Protoporphyrin IX: The good, the bad, and the ugly

Journal of Pharmacology and Experimental Therapeutics

Volumn 356, Issue 2, 2016, Pages 267-275

  Sachar, Madhav ^a   Anderson, Karl E ^b   Ma, Xiaochao ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFAMELANOTIDE; ANTIHISTAMINIC AGENT; ASCORBIC ACID; BETA CAROTENE; BREAST CANCER RESISTANCE PROTEIN; COPROPORPHYRINOGEN OXIDASE; CYTOCHROME P450; FERROCHELATASE; IRON REGULATORY FACTOR; PORPHOBILINOGEN DEAMINASE; PORPHOBILINOGEN SYNTHASE; PREGNANE X RECEPTOR; PROTEIN ALAS1; PROTEIN ALAS2; PROTOPORPHYRIN; PROTOPORPHYRINOGEN OXIDASE; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG; UROPORPHYRINOGEN III SYNTHASE;

ARTICLE; BINDING AFFINITY; BIOACCUMULATION; BIOSYNTHESIS; CIRCADIAN RHYTHM; ENZYME ACTIVITY; EXTRACELLULAR SPACE; HEME SYNTHESIS; HEPATOBILIARY DISEASE; HOMEOSTASIS; HUMAN; HYDROPHOBICITY; NONHUMAN; PHOTODYNAMIC THERAPY; PHOTOSENSITIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SKIN DEFECT; UPREGULATION; ANIMAL; CHOLESTASIS; GENETICS; LIVER; METABOLISM; PATHOLOGY; PHOTOSENSITIVITY DISORDER;

ANIMALS; CHOLESTASIS; HUMANS; LIVER; PHOTOSENSITIVITY DISORDERS; PROTOPORPHYRINS;

EID: 84959324818     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.115.228130     Document Type: Article

References (172)

1. Ajioka RS, Phillips JD, and Kushner JP (2006) Biosynthesis of heme in mammals. Biochim Biophys Acta 1763: 723-736.
2. Akilov OE, Kosaka S, O'Riordan K, Song X, Sherwood M, Flotte TJ, Foley JW, and Hasan T (2006) The role of photosensitizer molecular charge and structure on the efficacy of photodynamic therapy against Leishmania parasites. Chem Biol 13: 839-847.
3. Amo T, Kawanishi N, Uchida M, Fujita H, Oyanagi E, Utsumi T, Ogino T, Inoue K, Shuin T, Utsumi K, and Sasaki J (2009) Mechanism of cell death by 5-aminolevulinic acid-based photodynamic action and its enhancement by ferrochelatase inhibitors in human histiocytic lymphoma cell line U937. Cell Biochem Funct 27: 503-515.
4. Anderson KE, Drummond GS, Freddara U, Sardana MK, and Sassa S (1981) Porphyrogenic effects and induction of heme oxygenase in vivo by delta-aminolevulinic acid. Biochim Biophys Acta 676: 289-299.
5. Anderson KE, Freddara U, and Kappas A (1982) Induction of hepatic cytochrome P-450 by natural steroids: Relationship to the induction of d-aminolevulinate synthase and porphyrin accumulation in the avian embryo. Arch Biochem Biophys 217: 597-608.
6. Anderson KE, Sassa S, Peterson CM, and Kappas A (1977) Increased erythrocyte uroporphyrinogen-l-synthetase, d-aminolevulinic acid dehydratase and protoporphyrin in hemolytic anemias. Am J Med 63: 359-364.
7. Anstey AV and Hift RJ (2007) Liver disease in erythropoietic protoporphyria: Insights and implications for management. Postgrad Med J 83: 739-748.
8. Baart de la Faille H, Bijlmer-Iest JC, van Hattum J, Koningsberger J, Rademakers LH, and van Weelden H (1991) Erythropoietic protoporphyria: Clinical aspects with emphasis on the skin. Curr Probl Dermatol 20: 123-134.
9. Bayeva M, Khechaduri A, Wu R, Burke MA, Wasserstrom JA, Singh N, Liesa M, Shirihai OS, Langer NB, and Paw BH, et al. (2013) ATP-binding cassette B10 regulates early steps of heme synthesis. Circ Res 113: 279-287.
10. Bhasker CR, Burgiel G, Neupert B, Emery-Goodman A, Kühn LC, and May BK (1993) The putative iron-responsive element in the human erythroid 5-aminolevulinate synthase mRNA mediates translational control. J Biol Chem 268: 12699-12705.
11. Biolcati G, Marchesini E, Sorge F, Barbieri L, Schneider-Yin X, and Minder EI (2015) Long-term observational study of afamelanotide in 115 patients with erythropoietic protoporphyria. Br J Dermatol 172: 1601-1612.
12. Bishop DF, Henderson AS, and 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.
13. Blake E and Curnow A (2010) The hydroxypyridinone iron chelator CP94 can enhance PpIX-induced PDT of cultured human glioma cells. Photochem Photobiol 86: 1154-1160.
14. Bloomer JR (1988) The liver in protoporphyria. Hepatology 8: 402-407.
15. Bloomer JR and Enriquez R (1982) Evidence that hepatic crystalline deposits in a patient with protoporphyria are composed of protoporphyrin. Gastroenterology 82: 569-573.
16. Bloomer JR and Pierach CA (1982) Effect of hematin administration to patients with protoporphyria and liver disease. Hepatology 2: 817-821.
17. Boffa MJ, Ead RD, Reed P, and Weinkove C (1996) A double-blind, placebocontrolled, crossover trial of oral vitamin C in erythropoietic protoporphyria. Photodermatol Photoimmunol Photomed 12: 27-30.
18. Bonkowsky HL, Bloomer JR, Ebert PS, and Mahoney MJ (1975) Heme synthetase deficiency in human protoporphyria: Demonstration of the defect in liver and cultured skin fibroblasts. J Clin Invest 56: 1139-1148.
19. Bossi K, Lee J, Schmeltzer P, Holburton E, Groseclose G, Besur S, Hwang S, and Bonkovsky HL (2015) Homeostasis of iron and hepcidin in erythropoietic protoporphyria. Eur J Clin Invest 45: 1032-1041.
20. Brancaleon L, Magennis SW, Samuel ID, Namdas E, Lesar A, and Moseley H (2004) Characterization of the photoproducts of protoporphyrin IX bound to human serum albumin and immunoglobulin G. Biophys Chem 109: 351-360.
21. Braun J (1999) Erythrocyte zinc protoporphyrin. Kidney Int Suppl 69: S57-S60.
22. Bruguera M and Herrero C (2005) [Liver disease in erythropoietic protoporphyria]. Gastroenterol Hepatol 28: 632-636.
23. Cable EE, Miller TG, and Isom HC (2000) Regulation of heme metabolism in rat hepatocytes and hepatocyte cell lines: Delta-aminolevulinic acid synthase and heme oxygenase are regulated by different heme-dependent mechanisms. Arch Biochem Biophys 384: 280-295.
24. Casanova-González MJ, Trapero-Marugán M, Jones EA, and Moreno-Otero R (2010) Liver disease and erythropoietic protoporphyria: A concise review. World J Gastroenterol 16: 4526-4531.
25. Castano AP, Mroz P, and Hamblin MR (2006) Photodynamic therapy and antitumour immunity. Nat Rev Cancer 6: 535-545.
26. Chen FP, Risheg H, Liu Y, and Bloomer J (2002) Ferrochelatase gene mutations in erythropoietic protoporphyria: Focus on liver disease. Cell Mol Biol (Noisy-le-grand) 48: 83-89.
27. Chen W, Paradkar PN, Li L, Pierce EL, Langer NB, Takahashi-Makise N, Hyde BB, Shirihai OS, Ward DM, and Kaplan J, et al. (2009) Abcb10 physically interacts with mitoferrin-1 (Slc25a37) to enhance its stability and function in the erythroid mitochondria. Proc Natl Acad Sci USA 106: 16263-16268.
28. Cole SP and Marks GS (1984) Ferrochelatase and N-alkylated porphyrins. Mol Cell Biochem 64: 127-137.
29. Cole SP, Zelt DT, and Marks GS (1981) Comparison of the effects of griseofulvin and 3,5-diethoxycarbonyl-1,4-dihydro-2,4,6-trimethylpyridine on ferrochelatase activity in chick embryo liver. Mol Pharmacol 19: 477-480.
30. Collins P and Ferguson J (1995) Narrow-band UVB (TL-01) phototherapy: An effective preventative treatment for the photodermatoses. Br J Dermatol 132: 956-963.
31. Cotter PD, Willard HF, Gorski JL, and Bishop DF (1992) Assignment of human erythroid delta-aminolevulinate synthase (ALAS2) to a distal subregion of band Xp11.21 by PCR analysis of somatic cell hybrids containing X; autosome translocations. Genomics 13: 211-212.
32. Cox TC, Bawden MJ, Abraham NG, Bottomley SS, May BK, Baker E, Chen LZ, and Sutherland GR (1990) Erythroid 5-aminolevulinate synthase is located on the X chromosome. Am J Hum Genet 46: 107-111.
33. Cox TM, Alexander GJ, and Sarkany RP (1998) Protoporphyria. Semin Liver Dis 18: 85-93.
34. Dailey HA, Jr (1977) Purification and characterization of the membrane-bound ferrochelatase from Spirillum itersonii. J Bacteriol 132: 302-307.
35. Dailey HA and Meissner PN (2013) Erythroid heme biosynthesis and its disorders. Cold Spring Harb Perspect Med 3: A011676.
36. Dailey TA, Woodruff JH, and 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.
37. de Torres I, Demetris AJ, and Randhawa PS (1996) Recurrent hepatic allograft injury in erythropoietic protoporphyria. Transplantation 61: 1412-1413.
38. Dellon ES, Szczepiorkowski ZM, Dzik WH, Graeme-Cook F, Ades A, Bloomer JR, Cosimi AB, and Chung RT (2002) Treatment of recurrent allograft dysfunction with intravenous hematin after liver transplantation for erythropoietic protoporphyria. Transplantation 73: 911-915.
39. Desuzinges-Mandon E, Arnaud O, Martinez L, Huché F, Di Pietro A, and Falson P (2010) ABCG2 transports and transfers heme to albumin through its large extracellular loop. J Biol Chem 285: 33123-33133.
40. Donnelly RF, McCarron PA, and Tunney MM (2008) Antifungal photodynamic therapy. Microbiol Res 163: 1-12.
41. Doss MO and Frank M (1989) Hepatobiliary implications and complications in protoporphyria, a 20-year study. Clin Biochem 22: 223-229.
42. Dougherty TJ (2002) An update on photodynamic therapy applications. J Clin Laser Med Surg 20: 3-7.
43. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, and Peng Q (1998) Photodynamic therapy. J Natl Cancer Inst 90: 889-905.
44. Dowman JK, Gunson BK, Mirza DF, Badminton MN, and Newsome PN; UK Liver Selection and Allocation Working Party (2011) UK experience of liver transplantation for erythropoietic protoporphyria. J Inherit Metab Dis 34: 539-545.
45. Dubrey SW, Ghonim S, Chehab O, and Patel K (2015) Extreme photosensitivity in a patient with erythropoietic protoporphyria. Br J Hosp Med 76: 52-53.
46. Duke SO, Becerrill JM, Sherman TD, Lydon J, and Matsumoto H (1990) The role of protoporphyrin IX in the mechanism of action of diphenyl ether herbicides. Pestic Sci 30: 367-378.
47. Durantini EN (2006) Photodynamic inactivation of bacteria. Curr Bioact Compd 2: 127-142.
48. Fabrikant J, Touloei K, and Brown SM (2013) A review and update on melanocyte stimulating hormone therapy: Afamelanotide. J Drugs Dermatol 12: 775-779.
49. Felsher BF and Redeker AG (1967) Acute intermittent porphyria: Effect of diet and griseofulvin. Medicine 46: 217-223.
50. Fraser DJ, Podvinec M, Kaufmann MR, and Meyer UA (2002) Drugs mediate the transcriptional activation of the 5-aminolevulinic acid synthase (ALAS1) gene via the chicken xenobiotic-sensing nuclear receptor (CXR). J Biol Chem 277: 34717-34726.
51. Fraser DJ, Zumsteg A, and Meyer UA (2003) Nuclear receptors constitutive androstane receptor and pregnane X receptor activate a drug-responsive enhancer of the murine 5-aminolevulinic acid synthase gene. J Biol Chem 278: 39392-39401.
52. Frydman RB and Feinstein G (1974) Studies on porphobilinogen deaminase and uroporphyrinogen 3 cosynthase from human erythrocytes. Biochim Biophys Acta 350: 358-373.
53. Fujita H, Koizumi A, Furusawa T, and Ikeda M (1987) Decreased erythrocyte deltaaminolevulinate dehydratase activity after styrene exposure. Biochem Pharmacol 36: 711-716.
54. Fukuda H, Paredes S, and Batlle AM (1989) Tumor-localizing properties of porphyrins: In vitro studies using the porphyrin precursor, aminolevulinic acid, in free and liposome encapsulated forms. Drug Deliv 5: 133-139.
55. Garg AD, Nowis D, Golab J, and Agostinis P (2010) Photodynamic therapy: Illuminating the road from cell death towards anti-tumour immunity. Apoptosis 15: 1050-1071.
56. Gerhart-Hines Z, Feng D, Emmett MJ, Everett LJ, Loro E, Briggs ER, Bugge A, Hou C, Ferrara C, and Seale P, et al. (2013) The nuclear receptor Rev-erba controls circadian thermogenic plasticity. Nature 503: 410-413.
57. Giger U and Meyer UA (1981) Induction of delta-aminolevulinate synthase and cytochrome P-450 hemoproteins in hepatocyte culture: Effect of glucose and hormones. J Biol Chem 256: 11182-11190.
58. Gold MH and Goldman MP (2004) 5-aminolevulinic acid photodynamic therapy: Where we have been and where we are going. Dermatol Surg 30: 1077-1083; discussion 1083-1074.
59. Goldman MP, Atkin D, and Kincad S (2002) PDT/ALA in the treatment of actinic damage: Real world experience. J Lasers Surg Med 14(s): 24.
60. Gorchein A and Foster GR (1999) Liver failure in protoporphyria: Long-term treatment with oral charcoal. Hepatology 29: 995-996.
61. Gordeuk VR, Brittenham GM, Hawkins CW, Mukhtar H, and Bickers DR (1986) Iron therapy for hepatic dysfunction in erythropoietic protoporphyria. Ann Intern Med 105: 27-31.
62. Goslinski TKK, Piskorz J, Kryjewski M, Wierzehowski M, and Sobiak S (2008) Prospects for photodynamic antimicrobial chemotherapy-PACT. Postepy Mikrobiologii 47: 447-456.
63. Gouya L, Puy H, Lamoril J, Da Silva V, Grandchamp B, Nordmann Y, and Deybach JC (1999) Inheritance in erythropoietic protoporphyria: A common wild-type ferrochelatase allelic variant with low expression accounts for clinical manifestation. Blood 93: 2105-2110.
64. Gross U, Frank M, and Doss MO (1998) Hepatic complications of erythropoietic protoporphyria. Photodermatol Photoimmunol Photomed 14: 52-57.
65. Guernsey DL, Jiang H, Campagna DR, Evans SC, Ferguson M, Kellogg MD, Lachance M, Matsuoka M, Nightingale M, and Rideout A, et al. (2009) Mutations in mitochondrial carrier family gene SLC25A38 cause nonsyndromic autosomal recessive congenital sideroblastic anemia. Nat Genet 41: 651-653.
66. Gupta V, Liu S, Ando H, Ishii R, Tateno S, Kaneko Y, Yugami M, Sakamoto S, Yamaguchi Y, and Nureki O, et al. (2013) Salicylic acid induces mitochondrial injury by inhibiting ferrochelatase heme biosynthesis activity. Mol Pharmacol 84: 824-833.
67. Hamblin MR and Hasan T (2004) Photodynamic therapy: A new antimicrobial approach to infectious disease? Photochem Photobiol Sci 3: 436-450.
68. Handschin C, Lin J, Rhee J, Peyer AK, Chin S, Wu PH, Meyer UA, and Spiegelman BM (2005) Nutritional regulation of hepatic heme biosynthesis and porphyria through PGC-1alpha. Cell 122: 505-515.
69. Harms J, Lautenschlager S, Minder CE, and Minder EI (2009) An alpha-melanocytestimulating hormone analogue in erythropoietic protoporphyria. N Engl J Med 360: 306-307.
70. Henderson BW and Dougherty TJ (1992) How does photodynamic therapy work? Photochem Photobiol 55: 145-157.
71. Holme SA, Whatley SD, Roberts AG, Anstey AV, Elder GH, Ead RD, Stewart MF, Farr PM, Lewis HM, and Davies N, et al. (2009) Seasonal palmar keratoderma in erythropoietic protoporphyria indicates autosomal recessive inheritance. J Invest Dermatol 129: 599-605.
72. Holme SA, Worwood M, Anstey AV, Elder GH, and Badminton MN (2007) Erythropoiesis and iron metabolism in dominant erythropoietic protoporphyria. Blood 110: 4108-4110.
73. Horner ME, Alikhan A, Tintle S, Tortorelli S, Davis DM, and Hand JL (2013) Cutaneous porphyrias part I: Epidemiology, pathogenesis, presentation, diagnosis, and histopathology. Int J Dermatol 52: 1464-1480.
74. Hunter GA and Ferreira GC (2011) Molecular enzymology of 5-aminolevulinate synthase, the gatekeeper of heme biosynthesis. Biochim Biophys Acta 1814: 1467-1473.
75. Ishizuka M, Abe F, Sano Y, Takahashi K, Inoue K, Nakajima M, Kohda T, Komatsu N, Ogura S, and Tanaka T (2011) Novel development of 5-aminolevurinic acid (ALA) in cancer diagnoses and therapy. Int Immunopharmacol 11: 358-365.
76. Jonker JW, Buitelaar M, Wagenaar E, Van Der Valk MA, Scheffer GL, Scheper RJ, Plosch T, Kuipers F, Elferink RP, and Rosing H, et al. (2002) The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci USA 99: 15649-15654.
77. Jonker JW, Musters S, Vlaming ML, Plösch T, Gooijert KE, Hillebrand MJ, Rosing H, Beijnen JH, Verkade HJ, and Schinkel AH (2007) Breast cancer resistance protein (Bcrp1/Abcg2) is expressed in the harderian gland and mediates transport of conjugated protoporphyrin IX. Am J Physiol Cell Physiol 292: C2204-C2212.
78. Jordan PM and Shemin D (1973) Purification and properties of uroporphyrinogen I synthetase from Rhodopseudomonas spheroides. J Biol Chem 248: 1019-1024.
79. Juzeniene A, Iani V, and Moan J (2013) Clearance mechanism of protoporphyrin IX from mouse skin after application of 5-aminolevulinic acid. Photodiagn Photodyn Ther 10: 538-545.
80. Karu T and Letokhov V (1994) Possible benefits of two-quantum excitation in ALAPDT? J Photochem Photobiol B 23: 261-262.
81. Kennedy JC, Pottier RH, and Pross DC (1990) Photodynamic therapy with endogenous protoporphyrin IX: Basic principles and present clinical experience. J Photochem Photobiol B 6: 143-148.
82. Kirton SB, Murray CW, Verdonk ML, and Taylor RD (2005) Prediction of binding modes for ligands in the cytochromes P450 and other heme-containing proteins. Proteins 58: 836-844.
83. Kobuchi H, Moriya K, Ogino T, Fujita H, Inoue K, Shuin T, Yasuda T, Utsumi K, and Utsumi T (2012) Mitochondrial localization of ABC transporter ABCG2 and its function in 5-aminolevulinic acid-mediated protoporphyrin IX accumulation. PLoS One 7: E50082.
84. Kolluri S, Sadlon TJ, May BK, and Bonkovsky HL (2005) Haem repression of the housekeeping 5-aminolaevulinic acid synthase gene in the hepatoma cell line LMH. Biochem J 392: 173-180.
85. Komatsu H, Ishii K, Imamura K, Maruyama K, Yonei Y, Masuda H, Tsuchihashi T, and Sajima Y (2000) A case of erythropoietic protoporphyria with liver cirrhosis suggesting a therapeutic value of supplementation with alpha-tocopherol. Hepatol Res 18: 298-309.
86. Koningsberger JC, Rademakers LH, van Hattum J, de la Faille HB, Wiegman LJ, Italiaander E, van Berge Henegouwen GP, and Marx JJ (1995) Exogenous protoporphyrin inhibits Hep G2 cell proliferation, increases the intracellular hydrogen peroxide concentration and causes ultrastructural alterations. J Hepatol 22: 57-65.
87. Kosenow W (1954) Erythrozyten-Primärfluoreszenz bei Porphyrin-Dermatosen. Med Klin 49: 1099-1103.
88. Kosenow W and Treibs A (1953) [Light hypersensitivity and porphyrinemia]. Z Kinderheilkd 73: 82-92.
89. Krishnamurthy P and Schuetz JD (2011) The role of ABCG2 and ABCB6 in porphyrin metabolism and cell survival. Curr Pharm Biotechnol 12: 647-655.
90. Krishnamurthy PC, Du G, Fukuda Y, Sun D, Sampath J, Mercer KE, Wang J, Sosa- Pineda B, Murti KG, and Schuetz JD (2006) Identification of a mammalian mitochondrial porphyrin transporter. Nature 443: 586-589.
91. Krook G and Haeger-Aronsen B (1982) beta-Carotene in the treatment of erythropoietic protoporphyria: A short review. Acta Derm Venereol Suppl 100: 125-129.
92. Labbé RF, Vreman HJ, and Stevenson DK (1999) Zinc protoporphyrin: A metabolite with a mission. Clin Chem 45: 2060-2072.
93. Langendonk JG, Balwani M, Anderson KE, Bonkovsky HL, Anstey AV, Bissell DM, Bloomer J, Edwards C, Neumann NJ, and Parker C, et al. (2015) Afamelanotide for erythropoietic protoporphyria. N Engl J Med 373: 48-59.
94. Lathrop JT and Timko MP (1993) Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259: 522-525.
95. Lee RG, Avner DL, and Berenson MM (1984) Structure-function relationships of protoporphyrin-induced liver injury. Arch Pathol Lab Med 108: 744-746.
96. Lengweiler S, Kreim S, Barman-Aksözen J, Maurer M, and Minder EI (2015) Evaluation of the immunogenicity of the synthetic a-melanocyte-stimulating hormone (a-MSH) analogue afamelanotide ([Nle4-D-Phe7]-a-MSH, Scenesse®) in erythropoietic protoporphyria patients by ELISA detecting both anti-afamelanotide and anti-a-MSH antibodies. Skin Pharmacol Physiol 28: 103-113.
97. Lewis CA Jr and Wolfenden R (2008) Uroporphyrinogen decarboxylation as a benchmark for the catalytic proficiency of enzymes. Proc Natl Acad Sci USA 105: 17328-17333.
98. Li F, Lu J, Cheng J, Wang L, Matsubara T, Csanaky IL, Klaassen CD, Gonzalez FJ, and Ma X (2013) Human PXR modulates hepatotoxicity associated with rifampicin and isoniazid co-therapy. Nat Med 19: 418-420.
99. Lim HW (1989) Mechanisms of phototoxicity in porphyria cutanea tarda and erythropoietic protoporphyria. Immunol Ser 46: 671-685.
100. Lindblad B, Lindstedt S, and Steen G (1977) On the enzymic defects in hereditary tyrosinemia. Proc Natl Acad Sci USA 74: 4641-4645.
101. Ma J, Xiao S, An J, Wang X, Xu Q, Dong Y, Feng Y, and Wang J (2010) A novel splicing mutation and haplotype analysis of the FECH gene in a Chinese family with erythropoietic protoporphyria. J Eur Acad Dermatol Venereol 24: 726-729.
102. MacCormack MA (2008) Photodynamic therapy in dermatology: An update on applications and outcomes. Semin Cutan Med Surg 27: 52-62.
103. Magnus IA, Jarrett A, Prankerd TA, and Rimington C (1961) Erythropoietic protoporphyria: A new porphyria syndrome with solar urticaria due to protoporphyrinaemia. Lancet 2: 448-451.
104. Mathews-Roth MM, Rosner B, Benfell K, and Roberts JE (1994) A double-blind study of cysteine photoprotection in erythropoietic protoporphyria. Photodermatol Photoimmunol Photomed 10: 244-248.
105. McGuire BM, Bonkovsky HL, Carithers RL, Jr, Chung RT, Goldstein LI, Lake JR, Lok AS, Potter CJ, Rand E, and Voigt MD, et al. (2005) Liver transplantation for erythropoietic protoporphyria liver disease. Liver Transpl 11: 1590-1596.
106. Meerman L (2000) Erythropoietic protoporphyria: An overview with emphasis on the liver. Scand J Gastroenterol Suppl 232: 79-85.
107. Meerman L, Haagsma EB, Gouw AS, Slooff MJ, and Jansen PL (1999a) Long-term follow-up after liver transplantation for erythropoietic protoporphyria. Eur J Gastroenterol Hepatol 11: 431-438.
108. Meerman L, Koopen NR, Bloks V, Van Goor H, Havinga R, Wolthers BG, Kramer W, Stengelin S, Müller M, and Kuipers F, et al. (1999b) Biliary fibrosis associated with altered bile composition in a mouse model of erythropoietic protoporphyria. Gastroenterology 117: 696-705.
109. Melefors O, Goossen B, Johansson HE, Stripecke R, Gray NK, and HentzeMW(1993) Translational control of 5-aminolevulinate synthase mRNA by iron-responsive elements in erythroid cells. J Biol Chem 268: 5974-5978.
110. Meyer-Betz F (1913) Untersuchungen über die biologische (photodynamische) Wirkung des Hämatoporphyrins und anderer Derivate des Blut- und Gallenfarbstoffs. Dtsch Arch Klin Med 122: 476-503.
111. Mfouo-Tynga I and Abrahamse H (2015) Cell death pathways and phthalocyanine as an efficient agent for photodynamic cancer therapy. Int J Mol Sci 16: 10228-10241.
112. Minder EI and Schneider-Yin X (2015) Afamelanotide (CUV1647) in dermal phototoxicity of erythropoietic protoporphyria. Expert Rev Clin Pharmacol 8: 43-53.
113. Minder EI, Schneider-Yin X, Steurer J, and Bachmann LM (2009) A systematic review of treatment options for dermal photosensitivity in erythropoietic protoporphyria. Cell Mol Biol 55: 84-97.
114. Mordon S (2014) A commentary on the role of skin temperature on the effectiveness of ALA-PDT in dermatology. Photodiagn Photodyn Ther 11: 416-419.
115. Mroz P, Hashmi JT, Huang YY, Lange N, and Hamblin MR (2011a) Stimulation of anti-tumor immunity by photodynamic therapy. Expert Rev Clin Immunol 7: 75-91.
116. Mroz P, Szokalska A, Wu MX, and Hamblin MR (2010) Photodynamic therapy of tumors can lead to development of systemic antigen-specific immune response. PLoS One 5: E15194.
117. Mroz P, Yaroslavsky A, Kharkwal GB, and Hamblin MR (2011b) Cell death pathways in photodynamic therapy of cancer. Cancers 3: 2516-2539.
118. Munakata H, Sun JY, Yoshida K, Nakatani T, Honda E, Hayakawa S, Furuyama K, and Hayashi N (2004) Role of the heme regulatory motif in the heme-mediated inhibition of mitochondrial import of 5-aminolevulinate synthase. J Biochem 136: 233-238.
119. Napier I, Ponka P, and Richardson DR (2005) Iron trafficking in the mitochondrion: Novel pathways revealed by disease. Blood 105: 1867-1874.
120. Nelson JC, Westwood M, Allen KR, Newton KE, and Barth JH (1998) The ratio of erythrocyte zinc-protoporphyrin to protoporphyrin IX in disease and its significance in the mechanism of lead toxicity on haem synthesis. Ann Clin Biochem 35: 422-426.
121. Nestor MS, Gold MH, Kauvar AN, Taub AF, Geronemus RG, Ritvo EC, Goldman MP, Gilbert DJ, Richey DF, and Alster TS, et al. (2006) The use of photodynamic therapy in dermatology: Results of a consensus conference. J Drugs Dermatol 5: 140-154.
122. O'Riordan K, Akilov OE, and Hasan T (2005) The potential for photodynamic therapy in the treatment of localized infections. Photodiagn Photodyn Ther 2: 247-262.
123. Oleinick NL and Evans HH (1998) The photobiology of photodynamic therapy: Cellular targets and mechanisms. Radiat Res 150: S146-S156.
124. Oustric V, Manceau H, Ducamp S, Soaid R, Karim Z, Schmitt C, Mirmiran A, Peoc'h K, Grandchamp B, and Beaumont C, et al. (2014) Antisense oligonucleotide-based therapy in human erythropoietic protoporphyria. Am J Hum Genet 94: 611-617.
125. Paoli M, Marles-Wright J, and Smith A (2002) Structure-function relationships in heme-proteins. DNA Cell Biol 21: 271-280.
126. Pass HI (1993) Photodynamic therapy in oncology: Mechanisms and clinical use. J Natl Cancer Inst 85: 443-456.
127. Pastorino JG, Simbula G, Gilfor E, Hoek JB, and Farber JL (1994) Protoporphyrin IX, an endogenous ligand of the peripheral benzodiazepine receptor, potentiates induction of the mitochondrial permeability transition and the killing of cultured hepatocytes by rotenone. J Biol Chem 269: 31041-31046.
128. Podvinec M, Handschin C, Looser R, and Meyer UA (2004) Identification of the xenosensors regulating human 5-aminolevulinate synthase. Proc Natl Acad Sci USA 101: 9127-9132.
129. Poh-Fitzpatrick MB, Wang X, Anderson KE, Bloomer JR, Bolwell B, and Lichtin AE (2002) Erythropoietic protoporphyria: Altered phenotype after bone marrow transplantation for myelogenous leukemia in a patient heteroallelic for ferrochelatase gene mutations. J Am Acad Dermatol 46: 861-866.
130. Proulx KL, Woodard SI, and Dailey HA (1993) In situ conversion of coproporphyrinogen to heme by murine mitochondria: Terminal steps of the heme biosynthetic pathway. Protein Sci 2: 1092-1098.
131. Rand EB, Bunin N, Cochran W, Ruchelli E, Olthoff KM, and Bloomer JR (2006) Sequential liver and bone marrow transplantation for treatment of erythropoietic protoporphyria. Pediatrics 118: E1896-e1899.
132. Rank JM, Carithers R, and Bloomer J (1993) Evidence for neurological dysfunction in end-stage protoporphyric liver disease. Hepatology 18: 1404-1409.
133. Roberts AG and Elder GH (2001) Alternative splicing and tissue-specific transcription of human and rodent ubiquitous 5-aminolevulinate synthase (ALAS1) genes. Biochim Biophys Acta 1518: 95-105.
134. Rollakanti KR, Kanick SC, Davis SC, Pogue BW, and Maytin EV (2013) Techniques for fluorescence detection of protoporphyrin IX in skin cancers associated with photodynamic therapy. Photonics Lasers Med 2: 287-303.
135. Rouault TA and Tong WH (2005) Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol 6: 345-351.
136. Sadlon TJ, Dell'Oso T, Surinya KH, and May BK (1999) Regulation of erythroid 5-aminolevulinate synthase expression during erythropoiesis. Int J Biochem Cell Biol 31: 1153-1167.
137. Samuel D, Boboc B, Bernuau J, Bismuth H, and Benhamou JP (1988) Liver transplantation for protoporphyria: Evidence for the predominant role of the erythropoietic tissue in protoporphyrin overproduction. Gastroenterology 95: 816-819.
138. Sassa S and Granick S (1970) Induction of -aminolevulinic acid synthetase in chick embryo liver cells in cluture. Proc Natl Acad Sci USA 67: 517-522.
139. Sawyer TK, Sanfilippo PJ, Hruby VJ, Engel MH, Heward CB, Burnett JB, and Hadley ME (1980) 4-Norleucine, 7-D-phenylalanine-alpha-melanocyte-stimulating hormone: A highly potent alpha-melanotropin with ultralong biological activity. Proc Natl Acad Sci USA 77: 5754-5758.
140. Scassa ME, Varone CL, Montero L, and Cánepa ET (1998) Insulin inhibits deltaaminolevulinate synthase gene expression in rat hepatocytes and human hepatoma cells. Exp Cell Res 244: 460-469.
141. Schauder A, Avital A, and Malik Z (2010) Regulation and gene expression of heme synthesis under heavy metal exposure-review. J Environ Pathol Toxicol Oncol 29: 137-158.
142. Schwartz S, Raux WA, Schacter BA, Stephenson BD, and Shoffner RN (1980) Loss of hereditary uterine protoporphyria through chromosomal rearrangement in mutant Rhode Island red hens. Int J Biochem 12: 935-940.
143. Shaw GC, Cope JJ, Li L, Corson K, Hersey C, Ackermann GE, Gwynn B, Lambert AJ, Wingert RA, and Traver D, et al. (2006) Mitoferrin is essential for erythroid iron assimilation. Nature 440: 96-100.
144. Shimizu Y, Ida S, Naruto H, and Urata G (1978) Excretion of porphyrins in urine and bile after the administration of delta-aminolevulinic acid. J Lab Clin Med 92: 795-802.
145. Sinclair PR, Gorman N, Walton HS, Sinclair JF, Jacobs JM, and Jacobs NJ (1994) Protoporphyrinogen accumulation in cultured hepatocytes treated with the diphenyl ether herbicide, acifluorfen. Cell Mol Biol 40: 891-897.
146. Singal AK, Parker C, Bowden C, Thapar M, Liu L, and McGuire BM (2014) Liver transplantation in the management of porphyria. Hepatology 60: 1082-1089.
147. Smith KM (1979) Protoporphyrin IX: Some recent research. Acc Chem Res 12: 374-381.
148. Smith LJ, Kahraman A, and Thornton JM (2010) Heme proteins-diversity in structural characteristics, function, and folding. Proteins 78: 2349-2368.
149. Smith SJ and Cox TM (1997) Translational control of erythroid deltaaminolevulinate synthase in immature human erythroid cells by heme. Cell Mol Biol 43: 103-114.
150. Solazzo M, Fantappiè O, D'Amico M, Sassoli C, Tani A, Cipriani G, Bogani C, Formigli L, and Mazzanti R (2009) Mitochondrial expression and functional activity of breast cancer resistance protein in different multiple drug-resistant cell lines. Cancer Res 69: 7235-7242.
151. Szechcinski J, Skoczy-nska A, and Andreasik Z (1986) [Liver cirrhosis in congenital erythropoietic protoporphyria]. Pol Tyg Lek 41: 899-901.
152. Taketani S, Kohno H, Okuda M, Furukawa T, and Tokunaga R (1994) Induction of peripheral-type benzodiazepine receptors during differentiation of mouse erythroleukemia cells: A possible involvement of these receptors in heme biosynthesis. J Biol Chem 269: 7527-7531.
153. Thapar M and Bonkovsky HL (2008) The diagnosis and management of erythropoietic protoporphyria. Gastroenterol Hepatol 4: 561-566.
154. Tian Q, Li T, Hou W, Zheng J, Schrum LW, and Bonkovsky HL (2011) Lon peptidase 1 (LONP1)-dependent breakdown of mitochondrial 5-aminolevulinic acid synthase protein by heme in human liver cells. J Biol Chem 286: 26424-26430.
155. Tintle S, Alikhan A, Horner ME, Hand JL, and Davis DM (2014) Cutaneous porphyrias part II: Treatment strategies. Int J Dermatol 53: 3-24.
156. Todd DJ (1991) Gallstones in children. Am J Dis Child 145: 971-972.
157. Troadec MB,Warner D,Wallace J, Thomas K, Spangrude GJ, Phillips J, Khalimonchuk O, Paw BH, Ward DM, and Kaplan J (2011) Targeted deletion of the mouse Mitoferrin1 gene: From anemia to protoporphyria. Blood 117: 5494-5502.
158. Van Hattum J, Baart de la Faille H, Van den Berg JW, Edixhoven-Bosdijk A, and Wilson JH (1986) Chenodeoxycholic acid therapy in erythrohepatic protoporphyria. J Hepatol 3: 407-412.
159. Varone CL, Giono LE, Ochoa A, Zakin MM, and Cánepa ET (1999) Transcriptional regulation of 5-aminolevulinate synthase by phenobarbital and cAMP-dependent protein kinase. Arch Biochem Biophys 372: 261-270.
160. Wahlin S, Floderus Y, Stål P, and Harper P (2011a) Erythropoietic protoporphyria in Sweden: Demographic, clinical, biochemical and genetic characteristics. J Intern Med 269: 278-288.
161. Wahlin S and Harper P (2010) The role for BMT in erythropoietic protoporphyria. Bone Marrow Transplant 45: 393-394.
162. Wahlin S, Stal P, Adam R, Karam V, Porte R, Seehofer D, Gunson BK, Hillingsø J, Klempnauer JL, and Schmidt J, et al.; European Liver and Intestine Transplant Association (2011b) Liver transplantation for erythropoietic protoporphyria in Europe. Liver Transpl 17: 1021-1026.
163. Warren LJ and George S (1998) Erythropoietic protoporphyria treated with narrowband (TL-01) UVB phototherapy. Australas J Dermatol 39: 179-182.
164. Wendler G, Lindemann P, Lacapère JJ, and Papadopoulos V (2003) Protoporphyrin IX binding and transport by recombinant mouse PBR. Biochem Biophys Res Commun 311: 847-852.
165. Whatley SD, Ducamp S, Gouya L, Grandchamp B, Beaumont C, Badminton MN, Elder GH, Holme SA, Anstey AV, and Parker M, 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.
166. Whitcombe DM, Carter NP, Albertson DG, Smith SJ, Rhodes DA, and Cox TM (1991) Assignment of the human ferrochelatase gene (FECH) and a locus for protoporphyria to chromosome 18q22. Genomics 11: 1152-1154.
167. Wingert RA, Galloway JL, Barut B, Foott H, Fraenkel P, Axe JL, Weber GJ, Dooley K, Davidson AJ, and Schmid B, et al.; Tübingen 2000 Screen Consortium (2005) Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature 436: 1035-1039.
168. Wu N, Yin L, Hanniman EA, Joshi S, and Lazar MA (2009) Negative feedback maintenance of heme homeostasis by its receptor, Rev-erbalpha. Genes Dev 23: 2201-2209.
169. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, and Scarpulla RC, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
170. Yamamoto M, Arimura H, Fukushige T, Minami K, Nishizawa Y, Tanimoto A, Kanekura T, Nakagawa M, Akiyama S, and Furukawa T (2014) Abcb10 role in heme biosynthesis in vivo: Abcb10 knockout in mice causes anemia with protoporphyrin IX and iron accumulation. Mol Cell Biol 34: 1077-1084.
171. Zheng J, Shan Y, Lambrecht RW, Donohue SE, and Bonkovsky HL (2008) Differential regulation of human ALAS1 mRNA and protein levels by heme and cobalt protoporphyrin. Mol Cell Biochem 319: 153-161.
172. Zhou S, Zong Y, Ney PA, Nair G, Stewart CF, and Sorrentino BP (2005) Increased expression of the Abcg2 transporter during erythroid maturation plays a role in decreasing cellular protoporphyrin IX levels. Blood 105: 2571-2576.