Expression of murine 5-aminolevulinate synthase variants causes protoporphyrin IX accumulation and light-induced mammalian cell death

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Fratz, Erica J ^a   Hunter, Gregory A ^a   Ferreira, Gloria C ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINOLEVULINATE SYNTHASE; 5 AMINOLEVULINATE SYNTHASE 2; AMINOLEVULINIC ACID; ARGININE; DEFEROXAMINE; GLYCINE; HEME; ISOENZYME; LYSINE; PACLITAXEL; PROTOPORPHYRIN; UNCLASSIFIED DRUG; ALAS2 PROTEIN, MOUSE; CULTURE MEDIUM; GREEN FLUORESCENT PROTEIN; MUTANT PROTEIN;

ARTICLE; CATALYSIS; CELL DEATH; CELL MEMBRANE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FLOW CYTOMETRY; FLUORESCENCE; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LIGHT EXPOSURE; MAMMAL CELL; MITOCHONDRION; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PHOTOSENSITIZATION; PHOTOTOXICITY; PLASMID; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SYNTHESIS; PROTEIN TARGETING; TOXICITY TESTING; WHITE LIGHT; ANIMAL; CULTURE MEDIUM; DRUG EFFECTS; HELA CELL LINE; K562 CELL LINE; LIGHT; METABOLISM; RADIATION RESPONSE;

5-AMINOLEVULINATE SYNTHETASE; ANIMALS; CELL DEATH; CELL MEMBRANE; CULTURE MEDIA; DEFEROXAMINE; GLYCINE; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; K562 CELLS; LIGHT; MICE; MUTANT PROTEINS; PACLITAXEL; PLASMIDS; PROTOPORPHYRINS; TRANSFECTION;

EID: 84899497073     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093078     Document Type: Article

References (76)

1. Jordan PM (1990) In: Dailey HA, editor. Biosynthesis of Heme and Chlorophylls. New York: McGraw-Hill. 55-121.
2. Hunter GA, Ferreira GC (2011) Molecular enzymology of 5-aminolevulinate synthase, the gatekeeper of heme biosynthesis. Biochim Biophys Acta 11: 1467-1473.
3. Ferreira GC, Gong J (1995) 5-Aminolevulinate synthase and the first step of heme biosynthesis. J Bioenerg Biomembr 27: 151-159.
4. Riddle RD, Yamamoto M, Engel JD (1989) Expression of delta- aminolevulinate synthase in avian cells: separate genes encode erythroid-specific and nonspecific isozymes. Proc Natl Acad Sci USA 86: 792-796. (Pubitemid 19056242)
5. Sutherland GR, Baker E, Callen DF, Hyland VJ, May BK, et al. (1988) 5-Aminolevulinate synthase is at 3p21 and thus not the primary defect in X-linked sideroblastic anemia. Am J Hum Genet 43: 331-335.
6. Bishop DF, Henderson AS, Astrin KH (1990) Human delta-aminolevulinate synthase: assignment of the housekeeping gene to 3p21 and the erythroid-specific gene to the X chromosome. Genomics 7: 207-214. (Pubitemid 20235576)
7. Watanabe N, Hayashi N, Kikuchi G (1983) delta-Aminolevulinate synthase isozymes in the liver and erythroid cells of chicken. Biochem Biophys Res Commun 113: 377-383. (Pubitemid 13058449)
8. Cox TC, Bawden MJ, Abraham NG, Bottomley SS, May BK, et al. (1990) Erythroid 5-aminolevulinate synthase is located on the X chromosome. Am J Hum Genet 46: 107-111.
9. Yamauchi K, Hayashi N, Kikuchi G (1980) Translocation of delta-aminolevulinate synthase from the cytosol to the mitochondria and its regulation by hemin in the rat liver. J Biol Chem 255: 1746-1751. (Pubitemid 10113278)
10. Srivastava G, Borthwick IA, Brooker JD, May BK, Elliott WH (1983) Evidence for a cytosolic precursor of chick embryo liver mitochondrial delta-aminolevulinate synthase. Biochem Biophys Res Commun 110: 23-31. (Pubitemid 13117865)
11. Volland C, Urban-Grimal D (1988) The presequence of yeast 5-aminolevulinate synthase is not required for targeting to mitochondria. J Biol Chem 263: 8294-8299.
12. Neupert W (1997) Protein import into mitochondria. Annu Rev Biochem 66: 863-917.
13. Sadlon TJ, Dell'Oso T, Surinya KH, May BK (1999) Regulation of erythroid 5-aminolevulinate synthase expression during erythropoiesis. Int J Biochem Cell Biol 31: 1153-1167. (Pubitemid 29454551)
14. Ades IZ, Harpe KG (1981) Biogenesis of mitochondrial proteins. Identification of the mature and precursor forms of the subunit of delta-aminolevulinate synthase from embryonic chick liver. J Biol Chem 256: 9329-9333.
15. McKay R, Druyan R, Getz GS, Rabinowitz M (1969) Intramitochondrial localization of delta-aminolaevulate synthetase and ferrochelatase in rat liver. Biochem J 114: 455-461.
16. Zuyderhoudt FM, Borst P, Huijing F (1969) Intramitochondrial localization of 5-aminolaevulinate synthase induced in rat liver with allylisopropylacetamide. Biochim Biophys Acta 178: 408-411.
17. Dailey TA, Woodruff JH, Dailey HA (2005) Examination of mitochondrial protein targeting of haem synthetic enzymes: in vivo identification of three functional haem-responsive motifs in 5-aminolaevulinate synthase. Biochem J 386: 381-386. (Pubitemid 40343796)
18. Lathrop JT, Timko MP (1993) Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259: 522-525. (Pubitemid 23058711)
19. Zhang L, Guarente L (1995) Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J 14: 313-320.
20. Qi Z, O'Brian MR (2002) Interaction between the bacterial iron response regulator and ferrochelatase mediates genetic control of heme biosynthesis. Mol Cell 9: 155-162. (Pubitemid 34127779)
21. Gonzalez-Dominguez M, Freire-Picos MA, Cerdan ME (2001) Haem regulation of the mitochondrial import of the Kluyveromyces lactis 5-aminolaevulinate synthase: an organelle approach. Yeast 18: 41-48. (Pubitemid 32104862)
22. Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C, et al. (2001) Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J 20: 2835-2843.
23. de Haro C, Mendez R, Santoyo J (1996) The eIF-2alpha kinases and the control of protein synthesis. FASEB J 10: 1378-1387.
24. Goodfellow BJ, Dias JS, Ferreira GC, Henklein P, Wray V, et al. (2001) The solution structure and heme binding of the presequence of murine 5-aminolevulinate synthase. FEBS Lett 505: 325-331. (Pubitemid 32896689)
25. Hunter GA, Ferreira GC (1999) Pre-steady-state reaction of 5-aminolevulinate synthase. Evidence for a rate-determining product release. J Biol Chem 274: 12222-12228.
26. Hunter GA, Ferreira GC (1995) A continuous spectrophotometric assay for 5-aminolevulinate synthase that utilizes substrate cycling. Anal Biochem 226: 221-224.
27. Zhang J, Ferreira GC (2002) Transient state kinetic investigation of 5-aminolevulinate synthase reaction mechanism. J Biol Chem 277: 44660-44669. (Pubitemid 36159055)
28. Hunter GA, Zhang J, Ferreira GC (2007) Transient kinetic studies support refinements to the chemical and kinetic mechanisms of aminolevulinate synthase. J Biol Chem 282: 23025-23035. (Pubitemid 47311926)
29. Ferreira GC, Vajapey U, Hafez O, Hunter GA, Barber MJ (1995) Aminolevulinate synthase: lysine 313 is not essential for binding the pyridoxal phosphate cofactor but is essential for catalysis. Protein Sci 4: 1001-1006.
30. Tan D, Barber MJ, Ferreira GC (1998) The role of tyrosine 121 in cofactor binding of 5-aminolevulinate synthase. Protein Sci 7: 1208-1213. (Pubitemid 28237054)
31. Tan D, Harrison T, Hunter GA, Ferreira GC (1998) Role of arginine 439 in substrate binding of 5-aminolevulinate synthase. Biochemistry 37: 1478-1484. (Pubitemid 28093662)
32. Gong J, Hunter GA, Ferreira GC (1998) Aspartate-279 in aminolevulinate synthase affects enzyme catalysis through enhancing the function of the pyridoxal 5′-phosphate cofactor. Biochemistry 37: 3509-3517. (Pubitemid 28125579)
33. Lendrihas T, Zhang J, Hunter GA, Ferreira GC (2009) Arg-85 and Thr-430 in murine 5-aminolevulinate synthase coordinate acyl-CoA-binding and contribute to substrate specificity. Protein Sci 18: 1847-1859.
34. Lendrihas T, Hunter GA, Ferreira GC (2010) Serine 254 enhances an induced fit mechanism in murine 5-aminolevulinate synthase. J Biol Chem 285: 3351-3359.
35. Lendrihas T, Hunter GA, Ferreira GC (2010) Targeting the active site gate to yield hyperactive variants of 5-aminolevulinate synthase. J Biol Chem 285: 13704-13711.
36. Ferreira GC, Neame PJ, Dailey HA (1993) Heme biosynthesis in mammalian systems: evidence of a Schiff base linkage between the pyridoxal 5′-phosphate cofactor and a lysine residue in 5-aminolevulinate synthase. Protein Sci 2: 1959-1965. (Pubitemid 23328550)
37. Hunter GA, Ferreira GC (1999) Lysine-313 of 5-Aminolevulinate Synthase Acts as a General Base during Formation of the Quinonoid Reaction Intermediates. Biochemistry 38: 3711-3718.
38. Astner I, Schulze JO, van den Heuvel J, Jahn D, Schubert WD, et al. (2005) Crystal structure of 5-aminolevulinate synthase, the first enzyme of heme biosynthesis, and its link to XLSA in humans. EMBO J 24: 3166-3177. (Pubitemid 41348692)
39. Whatley SD, Ducamp S, Gouya L, Grandchamp B, Beaumont C, et al. (2008) C-terminal deletions in the ALAS2 gene lead to gain of function and cause X-linked dominant protoporphyria without anemia or iron overload. Am J Hum Genet 83: 408-414.
40. Gagnebin J, Brunori M, Otter M, Juillerat-Jeanneret L, Monnier P, et al. (1999) A photosensitising adenovirus for photodynamic therapy. Gene Ther 6: 1742-1750. (Pubitemid 29485950)
41. Issa MC, Manela-Azulay M (2010) Photodynamic therapy: a review of the literature and image documentation. An Bras Dermatol 85: 501-511.
42. Buzzeo R, Enkemann S, Nimmanapalli R, Alsina M, Lichtenheld MG, et al. (2005) Characterization of a R115777-resistant human multiple myeloma cell line with cross-resistance to PS-341. Clin Cancer Res 11: 6057-6064. (Pubitemid 41170338)
43. Yanamandra N, Buzzeo RW, Gabriel M, Hazlehurst LA, Mari Y, et al. (2011) Tipifarnib-induced apoptosis in acute myeloid leukemia and multiple myeloma cells depends on Ca2+ influx through plasma membrane Ca2+ channels. J Pharmacol Exp Ther 337: 636-643.
44. Boshart M, Weber F, Jahn G, Dorsch-Hasler K, Fleckenstein B, et al. (1985) A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41: 521-530. (Pubitemid 16219422)
45. Tan D, Ferreira GC (1996) Active site of 5-aminolevulinate synthase resides at the subunit interface. Evidence from in vivo heterodimer formation. Biochemistry 35: 8934-8941. (Pubitemid 26243734)
46. Schiff PB, Horwitz SB (1980) Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci U S A 77: 1561-1565. (Pubitemid 10073801)
47. Manfredi JJ, Parness J, Horwitz SB (1982) Taxol binds to cellular microtubules. J Cell Biol 94: 688-696. (Pubitemid 13241201)
48. Mole-Bajer J, Bajer AS (1983) Action of taxol on mitosis: modification of microtubule arrangements and function of the mitotic spindle in Haemanthus endosperm. J Cell Biol 96: 527-540. (Pubitemid 13115859)
49. Krammer B, Plaetzer K (2008) ALA and its clinical impact, from bench to bedside. Photochem Photobiol Sci 7: 283-289. (Pubitemid 351501306)
50. Ryan WL, Carver MJ (1966) Free amino acids of human foetal and adult liver. Nature 212: 292-293.
51. Andersson LC, Nilsson K, Gahmberg CG (1979) K562-a human erythroleukemic cell line. Int J Cancer 23: 143-147. (Pubitemid 9110047)
52. Hoffbrand AV, Wonke B (1997) Iron chelation therapy. J Intern Med Suppl 740: 37-41.
53. Roberts DJ, Rees D, Howard J, Hyde C, Alderson P, et al. (2005) Desferrioxamine mesylate for managing transfusional iron overload in people with transfusion-dependent thalassaemia. Cochrane Database Syst Rev: CD004450.
54. Nikcevic G, Kovacevic-Grujicic N, Stevanovic M (2003) Improved transfection efficiency of cultured human cells. Cell Biol Int 27: 735-737. (Pubitemid 37101355)
55. Agostinis P, Berg K, Cengel KA, Foster TH, Girotti AW, et al. (2011) Photodynamic therapy of cancer: an update. CA Cancer J Clin 61: 250-281.
56. Dolmans DE, Fukumura D, Jain RK (2003) Photodynamic therapy for cancer. Nat Rev Cancer 3: 380-387. (Pubitemid 37328858)
57. Darlenski R, Fluhr JW (2013) Photodynamic therapy in dermatology: past, present, and future. J Biomed Opt 18: 061208.
58. Babilas P, Landthaler M, Szeimies RM (2006) Photodynamic therapy in dermatology. Eur J Dermatol 16: 340-348. (Pubitemid 44328972)
59. Warren CB, Karai LJ, Vidimos A, Maytin EV (2009) Pain associated with aminolevulinic acid-photodynamic therapy of skin disease. J Am Acad Dermatol 61: 1033-1043.
60. Hunter GA, Ferreira GC (1999) Lysine-313 of 5-aminolevulinate synthase acts as a general base during formation of the quinonoid reaction intermediates. Biochemistry 38: 3711-3718.
61. Hunter GA, Ferreira GC (1999) Lysine-313 of 5-aminolevulinate synthase acts as a general base during formation of the quinonoid reaction intermediates. Biochemistry 38: 12526. (Pubitemid 29453316)
62. Bishop DF, Tchaikovskii V, Hoffbrand AV, Fraser ME, Margolis S (2012) X-linked sideroblastic anemia due to carboxyl-terminal ALAS2 mutations that cause loss of binding to the beta-subunit of succinyl-CoA synthetase (SUCLA2). J Biol Chem 287: 28943-28955.
63. Andersson LC, Jokinen M, Klein E, Klein G, Nilsson K (1979) Presence of erythrocytic components in the K562 cell line. Int J Cancer 24: 514. (Pubitemid 10244706)
64. Ji Z, Yang G, Vasovic V, Cunderlikova B, Suo Z, et al. (2006) Subcellular localization pattern of protoporphyrin IX is an important determinant for its photodynamic efficiency of human carcinoma and normal cell lines. J Photochem Photobiol B 84: 213-220. (Pubitemid 44184915)
65. Lendrihas T, Hunter GA, Ferreira GC (2010) Targeting the active site gate to yield hyperactive variants of 5-aminolevulinate synthase. J Biol Chem 285: 13704-13711.
66. Juknat AA, Kotler ML, Quaglino A, Carrillo NM, Hevor T (2003) Necrotic cell death induced by delta-aminolevulinic acid in mouse astrocytes. Protective role of melatonin and other antioxidants. J Pineal Res 35: 1-11. (Pubitemid 36819164)
67. Weiss TS, Pahernik S, Scheruebl I, Jauch KW, Thasler WE (2003) Cellular damage to human hepatocytes through repeated application of 5-aminolevulinic acid. J Hepatol 38: 476-482. (Pubitemid 36399251)
68. Felitsyn N, McLeod C, Shroads AL, Stacpoole PW, Notterpek L (2008) The heme precursor delta-aminolevulinate blocks peripheral myelin formation. J Neurochem 106: 2068-2079.
69. Hunter GA, Rivera E, Ferreira GC (2005) Supraphysiological concentrations of 5-aminolevulinic acid dimerize in solution to produce superoxide radical anions via a protonated dihydropyrazine intermediate. Arch Biochem Biophys 437: 128-137. (Pubitemid 40585814)
70. Cheung MC, Pantanowitz L, Dezube BJ (2005) AIDS-related malignancies: emerging challenges in the era of highly active antiretroviral therapy. Oncologist 10: 412-426. (Pubitemid 40993569)
71. Sparano JA, Wang M, Martino S, Jones V, Perez EA, et al. (2008) Weekly paclitaxel in the adjuvant treatment of breast cancer. N Engl J Med 358: 1663-1671. (Pubitemid 351549913)
72. Ramalingam SS, Khuri FR (2009) The role of the taxanes in the treatment of older patients with advanced stage non-small cell lung cancer. Oncologist 14: 412-424.
73. Katsumata N, Yasuda M, Takahashi F, Isonishi S, Jobo T, et al. (2009) Dose-dense paclitaxel once a week in combination with carboplatin every 3 weeks for advanced ovarian cancer: a phase 3, open-label, randomised controlled trial. Lancet 374: 1331-1338.
74. Horwitz SB (1992) Mechanism of action of taxol. Trends Pharmacol Sci 13: 134-136.
75. Canti G, Lattuada D, Nicolin A, Taroni P, Valentini G, et al. (1994) Antitumor immunity induced by photodynamic therapy with aluminum disulfonated phthalocyanines and laser light. Anticancer Drugs 5: 443-447. (Pubitemid 24237076)
76. Korbelik M (2010) Photodynamic therapy-generated cancer vaccines. Methods Mol Biol 635: 147-153.