HISTORICAL BACKGROUND OF PHOTODYNAMIC THERAPY (PDT) BIOLOGICAL EVIDENCE FOR HEMATOPORPHYRIN AS A PDT DRUG
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1 HISTORICAL BACKGROUND OF PHOTODYNAMIC THERAPY (PDT) MECHANISTIC STUDIES IN PHOTODYNAMIC THERAPY Lisa Johnson 903- Niels Finsen is awarded the Nobel Prize for using light to treat Small Pox and TB 903- Tappeiner and Jesionek treated skin cancer with eosin 93- Friedrich Meyer-Betz used hematoporphyrin on his hands 955- Samuel Swartz developed Hematoporphyrin Derivative (HPD) 960- Lipson and Blades studied HPD in tumor cells 972- I. Diamond demonstrated phototoxicity of hematoporphyrin in gliomas 978- Dougherty performed the first clinical trials 999- The first PDT drug was approved 2 Dolmans, D; Fukumura, D; Jain, RK. Photodynamic therapy for cancer. Nat. Rev. Cancer, 2003, 3, BENEFITS OF PDT AS A TREATMENT FOR CANCER BIOLOGICAL EVIDENCE FOR HEMATOPORPHYRIN AS A PDT DRUG Dual Selectivity Non-invasive Multiple biological effects Timing Cancer Cells -increased vasculature -retention of some compounds Dolmans, D; Fukumura, D; Jain, RK. Photodynamic therapy for cancer. Nat. Rev. Cancer, 2003, 3, Lysed blood cells 9 W. Hausman Caused tissue necrosis 93 F. Meyer-Betz Derivatives ves had more activity ty Hematoporphyrin 955- S. Swartz Accumulated in tumors HPD 960- Lipson and Baldes Killed gliomas both in vitro and in vivo 972- I. Diamond Treated patients 975- T. Dougherty and J.F. Kelly Dolmans, D; Fukumura, D; Jain, RK. Photodynamic therapy for cancer. Nat. Rev. Cancer, 2003, 3, PROBLEMS WITH HEMATOPORPHYRIN DERIVATIVE BIOLOGISTS IDENTIFIED THREE NECESSARY COMPONENTS FOR PDT IN VIVO Complex Mixture that was hard to reproduce Weak absorption at 630 nm (ε =,7070 M - cm - ) Side effects increased sensitivity to sunlight HPLC trace of HPD Photosensitizer absorbs between nm Light Oxygen 5 Bonnet, Raymon. Chemical Aspects of Photodynamic Therapy. Gordon and Breach Science Publishers: Australia, Castano, A; Demidova, T; Hamblin, M. Photodiagnosis and Photodynamic Therapy, 2004,,
2 TWO MECHANISMS PROPOSED TO EXPLAIN OXYGEN DEPENDENCE JABLONSKI DIAGRAM OF REACTION Type I (O 2 ) Mechanism OR To improve the next generation of PDT drugs, the photochemical mechanism should be known To determine the photochemical mechanism, chemical tools need to discriminate between O 2 and O 2 7 Castano, A; Demidova, T; Hamblin, M. Photodiagnosis and Photodynamic Therapy, 2004,, Type II ( O 2 ) Mechanism 8 THE COMPARISON BETWEEN THE TWO REACTIVE OXYGEN SPECIES O 2 Type I O 2 Type II Electron Transfer/ Energy Transfer Hydrogen abstraction Dependent on Radical Dependent O 2 Formation formation Distinguishing between O 2 and O 2 is difficult 9 ACTIVATORS AND INHIBITORS OF TYPE I (O 2 ) MECHANISM Activator Nicotinamide Adenine Dinucleotide (NADH/NAD + ) good reducing agent Inhibitor Enzyme Superoxide Dismutase (SOD) substrate is superoxide 0 DATA FOR TYPE I (O 2 ) ACTIVATION WITH NADH Many PDT drugs localize in the mitochondria, where NADH concentrations are high Qualitative Assessment verteporfin INHIBITORS OF TYPE II ( O 2 ) MECHANISM Chemical Reactions: 2+2, Diels-Alder, Ene Quenchers- tertiary amines and β-carotene light NADH (absorption 350 nm, excitation 450 nm) Pogue, B; Pitts, J; Mycek, MA; Sloboda, RD; Wilmot, CM; Brandsema, JF; O Hara, JA. Photochem. Photobiol. 200, 74, Bonnet, Raymon. Chemical Aspects of Photodynamic Therapy. Gordon and Breach Science Publishers: Australia,
3 EVIDENCE THAT HPD GOES THROUGH A TYPE II ( O 2 ) MECHANISM HPD Cancer Cell HPD & DPF Hematoporphyrin Derivative (HPD),3 diphenylisobenzyl- furan (DPF) THE COMPARISON BETWEEN THE TWO REACTIVE OXYGEN SPECIES O 2 Type I O 2 Type II Electron Transfer/ Energy Transfer Hydrogen abstraction Dependent on Radical Formation Activator: NADH Dependent O 2 formation Inhibitors: Molecules l Inhibitor: Superoxide Dismutase that can react via the 4+2, 2+2, and ene Dies Lives Weishaupt, KR; Gomer, CJ; Dougherty, TJ. J. Cancer Res. 976, 36, DETECTION OF RADICALS WITH ELECTRON SPIN RESONANCE (ESR) SPECTROSCOPY Microwave frequencies to excite electron spin states Similar to NMR g-factor (chemical shift) hyperfine splitting (J-coupling) interaction with nuclear spin states CHALLENGE OF NITROXIDE ESR SPECTRA FOR TYPE I (O 2 ) MEASUREMENTS t /2 = min t /2 =60 min 5 Nishizawa, M; Shioji, K; Kurauchi, Y; Okuma, K; Kohno, M. Bull. Chem. Soc. Jpn. 2007, 80, EVIDENCE THAT HPD GOES THROUGH TYPE II ( O 2 ) MECHANISM USING ESR SOLVENT AFFECTS THE O 2 LIFETIME (μμ) TEMPO Luminescence at 270 nm (near-ir) dependence on solvent IR vibrations ( O-H and C-H) Considered the best evidence for O 2 Solvent H 2 O 3.8 MeOH 0 D 2O 62 C 6 H 6 30 C 6 D C 6 F CHCl Lifetime of O 2 (μs) All solutions contain 00 mm TEMP and mm HPD in Phosphate Buffer at ph 7.4 Ando, T; Yoshikawa, T; Tanigawa, T; Kohno, M; Yoshida, N; Kondo, M. Life Sciences, 997, 6, Foote, CS; Valentine, JS; Greenberg, A; Leibman JF. Active Oxygen in Chemistry, Blackie Academic and Professional: London,
4 THE COMPARISON BETWEEN THE TWO REACTIVE OXYGEN SPECIES O 2 Type I O 2 Type II Electron Transfer/ Energy Transfer Hydrogen abstraction Dependent on Radical Formation Activators: NADH Dependent O 2 formation Inhibitors: Molecules l Inhibitors: Superoxide Dismutase ESR can detect nitroxide-ooh adduct that can react via the 4+2, 2+2, and ene Luminescence at 270 nm HPD WAS THE FIRST GENERATION FOR PDT PHOTOSENSITIZERS Hematoporphyrin Derivative was first identified based on its biological activity, and further experiments suggest it favors a Type II ( O 2 ) Mechanism. The reverse strategy would be to think of a molecule with good photochemical properties and test it for biological activity. triplet state lifetime quantum yield of O 2 and O EXAMPLE OF AN EFFICIENT PHOTOSENSITIZER: FULLERENES FULLERENES: C 60 /PVP FAVORS A TYPE I (O 2 ) MECHANISM Advantages high quantum yield of O 2 (~.0) Triplet State lifetime i ~ μs ISC ~0 8 s - Capable of functionalizing Disadvantages Absorbance is low and in the wrong range ( nm) Solubility Formulation: 5% polyvinylpyrrolidone/h 2 O Micelle system Tests Cleave DNA O 2 Luminescence ESR C 60 /PVP Mroz, P; Tegos, GP; Gali, H; Wharton, T; Sarna, T; Hamblin, MR. Photochem. Photobiol. Sci. 2007, 6, Yamakoshi, Y; Umezawa, N; Ryu, A; Arkane, K; Miyata, N; Goda, Y; Masumizu, T; Nagano, T. J Am. Chem. Soc. 2003, 25, PLASMID DNA ASSAY SUGGESTS THAT C 60 /PVP REACTS VIA A TYPE I (O 2 ) MECHANISM Two Possible Forms of DNA Form I (supercoiled)& Form II (nicked) Form I hυ C 60 /PVP, NADH Form II NEAR IR LUMINESCENCE SUGGESTS THAT C 60 /PVP DOES NOT REACT VIA A TYPE II ( O 2 ) MECHANISM Near Infrared Luminescence at 270 nm not detectable C 60 in PVP/H 2 O Sodium Azide, Histidine, and 2,5-dimethylfuran show only form I 23 Does not generate O 2 in aqueous environment 24 JACS. 2003, 25, JACS. 2003, 25,
5 ESR SPECTRA OF 4-OXO-TEMP SUGGEST THE MECHANISM IS NOT TYPE II ( O 2 ) FOR C 60 /PVP ESR SPECTRA OF DMPO & DEPMPO SUGGEST THE MECHANISM IS TYPE I (O 2 ) FOR C 60 /PVP a) TEMPO b) TEMPO signal with signal with Rose Bengal C 60 /PVP a) d) Assumption: Signal is produced by O JACS. 2003, 25, JACS. 2003, 25, Bull. Chem. Soc. Jpn. 2007, 80, DATA FAVORS A TYPE I (O 2 ) MECHANISM FOR C 60 /PVP Cleave DNA (favor Type I) O 2 Luminescence (Not Type II) ESR 4-oxo-TEMP (Not Type II) DEPMPO (Favor Type I) MONO-PYRROLIDINIUM C 60 HAS PHOTODYNAMIC ACTIVITY AGAINST CANCER CELLS Breaking aromaticity reduced O 2 yields shorter triplet state lifetimes reduced absorbance Biologically Active Death Cancer Cell All evidence is consistent 27 Light Energy Mroz, P; Pawlak, A; Satti, M; Lee, H; Wharton, T; Gali, H; Sarna, T; Hamblin, MR. Free Radic. Biol. Med. 2007, 43, QUANTUM YIELD OF O 2 MEASURED BY TIME DECAY CURVES OF O 2 LUMINESCENCE AT 270 NM Solvent O 2 quantum yield Deuterated Methanol D 2 O (PBS) 0.27 not detectable DETECTION OF DMPO-OOH WITH ADDITIVES FOR TYPE I AND TYPE II MECHANISMS Detecting Superoxide Type I BF4 BF4 BF4 produces O 2 weakly in methanol, but not in D 2 O Evidence against a O 2 Type II Mechanism Free Radic. Biol. Med. 2007, 43, Additive Histidine inhibits Type II NADH activates Type I No Controls Data is inconclusive Free Radic. Biol. Med. 2007, 43,
6 ESR OXIMETRY DATA FAVORS A TYPE II ( O 2 ) MECHANISM BF4 Not Significantly Different Significantly Different DATA FOR MONO-PYRROLIDINIUM FULLERENE WEAKLY FAVORS TYPE II ( O 2 ) Results O 2 luminescence (only in CH 3 OD) ESR with DMPO-OOH (inconclusive) ESR Oximetry (Favors Type II) The preferred method in the field Conclusion: Type I & II Broadening due to O 2 Free Radic. Biol. Med. 2007, 43, Halpern, H; Peric, M; Nguyen, TD, Spencer, D. J. Magn. Reson. 990, 90, SUMMARY Improving purity of possible PDT therapeutics and using a diverse set of structures as photosensitizers Improving experiments that distinguish Type I (O 2 ) versus Type II ( O 2 ) multiple tests Expanding the knowledge of using photosensitizers, light, and oxygen to cure certain forms of cancer FUTURE OF PDT Use Fluorescence to determine PDT drug concentration in the tumor Two Photon photosensitizers Ruthenium Complexes that release NO Photosensitizers conjugated to antibodies and sugars Tailoring the photosensitizer for specific forms of cancer (bronchial, skin, bladder, etc) ACKNOWLEDGEMENTS Sam Gellman The Gellman Group Jay, Matt, Brooke, Aaron, Pil Seok, Seth, Mike, Li, Brendan, Kim, Holly, Jonathan, Emily, Nikki, Soo Hyuk Practice Talk Attendees The Gellman Group Danielle CBI 35 6
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