Salicylic acid induces mitochondrial injury by inhibiting ferrochelatase heme biosynthesis activity

Molecular Pharmacology

Volumn 84, Issue 6, 2013, Pages 824-833

  Gupta, Vipul ^a   Liu, Shujie ^a   Ando, Hideki ^a   Ishii, Ryohei ^b   Tateno, Shumpei ^a   Kaneko, Yuki ^a   Yugami, Masato ^a   Sakamoto, Satoshi ^a   Yamaguchi, Yuki ^a   Nureki, Osamu ^b   Handa, Hiroshi ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BINDING PROTEIN; DIMER; FERROCHELATASE; SALICYLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BRAIN INJURY; CELL DAMAGE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DRUG INHIBITION; ELUTION; ENZYME ACTIVITY; ENZYME PURIFICATION; GEL FILTRATION; GENE OVEREXPRESSION; HEME SYNTHESIS; HUMAN; HUMAN CELL; LIVER INJURY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION DAMAGE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RAT; ZEBRA FISH;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE, TUMOR; CRYSTALLOGRAPHY, X-RAY; EMBRYO, NONMAMMALIAN; ESCHERICHIA COLI PROTEINS; FERROCHELATASE; HEME; HUMANS; MITOCHONDRIA; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTOPORPHYRINS; SALICYLIC ACID; ZEBRAFISH;

EID: 84888867797     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.087940     Document Type: Article

References (50)

1. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, and Adams PD (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr 68:352-367.
2. Antonicka H, Mattman A, Carlson CG, Glerum DM, Hoffbuhr KC, Leary SC, Kennaway NG, and Shoubridge EA (2003) Mutations in COX15 produce a defect in the mitochondrial heme biosynthetic pathway, causing early-onset fatal hypertrophic cardiomyopathy. Am J Hum Genet 72:101-114.
3. Atamna H, Killilea DW, Killilea AN, and Ames BN (2002) Heme deficiency may be a factor in the mitochondrial and neuronal decay of aging. Proc Natl Acad Sci USA 99:14807-14812.
4. Atamna H, Liu J, and Ames BN (2001) Heme deficiency selectively interrupts assembly of mitochondrial complex IV in human fibroblasts: revelance to aging. J Biol Chem 276:48410-48416.
5. Baggott JE, Morgan SL, Ha T, Vaughn WH, and Hine RJ (1992) Inhibition of folate-dependent enzymes by non-steroidal anti-inflammatory drugs. Biochem J 282: 197-202.
6. Berridge MV, Herst PM, and Tan AS (2005) Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev 11:127-152.
7. Braun FK, Al-Yacoub N, Plötz M, Möbs M, Sterry W, and Eberle J (2012) Nonsteroidal anti-inflammatory drugs induce apoptosis in cutaneous T-cell lymphoma cells and enhance their sensitivity for TNF-related apoptosis-inducing ligand. J Invest Dermatol 132:429-439.
8. Burden AE, Wu C, Dailey TA, Busch JL, Dhawan IK, Rose JP, Wang B, and Dailey HA (1999) Human ferrochelatase: crystallization, characterization of the [2Fe-2S] cluster and determination that the enzyme is a homodimer. Biochim Biophys Acta 1435:191-197.
9. Chen YN and Marnett LJ (1989) Heme prosthetic group required for acetylation of prostaglandin H synthase by aspirin. FASEB J 3:2294-2297.
10. Childs S, Weinstein BM, Mohideen MA, Donohue S, Bonkovsky H, and Fishman MC (2000) Zebrafish dracula encodes ferrochelatase and its mutation provides a model for erythropoietic protoporphyria. Curr Biol 10:1001-1004.
11. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763.
12. Cronstein BN (1994) Adenosine, an endogenous anti-inflammatory agent. J Appl Physiol 76:5-13.
13. Cronstein BN, Montesinos MC, and Weissmann G (1999) Salicylates and sulfasalazine, but not glucocorticoids, inhibit leukocyte accumulation by an adenosine-dependent mechanism that is independent of inhibition of prostaglandin synthesis and p105 of NFkappaB. Proc Natl Acad Sci USA 96:6377-6381.
14. Dailey HA, Wu CK, Horanyi P, Medlock AE, Najahi-Missaoui W, Burden AE, Dailey TA, and Rose J (2007) Altered orientation of active site residues in variants of human ferrochelatase. Evidence for a hydrogen bond network involved in catalysis. Biochemistry 46:7973-7979.
15. Doi H and Horie T (2010) Salicylic acid-induced hepatotoxicity triggered by oxidative stress. Chem Biol Interact 183:363-368.
16. Durner J, Shah J, and Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:266-274.
17. Emsley P and Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132.
18. Gatta LB, Vitali M, Verardi R, Arosio P, and Finazzi D (2009) Inhibition of heme synthesis alters Amyloid Precursor Protein processing. J Neural Transm 116:79-88.
19. Grosser T, Emer S, and Garret AFD (2009) Anti-inflammatory, antipyretic, and analgesic agents; pharmacotherapy of gout, in Goodman & Gilman's The Pharmacological Basis of Therapeutics (Brunton LL, Chabner BA, and Knollmann BC eds) pp 959-1004, McGraw-Hill Companies, New York.
20. Hawley SA, Fullerton MD, Ross FA, Schertzer JD, Chevtzoff C, Walker KJ, Peggie MW, Zibrova D, Green KA, and Mustard KJ et al. (2012) The ancient drug salicylate directly activates AMP-activated protein kinase. Science 336:918-922.
21. Ito T, Ando H, Suzuki T, Ogura T, Hotta K, Imamura Y, Yamaguchi Y, and Handa H (2010) Identification of a primary target of thalidomide teratogenicity. Science 327:1345-1350.
22. Klampfer L, Cammenga J, Wisniewski HG, and Nimer SD (1999) Sodium salicylate activates caspases and induces apoptosis of myeloid leukemia cell lines. Blood 93:2386-2394.
23. Kopp E and Ghosh S (1994) Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 265:956-959.
24. Kunze H, Rehbock G, and Vogt W (1972) Absorption of salicylic acid and its isomers from the rat jejunum. Naunyn Schmiedebergs Arch Pharmacol 273:331-340.
25. Langenbach R, Loftin CD, Lee C, and Tiano H (1999) Cyclooxygenase- deficient mice. A summary of their characteristics and susceptibilities to inflammation and carcinogenesis. Ann N Y Acad Sci 889:52-61.
26. Li FM, Lim CK, and Peters TJ (1987) An HPLC assay for rat liver ferrochelatase activity. Biomed Chromatogr 2:164-168.
27. Lim JW, Kim H, and Kim KH (2001) Nuclear factor-kappaB regulates cyclooxygenase-2 expression and cell proliferation in human gastric cancer cells. Lab Invest 81:349-360.
28. Loll PJ, Picot D, and Garavito RM (1995) The structural basis of aspirin activity inferred from the crystal structure of inactivated prostaglandin H2 synthase. Nat Struct Biol 2:637-643.
29. Mauro C, Leow SC, Anso E, Rocha S, Thotakura AK, Tornatore L, Moretti M, De Smaele E, Beg AA, and Tergaonkar V et al. (2011) NF-κB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat Cell Biol 13:1272-1279.
30. Medlock AE, Dailey TA, Ross TA, Dailey HA, and Lanzilotta WN (2007a) A pi-helix switch selective for porphyrin deprotonation and product release in human ferrochelatase. J Mol Biol 373:1006-1016.
31. Medlock A, Swartz L, Dailey TA, Dailey HA, and Lanzilotta WN (2007b) Substrate interactions with human ferrochelatase. Proc Natl Acad Sci USA 104:1789-1793.
32. Medlock AE, Carter M, Dailey TA, Dailey HA, and Lanzilotta WN (2009) Product release rather than chelation determines metal specificity for ferrochelatase. J Mol Biol 393:308-319.
33. Medlock AE, Najahi-Missaoui W, Ross TA, Dailey TA, Burch J, O'Brien JR, Lanzilotta WN, and Dailey HA (2012) Identification and characterization of solvent-filled channels in human ferrochelatase. Biochemistry 51:5422-5433.
34. Mitchell JA, Akarasereenont P, Thiemermann C, Flower RJ, and Vane JR (1993) Selectivity of nonsteroidal antiinflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase. Proc Natl Acad Sci USA 90:11693-11697.
35. Möbius K, Arias-Cartin R, Breckau D, Hännig AL, Riedmann K, Biedendieck R, Schröder S, Becher D, Magalon A, and Moser J et al. (2010) Heme biosynthesis is coupled to electron transport chains for energy generation. Proc Natl Acad Sci USA 107:10436-10441.
36. Najahi-Missaoui W and Dailey HA (2005) Production and characterization of erythropoietic protoporphyric heterodimeric ferrochelatases. Blood 106:1098-1104.
37. Needs CJ and Brooks PM (1985) Clinical pharmacokinetics of the salicylates. Clin Pharmacokinet 10:164-177.
38. Nicolaou KC and Montagnon T (2008) Molecules That Changed the World, Wiley-VCH, Weinheim, Germany.
39. Otwinowski Z and Minor W (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
40. Ransom DG, Haffter P, Odenthal J, Brownlie A, Vogelsang E, Kelsh RN, Brand M, van Eeden FJ, Furutani-Seiki M, and Granato M et al. (1996) Characterization of zebrafish mutants with defects in embryonic hematopoiesis. Development 123:311-319.
41. Sakamoto S, Kabe Y, Hatakeyama M, Yamaguchi Y, and Handa H (2009) Development and application of high-performance affinity beads: toward chemical biology and drug discovery. Chem Rec 9:66-85.
42. Shimizu N, Sugimoto K, Tang J, Nishi T, Sato I, Hiramoto M, Aizawa S, Hatakeyama M, Ohba R, and Hatori H et al. (2000) High-performance affinity beads for identifying drug receptors. Nat Biotechnol 18:877-881.
43. Steiner RA, Lebedev AA, and Murshudov GN (2003) Fisher's information in maximum-likelihood macromolecular crystallographic refinement. Acta Crystallogr D Biol Crystallogr 59:2114-2124.
44. Uga H, Kuramori C, Ohta A, Tsuboi Y, Tanaka H, Hatakeyama M, Yamaguchi Y, Takahashi T, Kizaki M, and Handa H (2006) A new mechanism of methotrexate action revealed by target screening with affinity beads. Mol Pharmacol 70:1832-1839.
45. Vagin A and Teplyakov A (2010) Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66:22-25.
46. Vane JR and Botting RM (2003) The mechanism of action of aspirin. Thromb Res 110:255-258.
47. Vane JR (1971) Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 231:232-235.
48. Wu CK, Dailey HA, Rose JP, Burden A, Sellers VM, and Wang BC (2001) The 2.0 A structure of human ferrochelatase, the terminal enzyme of heme biosynthesis. Nat Struct Biol 8:156-160.
49. Yin MJ, Yamamoto Y, and Gaynor RB (1998) The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature 396:77-80.
50. You K (1983) Salicylate and mitochondrial injury in Reye's syndrome. Science 221:163-165.