Hypoxia and HIF pathway in cancer and the placenta

Placenta

Volumn 56, Issue , 2017, Pages 8-13

  Macklin, Philip S ^a   McAuliffe, James ^a   Pugh, Christopher W ^a   Yamamoto, Atsushi ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cancer; Hypoxia inducible factor; Oxygen; Placenta; Trophoblast

Indexed keywords

CELL ADHESION MOLECULE; HYPOXIA INDUCIBLE FACTOR; MATRIX METALLOPROTEINASE; HYPOXIA INDUCIBLE FACTOR 1; OXYGEN;

ANGIOGENESIS; ANTIGEN PRESENTATION; ARTICLE; BLOOD VESSEL; CELL DEATH; CELL PROLIFERATION; HUMAN; HYPOXIA; IMMUNE SYSTEM; MALIGNANT NEOPLASM; MICROENVIRONMENT; NONHUMAN; OXYGEN SENSING; PLACENTA; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR INVASION; VASCULARIZATION; ANIMAL; FEMALE; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; PLACENTA DEVELOPMENT; PREGNANCY; SIGNAL TRANSDUCTION;

ANIMALS; FEMALE; HUMANS; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR 1; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OXYGEN; PLACENTA; PLACENTATION; PREGNANCY; SIGNAL TRANSDUCTION;

EID: 85015619923     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2017.03.010     Document Type: Article

References (60)

1. Eltzschig, H.K., Carmeliet, P., Hypoxia and inflammation. N. Engl. J. Med. 364:7 (2011), 656–665.
2. Semenza, G.L., Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 365:6 (2011), 537–547.
3. Tal, R., The role of hypoxia and hypoxia-inducible factor-1alpha in preeclampsia pathogenesis. Biol. Reprod., 87(6), 2012, 134.
4. Thompson, C.B., Into thin air: how we sense and respond to hypoxia. Cell 167:1 (2016), 9–11.
5. Wang, G.L., et al. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. U. S. A. 92:12 (1995), 5510–5514.
6. Tian, H., McKnight, S.L., Russell, D.W., Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 11:1 (1997), 72–82.
7. Ema, M., et al. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. U. S. A. 94:9 (1997), 4273–4278.
8. Makino, Y., et al. Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus. J. Biol. Chem. 277:36 (2002), 32405–32408.
9. Maxwell, P.H., et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:6733 (1999), 271–275.
10. Ivan, M., et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:5516 (2001), 464–468.
11. Jaakkola, P., et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:5516 (2001), 468–472.
12. Epstein, A.C., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107:1 (2001), 43–54.
13. Lando, D., et al. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295:5556 (2002), 858–861.
14. Hewitson, K.S., et al. Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family. J. Biol. Chem. 277:29 (2002), 26351–26355.
15. Loenarz, C., Schofield, C.J., Physiological and biochemical aspects of hydroxylations and demethylations catalyzed by human 2-oxoglutarate oxygenases. Trends Biochem. Sci. 36:1 (2011), 7–18.
16. Brugarolas, J.B., et al. TSC2 regulates VEGF through mTOR-dependent and -independent pathways. Cancer Cell 4:2 (2003), 147–158.
17. Hewitson, K.S., et al. Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarboxylic acid cycle intermediates. J. Biol. Chem. 282:5 (2007), 3293–3301.
18. Koivunen, P., et al. Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J. Biol. Chem. 282:7 (2007), 4524–4532.
19. Pugh, C.W., Modulation of the hypoxic response. Adv. Exp. Med. Biol. 903 (2016), 259–271.
20. Schofield, C.J., Ratcliffe, P.J., Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5:5 (2004), 343–354.
21. Fryer, B.H., Simon, M.C., Hypoxia, HIF and the placenta. Cell Cycle 5:5 (2006), 495–498.
22. Kozak, K.R., Abbott, B., Hankinson, O., ARNT-deficient mice and placental differentiation. Dev. Biol. 191:2 (1997), 297–305.
23. Cowden Dahl, K.D., et al. Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol. Cell Biol. 25:23 (2005), 10479–10491.
24. Gnarra, J.R., et al. Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 94:17 (1997), 9102–9107.
25. Takeda, K., et al. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol. Cell Biol. 26:22 (2006), 8336–8346.
26. Greaves, M., Maley, C.C., Clonal evolution in cancer. Nature 481:7381 (2012), 306–313.
27. Raval, R.R., et al. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol. Cell Biol. 25:13 (2005), 5675–5686.
28. Gordan, J.D., et al. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 11:4 (2007), 335–347.
29. Adam, J., et al. Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: roles for fumarate in KEAP1 succination and Nrf2 signaling. Cancer Cell 20:4 (2011), 524–537.
30. Athanassiades, A., Hamilton, G.S., Lala, P.K., Vascular endothelial growth factor stimulates proliferation but not migration or invasiveness in human extravillous trophoblast. Biol. Reprod. 59:3 (1998), 643–654.
31. Liang, Y., Brekken, R.A., Hyder, S.M., Vascular endothelial growth factor induces proliferation of breast cancer cells and inhibits the anti-proliferative activity of anti-hormones. Endocr. Relat. Cancer 13:3 (2006), 905–919.
32. Devery, A.M., et al. Vascular endothelial growth factor directly stimulates tumour cell proliferation in non-small cell lung cancer. Int. J. Oncol. 47:3 (2015), 849–856.
33. Forsythe, J.A., et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell Biol. 16:9 (1996), 4604–4613.
34. Gerber, H.P., et al. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J. Biol. Chem. 272:38 (1997), 23659–23667.
35. Athanassiades, A., Lala, P.K., Role of placenta growth factor (PIGF) in human extravillous trophoblast proliferation, migration and invasiveness. Placenta 19:7 (1998), 465–473.
36. Kim, K.J., Cho, C.S., Kim, W.U., Role of placenta growth factor in cancer and inflammation. Exp. Mol. Med. 44:1 (2012), 10–19.
37. Li, F., et al. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 396:6711 (1998), 580–584.
38. Lehner, R., et al. Localization of telomerase hTERT protein and survivin in placenta: relation to placental development and hydatidiform mole. Obstet. Gynecol. 97:6 (2001), 965–970.
39. Bai, H., et al. Hypoxia inducible factor-1alpha-mediated activation of survivin in cervical cancer cells. J. Obstet. Gynaecol. Res. 39:2 (2013), 555–563.
40. Sharp, A.N., et al. Placental apoptosis in health and disease. Am. J. Reprod. Immunol. 64:3 (2010), 159–169.
41. Mellor, H.R., Harris, A.L., The role of the hypoxia-inducible BH3-only proteins BNIP3 and BNIP3L in cancer. Cancer Metastasis Rev. 26:3–4 (2007), 553–566.
42. Mourad-Zeidan, A.A., et al. Expression profiling of Galectin-3-depleted melanoma cells reveals its major role in melanoma cell plasticity and vasculogenic mimicry. Am. J. Pathol. 173:6 (2008), 1839–1852.
43. Maquoi, E., et al. Changes in the distribution pattern of galectin-1 and galectin-3 in human placenta correlates with the differentiation pathways of trophoblasts. Placenta 18:5–6 (1997), 433–439.
44. Donnem, T., et al. Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment?. Cancer Med. 2:4 (2013), 427–436.
45. Shibuya, M., Involvement of Flt-1 (VEGF receptor-1) in cancer and preeclampsia. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 87:4 (2011), 167–178.
46. Cowden Dahl, K.D., et al. Hypoxia-inducible factor regulates alphavbeta3 integrin cell surface expression. Mol. Biol. Cell 16:4 (2005), 1901–1912.
47. Zhou, Y., et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?. J. Clin. Invest. 99:9 (1997), 2139–2151.
48. Soundararajan, R., Rao, A.J., Trophoblast ‘pseudo-tumorigenesis’: significance and contributory factors. Reprod. Biol. Endocrinol., 2, 2004, 15.
49. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144:5 (2011), 646–674.
50. Barsoum, I.B., et al. Mechanisms of hypoxia-mediated immune escape in cancer. Cancer Res. 74:24 (2014), 7185–7190.
51. Vinay, D.S., et al. Immune evasion in cancer: mechanistic basis and therapeutic strategies. Semin. Cancer Biol. 35:Suppl (2015), S185–S198.
52. Holtan, S.G., et al. Cancer and pregnancy: parallels in growth, invasion, and immune modulation and implications for cancer therapeutic agents. Mayo Clin. Proc. 84:11 (2009), 985–1000.
53. Bubenik, J., Tumour MHC class I downregulation and immunotherapy (Review). Oncol. Rep. 10:6 (2003), 2005–2008.
54. Yaghi, L., et al. Hypoxia inducible factor-1 mediates the expression of the immune checkpoint HLA-G in glioma cells through hypoxia response element located in exon 2. Oncotarget 7:39 (2016), 63690–63707.
55. Nagamine, Y., et al. Inhibition of prolyl hydroxylase attenuates Fas ligand-induced apoptosis and lung injury in mice. Am. J. Respir. Cell Mol. Biol. 55:6 (2016), 878–888.
56. Guleria, I., et al. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J. Exp. Med. 202:2 (2005), 231–237.
57. Barsoum, I.B., et al. A mechanism of hypoxia-mediated escape from adaptive immunity in cancer cells. Cancer Res. 74:3 (2014), 665–674.
58. Holets, L.M., Hunt, J.S., Petroff, M.G., Trophoblast CD274 (B7-H1) is differentially expressed across gestation: influence of oxygen concentration. Biol. Reprod. 74:2 (2006), 352–358.
59. Baumann, M.U., Zamudio, S., Illsley, N.P., Hypoxic upregulation of glucose transporters in BeWo choriocarcinoma cells is mediated by hypoxia-inducible factor-1. Am. J. Physiol. Cell Physiol. 293:1 (2007), C477–C485.
60. Tian, Q., et al. Overexpression of hypoxia-inducible factor 1alpha induces migration and invasion through Notch signaling. Int. J. Oncol. 47:2 (2015), 728–738.