Effect of proline analogues on activity of human prolyl hydroxylase and the regulation of HIF signal transduction pathway

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Ma, Xiaoyan ^a   Wang, Xiaoxin ^a   Cao, Jing ^a   Geng, Zhirong ^a   Wang, Zhilin ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ENOLASE 1; COBALT DERIVATIVE; DEFEROXAMINE MESYLATE; ENOLASE; ENZYME INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1ALPHA INHIBITOR; ISOENZYME; PA 1; PA 2; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLINE DERIVATIVE; PROLYL HYDROXYLASE 3; PYRUVATE KINASE; PYRUVATE KINASE ISOZYME M1; PYRUVATE KINASE ISOZYME M2; UNCLASSIFIED DRUG; VASCULOTROPIN; EGLN3 PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; PROLINE; RECOMBINANT PROTEIN; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; DRUG SCREENING; ENZYME ACTIVITY; GLYCOLYSIS; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UPREGULATION; ANALOGS AND DERIVATIVES; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; HYDROXYLATION; KINETICS; METABOLISM; PROTEOMICS; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL SURVIVAL; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMANS; HYDROXYLATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; KINETICS; PROLINE; PROTEOMICS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84899754548     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095692     Document Type: Article

References (72)

1. Kulkarni AC, Kuppusamy P, Parinandi N (2007) Oxygen, the Lead Actor in the Pathophysiologic Drama: Enactment of the Trinity of Normoxia, Hypoxia, and Hyperoxia in Disease and Therapy. Antioxidants & Redox Signaling. 9: 1717-1730. (Pubitemid 47462974)
2. Chowdhury R, Hardy A, Schofield CJ (2008) The human oxygen sensing machinery and its manipulation. Chem Soc Rev 37: 1308-1319.
3. Semenza GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148: 399-408.
4. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol Cell Biol 5: 343-354. (Pubitemid 38579472)
5. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, Rourke JO, et al. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54. (Pubitemid 32972036)
6. Bruick RK, McKnight SL (2001) A Conserved Family of Prolyl-4-Hydroxylases That Modify HIF. Science 294: 1337-1340. (Pubitemid 33063099)
7. Ivan M, Kondo K, Yang H, Kim W, Valiando J, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468. (Pubitemid 32335941)
8. Bardos JI, Ashcroft M (2005) Negative and positive regulation of HIF-1: a complex network. Biochim Biophys Acta 1755: 107-20. (Pubitemid 40982561)
9. Melnikova I (2006) Anaemia therapies. Nat Rev Drug Discovery 5: 627-628.
10. Ratan RR, Siddiq A, Aminova L, Lange PS, Langley B, et al. (2004) Translation of ischemic preconditioning to the patient: prolyl hydroxylase inhibition and hypoxia inducible factor-1 as novel targets for stroke therapy. Stroke 35: 2687-2689. (Pubitemid 39458369)
11. Paul SA, Simons JW, Mabjeesh NJ (2004) HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol 200: 20-30. (Pubitemid 38720618)
12. Siddiq A, Ayoub IA, Chavez JC, Aminova L, Shah S, et al. (2005) Hypoxia-inducible factor prolyl 4-hydroxylase inhibition. A target for neuroprotection in the central nervous system. J Biol Chem 280: 41732-41743. (Pubitemid 41832236)
13. Wang GL, Semenza GL (1993b) Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 82: 3610-3615. (Pubitemid 24006041)
14. Lienard BM, Stolze I, Loenarz C, Oldham NJ, Ratcliffe PJ, et al. (2008) Evaluation of aspirin metabolites as inhibitors of hypoxia-inducible factor hydroxylases. Chem Commun 6393-6395.
15. Yan L, Colandrea VJ, Hale JJ (2010) Prolyl hydroxylase domain-containing protein inhibitors as stabilizers of hypoxia-inducible factor: small molecule-based therapeutics for anemia. Expert Opin Ther Pat 20: 1219-1245.
16. Davidson TL, Chen HB, DiToro DM, D'Angelo G, Costa M (2006) Soluble nickel inhibits HIF-prolyl-hydroxylases creating persistent hypoxic signaling in A549 cells. Mol Carcinog 45: 479-489.
17. Jones SM, Novak AE, Elliott JP (2013) The role of HIF in cobalt-induced ischemic tolerance. Neuroscience 252C: 420-430.
18. Wu Y, Li X, Xie W, Jankovic J, Le W, et al. (2010) Neuroprotection of deferoxamine on rotenone-induced injury via accumulation of HIF-1 alpha and induction of autophagy in SH-SY5Y cells. Neurochem Int 57: 198-205.
19. Tegley CM, Viswanadhan VN, Biswas K, Frohn MJ, Hungate RW (2008) Discovery of novel hydroxyl-thiazoles as HIF-α prolyl hydroxylase inhibitors: SAR, synthesis, and modeling evaluation. Bioorg Med Chem Lett 18: 3925-3928.
20. McDonough MA, McNeill LA, Tilliet M, Papamicael CA, Chen QY, et al. (2005) Selective Inhibition of Factor Inhibiting Hypoxia-Inducible Factor. J Am Chem Soc 127: 7680-7681. (Pubitemid 40745948)
21. Mecinovic J, Loenarz C, Chowdhury R, Schofield CJ (2009) 2-Oxoglutarate analogue inhibitors of prolyl hydroxylase domain 2. Bioorg Med Chem Lett 19: 6192-6195.
22. Mole DR, Schlemminger I, McNeill LA, Hewitson KS, Pugh CW, et al. (2003) 2-oxoglutarate analogue inhibitors of HIF prolyl hydroxylase. Bioorg Med Chem Lett 13: 2677-2680. (Pubitemid 36851548)
23. Prockop DJ, Kivirikko KI (1969) Effect of Polymer Size on the Inhibition of Protocollagen Proline Hydroxylase by Polyproline II. J Biol Chem 244: 4838-4842.
24. Gorres KL, Edupuganti R, Krow GR, Raines RT (2008) Conformational Preferences of Substrates for Human Prolyl 4-Hydroxylase. Biochemistry 47: 9447-9455.
25. Li DX, Koivunen P, Brenner MC, Xu L, Yang C, et al. (2004) Many Amino Acid Substitutions in a Hypoxia-inducible Transcription Factor (HIF)-1α -like Peptide Cause Only Minor Changes in Its Hydroxylation by the HIF Prolyl 4-Hydroxylases. J Biol Chem 279: 55051-55059.
26. Jaakkola P (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
27. Cummins EP, Seeballuck F, Keely SJ, Mangan NE, Callanan JJ, et al. (2008) The Hydroxylase Inhibitor Dimethyloxalylglycine Is Protective in a Murine Model of Colitis. Gastroenterology 134: 156-165.
28. Mole DR (2010) Iron Homeostasis and Its Interaction with Prolyl Hydroxylases. Antioxid Redox Signaling 12: 445-458.
29. Yu F, White SB, Zhao Q, Lee FS (2001) HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 98: 9630-9635. (Pubitemid 32769354)
30. Kwon HS, Choi YK, Kim JW, Park YK, Yang EG, et al. (2011) Inhibition of a prolyl hydroxylase domain (PHD) by substrate analog peptides. Bioorganic Medicinal Chemistry Letters 21: 4325-4328.
31. Ratcliffe PJ, O'Rourke JF, Maxwell PH, Pugh CW (1998) Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J Exp Biol 201: 1153-1162. (Pubitemid 28278320)
32. Semenza GL (2004) O2-regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF-1. J Appl Physiol 96: 1173-1177.
33. Ratcliffe PJ (2004) HIF hydroxylation and cellular oxygen sensing. Biol Chem 385: 223-230.
34. Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A (2001) Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J Biol Chem 276: 9519-9525.
35. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, 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: 32529-32537.
36. Minchenko A, Leshchinsky I, Opentanova I, Sang N, Srinivas V, et al. (2002) Hypoxia-inducible factor-1-mediated expression of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) gene. Its possible role in the Warburg effect. J Biol Chem 277: 6183-6187. (Pubitemid 34968408)
37. Semenza GL, Roth PH, Fang HM, Wang GL (1994) Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269: 23757-23763. (Pubitemid 24293585)
38. Yu X, Fang Y, Ding X, Liu H, Zhu J, et al. (2012) Transient hypoxia-inducible factor activation in rat renal ablation and reduced fibrosis with L-mimosine. Nephrology 17: 58-67.
39. Pérez AS, Planas AM, O'Mara AN, Berra E, Villoria JG, et al. (2010) Extended Ischemia Prevents HIF1α Degradation at Reoxygenation by Impairing Prolyl-hydroxylation : Role of krebs cycle metabolites. J Biol Chem 285: 18217-18224.
40. Wheaton WW, Chandel NS (2011) Hypoxia. 2. Hypoxia regulates cellular metabolism. Am J Physiol Cell Physiol 300: C385-393.
41. Berger A, Kurtz J, Katchalski E (1954) Poly-L-proline. J Am Chem Soc 76: 5552-5554.
42. Weeks CL, Turner P, Fenton RR, Lay PA (2002) Nickel(II) complexes with amide ligands: oxidative dehydrogenation of the amines in a tetradentate diamide-diamine ligand. Dalton Trans 931-940. (Pubitemid 35202088)
43. Geng Z, Zhu J, Cao J, Geng J, Song X, et al. (2011) Effects of polynitrogen compounds on the activity of recombinant human HIF-1α prolyl hydroxylase 3 in E. coli. J Inorg Biochem 105: 391-399.
44. Cao J, Ma XY, Wang XX, Wang XB, Zhang Z, et al. (2013) Azole derivatives as novel non-iron-chelating inhibitors of prolyl hydroxylase 3 for HIF-1 activation. Med Chem Commun 4: 1222-1230.
45. McNeill LA, Bethge L, Hewitson KS, Schofield CJ (2005) A fluorescence-based assay for 2-oxoglutarate-dependent oxygenases. Anal Biochem 336: 125-131. (Pubitemid 39593508)
46. Muhling J, Fuchs M, Campos ME, Gonter J, Engel JM, et al. (2003) Assaying protein unbound drugs using microdialysis techniques. B: Anal Technol Biomed Life Sci 789: 383-392.
47. Little CD (1983) Amplification and expression of the c-myc oncogene in human lung cancer cell lines. Nature 306: 194-196.
48. Carney DN (1985) Establishment and identification of small cell lung cancer cell lines having classic and variant features. Cancer Res. 45: 2913-2923.
49. Cao J, Geng Z, Ma X, Wen J, Yin Y, et al. (2012) Evidence for inhibition of HIF-1α prolyl hydroxylase 3 activity by four biologically active tetraazamacrocycles. Org Biomol Chem 10: 3913-3923.
50. Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27-31.
51. Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
52. Semenza GL (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29: 625-634.
53. Ong SG, Hausenloy DJ. (2012) Hypoxia-inducible factor as a therapeutic target for cardioprotection. Pharmacology Therapeutics 136: 69-81.
54. Semenza GL (2012) Hypoxia-Inducible Factors in Physiology and Medicine. Cell 148: 399-408.
55. Agis H, Watzek G, Gruber R (2012) Prolyl hydroxylase inhibitors increase the production of vascular endothelial growth factor by periodontal fibroblasts. J Periodontal Res 47: 165-173.
56. Nagel S, Papadakis M, Chen R, Hoyte LC, Brooks KJ, et al. (2011) Neuroprotection by dimethyloxalylglycine following permanent and transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 31: 132-143.
57. Asikainen TM, Schneider BK, Waleh NS, Clyman RI, Ho WB, et al. (2005) Activation of hypoxia-inducible factors in hyperoxia through prolyl 4-hydroxylase blockade in cells and explants of primate lung. Proc Natl Acad Sci USA 102: 10212-10217. (Pubitemid 41023351)
58. Robin ED, Murphy BJ, Theoclore J (1984) Coordinate regulation of glycolysis by hypoxia in mammalian cells. J Cell Physiol 11: 287-290. (Pubitemid 14162998)
59. Ptashne KA, Morin ME, Hance A, Robin ED (1985) Increased biosynthesis of pyrutate kinase under hypoxic conditions in mammalian cells. Biochim Biophys Acta 844: 19-23. (Pubitemid 15157638)
60. Liedtke AJ, Lynch ML (1999) Alteration of gene expression for glycolytic enzymes in aerobic and ischemic myocardium. Am J Physiol 277: H1435-1440. (Pubitemid 29522673)
61. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
62. Marrif H, Juurlink BHJ (1999) Astrocytes respond to hypoxia by increasing glycolytic capacity. J Neurosci Res 57: 255-260. (Pubitemid 29300328)
63. Lai JC, White BK, Buerstatte CR, Haddad GG, Novotny EJ, et al. (2003) Chronic hypoxia in development selectively alters the activities of key enzymes of glucose oxidative metabolism in brain regions. Neurochem Res 28: 933-940. (Pubitemid 36438412)
64. Giallongo A, Oliva D, Cali L, Barba G, Barbieri G, et al. (1990) Structure of the human gene for alpha-enolase. Eur J Biochem 190(3): 567-573.
65. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, 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: 32529-32537.
66. Aaronson RM, Graven KK, Tucci M, McDonald RJ, Farber HW (1995) Non-neuronal enolase is an endothelial hypoxic stress protein. J Biol Chem 270: 27752-27757.
67. 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: 5510-5514.
68. Wang GL, Semenza GL (1995) Purification and Characterization of Hypoxia-inducible Factor 1. J Biol Chem 270: 1230-1237.
69. Mizukami Y, Iwamatsu A, Aki T (2004) ERK1/2 regulates intracellular ATP levels through α-enolase expression in cardiomyocytes exposed to ischemic hypoxia and reoxygenation. J Biol Chem 279 (48) : 50120-50131. (Pubitemid 39577824)
70. Forsythe JA, Jiang BH, Zheng JZ, Leung SW, Roe R, et al. (1996) Activation of Vascular Endothelial Growth Factor Gene Transcription by Hypoxia-Inducible Factor 1. Molecular and Cellular biology 16: 4604-4613. (Pubitemid 26272112)
71. Dai Y, Xu M, Wang Y, Pasha Z, Li T, et al. (2007) HIF-1alpha induced-VEGF overexpression in bone marrow stem cells protects cardiomyocytes against ischemia. J Mol Cell Cardiol 42: 1036-1044. (Pubitemid 46829200)
72. Okuda T, Mohtani TA, Matsunaga S, Masaki R, Satomi S, et al. (2006) Hypoxia-inducible factor-1 alpha and vascular endothelial growth factor expression in ischaemic colitis and ulcerative colitis. Aliment Pharmacol Ther symp ser 2: 182-188.