PHOTOBIOLOGY The Science and Its Applications

Edited by

Emanuel Riklis Israel Atomic E n e r g y Commlssion B e e r - S h e v a , Israel

PLENUM PRESS • NEW YORK AND LONDON

Contents

Opening of the Congress R. Latarjet, Honorary P r e s i d e n t 1

AIP Presidential Lecture: Themes and Trends in Photobiology K . K . R o h a t g i - M u k h e r j e e 3

A Half Century of Photobiology: The Alexander Hollaender Memorial Symposium Alexander Hollaender (1898-1986)

R. L a t a r j e t 15 Alexander Hollaender: The Man and His Work

R . B . Setlow 17 Defective DNA Repair and Human Disease

A . R. L e h m a n n 21 DNA-Protein Crosslinking in UV-Irradiated Human and ICR 2A Cell Lines

B . S. Rosenstein a n d L i - W e n L a i 27 Retroviral Based Shuttle Vectors and Endogenous Cellular Genes: Complementary

Approaches for Investigations of Mutational Specificity E . A . D r o b e t s k y , AJ. Grosovsky, A . S k a n d a l i s , L . R. Shekter

and B . W. G l i c k m a n 35

Ultraviolet and Ionizing Radiations: From Molecules to Cells Photobiology and Radiobiology: Divisions and Common Ground

J . Z. Beer 43 Comparative Effects of Ultraviolet and Ionizing Radiations on Nucleic Acids

/. Cadet, M. B e r g e r , P . C. J o s h i , A . Shaw, L . Voituriez, L . - S i n g K a n a n d R. W a g n e r 49

Interaction Between Ultraviolet and Ionizing Radiation in Eukaryotic Cells J . Kiefer 61

xi

A Molecular Model for the Cytotoxic Action of UV and Ionizing Radiation H . P . Leenhouts and K H . Chadwick 71

Mutagenic Effects of Ultraviolet and Ionizing Radiation H . H . Evans 83

Malignant Transformation by Ultraviolet and Ionizing Radiations J . B . L i n i e 97

Between Ultraviolet and Ionizing Radiation: Action Spectra for Cytotoxicity in the Vacuum-UV Region

T. I t o 105

UV Light and DNA Damage, Repair and Mutagenesis Brief Methodological Survey of the Photochemistry of Nucleic Acid Constituents and

Analogues, and Some Biological Applications, Including Photo-Affinity Labeling D . Shugar, B . Kierdaszuk and R. S t o l a r s k i 115

The Sequence Specificity of Ultraviolet Light Damage to DNA Containing Bromodeoxyuridine or Iododeoxyuridine V. Murray and R. F . Martin 135

UV-Light Induced Perturbation of DNA Tertiary Structure: Consequences on the Enzymes Controlling Chromosome Superhelicity A M . P e d r i n i , F . S p i r i t o , a n d S. T o r n a l e t t i 141

Excision-Repair Capacity in UV Irradiated Strains of S. pneumoniae A . M. Estevenon and N . S i c a r d 149

UV-Inducible Repair in Yeast F . E c k a r d t - S c h u p p , A . Ahne, S. O b e r m a i e r a n d S. Wendel 155

Mutant 112X86 Versus Wild-Type L a c Repressor Photochemistry M . Spotheim-Maurizot, F . C u l a r d , P . G r e b e r t , J . - C . Maurizot and M. C h a r l i e r 163

M/nwC-Independent, recA-Dependent Mutagenesis K . C. Smith and N . J . S a r g e n t i n i 169

What Is The Molecular Mechanism Of UV Mutagenesis in E s c h e r i c h i a coli? J . R. B a t t i s t a , T. N o h m i , C. E. D o n n e l l y , and G. C.Walker 177

Ultraviolet Mutagenesis of a Shuttle Vector Plasmid in Repair Proficient and Deficient Human Cells M.M. Seidman, D . B r a s h , S. S e t t h a r a m , K M . K r a e m e r and A . B r e d b e r g 183

Mutational Hotspots in Mammalian Cells C h a r l e s R. Ashman 193

Spectra of Mutations Induced by Structurally-Related Aromatic Polycyclic Carcinogens during Replication of a Shuttle Vector in Human Cells V. M. Mäher, J - L . Yang, M . C-M. M a h , a n d JJ. M c C o r m i c k 199

Twenty Years of Research on Xeroderma Pigmentosum at the National Institutes of Health K . H . K r a e m e r 211

xii

The Edna Roe Memorial Lecture Repair Control of Photoinduced Cross-Links and Monoadducts in DNA:

Genetic, Molecular and Evolutionary Features E . M o u s t a c c h i 223

Photochemistry and Photophysics: Probing the Unknown Pulse Radiolysis and Flash Photolysis

T.G. T r u s c o t t 237 Discrimination and Coverage in Hybridization: Advantages Afforded by Crosslinkable

Oligonucleotide Probes G. D . C i m i n o , H . B . Gamper, M. F e r g u s o n , S. T. Isaacs and J . E . Hearst 249

The Analytical Uses of Luminescence G. G a b o r 267

Electric Parameters of Purple Membrane Fragments S.G. T a n e v a a n d L B . P e t k a n c h i n 277

Probing the Internal Spectral Distribution of UV Radiation in Plants with Fibre Optics J.F. B o r n m a n and T.C. Vogelmann 287

Cancer Diagnosis by Fluorescence Polarization A . W e i n r e b , M. D e u t s c h and S. C h a i t c h i k 293

Microspectrofluorometry of Human Melanoma Cells and Fibroblasts Treated with Azelaic Acid E . K o h e n , C. K o h e n , D . O . Schachtschabel, J . G . H i r s c h b e r g , B . L . Shapiro and A . M c h e i l e h 305

Recent Advances in Chemical Modeling of Bacterial Bioluminescence Mechanism S.-C. T u a n d H I . X . M a g e r 319

Use of Image Analysis in Photobiology D - P . Hader 329

Degradation of Oligonucleotides and DNA by VUV Radiation in Solids T. I t o 345

Photolysis of Water by VUV Radiation and Reactions with DNA and Related Compounds in Aqueous Systems M. K u w a b a r a , A . M i n e g i s h i , K . T a k a k u r a , K . Hieda and T. I t o 355

Light Regulated Biological Processes — Photosynthesis Trapping of Excitation Energy in Photosynthetic Purple Bacteria

R. v a n G r o n d e l l e , H . Bergström and V. Sundström 367 The Supramolecular Structure of the Light-Harvesting System of Cyanobacteria and Red

Algae E . Mörschel, G.-H. Schatz, W. L a n g e 379

Quinone Substituted Porphyrin Dimers: New Photosynthetic Model Systems J L . Sessler,M.R. J o h n s o n , S.E. C r e a g e r J . F e t t i n g e r , J A . I b e r s , J . R o d r i g u e z , C. K i r m a i e r , a n d D . H o l t e n 391

xiii

Organization of the Photosynthetic Membrane of Rhodopseudomonas Viridis Using Biochemical, Immunological and Electron Microscopical Methods F . A . J a y 401

Photoreceptors: Phytochrome The Chromophore and its Role in the Phototransformation of Phytochrome

Conformational Changes Probed with bis-ANS, Monoclonal Antibodies and Phosphorylation P.S. Song, U. B a i , I . - S . K i m , G. C. Whitelam a n d J . P . Markwell 411

Molecular Properties of Phytochrome W.Rüdiger 423

Studies of the Mechanism of the Phototransformation of Phytochrome C. B o n a z z o l a , G. Valduga, P . L i n d e m a n n , Y. Kajil, S.E. Braslavsky a n d K . Schaffner 435

The Significance of Mutants in Phytochrome Research R.E. Kendrick, P . Adamse, E . Lopez-Juez, M. Koornneef J . L . Peters and J . C . Wesselius 437

Mode of Coaction between Phytochrome and Blue/UV Photoreceptors H . Mohr and H . Drumm-Herrel 445

Phytochrome Regulated Expression of Cab Genes in Higher Plants F . Nagy, E . Fejes, A . Pay and E . A d a m 455

Phytochrome Structure/Function Relationships as Probed by Monoclonal Antibodies L . H . P r a t t , M.-M. C o r d o n n i e r and L . C r o s s l a n d 461

Phytochrome from Green A v e n a Characterized with Monoclonal Antibodies Directedtolt Af.-M. Cordonnier and L . H . P r a t t 469

Phytochrome and Cryptochrome: Coaction or Interaction in the Control of Chloroplast Orientation W. H a u p t 479

Photochemistry and Photophysics of Biliprotein Chromophores: A Case of Molecular Ecology

H. Scheer 491 Strategy of Orientation in Flagellates

D . P . Hader 497 Polarized Spectra of Immobilized Phycobilisomes Isolated from Various Cyanobacteria

D . F r a c k o w i a k , Y. Fujita, L . G . E r o k h i n a , M . M i m u r o , Y. Yamazaki, N . T a m a i , M. N i e d b a l s k a , M . R o m a n o w s k i and J.Szurkowski 511

Rhodopsins Spectra and Structures of Photorhodopsin and Bathorhodopsin Studied by Picosecond Laser Photolysis

T. Yoshizawa, Y. Shichida and H . Kandori 521

xiv

The Primary Photochemical Process in Bacteriorhodopsin W. Z i n t h a n d D . Oesterhelt 531

Functional Domains in Octopus Rhodopsin Af. Tsuda, T. Tsuda, N . G . Abdulaev, a n d S. M i t a k u 537

Picosecond Time-resolved Spectroscopy of the Initial Events in the Bacteriorhodopsin Photocycle George H . A t k i n s o n 547

Primary Processes in Sensory Rhodopsin and Retinochrome T. Kobayashi, H . O h t a n i , M . Tsuda, K . O g a s a w a r a , S. K o s h i h a r a , K . I c h i m u r a , R. H a r a , a n d M . T e r a u c h i 561

Circadian Rhythms Seasonal Changes in Circadian Rhythm of Thermoregulation in Greenfinches and

Siskins at Different Ambient Temperatures S. S a a r e l a , B . Klapper a n d G. H e l d m a i e r . . . 573

Light and Circadian Activity in the Blind Mole Rat R. Rado, H . Gev, B . D . G o l d m a n , a n d J. T e r k e l 581

Photoperiod Changes and Heat Production in M e r i o n e s Crassus — The Role of Circadian Rhythms of Body Temperature in Seasonal Acclimatization

A . H a i m , a n d G. L e v i 591 Physiological Responses of Melatonin-Implanted Pigeons to Changes in Ambient

Temperature T M . John a n d J . C . George 597

Metatonin Binding Sites in Discrete Brain Areas: Coincidence with Physiological Responsiveness N . Z i s a p e l 607

Solar UV Light Effects on Growth and Development Signal Transduction in Blue Light-Mediated Growth Responses

T. W. Short, M . Laskowski, S. G a l l a g h e r , and W. R. B r i g g s 615 Potential Impacts of Increased Solar UV-B on Global Plant Productivity

A . H . T e r a m u r a a n d J . H . S u l l i v a n 625 Effects of Enhanced Solar UV-B Radiation on Growth and Function of Selected Crop

Plant Seedlings Af. T e v i n i , U. M a r k , G. Fieser a n d Af. Salle 635

Man and Ultraviolet Light — Photosensitization and Photocarginogenesis Sources of Human Exposure to Ultraviolet Radiation

B . L . Diffey 653 Drug Products and Photocarcinogenesis

PjD. F o r b e s , R.E. Davies and C.P. Sambuco 663

xv

Investigating Contact Photoallergy in the Mouse G.F. G e r b e r i c k and C A . Ryan 671

Relation Between the Molecular Structure of a Drug and its Photobiological Activity by Combination of In vivo and I n vitro Research

G.M.J. Beijersbergen v a n H e n e g o u w e n 683 Screening Materials for Photosensitization Eye Effects

P . D a y h a w - B a r k e r , P h D . and F . M. B a r k e r , O D 693

UV and Cancer Solar Ultraviolet Radiation and Skin Cancer in Man

F . U r b a c h 705 The Finsen Medal Presentations:

to: D.I. Arnon L . O . Björn 715

to: I.A. Magnus AR. Young 717

The Finsen Lecture: Monodelphis domestica: An Animal Model for Studies in

Photodermatology Including the Induction of Melanoma R. D . Ley 719

Prolonged UVR-Induced Erythema and Melanoma Risk Factors E . A z i z i M D . , Y. Wax P h D . , A . Lusky M . S c , A . Kushelevsky P h D . , and M . S c h e w a c h - M i l l e t M D 723

Ultraviolet Radiation Induces Cytoskeletal Damage in Human Cells G. B . Zamansky and I . - N . Chou 727

Photoimmunology Overview: Photoimmunology

M L . Kripke 735 Immunology of UV-Induced Human Skin Cancer

G. F r e n t z 743 Immunological Mediators Produced by UV-Irradiated Keratinocytes

T. S c h w a r z , A . Urbanski, J . K r u t m a n n , T A . L u g e r 749

The Franz Greiter Memorial Symposium: Physiological Effects of UV Radiation on the Immune System and on the Eye Franz Gleiter — The Man and His Work

F . U r b a c h 761 Immune Suppression by Ultraviolet B Irradiation and Urocanic Acid

F . P . Noonan and E . C . D e Fabo 763

xvi

Effects of Radiant Energy on the Ocular Tissues S. Z i g m a n , P h D 769

On the Effect of Ultraviolet Radiation on the Eye 0. H o c k w i n , J . Schmidt, and C. Schmitt 787

Photodynamic Therapy Model System Studies on Photosensitization in Light Scattering Media

L J . G r o s s w e i n e r , M J . Schifano, J L . K a r a g i a n n e s , Z. Zhang and Q . A . B l a n 795 I n Vitro and I n Vivo Spectral Properties of Porphyrins

R . P o t t i e r 807 Photosensitization of Microbial Cells

Y. N i t z a n , Z. M a l i k , a n d B . E h r e n b e r g 815 Effects of PDT on DNA and Chromosomes

/. M o a n , E . K v a m , E . Hovig and K . Berg 821 Photophysical and Photosensitizing Properties of Phthalocyanines

/. D . Spikes 831 Zinc(II)-Phthalocyanine as a Second-Generation Photosensitizing Agent in

Tumour Phototherapy G. J o r i , R- B i o l o , C. M i l a n e s i , E . Reddi and G. Valduga 839

Photosensitization by Phthalocyanines. Chemical Structure — Photodynamic Activity Relationship

/. R o s e n t h a l and E . B e n - H u r 847

Photoprotection A. Celhilar Mechanisms

Cellular Effects of UVA: DNA Damages M J . Peak and J . G . Peak 855

Cellular Defense Against UV A (320-380 nm) and UVB (290-320 nm) Radiations R . M . Tyrrell, S.M. Keyse and E . C . M o r a e s 861

Melanin is a Double-Edged Sword /. M. M e n t e r , I . Willis, M . E . Townsel, G. D . Williamson and C. L . Moore 873

B. Protection Measures Sun Protection Factors

R.E. M a s c o t t o 889 The Reliability of Sun Protection Factor

E . A z i z i M D . , M . Modan, A . Kushelevsky P h D . and Af. Schewach Millet M D 897

Sunscieens — A Photochemical Perspective F . P . G a s p a r r o 901

The Protective Ability of Sunscreens G. A . G r o v e s 903

The Broad Spectrum Concept in Sunscreens G A . Groves 909

Trends in Sun Protection RS. Summers a n d B . Summers 917

Psoralens: Effects and Mechanisms Photochemoprotection: Protective Effects of Psoralen-Induced Tan

P . F o r l o t 925 Mutagenic Effects of Psoralen-Induced Photoadducts and their Repair in Eukaryotic Cells

D . Averbeck. M . D a r d a l h o n a n d N . MagahaSchwencke 933 Quantification of 8-MOP Photoadducts in Lymphocytes

F . P . G a s p a r r o , D . Weingold, E. Simmons, D . G o l d m i n z , R. Edelson 951 New Aspects of the Mechanism of Action of Furocoumarins (Psoralens and Angelicins)

G. R o d i g h i e r o 963 Photodynamic Carcinogenicity and its Prevention by Carotenoids as Oxygen Radical

Quenchers: Relevance in Animals and Human Intervention L . S a n t a m a r i a 975

UV and the Environment UV and the Environment: An Introduction

E. R i k l i s 1011 UV and Exobiology: Can Micro-Organisms Survive the Space Environment?

H . - D . M e n n i g m a n n 1015 Further Solar UV Spectral Measurements at the Dead Sea

A . P . Kushelevsky 1023 Ozone and Ultraviolet Light are Additive Co-Carcinogens In Vitro

C. B o r e k 1027

UV Risks and Regulations Skin Photobiology and Regulations on UV Radiation

/. C. van der Leun 1033 Pattems of Human Exposure to Ultraviolet Radiation

F r e d e r i c k U r b a c h 1037 Cutaneous Photosensitization: Hazard and Regulation

B . E.Johnson 1045 UV Regulatory Strategies

SM. Sykes and E . D . Jacobson 1057

Round Table: Photobiology in Developing Countries 1069 Author Index 1073 Subject Index 1077

xviii

The Primary Photochemical Process in Bacteriorhodopsin

W. ZINTH* AND D. OESTERHELT+ *Physik Department Technische Universität München D - 8 0 0 0 München + M a x - P l a n c k - l n s t i t u t für Biochemie D - 8 0 3 3 M a r t i n s r i e d , FRG

Introduction

In the halobacterial branch of archaebacteria a special kind of retinal-based photosynthesis is found. Two light-driven ion pumps, bacteriorhodopsin (BR) as a proton pump and halorhodopsion (HR) as a Chloride pump occur in the cell membrane and mediate phototrophic growth of halobacterial cells (for review see Lanyi et al., 1984).

Similar basic principles of ion transport are effective in BR and HR: In the active State the proteins contain retinal in the M-trans configuration linked via a protonated Schiffs base to a lysine residue of the amino acid sequence. After the absorption of a photon the chromophore retinal changes its configuration and acquired the 13-cis form (Nuss et al. 1985; Polland et al., 1984a, 1984b, 1986; Dobler et al., 1988; Zinth et al., 1988; Mathies et al., 1988). This isomerization induces the ion transport which must proceed via polar side groups of the protein structure (Oesterhelt and Tittor, 1989). After about 10 ms ion transport is finished and the chromoprotein has returned to its initial State. In this paper we focus on the very early Steps of the photosynthetic reaction in bacteriorhodopsin prior to and during the isomerization of the retinal chromophore. We describe absorption changes seen in spectroscopic experiments with femtosecond time-resolution and discuss the related molecular processes.

Materials and Methods

Bacteriorhodopsin (purple membrane) was prepared according to the procedure published by Oesterhelt and Stoeckenius (1974). The samples were kept in the light-adapted form by appropriate background illumination. Time-resolved excite and probe experiments were performed using 80 fs pulses from a colliding pulse mode-locked (CPM) laser-amplifier System operated at a repetition rate of 7 kHz. Part of the Output (10%) of the laser-amplifier System served as the exciting pulse. The excitation wavelength was X = 620 nm. The residual of the laser Output produced the probe pulses via femtosecond continuum generation. The change of transmission of the sample

Photobiology, Edited by E . Riklis Plenum Press, New York, 1991 531

W. Z i n t h and D . Oesterhelt Primary Photochemical Process in Bacteriorhodopsin

induced by the exciting pulses was measured with high precision as a function of time delay. The time resolution of the experiment depended on the width At = 90 fs were obtained from the System permitting the investigation of dynamic processes faster than 50 fs.

The choice of the probing wavelength is of major importance for the interpretation of the observed absorption transients. At Short probing wavelengths, in the region of the 0-0 transition of the molecule and below, the absorption changes may be related to different processes, e.g. to cross relaxation of an inhomogeneous ground-state distribution, to excited-state processes, and to the formation of photoproducts. Working at longer wavelengths, i.e. in the fluorescent region of the molecule, the ground-state processes may be neglected, i.e. a more straight-forward interpretation of the experiment is possible (Dobler et al., 1988; Zinth et al., 1988).

Results

Time-resolved changes of absorption observed on light-adapted bacteriorhodopsin samples at room temperature are shown in Fig. 1 (circles) for three probing wavelengths in the gain region of BR. Only the very rapid processes occurring within 1.5 ps after excitation are shown. At long probing wavelengths (k = 850 nm, Fig. la) a pronounced gain is found, i.e. the transmitted pulse is more intense than the incident pulse. The gain decays at later times with a time-constant of approximately 500 fs. A more careful inspection of the data points shows that a faster process (x = 180 fs, see below) also contributes to the absorption change. With decreasing probing wavelengths the 500 fs contribution diminishes and at 735 nm (Fig. lb) the faster (180 fs) process dominates the decay of the gain. Fig. lc shows the absorption changes at a still shorter probing wavelength of 660 nm, where, on the other hand, the Srj-Si absorption of BR may still be neglected. An induced absorption due to the intermediate J is built up with 500 fs. Around time zero a very short-lived (x < 100 fs) gain is found.

Discussion

The experimental data per se suggest a qualitative view of the primary reactions. To obtain a more quantitative picture of the ultrafast molecular processes the observed absorption changes have to be compared with the predictions from a simplifying mathematical model (Polland et al., 1984b). We assume that the reaction proceeds via several intermediate levels / i > which are characterized by their absorption spectra. The occupation of the product levels decays exponentially with decay times x \ . While this description is well justified on the time scale of picoseconds, one should keep in mind that this model may fail when coherent motions with large amplitude along special normal coordinates take place.

A detailed analysis of the experimental data together with a precise determination of the experimental response function now reveals an interesting rapid sequence of events: Three intermediate levels appear during the first picosecond. Their decay times are t i = 50

532

Primary Photochemical Process in Bacteriorhodopsin W. Z i n t h and D . Oesterhelt

- 1 . 0 -

N

O E o c

0> Ol c o -c u

0> u c o -O v. o w <

-0 .5 -

0 0.5 1.0 D e l a y T im-e t p C p s J

Figure 1. Time-dependent changes of absorption (negative values correspond to gain) induced by exciting femtosecond pulses at X, = 850 nm (a), X - 735 nm (b), X = 660 nm (c). The solid curves are calculated using the decay kinetics discussed in the text. The broken curves are calculated for two different sets of amplitude parameters excluding the 50 fs kinetics.

fs ± 30 fs, x 2 = 180 fs ± 70 fs and x 3 = 500 fs ± 100 fs. The gain related to all three levels proves that they exist in the electronically excited (SO State of BR.

Taking into account the spectral properties of the transient signal and the known molecular data of retinal the following microscopic picture of the very early reactions is suggested (see Fig. 2). The incident photons promote the retinal to the Franck-Condon

533

W. Z i n t h and D . Oesterhelt Primary Photochemical Process in Bacteriorhodopsin

s ,

B R L A j K

High Frequency ^ Coordinate React ion Coordinate

I somer izat ion

Figure 2. Scheme of the ground-state (S0) and excited-state (Sj) potential energy surfaces as a function of the high-frequency vibrational and low-frequency reactive coordinates.

State Si** on the Sj potential energy surface. Here a number of vibrational modes are displaced relative to the S\ equilibrium position (Heller, 1981). Within 50 fs after light absorption an equilibration of high-frequency vibrational modes to the State Si* occurs. Düring this first reaction the molecule does not have the time to move along the coordinates of the low-frequency (reactive) modes. The following slower reactive motion of the retinal is related to the 180 fs gain kinetics. In this process, part of the isomerization (presumably a rotation by 60 to 90 degrees around the C13-C14 double bond) takes place and the molecules arrive at the bottom of the S\ potential surface (level S'i R e l). The System leaves this area via internal conversion with a time constant X2 = 500 fs. Two decay pathways are possible: more than 60% of the molecules form the intermediate photoproduct J, while the rest returns to the original ground State of BR. The following reaction in the active branch proceeds from J with a 3 ps time constant leading to the intermediate K which is stable on the picosecond time scale.

Conclusions

Time resolved absorption experiments on bacteriorhodopsin performed on the femtosecond time scale show strong absorption and gain dynamics which are related to the excited-state reaction of the retinal chromophore. Extremely rapid (50 fs) absorption

534

Primary Photochemical Process in Bacteriorhodopsin W. Z i n t h and D . Oesterhelt

changes reflect the relaxation of high-frequency modes. The slower kinetics are related to

the isomerization of the retinal: Isomerization Starts in the excited electronic State and is

finished directly after the 500 fs internal conversion process during the formation of the

first ground State photoproduct J .

Acknowledgements

The authors acknowledge valuable contributions by W. Kaiser, J. Dobler and K. Dressler.

References Dobler, J. Zinth, W. Kaiser, W. Oesterhelt, D. C h e m . Phys. L e u . 144 (1988) 215. Heller, E.J. Acc. C h e m . Res. 14 (1981) 368. Lanyi, J.K. in Bioenergetics, ed. Ernster, L. (Elsevier, Amsterdam) 1984, p. 315. Mathies, R.A. BritoCruz, C.H. Pollard, W.T. Shank, C . V S c i e n c e 240 (1988) 777. Nuss, M.C. Zinth, W. Kaiser, W. Kölling, E. Oesterhelt, D. C h e m . Phys. Lett. 117, (1985) 1. Oesterhelt, D. Stoeckenius, W. M e t h . Enzymol. 31A (1974) 667. Oesterhelt, D. Tittor, J. TIBS 14 (1989) 57. Polland, H J . Franz, M.A. Zinth, W. Kaiser, W. Kölling, E. Oesterhelt, D. Biochem. Biophys.

Acta 767 (1984) p. 635. Polland, H J . Franz, M.A. Zinth, W. Kaiser, W. Kölling, E. Oesterhelt, D. Biophys. J. 49

(1986). 651. Polland, H J . Zinth, W. Kaiser, W. in Ultrashort Phenomena, vol. 4, eds. Auston, D.H.

Eisenthal, K.B. (Springer, Heidelberg, 1984) p. 456. Zinth, W. Naturwiss. 751 (1988) 173.

535