THE EFFECTS OF TAURINE ON EXCITADLE TISSUES

Monographs of the Physiological Society of Philadelphia

Volume 1 IMMUNOPHARMACOLOGY Proceedings of the Conference on Immunopharmacology Philadelphia, January 27-28, 1975 Marvin E. Rosenthale and Herbert C. Mansmann, Jr., Editors

Volume 2 NEW ANTIHYPERTENSIVE DRUGS Proceedings of the A. N. Richards Symposium King of Prussia, Pennsylvania, May 19-20, 1975 Alexander Scriabine and Charles S. Sweet, Editors

Volume 3 PROSTAGLANDINS IN HEMATOLOGY Proceedings of the International Symposium on Prostaglandins in Hematology Philadelphia, March 4-5, 1976 M. J. Silver, J. B. Smith and J. J. Kocsis, Editors

Volume 4 PATHOPHYSIOLOGY AND THERAPEUTICS OF MYOCARDIAL ISCHEMIA Proceedings of the A. N. Symposium Philadelphia, May 6-7, 1976 Allan M. Lefer, Gerald J. Kelliher and Michael J. Rovetto, Editors

Volume 5 HISTAMINE RECEPTORS Proceedings of the A. N. Richards Symposium Philadelphia, March 21-22, 1977 Tobias O. Yellin, Editor

Volume 6 PROSTAGLANDINS IN CARDIOVASCULAR AND RENAL FUNCTION Proceedings of the A. N. Richards Symposium King of Prussia, Pennsylvania, May 8-9, 1978 Alexander Scriabine, Allan M. Lefer and Frederick A. Kuehl, Jr., Editors

Volume 7 THE EFFECTS OF TAURINE ON EXCITABLE TISSUES Proceedings of the A. N. Richards Symposium Valley Forge, Pennsylvania, April 23-24, 1979 S. W. Schaffer, Steven I. Baskin and James J. Kocsis, Editors

THE EFFECTS OF TAURINE ON EXCITABLE TISSUES Proceedings of the 21st Annual A. N. Richards Symposium of the Physiological Society of Philadelphia, Valley Forge, Pennsylvania, April 23-24, 1979 Edited by S. W. Schaffer, Ph.D. Department of Physiology and Biophysics Hahnemann Medical College, Philadelphia Steven I. Baskin, Ph.D. Department of Pharmacology Medical College of Pennsylvania, Philadelphia James J. Kocsis, Ph.D. Department of Pharmacology Jefferson Medical College, Philadelphia

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ISBN -13 :978-94-009-8095-2 DOl: 10.1007/978-94-009-8093-8

e-ISBN-13:978-94-009-8093-8

R. M. ADEME Centro de I nvestigaciones en Fisiologia

Celular Universidad Nacional Aut6noma de Mexico Mexico

L. E. ALTO Departments of Medicine and Physiology University of Manitoba Winnipeg, Canada

A. BABA Department of Pharmacology Osaka University Osaka, Japan

J. BAHL Department of I nternal Medicine University of Arizona Tucson, Arizona

S. I. BASKIN The Medical College of Pennsylvania Department of Pharmacology Philadelphia, Pennsylvania

H. F. BRADFORD Department of Biochemistry Imperial College of Science and Technology London, England

N. BRESOL!N Department of Pharmacology College of Medicine University of Arizona Health Sciences Center Tucson, Arizona

Contributors

R. BRESSLER Department of Internal Medicine University of Arizona Tucson, Arizona

S. CHANG Department of Internal Medicine University of Arizona Tucson, Arizona

J. CHOVAN Department of Physiology and Biophysics Hahnemann Medical College Philadelphia, Pennsylvania

M. F. CRASS, III Department of Physiology Texas Tech University School of Medicine Lubbock, Texas

A. N . DAVISON Department of Neurochemistry Institute of Neurology London, England

N. S. DHALLA Department of Physiology University of Manitoba Winnipeg, Canada

L. DURELL! Clinica Neurologica Universita di Sassari Sassari, Italy

L. FEUER Chinoin Pharmaceutical and Chemical Works

Ltd. Budapest, Hungary

C. M. FINNEY College of Marine Studies University of Delaware Newark, Delaware

C. J. FRANGAKIS Department of Internal Medicine University of Arizona Tucson, Arizona

K. FURUKAWA Department of Pharmacology Toho University School of Medicine Tokyo, Japan

G. GAULL Department of Human Development and

Nutrition New York State Institute for Basic Research

in Mental Retardation Staten Island, New York

D. GROSSO Department of Internal Medicine University of Arizona Tucson, Arizona

R. J. HOESCHEN Departments of Medicine and Physiology University of Manitoba Winnipeg, Canada

N. HOMMA Department of Pharmacology Toho University School of Medicine Tokyo, Japan

R. HORIE Japan Stroke Prevention Center and

Department of Pathology Shimane Medical University Izumo, Japan

F. C. G. HOSKIN Department of Biology Illinois Institute of Technology Chicago, Illinois

R.E.HRUSKA Department of Pharmacology College of Medicine University of Arizona Health Sciences Center Tucson, Arizona

R. J. HUXTABLE Department of Pharmacology University of Arizona Health Sciences Center Tucson, Arizona

R. ITO Department of Pharmacology Toho University School of Medicine Tokyo, Japan

H. IWATA Department of Pharmacology Osaka University Osaka, Japan

A. KARPPINEN Department of Biochemistry University of Oulu Oulu, Finland

Y. KATAYAMA Institute for Neurobiology Okayama University Medical School Okayama, Japan

J. C. KHATTER Departments of Medicine and Physiology University of Manitoba Winnipeg, Canada

D. C. KLEIN Laboratory of Developmental Neurobiology National Institute of Child Health and

Human Development National Institutes of Health Bethesda, Maryland

J. J. KOCSIS Department of Pharmacology Jefferson Medical College of Thomas

Jefferson University Philadelphia, Pennsylvania

P.KONTRO Department of Biomedical Sciences University of Tampere Tampere, Finland

J. KRAMER Department of Physiology and Biophysics Hahnemann Medical College Philadelphia, Pennsylvania

E. KULAKOWSKI Department of Physiology and Biophysics Hahnemann Medical College Philadelphia, Pennsylvania

E. KUMPULAINEN Department of Biochemistry University of Oulu Oulu, Finland

K. KURIYAMA Department of Pharmacology Kyoto Prefectural University of Medicine Kyoto, Japan

P. LAHDESMAKI Department of Biochemistry University of Oulu Oulu, Finland

H. E. LAIRD Department of Pharmacology and Toxicology University of Arizona Tucson, Arizona

N. LAKE Department of Visual Science Institute of Ophthalmology University of London London, England

B. LARSEN Department of Internal Medicine University of Arizona Tucson, Arizona

S. LIPPINCOTT Department of Pharmacology University of Arizona Health Sciences Center Tucson, Arizona

J. B. LOMBARDINI Department of Pharmacology and

Therapeutics Texas Tech University School of Medicine Lubbock, Texas

, ,

A. M. LOPEZ-COLOME Centro de Investigaciones en Fisiologia

Celular Universidad Nacional Autonoma de Mexico Oexico

W. LOVEN BERG Section on Biochemical Pharmacology National Heart, Lung and Blood Institute National Institutes of Health Bethesda, Maryland

K.-M. MARNELA Institute of Biomedical Sciences University of Tampere Tampere, Finland

J. MARSHALL Department of Visual Science Institute of Ophthalmology University of London London, England

M. MATSUMOTO Institute for Neurobiology Okayama University Medical School Okayama, Japan

B. A. MEINERS Department of Pharmacology College of Medicine University of Arizona Health Sciences Center Tucson, Arizona

A. MORI Institute for Neurobiology Okayama University Medical School Okayama, Japan

R. MUTANI Clinica Neurologica U niversita di Sassari Sassari, Italy

M. MURAMATSU Department of Pharmacology Kyoto Prefectural University of Medicine Kyoto, Japan

Y. NARA Japan Stroke Prevention Center and

Department of Pathology Shimane Medical University lzumo, Japan

C. NAUSS-KAROL Department of Biochemical Nutrition Hoffmann-LaRoche Inc. Nutley, New Jersey

S.OHKUMA Department of Pharmacology Kyoto Prefectural University of Medicine Kyoto, Japan

S. S. OJA Department of Biomedical Sciences University of Tampere Tampere, Finland

A.OOSHIMA Japan Stroke Prevention Center and

Department of Pathology Shimane Medical University lzumo, Japan

A.C./. ORAEDU Department of Visual Science Institute of Ophthalmology University of London London, England

H. PASANTES-MORALES Centro de I nvestigaciones en Fisiologia

Celular Universidad Nacional Aut6noma de Mexico Mexico

D. K. RASSIN Department of Human Development and

Nutrition New York State Institute for Basic Research

in Mental Retardation Staten Island, New York

S. W. SCHAFFER Department of Physiology and Biophysics Hahnemann Medical College Philadelphia, Pennsylvania

S. Y. SCHMIDT Berman-Gund Laboratory for the Study of

Retinal Degenerations Harvard Medical School, Mass Eye and Ear Boston, Massachusetts

J. SHAFFER Department of Pharmacology Jefferson Medical College of Thomas

Jefferson University Philadelphia, Pennsylvania

P. L. SONI Departments of Medicine and Physiology University of Manitoba Winnipeg, Canada

R. C. SPETH Department of Pharmacology College of Medicine University of Arizona Health Sciences Center Tucson, Arizona

J. A. STURMAN Developmental Neurochemistry Laboratory Department of Pathological Neurobiology Institute for Basic Research in Mental

Retardation Staten Island, New York

E. J. THOMPSON Department of Neurochemistry Institute of Neurology London, England

T. UCHIYAMA Department of Pharmacology Toho University School of Medicine Tokyo, Japan

C. VANDERWENDE College of Pharmacy Rutgers - The State University Piscataway, New Jersey

M. J. VOADEN Department of Visual Science Institute of Ophthalmology University of London London, England

J. D. WELTY Division of Biochemistry, Physiology and

Pharmacology The University of South Dakota School of

Medicine Vermillion, South Dakota

M. C. WELTY Division of Biochemistry, Physiology and

Pharmacology The University of South Dakota School of

Medicine Vermillion, South Dakota

G.H.T. WHELER Laboratory of Developmental Neurobiology National Institute of Child Health and

Human Development National Institutes of Health Bethesda, Maryland

S. YAMAGAMI Department of Pharmacology Osaka University Osaka, Japan

K. YAMAGUCHI Department of Medical Chemistry Osaka Medical College Osaka, Japan

H. I. Y AMAMURA Department of Pharmacology College of Medicine University of Arizona Health Sciences Center Tucson, Arizona

Y. YAMORI Japan Stroke Prevention Center and

Department of Pathology Shimane Medical University Izumo, Japan

S. YODA Department of Pharmacology Toho University School of Medicine Tokyo, Japan

I. YOKOI Institute for Neurobiology Okayama University Medical School Okayama, Japan

Preface

It has become an annual custom for the Physiological Society of Philadel­phia to sponsor a spring symposium in honor of A. N. Richards (\876-1966), a research pharmacologist who developed the classical micropuncture tech­nique for studying kidney function. The A. N. Richards Symposium for 1979 was held on April 23-24 in Valley Forge, Pennsylvania. The theme of this symposium was "The Actions of Taurine on Excitable Tissues." Although taurine was discovered as a constituent of bile salts in 1857 by a chemist and an anatomist (Gmelin and Tiedemann), interest today centers chiefly on the extrahepatic actions of taurine, especially in brain, heart, and other excitable tissues. Research on taurine is clearly in a period of exponential growth.

We can be sure that the research reports presented and described herein as the "Proceedings of the Symposium" will provide impetus for further growth. Thus the report describing macromolecular receptors for taurine in myocardial sarcolemma may provide a model for exploring the molecular mechanisms that underlie the action(s) of taurine. Stabilization of mem­branes and modulation of ion fluxes are two fundamental actions of taurine dealt with in many of these reports. It is just these actions of taurine that have been reported by several investigators as being involved in human myotonia, diabetes, and heart failure.

Other presentations at the symposium will add to the growing consensus that taurine acts as a modulator rather than a transmitter in the eNS. Hyper­tension, epilepsy, and feline retinal degeneration have been described here by other investigators as diseases in which either the biosynthesis, uptake, or re­lease of tissue taurine may be critical.

The biological effects of the newly discovered taurine analogue y­glutamyl taurine, along with those of hypotaurine and taurocyamine, again raise the question as to whether it is taurine or its analogues that mediate "the effects of taurine." Reports describing methods for reducing tissue taurine levels provide another approach to answering this same question. Altogether the proceedings of this symposium should provide a useful summary of the rapidly growing knowledge about taurine and its biological effects.

We wish to thank the Physiological Society of Philadelphia for their sponsorship and financial support, and the officers of the society for their per­sonal assistance in making the symposium a success. We also gratefully

acknowledge the support of the many foreign participants who attended the symposium (especially our Japanese colleagues) as well as the contributions made by our respective educational institutions, especially our graduate stu­dents and technicians. We also thank the following companies for additional financial support: Merck & Co.; Arnar-Stone Laboratories; Smith, Kline & French; ICI Americas, Inc.; Upjohn Co.; Fujisawa Pharmaceutical Corpora­tion; and Wyeth, Inc.

S. W. Schaffer S. I. Baskin J. J. Kocsis

THE EFFECTS OF TAURINE ON EXCITADLE TISSUES

Contents

Preface

Part I-Metabolism and Function of Taurine Analogues Introduction 3 I. Cysteine Dioxygenase and Its Possible Role on Taurine

Formation in Rats 5 K. Yamaguchi

2. Uptake and Metabolism of Cysteine in Rat Brain 21 H. Iwata. A. Baba. and S. Yamagami

3. Biological Effects of Gamma r-Glutamyl Taurine (Glutaurine): A New Parathyroid Hormone 31

L. Feuer 4. Inhibition of Taurocyamine (Guanidinotaurine)-induced Seizures

by Taurine 41 A. M ori. Y. Katayama. I. Yokoi. and M. Matsumoto

5. Properties of Hypotaurine Uptake in Mouse Brain Slices 49 P. K antra and S. S. Oja

6. Cephalopod Nerve as a Model System for the Study of the Metabolism of Taurine and Related Sulfur Compounds 59

F.c.G. Hoskin Discussion 67

Part II-Actions of Taurine in the Central Nenous System Introduction 71 7. Effect of Kainic Acid Lesions on Taurine Transport into

Rat Brain Synaptosomes 73 H. I. Yamamura. R. C. Speth. R. E. Hruska. N. Bresolin. B. A. Meiners. and R. J. Huxtable

8. High Affinity Taurine Uptake in Human Blood Platelets 81 C. Nauss-Karol and C. Vander Wende

9. Uptake and Stimulated Release of Taurine by Preparations of Cerebral Cortex 93

G.H. T. Wheler. H. F. Bradford. A. N. Davison. and E. J. Thompson

10. Function and Regulation of Taurine in the Pineal Gland 107 G.H. T. Wheler and D. C. Klein

11. Enrichment of Taurine in Synaptosomes and Synaptic Vesicles of Bovine Brain Regions 123

S. S. Oja. K-M. Marnela. and P. Kontro 12. Subcellular Distribution of Intracerebrally Injected Taurine and

Certain Other Amino Acids in Mouse Brain 135 E. Kumpulainen. A. Karppinen. K-M. Marnela. and P. Liihdesmiiki

13. Taurine in the Retina 145 M. J. Voaden. A.C./. Oraedu. J. Marshall. and N. Lake

14. The Effect of Taurine on 45Calcium Transport by Retinal Subcellular Fractions 161

H. Pasantes-Morales. R. M. Ademe. and A. M. Lopez-Colome 15. Taurine in Retinas of Taurine-deficient Cats and RCS Rats 177

S. Y. Schmidt 16. Axonal Transport of Taurine 187

J.A. Sturman Discussion 209

Part III-Actions of Taurine in the Cardiovascular System Introduction 217 17. Methods of Reducing Tissue Taurine Levels 219

J. E. Shaffer and J. J. Kocsis 18. Rapid Depletion of Tissue Taurine Content by Guanidinoethyl

Sulfonate 231 R. J. Huxtable. H. E. Laird. and S. Lippincott

19. Accumulation of Taurine by Isolated Rat Heart Cells and Rat Heart Slices 247

J. Bahl. C. J. Frangakis. B. Larsen. S. Chang. D. Grosso. R. Bressler

20. The Role of Taurine Receptors in the Heart 261 S. W. Schaffer. J. Chovan. J. Kramer. and E. Kulakowski

21. Subcellular Effects of Taurine on Guinea Pig Heart 281 J. C. Khatter. P. L. Soni. R. J. Hoeschen. L. E. Alto. and N. S. Dhalla

22. Effects of Taurine on Subcellular Calcium Dynamics in the Normal and Cardiomyopathic Hamster Heart 295

J. D. Welty and M. C. Welty 23. Cardiovascular Actions of Taurine, Y-Aminobutyric Acid

(GABA), and Y -Amino-{1-hydroxybutyric Acid (GABOB) after Chemical Denervation 313

R. Ito. T. Uchiyama. S. Yoda. N. Homma. and K Furukawa Discussion 329

Part IV -Clinical Implications of Taurine Introduction 339 24. Taurine: A Sulfur-containing Amino Acid Possibly Important

for Maintaining Cellular Integrity 341 K. Kuriyama. S. Ohkuma. and M. Muramatsu

25. Taurine Treatment of Human Myotonia: In Vivo Study of the Correlations between Taurine and Transmembrane Ion Fluxes 363

L. Durelli and R. Mutani 26. Taurine: Significance in Human Nutrition 379

D. K. Rassin and G. E. Gault 27. Pathophysiological Role of Taurine in Blood Pressure

Regulation in Stroke-Prone Spontaneously Hypertensive Rats (SHR) 391

Y. Yamori. Y. Nara. R. Horie. A. Ooshima. and W. Lovenberg

28. Factors that Modify the Tissue Concentration or Metabolism of Taurine 405

S. I. Baskin and C. M. Finney 29. Taurine and Myocardial Ischemia 419

J. B. Lombardini and M. F. Crass III Discussion 437

Index 441