Hypoxia-inducible factor 3 biology: Complexities and emerging themes

American Journal of Physiology - Cell Physiology

Volumn 310, Issue 4, 2016, Pages C260-C269

  Duan, Cunming ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Alternative splicing; Gene expression; Hypoxia inducible factor; Oxygen dependent degradation

Indexed keywords

AMINO ACID; ENDOTHELIN 1; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 2ALPHA; HYPOXIA INDUCIBLE FACTOR 3ALPHA; MESSENGER RNA; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; OXYGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN P53; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HIF3A PROTEIN, HUMAN; HIF3A PROTEIN, MOUSE; ISOPROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; HUMAN; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UBIQUITINATION; ALTERNATIVE RNA SPLICING; ANIMAL; ANOXIA; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

ALTERNATIVE SPLICING; ANIMALS; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; OXYGEN; PROTEIN CONFORMATION; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84958551663     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00315.2015     Document Type: Article

References (57)

1. Augstein A, Poitz DM, Braun-Dullaeus RC, Strasser RH, Schmeisser A. Cell-specific and hypoxia-dependent regulation of human HIF-3α: inhibition of the expression of HIF target genes in vascular cells. Cell Mol Life Sci 68: 2627-2642. 2011.
2. Chen N, Chen LP, Zhang J, Chen C, Wei XL, Gul Y, Wang WM, Wang HL. Molecular characterization and expression analysis of three hypoxia-inducible factor alpha subunits, HIF-1α/2α/3α of the hypoxiasensitive freshwater species, Chinese sucker. Gene 498: 81-90, 2012.
3. Fala AM, Oliveira JF, Adamoski D, Aricetti JA, Dias MM, Dias MV, Sforça ML, Lopes-de-Oliveira PS, Rocco SA, Caldana C, Dias SM, Ambrosio AL. Unsaturated fatty acids as high-affinity ligands of the C-terminal Per-ARNT-Sim domain from the hypoxia-inducible factor 3α. Sci Rep 5: 12698, 2015.
4. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL. Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 59: 3915-3918, 1999.
5. Gao S, Lu L, Bai Y, Zhang P, Song W, Duan C. Structural and functional analysis of amphioxus HIFalpha reveals ancient features of the HIFalpha family. FASEB J 28: 1880-1890, 2014.
6. Gits CM, van Kuijk PF, de Rijck JC, Muskens N, Jonkers MB, van Ijcken WF, Mathijssen RH, Verweij J, Sleijfer S, Wiemer EA. MicroRNA response to hypoxic stress in soft tissue sarcoma cells: microRNA mediated regulation of HIF3α. BMC Cancer 14: 429, 2014.
7. Gorr TA, Tomita T, Wappner P, Bunn HF. Regulation of Drosophila hypoxia-inducible factor (HIF) activity in SL2 cells: identification of a hypoxia-induced variant isoform of the HIFalpha homolog gene similar. J Biol Chem 279: 36048-36058, 2004.
8. Goryo K, Torii S, Yasumoto K, Sogawa K. Tumour necrosis factor-α suppresses the hypoxic response by NF-κB-dependent induction of inhibitory PAS domain protein in PC12 cells. J Biochem 150: 311-318, 2011.
9. Greer SN, Metcalf JL, Wang Y, Ohh M. The updated biology of hypoxia-inducible factor. EMBO J 31: 2448-2460, 2012.
10. Gu YZ, Moran SM, Hogenesch JB, Wartman L, Bradfield CA. Molecular characterization and chromosomal localization of a third alphaclass hypoxia inducible factor subunit, HIF3alpha. Gene Expr 7: 205-213, 1998.
11. Han WQ, Zhu Q, Hu J, Li PL, Zhang F, Li N. Hypoxia-inducible factor prolyl-hydroxylase-2 mediates transforming growth factor beta 1-induced epithelial-mesenchymal transition in renal tubular cells. Biochim Biophys Acta 1833: 1454-1462, 2013.
12. Hara S, Hamada J, Kobayashi C, Kondo Y, Imura N. Expression and characterization of hypoxia-inducible factor (HIF)-3alpha in human kidney: suppression of HIF-mediated gene expression by HIF-3alpha. Biochem Biophys Res Commun 287: 808-813, 2001.
13. Hatanaka M, Shimba S, Sakaue M, Kondo Y, Kagechika H, Kokame K, Miyata T, Hara S. Hypoxia-inducible factor-3alpha functions as an accelerator of 3T3-L1 adipose differentiation. Biol Pharm Bull 32: 1166- 1172, 2009.
14. Heidbreder M, Frohlich F, Johren O, Dendorfer A, Qadri F, Dominiak P. Hypoxia rapidly activates HIF-3alpha mRNA expression. FASEB J 17: 1541-1543, 2003.
15. Heidbreder M, Qadri F, Jöhren O, Dendorfer A, Depping R, Fröhlich F, Wagner KF, Dominiak P. Non-hypoxic induction of HIF-3alpha by 2-deoxy-D-glucose and insulin. Biochem Biophys Res Commun 352: 437- 443, 2007.
16. Heikkilä M, Pasanen A, Kivirikko KI, Myllyharju J. Roles of the human hypoxia-inducible factor (HIF)-3α variants in the hypoxia response. Cell Mol Life Sci 68: 3885-3901, 2011.
17. Huang Y, Kapere Ochieng J, Kempen MB, Munck AB, Swagemakers S, van Ijcken W, Grosveld F, Tibboel D, Rottier RJ. Hypoxia inducible factor 3α plays a critical role in alveolarization and distal epithelial cell differentiation during mouse lung development. PLoS One 8: e57695, 2013.
18. Hubbi ME, Semenza GL. Regulation of cell proliferation by hypoxiainducible factors. Am J Physiol Cell Physiol 309: C775-C782, 2015.
19. Johnson RW, Schipani E, Giaccia AJ. HIF targets in bone remodeling and metastatic disease. Pharmacol Ther 150: 169-177, 2015.
20. Kajimura S, Aida K, Duan C. Insulin-like growth factor-binding protein- 1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proc Natl Acad Sci USA 102: 1240-1245, 2005.
21. Kajimura S, Aida K, Duan C. Understanding hypoxia-induced gene expression in early development: in vitro and in vivo analysis of hypoxiainducible factor 1-regulated zebra fish insulin-like growth factor binding protein 1 gene expression. Mol Cell Biol 26: 1142-1155, 2006.
22. Kamei H, Lu L, Jiao S, Li Y, Gyrup C, Laursen LS, Oxvig C, Zhou J, Duan C. Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. PLoS One 3: e3091, 2008.
23. Kamei H, Ding Y, Kajimura S, Wells M, Chiang P, Duan C. Role of IGF signaling in catch-up growth and accelerated temporal development in zebrafish embryos in response to oxygen availability. Development 138: 777-786, 2011.
24. Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 12: 9-22, 2011.
25. Köblitz L, Fiechtner B, Baus K, Lussnig R, Pelster B. Developmental expression and hypoxic induction of hypoxia inducible transcription factors in the zebrafish. PLoS One 10: e0128938, 2015.
26. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 16: 1466- 1471, 2002.
27. Li QF, Wang XR, Yang YW, Lin H. Hypoxia upregulates hypoxia inducible factor (HIF)-3alpha expression in lung epithelial cells: characterization and comparison with HIF-1alpha. Cell Res 16: 548-558, 2006.
28. Loenarz C, Coleman ML, Boleininger A, Schierwater B, Holland PW, Ratcliffe PJ, Schofield CJ. The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens. EMBO Rep 12: 63-70, 2011.
29. Lykke-Andersen S, Jensen TH. Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol 16: 665-677, 2015.
30. Makino Y, Cao R, Svensson K, Bertilsson G, Asman M, Tanaka H, Cao Y, Berkenstam A, Poellinger L. Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature 414: 550-554, 2001.
31. Makino Y, Kanopka A, Wilson WJ, Tanaka H, Poellinger L. Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus. J Biol Chem 277: 32405-32408, 2002.
32. Makino Y, Uenishi R, Okamoto K, Isoe T, Hosono O, Tanaka H, Kanopka A, Poellinger L, Haneda M, Morimoto C. Transcriptional up-regulation of inhibitory PAS domain protein gene expression by hypoxia-inducible factor 1 (HIF-1): a negative feedback regulatory circuit in HIF-1-mediated signaling in hypoxic cells. J Biol Chem 282: 14073- 14082, 2007.
33. Marques IJ, Leito JT, Spaink HP, Testerink J, Jaspers RT, Witte F, van den Berg S, Bagowski CP. Transcriptome analysis of the response to chronic constant hypoxia in zebrafish hearts. J Comp Physiol B 178: 77-92, 2008.
34. Maures TJ, Duan C. Structure, developmental expression, and physiological regulation of zebrafish IGF binding protein-1. Endocrinology 143: 2722-2731, 2002.
35. Maynard MA, Qi H, Chung J, Lee EH, Kondo Y, Hara S, Conaway RC, Conaway JW, Ohh M. Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem 278: 11032-11040, 2003.
36. Maynard MA, Evans AJ, Hosomi T, Hara S, Jewett MA, Ohh M. Human HIF-3alpha4 is a dominant-negative regulator of HIF-1 and is down-regulated in renal cell carcinoma. FASEB J 19: 1396-1406, 2005.
37. Maynard MA, Evans AJ, Shi W, Kim WY, Liu FF, Ohh M. Dominantnegative HIF-3 alpha 4 suppresses VHL-null renal cell carcinoma progression. Cell Cycle 15: 2810-2816, 2007.
38. Pasanen A, Heikkila M, Rautavuoma K, Hirsila M, Kivirikko KI, Myllyharju J. Hypoxia-inducible factor (HIF)-3a is subject to extensive alternative splicing in human tissues and cancer cells and is regulated by HIF-1 but not HIF-2. Int J Biochem Cell Biol 42: 1189-1200, 2010.
39. Prabhakar NR, Semenza GL. Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia- inducible factors 1 and 2. Physiol Rev 92: 967-1003, 2012.
40. Rytkönen KT, Akbarzadeh A, Miandare HK, Kamei H, Duan C, Leder EH, Williams TA, Nikinmaa M. Subfunctionalization of cyprinid hypoxia-inducible factors for roles in development and oxygen sensing. Evolution 67: 873-882, 2013.
41. Rytkönen KT, Prokkola JM, Salonen V, Nikinmaa M. Transcriptional divergence of the duplicated hypoxia-inducible factor alpha genes in zebrafish. Gene 541: 60-66, 2014.
42. Scharf JG, Unterman TG, Kietzmann T. Oxygen-dependent modulation of insulin-like growth factor binding protein biosynthesis in primary cultures of rat hepatocytes. Endocrinology 146: 5433-5443, 2005.
43. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell 148: 399-408, 2012.
44. Shay JE, Celeste Simon M. Hypoxia-inducible factors: crosstalk between inflammation and metabolism. Semin Cell Dev Biol 23: 389-394, 2012.
45. Shen C, Kaelin WG Jr. The VHL/HIF axis in clear cell renal carcinoma. Semin Cancer Biol 23: 18-25, 2013.
46. Tanaka T, Wiesener M, Bernhardt W, Eckardt KU, Warnecke C. The human HIF (hypoxia-inducible factor)-3alpha gene is a HIF-1 target gene and may modulate hypoxic gene induction. Biochem J 23: 143-151, 2009.
47. Tazuke SI, Mazure NM, Sugawara J, Carland G, Faessen GH, Suen LF, Irwin JC, Powell DR, Giaccia AJ, Giudice LC. Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Proc Natl Acad Sci USA 95: 10188-10193, 1998.
48. Torii S, Goto Y, Ishizawa T, Hoshi H, Goryo K, Yasumoto K, Fukumura H, Sogawa K. Pro-apoptotic activity of inhibitory PAS domain protein (IPAS), a negative regulator of HIF-1, through binding to pro-survival Bcl-2 family proteins. Cell Death Differ 18: 1711-1725, 2011.
49. Torii S, Sakaki K, Otomo M, Saka K, Yasumoto K, Sogawa K. Nucleocytoplasmic shuttling of IPAS by its unique nuclear import and export signals unshared with other HIF-3α splice variants. J Biochem 154: 561-567, 2013.
50. Treins C, Giorgetti-Peraldi S, Murdaca J, Monthouël-Kartmann MN, Van Obberghen E. Regulation of hypoxia-inducible factor (HIF)-1 activity and expression of HIF hydroxylases in response to insulin-like growth factor I. Mol Endocrinol 19: 1304-1317, 2005.
51. van Uden P, Kenneth NS, Rocha S. Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem J 412: 477-484, 2008.
52. Yamashita T, Ohneda O, Nagano M, Iemitsu M, Makino Y, Tanaka H, Miyauchi T, Goto K, Ohneda K, Fujii-Kuriyama Y, Poellinger L, Yamamoto M. Abnormal heart development and lung remodeling in mice lacking the hypoxia-inducible factor-related basic helix-loop-helix PAS protein NEPAS. Mol Cell Biol 28: 1285-1297, 2008.
53. Yang SL, Wu C, Xiong ZF, Fang X. Progress on hypoxia-inducible factor-3: its structure, gene regulation and biological function (Review). Mol Med Rep 12: 2411-2416, 2015.
54. Zhang P, Duan C. Dissecting oxygen-dependent and -independent actions of hypoxia-inducible factor 3 using CRISPR/Cas9-based gene editing (Abstract). In: Hypoxia: From Basic Mechanisms to Therapeutics. Silverthorne, CO, Keystone Symposia, 2015, p. 53.
55. Zhang P, Lu L, Yao Q, Li Y, Zhou J, Liu Y, Duan C. Molecular, functional, and gene expression analysis of zebrafish hypoxia-inducible factor-3α. Am J Physiol Regul Integr Comp Physiol 303: R1165-R1174, 2012.
56. Zhang P, Yao Q, Lu L, Li Y, Chen PJ, Duan C. Hypoxia-inducible factor 3 is an oxygen-dependent transcription activator and regulates a distinct transcriptional response to hypoxia. Cell Rep 6: 1110-1121, 2014.
57. Zhu X, Wang F, Zhao Y, Yang P, Chen J, Sun H, Liu L, Li W, Pan L, Guo Y, Kou Z, Zhang Y, Zhou C, He J, Zhang X, Li J, Han W, Li J, Liu G, Gao S, Yang Z. A gain-of-function mutation in Tnni2 impeded bone development through increasing Hif3a expression in DA2B mice. PLoS Genet 10: e1004589, 2014.