Fan M, Snider HC, Habib FA (1997) Lymph node micrometastases from breast carcinoma: Reviewing the dilemma. Cancer 80:1188-1197. (Pubitemid 27407219)
17. Liang X, et al. (2008) Hypoxia inducible factor-α expression correlates with vascular endothelial growth factor-C expression and lymphangiogenesis/angiogenesis in oral squamous cell carcinoma. Anticancer Res 28(3A):1659-1666. (Pubitemid 351892941)
18. Mikhaylova M, et al. (2008) Hypoxia increases breast cancer cell-induced lymphatic endothelial cell migration. Neoplasia 10:380-389.
19. Koyama Y, et al. (2003) Vascular endothelial growth factor-C and vascular endothelial growth factor-D messenger RNA expression in breast cancer: Association with lymph node metastasis. Clin Breast Cancer 4:354-360. (Pubitemid 38139591)
20. Bos R, et al. (2005) Hypoxia-inducible factor-1α is associated with angiogenesis, and expression of bFGF, PDGF-BB, and EGFR in invasive breast cancer. Histopathology 46: 31-36. (Pubitemid 40193695)
21. Kodama M, et al. (2010) Expression of platelet-derived growth factor (PDGF)-B and PDGF-receptor β is associated with lymphatic metastasis in human gastric carcinoma. Cancer Sci 101:1984-1989.
22. Cao R, et al. (2004) PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 6:333-345. (Pubitemid 39361435)
23. Jaakkola P, et al. (2001) Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468-472. (Pubitemid 32335942)
24. Kelly BD, et al. (2003) Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res 93:1074-1081. (Pubitemid 37485038)
25. Ullerås E, Wilcock A, Miller SJ, Franklin GC (2001) The sequential activation and repression of the human PDGF-B gene during chronic hypoxia reveals antagonistic roles for the depletion of oxygen and glucose. Growth Factors 19:233-245. (Pubitemid 34071670)
26. Zhang SX, et al. (2003) Hypoxia induces an autocrine-paracrine survival pathway via platelet-derived growth factor (PDGF)-B/PDGF-β receptor/phosphatidylinositol 3-kinase/Akt signaling in RN46A neuronal cells. FASEB J 17:1709-1711.
27. Buchdunger E, O'Reilly T, Wood J (2002) Pharmacology of imatinib (STI571). Eur J Cancer 38(Suppl 5):S28-S36.
28. Buchdunger E, et al. (1996) Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res 56:100-104.
29. Bloom HJ, RichardsonWW(1957) Histological grading and prognosis in breast cancer; a study of 1409 cases of which 359 have been followed for 15 years. Br J Cancer 11: 359-377.
30. Amat S, et al. (2002) Scarff-Bloom-Richardson (SBR) grading: A pleiotropic marker of chemosensitivity in invasive ductal breast carcinomas treated by neoadjuvant chemotherapy. Int J Oncol 20:791-796.
31. Ohta Y, et al. (1999) VEGF and VEGF type C play an important role in angiogenesis and lymphangiogenesis in human malignant mesothelioma tumours. Br J Cancer 81: 54-61. (Pubitemid 29415491)
32. Gleadle JM, Ebert BL, Firth JD, Ratcliffe PJ (1995) Regulation of angiogenic growth factor expression by hypoxia, transition metals, and chelating agents. Am J Physiol 268:C1362-C1368.
33. Yoshida D, Kim K, Noha M, Teramoto A (2006) Hypoxia inducible factor 1-α regulates of platelet derived growth factor-B in human glioblastoma cells. J Neurooncol 76:13-21. (Pubitemid 43115754)
34. Björndahl MA, et al. (2005) Vascular endothelial growth factor-A promotes peritumoral lymphangiogenesis and lymphatic metastasis. Cancer Res 65:9261-9268. (Pubitemid 41507992)
35. Hirakawa S, et al. (2005) VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 201:1089-1099. (Pubitemid 40524677)
36. Nagy JA, et al. (2002) Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J Exp Med 196:1497-1506. (Pubitemid 35424943)
37. Pal SK, Childs BH, Pegram M (2011) Triple negative breast cancer: Unmet medical needs. Breast Cancer Res Treat 125:627-636.
38. Cooke VG, et al. (2012) Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell 21:333-345.
39. Elston CW, Ellis IO (1991) Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: Experience from a large study with longterm follow-up. Histopathology 19:403-410.