Taurine

Dietary Taurine and Feline Reproduction and Development12 JOHN A. STURMAH3 Department of Developmental Biochemistry, Hew York State Office of Mental Retardation and Developmental Disabilities, Institute for Basic Research in Developmental Disabilities, Staten Island, MY 10314 erally considered to be the rate-limiting step in taurine biosynthesis, dogs probably have no nutritional re quirement for taurine. The opposite situation pertains to cats. If cats are fed a diet deficient in taurine they become taurine-depleted. This occurs most rapidly in plasma and soft tissues, such as liver, lung and spleen. In due course other tissues become depleted, such as muscles, including the heart, which are the chief body stores of taurine, and nervous tissues, including brain and retina. The biological consequences of taurine de pletion in cats include retinal degeneration and im paired visual function, first reported in 1975; degen eration of the tapetum lucidum, the reflecting layer of cells behind the retina; severely impaired repro duction in females; cardiac abnormalities; and im paired immune function (2). We have been especially interested in the role of taurine in development in general, and in particular, in brain development. During the last few years we have documented the reproductive wastage in taurinedéficientfemale cats (3), which includes frequent abortions and résorptionsof fetuses before term and an increased incidence of stillbirths at term (Fig. 1). We have observed severe hydrocephalus in three aborted fetuses, anencephaly in one stillborn kitten and hydrocephalus in one live surviving kitten (Fig. 2). Kittens born live have a significantly smaller body and brain weight than kittens born to females con-

ABSTRACT The reproductive performance of female cats is severely affected by dietary taurine deficiency resulting in excessive reproductive wastage, including frequently resorbed or aborted fetuses and stillborn or low birth-weight live kittens. These studies were per formed using female cats fed a completely defined pu rified diet (taurine-free) alone or supplemented with taurine for >6 mo before mating, and their breeding performance was monitored for several years. Diets containing 0, 0.005 or 0.01% taurine produced severe taurine depletion and poor reproductive performance. Those containing 0.05, 0.2 or 1% taurine resulted in no apparent abnormalities and a normal breeding per formance. A diet containing 0.02% taurine resulted in modest taurine depletion and a partially compromised reproductive performance. Kittens from taurine-deflcient mothers have a poor survival rate and grow at a slower rate than kittens from females fed an adequate taurine diet. The brain weights of kittens from taurinedéficient mothers are significantly smaller than normal, both at birth and at weaning at 8 wk. Surviving kittens exhibit a number of abnormalities. The differences in maternal dietary taurine are reflected in the taurine concentrations found in the milk of lactating females. Our results strongly suggest that a certain amount of taurine is mandatory for survival and normal develop ment in the cat. J. Nutr. 121: S166-S170, 1991. INDEXINGKEY WORDS: •symposium •cats •taurine •deuelopment •reproduction

1Presented as part of the Waltham International Symposium on Nutrition of Small Companion Animals, at University of California, Davis, CA 95616, on September 4-8, 1990. Guest editors for the symposium were James G. Morris, D'Ann C. Finley and Quinton R. Rogers. 1This research was supported in part by NIH grant HD-16634 and by the New York State Office of Mental Retardation and De velopmental Disabilities. 3To whom correspondence should be addressed: Department of Developmental Biochemistry, New York State Office of Mental Re tardation and Developmental Disabilities, Institute for Basic Re search in Developmental Disabilities, 1050 Forest Hill Road, Staten Island, NY 10314.

The cat has played a major role in defining the nu tritional importance of taurine, just as taurine has served the cat well in maintaining a number of its bodily functions. It is interesting that the two major small companion animals featured in this symposium, cats and dogs, are entirely different in their nutritional requirements for taurine. Dogs have an ~ 100-fold greater capacity to decarboxylate cysteinesulfinic acid in their livers than do cats (1), and, since this is gen0022-3166/91 53.00 ©1991 American Institute of Nutrition.

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DIETARY TAURINE

AND FELINE REPRODUCTION

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FIGURE 1 Reproductive performance of females fed 0% or 0.05% taurine. These data are derived from 96 pregnancies of females fed 0% and 73 pregnancies of females fed 0.05% taurine.

FIGURE 2 Abnormal offspring from taurine-depleted mothers. A. Fetus aborted preterm showing extreme hydrocephalus. B. Full-term stillborn with anencephaly. C. Brain from a 1-y-old kitten showing severe hydrocephalus.

Brain Weight

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Newborn 8-Weeks-Old Newborn 8-Weeks-Old FIGURE 3 Body and brain weights (g) of newborn and 8-wk-old kittens from mothers fed 0% or 0.05% taurine. Mean ±SD. Downloaded from https://academic.oup.com/jn/article-abstract/121/suppl_11/S166/4744131 by University of Glasgow user on 03 April 2018

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FIGURE 4 80 um sections of kitten visual cortex stained by the rapid Golgi method. A. Visual cortex of a newborn kitten from a taurine-supplemented mother showing differential levels of migration and maturation of postmitotic cellular plaques contributing to the trilaminar nature. The cellular plaques in the middle region show more signs of isolation and maturation of component cells. B. Visual cortex of a newborn kitten from a taurine-déficientmother in which most of the postmitotic cellular plaques remain aggregated at the ventricular zone. The few cellular plaques that have migrated to the pial surface remain aggregated there. A trilaminar nature is not evident. C. Visual cortex of an 8-wk-old kitten from a taurine-supplemented mother of a portion of the cortical parenchyma from the region of gyri showing extensive arborization of axonal and dendritic processes. The peripheral concentration of horizontal neuritic fibers is evident. Typical pyramidal neurons are obscured among the fibrous population and prominent dendritic processes are not distinguishable. Protoplasmic astrocytes with elaborate radial processes are scattered throughout. D. Visual cortex of an 8-wk-old kitten from a taurine-déficientmother illustrating the nonfibrous nature of the cortical parenchyma. Few pyramidal neurons are seen along the submarginai zone of the gyri. The thick and prominent dendritic processes of such neurons are conspicuously spiny and are directed towards the pial surface without significant arborization. Magnification A, B, x60; C, D X90. Downloaded from https://academic.oup.com/jn/article-abstract/121/suppl_11/S166/4744131 by University of Glasgow user on 03 April 2018

DIETARY TAURINE

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S169

NEWBORN KITTENS 10 0% Taurine 0.05% Taurine

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Heart

8-WEEK-OLD KITTENS

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Heart Cerebellum Liver Occipital lobe FIGURE 5 Concentration of taurine (/tmol/g) in various tissues from newborn (top panel) and 8-wk-old (bottom panel) kittens from mothers fed 0% or 0.05% taurine. Mean ±SD.

suming the same diet supplemented with 0.05% tau rine (Fig. 3). Such kittens do not grow as well as normal kittens and have a poor survival rate. Surviving kittens at 8 wk after birth, the approximate time of weaning, still have significantly smaller body and brain weights than kittens from taurine-supplemented mothers. These kittens exhibit a number of neurologic and morphologic abnormalities such as abnormal hind leg development and a peculiar gait characterized by ex cessive abduction and paresis, reduced patellar and achilles tendon jerks, thoracic kyphosis and a persis tence of cells in the cerebellar external granule cell layer, including cells still dividing (4). Abnormalities in the visual system include degeneration or abnormal development of the retina and tapetum lucidum and abnormal migration and differentiation of cells in the visual cortex (5-7) (Fig. 4). These abnormalities are accompanied by reduced concentrations of taurine throughout the body, which are present at birth and persist through lac tation to weaning at 8 wk after birth (Fig. 5). Con centration of taurine in milk from lactating taurinedéficientfemales is only 10% of that in similar fe males consuming the diet containing 0.05% taurine Downloaded from https://academic.oup.com/jn/article-abstract/121/suppl_11/S166/4744131 by University of Glasgow user on 03 April 2018

(3). We have further examined the brains of these kittens by immunohistochemical methods, using an antibody raised against taurine conjugated to bovine serum albumin with glutaraldehyde (8-11). These studies show that not only is the concentration of taurine greatly reduced in the brains of these kittens, but also the distribution is changed. In the cerebel lum, for example, Purkinje cells and their dendrites are almost devoid of taurine-like reactivity (Fig. 6A, B). Granule cells also have reduced reactivity, but not all are affected equally. These brains are also characterized by the presence of large numbers of reactive astrocytes, as shown by their reaction to a commercial antibody to glial fibrillary acidic protein (GFAP), suggesting some damage within (Fig. 6C, D). This is further supported by the presence of sub stantial amounts of IgG, suggesting abnormal per meability of the blood-brain barrier. These studies are still in progress and will be reported in full at a later date. It is clear from our evidence to date that nutri tional taurine deficiency affects development in many ways. It interferes with normal pregnancy and does not permit normal growth and development of

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FIGURE 6 Sagittal sections of 8-wk-old kitten cerebellum. A. From mother fed 0.05% taurine; B. from mother fed 0% taurine, stained with taurine antibody. These figures show the heavy staining of Purkinje cells and their dendrites and of most granule cells in the control, whereas in the taurine-déficientkitten the Purkinje cells and dendrites have no immunoreactivity and are outlined as ghosts, and almost no granule cells are stained. C. From mother fed 0.05% taurine; D. from mother fed 0% taurine, stained with GFAP antibody. These figures show the sparse occurrence of astrocytes in the white matter of control kittens and the abundance of these astrocytes in the white matter of the taurine-déficientkittens.

the fetuses; it interferes with normal postnatal growth and development, in particular the brain de velopment is abnormal, demonstrating features of delayed development and other problems that appear to be related to increased permeability of the bloodbrain barrier. ACKNOWLEDGMENTS

The following collaborators have contributed to various aspects of the research: Humi Imaki, Jeffrey Messing, Peimin Lu and Thomas Palackal. The art work of Sharon Mathier, secretarial assistance of Ann Páreseand practical help from Michael Natelli, Lorinda Matarazzo and other members of the IBR Animal Colony Facility throughout these studies is gratefully acknowledged.

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LITERATURE CITED 1. STURMAN,J. A. (1980) Cysteinesulfinic acid decarboxylase ac tivity in the mammalian nervous system: absence from axons. /. Neurochem. 36: 304-306. 2. PASANTES-MORALES, H., MARTIN, D. L., SHAIN, W. &. MARTIN DEL Rio, R. (1990) Taurine: Functional Neuiochemistry, Physiology and Cardiology, Wiley-Liss, New York, NY. 3. STURMAN, J. A., GARGANO, A. D., MESSING, J. M. &. IMAKI, Downloaded from https://academic.oup.com/jn/article-abstract/121/suppl_11/S166/4744131 by University of Glasgow user on 03 April 2018

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H. (1986) Feline maternal taurine deficiency: effect on mother and offspring. /. Nutr. 116: 655-667. STURMAN,J. A., MORETZ, R. C., FRENCH,J. H. & WISNIEWSKI, H. M. (1985) Taurine deficiency in the developing cat: persis tence of the cerebellar external granule cell layer. /. Neurosci. Res. 13: 405-416. IMAKI, H., MORETZ, R. C., WISNIEWSKI,H. M. & STURMAN, J. A. (1986) Feline maternal taurine deficiency: effects on retina and tapetum of the offspring. Dev. Neurosci. 8: 160-181. PALACKAL,T., MORETZ, R., WISNIEWSKI, H. & STURMAN, J. (1986) Abnormal visual cortex development in the kitten as sociated with maternal dietary taurine deprivation. /. Neurosci. Res. 15: 223-239. PALACKAL,T., MORETZ, R. C., WISNIEWSKI,H. M. & STURMAN, J. A. (1988) Ultrastructural abnormalities in the visual cortex of kittens from taurine-déficient mothers. Brain Dysfunction, 1:71-89. OTTERSEN,O. P., MADSEN,S., MELDRUM,B. S. Si STORM-MATHISEN,J. (1985) Taurine in the hippocampal formation of the Se negalese baboon, Papio papio: an immunocytochemical study with an antiserum against conjugated taurine. Exp. Brain Res. 59: 457-462. STORM-MATHISEN, J. & OTTERSEN, O. P. (1986) In: Neurohistochemistry: Modern Methods and Applications (Panula, P., Paivarinta, H. & Scinila, S., eds) pp. 108-136, Alan R. Liss, New York, NY. OTTERSEN, O.P. &STORM-MATHISEN,].(1987) Localization of amino acid neurotransmitters by immunocytochemistry. TINS 10: 250-255. LAKE,N. &.VERDONE-SMITH, C. (1989) Immunocytochemical localization of taurine in the mammalian retina. Curr. Eye Res. 8: 163-173.

Dietary taurine and feline reproduction and development.

The reproductive performance of female cats is severely affected by dietary taurine deficiency resulting in excessive reproductive wastage, including ...
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