Protoporphyrin IX generation from δ-aminolevulinic acid elicits pulmonary artery relaxation and soluble guanylate cyclase activation

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 291, Issue 3, 2006, Pages

  Mingone, Christopher J ^a   Gupte, Sachin A ^a   Chow, Joseph L ^a   Ahmad, Mansoor ^a   Abraham, Nader G ^a   Wolin, Michael S ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Guanosine 3 ,5 cyclic monophosphate; Heme metabolism; Iron; Vasodilation

Indexed keywords

1H (1,2,4)OXADIAZOLO(4,3 A)QUINOXALIN 1 ONE; AMINOLEVULINIC ACID; CYCLIC GMP; DEFEROXAMINE; FERROUS SULFATE; GUANYLATE CYCLASE; HEME; NITROUS OXIDE; PROTOPORPHYRIN; QUINOXALINE DERIVATIVE; SEROTONIN; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL TISSUE; BLOOD VESSEL REACTIVITY; CONTROLLED STUDY; COW; DRUG EFFECT; ENZYME ACTIVATION; EPIFLUORESCENCE MICROSCOPE; LUNG ARTERY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW;

AMINOLEVULINIC ACID; ANIMALS; CATTLE; DEFEROXAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GUANYLATE CYCLASE; HEME; IRON; MODELS, BIOLOGICAL; ORGAN CULTURE TECHNIQUES; OXIDATION-REDUCTION; PHOTOSENSITIZING AGENTS; PROTOPORPHYRINS; PULMONARY ARTERY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SEROTONIN; VASODILATION;

EID: 33748437538     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00482.2005     Document Type: Review

References (34)

1. Abraham NG, Camadro JM, Hoffstein ST, and Levere RD. Effects of iron deficiency and chronic iron overloading on mitochondrial heme biosynthetic enzymes in rat liver. Biochim Biophys Acta 870: 339-349, 1986.
2. Archer SL, Huang JM, Hampl V, Nelson DP, Shultz PJ, and Weir EK. Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin-sensitive K channel by cGMP-dependent protein kinase. Proc Natl Acad Sci USA 91: 7583-7587, 1994.
3. Atamna H, Killilea DW, Killilea AN, and Ames BN. Heme deficiency may be a factor in the mitochondrial and neuronal decay of aging. Proc Natl Acad Sci USA 99: 14807-14812, 2002.
4. Brune B and Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 32: 497-504, 1987.
5. Burstyn JN, Yu AE, Dierks EA, Hawkins BK, and Dawson JH. Studies of the heme coordination and ligand binding properties of soluble guanylyl cyclase (sGC): characterization of Fe(II)sGC and Fe(II)sGC(CO) by electronic absorption and magnetic circular dichroism spectroscopies and failure of CO to activate the enzyme. Biochemistry 34: 5896-5903, 1995.
6. Craven PA and DeRubertis FR. Requirement for heme in the activation of purified guanylate cyclase by nitric oxide. Biochim Biophys Acta 745: 310-321, 1983.
7. Dalton JT, Yates CR, Yin D, Straughn A, Marcus SL, Golub AL, and Meyer MC. Clinical pharmacokinetics of 5-aminolevulinic acid in healthy volunteers and patients at high risk for recurrent bladder cancer. J Pharmacol Exp Ther 301: 507-512, 2002.
8. Foresti R, Hammad J, Clark JE, Johnson TR, Mann BE, Friebe A, Green CJ, and Motterlini R. Vasoactive properties of CORM-3, a novel water-soluble carbon monoxide-releasing molecule. Br J Pharmacol 142: 453-460, 2004.
9. Gerzer R, Bohme E, Hofmann F, and Schultz G. Soluble guanylate cyclase purified from bovine lung contains heme and copper. FEBS Lett 132: 71-74, 1981.
10. Granick S. The induction in vitro of the synthesis of delta-aminolevulinic acid synthetase in chemical porphyria: a response to certain drugs, sex hormones, and foreign chemicals. J Biol Chem 241: 1359-1375, 1966.
11. Gupte SA, Rupawalla T, Phillibert D Jr, and Wolin MS. NADPH and heme redox modulate pulmonary artery relaxation and guanylate cyclase activation by NO. Am J Physiol Lung Cell Mol Physiol 277: L1124-L1132, 1999.
12. Hassoun PM, Filippov G, Fogel M, Donaldson C, Kayyali US, Shimoda LA, and Bloch KD. Hypoxia decreases expression of soluble guanylate cyclase in cultured rat pulmonary artery smooth muscle cells. Am J Respir Cell Mol Biol 30: 908-913, 2004.
13. Herman MA, Webber J, Fromm D, and Kessel D. Hemodynamic effects of 5-aminolevulinic acid in humans. J Photochem Photobiol B 43: 61-65, 1998.
14. Hosein S, Marks GS, Brien JF, McLaughlin BE, and Nakatsu K. An extracellular source of heme can induce a significant heme oxygenase mediated relaxation in the rat aorta. Can J Physiol Pharmacol 80: 761-765, 2002.
15. Iesaki T, Gupte SA, and Wolin MS. A flavoprotein mechanism appears to prevent an oxygen-dependent inhibition of cGMP-associated nitric oxide-elicited relaxation of bovine coronary arteries. Circ Res 85: 1027-1031, 1999.
16. Ignarro LJ, Ballot B, and Wood KS. Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins. J Biol Chem 259: 6201-6207, 1984.
17. Ignarro LJ, Burke TM, Wood KS, Wolin MS, and Kadowitz PJ. Association between cyclic GMP accumulation and acetylcholine-elicited relaxation of bovine intrapulmonary artery. J Pharmacol Exp Ther 228: 682-690, 1984.
18. Ignarro LJ, Byrns RE, Buga GM, and Wood KS. Mechanisms of endothelium-dependent vascular smooth muscle relaxation elicited by bradykinin and VIP. Am J Physiol Heart Circ Physiol 253: H1074-H1082, 1987.
19. Ignarro LJ, Wood KS, and Wolin MS. Activation of purified soluble guanylate cyclase by protoporphyrin IX. Proc Natl Acad Sci USA 79: 2870-2873, 1982.
20. Ignarro LJ, Wood KS, and Wolin MS. Regulation of purified soluble guanylate cyclase by porphyrins and metalloporphyrins: a unifying concept. Adv Cyclic Nucleotide Protein Phosphorylation Res 17: 267-274, 1984.
21. Jenkins MP, Buonaccorsi G, MacRobert A, Bishop CC, Bown SG, and McEwan JR. Intra-arterial photodynamic therapy using 5-ALA in a swine model. Eur J Vasc Endovasc Surg 16: 284-291, 1998.
22. Johnson FK and Johnson RA. Carbon monoxide promotes endothelium-dependent constriction of isolated gracilis muscle arterioles. Am J Physiol Regul Integr Comp Physiol 285: R536-R541, 2003.
23. Lincoln TM, Dey N, and Sellak H. Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression. J Appl Physiol 91: 1421-1430, 2001.
24. Mansfield R, Bown S, and McEwan J. Photodynamic therapy: shedding light on restenosis. Heart 86: 612-618, 2001.
25. Mingone CJ, Gupte SA, Ali N, Oeckler RA, and Wolin MS. Thiol oxidation inhibits nitric oxide-mediated pulmonary artery relaxation and guanylate cyclase stimulation. Am J Physiol Lung Cell Mol Physiol 290: L549-L557, 2006.
26. Mingone CJ, Gupte SA, Iesaki T, and Wolin MS. Hypoxia enhances a cGMP-independent nitric oxide relaxing mechanism in pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 285: L296-L304, 2003.
27. Moesta KT, Ebert B, Handke T, Nolte D, Nowak C, Haensch WE, Pandey RK, Dougherty TJ, Rinneberg H, and Schlag PM. Protoporphyrin IX occurs naturally in colorectal cancers and their metastases. Cancer Res 61: 991-999, 2001.
28. Nyamekye I, Anglin S, McEwan J, MacRobert A, Bown S, and Bishop C. Photodynamic therapy of normal and balloon-injured rat carotid arteries using 5-amino-levulinic acid. Circulation 91: 417-425, 1995.
29. Schrammel A, Behrends S, Schmidt K, Koesling D, and Mayer B. Characterization of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a heme-site inhibitor of nitric oxide-sensitive guanylyl cyclase. Mol Pharmacol 50: 1-5, 1996.
30. Smits T, Robles CA, van Erp PE, van de Kerkhof PC, and Gerritsen MJ. Correlation between macroscopic fluorescence and protoporphyrin IX content in psoriasis and actinic keratosis following application of aminolevulinic acid. J Invest Dermatol 125: 833-839, 2005.
31. Stone JR and Marletta MA. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 33: 5636-5640, 1994.
32. Taketani S, Adachi Y, and Nakahashi Y. Regulation of the expression of human ferrochelatase by intracellular iron levels. Eur J Biochem 267: 4685-4692, 2000.
33. Tzao C, Nickerson PA, Russell JA, Gugino SF, and Steinhorn RH. Pulmonary hypertension alters soluble guanylate cyclase activity and expression in pulmonary arteries isolated from fetal lambs. Pediatr Pulmonol 31: 97-105, 2001.
34. Wolin MS, Wood KS, and Ignarro LJ. Guanylate cyclase from bovine lung. A kinetic analysis of the regulation of the purified soluble enzyme by protoporphyrin IX, heme, and nitrosyl-heme. J Biol Chem 257: 13312-13320, 1982.