Up-regulation of glycolytic metabolism is required for HIF1α-driven bone formation

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

Volumn 111, Issue 23, 2014, Pages 8673-8678

  Regan, Jenna N ^a,d   Lim, Joohyun ^a   Shi, Yu ^a   Joeng, Kyu Sang ^a,e   Arbeit, Jeffrey M ^a   Shohet, Ralph V ^b   Longa, Fanxin ^a,c  

^a Department of Orthopaedic Surgery ^*  (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; PYRUVATE DEHYDROGENASE KINASE; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; BONE REGENERATION; CELL DIFFERENTIATION; CELL METABOLISM; CONTROLLED STUDY; FEMUR; GLYCOLYSIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; NEWBORN; NONHUMAN; OSSIFICATION; OSTEOBLAST; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; TIBIA; WESTERN BLOTTING;

ANIMALS; ANOXIA; BLOTTING, WESTERN; BONE AND BONES; BONE MARROW; BONE MARROW CELLS; CELL HYPOXIA; FEMALE; GLYCOLYSIS; GREEN FLUORESCENT PROTEINS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; OSTEOBLASTS; OSTEOGENESIS; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84902214157     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1324290111     Document Type: Article

References (33)

1. Simon MC, Keith B (2008) The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9(4):285-296. (Pubitemid 351430845)
2. Lendahl U, Lee KL, Yang H, Poellinger L (2009) Generating specificity and diversity in the transcriptional response to hypoxia. Nat Rev Genet 10(12):821-832.
3. Huang LE, Gu J, Schau M, Bunn HF (1998) Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95(14):7987-7992.
4. Maxwell PH, et al. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399(6733):271-275. (Pubitemid 29246458)
5. Jaakkola P, et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292(5516):468-472. (Pubitemid 32335942)
6. Semenza GL, et al. (1996) Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 271(51):32529-32537.
7. Wang GL, Jiang BH, Rue EA, Semenza GL (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 92(12):5510-5514.
8. Benita Y, et al. (2009) An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res 37(14):4587-4602.
9. Mole DR, et al. (2009) Genome-wide association of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha DNA binding with expression profiling of hypoxia-inducible transcripts. J Biol Chem 284(25):16767-16775.
10. Schödel J, et al. (2011) High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 117(23):e207-e217.
11. Warburg O (1956) On the origin of cancer cells. Science 123(3191):309-314.
12. Semenza GL (2013) HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations. J Clin Invest 123(9):3664-3671.
13. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 324(5930):1029-1033.
14. Wang Y, et al. (2007) The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 117(6):1616-1626. (Pubitemid 46871346)
15. Shomento SH, et al. (2010) Hypoxia-inducible factors 1alpha and 2alpha exert both distinct and overlapping functions in long bone development. J Cell Biochem 109(1):196-204.
16. Maes C, et al. (2012) VEGF-independent cell-autonomous functions of HIF-1alpha regulating oxygen consumption in fetal cartilage are critical for chondrocyte survival. J Bone Miner Res 27(3):596-609.
17. Chow DC, Wenning LA, Miller WM, Papoutsakis ET (2001) Modeling pO(2) distributions in the bone marrow hematopoietic compartment. II. Modified Kroghian models. Biophys J 81(2):685-696. (Pubitemid 32721444)
18. Arteel GE, Thurman RG, Yates JM, Raleigh JA (1995) Evidence that hypoxia markers detect oxygen gradients in liver: Pimonidazole and retrograde perfusion of rat liver. Br J Cancer 72(4):889-895.
19. Long F, et al. (2004) Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development 131(6):1309-1318. (Pubitemid 38443885)
20. Rodda SJ, McMahon AP (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133(16):3231-3244. (Pubitemid 44404346)
21. Bekeredjian R, et al. (2010) Conditional HIF-1alpha expression produces a reversible cardiomyopathy. PLoS ONE 5(7):e11693.
22. Madisen L, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13(1):133-140.
23. Forsythe JA, et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16(9):4604-4613. (Pubitemid 26272112)
24. Maes C, et al. (2010) Increased skeletal VEGF enhances beta-catenin activity and results in excessively ossified bones. EMBO J 29(2):424-441.
25. Gerber HP, et al. (1999) VEGF is required for growth and survival in neonatal mice. Development 126(6):1149-1159.
26. Semenza GL (2011) Regulation of metabolism by hypoxia-inducible factor 1. Cold Spring Harb Symp Quant Biol 76:347-353.
27. Whitehouse S, Cooper RH, Randle PJ (1974) Mechanism of activation of pyruvate dehydrogenase by dichloroacetate and other halogenated carboxylic acids. Biochem J 141(3):761-774.
28. Hilton MJ, Tu X, Cook J, Hu H, Long F (2005) Ihh controls cartilage development by antagonizing Gli3, but requires additional effectors to regulate osteoblast and vascular development. Development 132(19):4339-4351. (Pubitemid 41576695)
29. Wan C, et al. (2008) Activation of the hypoxia-inducible factor-1alpha pathway accelerates bone regeneration. Proc Natl Acad Sci USA 105(2):686-691. (Pubitemid 351171769)
30. Imai S, et al. (2000) Sir2: An NAD-dependent histone deacetylase that connects chromatin silencing, metabolism, and aging. Cold Spring Harb Symp Quant Biol 65:297-302. (Pubitemid 32611950)
31. Wellen KE, et al. (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324(5930):1076-1080.
32. Lu C, et al. (2012) IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483(7390):474-478.
33. Esen E, et al. (2013) WNT-LRP5 signaling induces Warburg effect through mTORC2 activation during osteoblast differentiation. Cell Metab 17(5):745- 755.