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Graduate School of Pharmaceutical Sciences, Hokkaido University, Sapporo, Japan 060-0812
2To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT History of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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KEY WORDS: • dogs • synergism • taste nerve response • glutamate agonists • amino acids
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History of physiological studies on umami taste |
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TOPABSTRACTHistory of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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).
When the umami constituents are eliminated, the characteristic taste of
the crab meat disappears. Thus, umami substances are essential for
producing the unique taste of many natural foods.
Europeans and Americans have considered that umami substances
potentiate flavor by enhancing the four basic tastes, although no
reliable scientific data supporting this idea have been published.
Yamaguchi (1987)
showed that MSG has no enhancing effect
on the four basic tastes in humans, but these data have not been
accepted readily by Europeans and Americans.
The umami substances are originally acids; hence, at neutral pH, they
exist in the salt form. Usually they are sodium salts, i.e., monosodium
glutamate, disodium inosinate and disodium guanylate. Thus, the umami
substances contain the sodium ion. The first electrophysiologic studies
on reception of the umami substances were conducted with rats
(Sato et al. 1967
) and cats (Adachi et al. 1967
) In these animals, single fibers of the chorda tympani
nerve responded to MSG, but also to NaCl. Hence the response to MSG was
considered to be related to the salt response.
In humans, a remarkable synergism exists between MSG and IMP or GMP
(Kuninaka 1967
). For example, 0.5 mmol/L GMP alone or
1.5 mmol/L MSG alone elicits practically no taste, but a mixture of GMP
and MSG at these concentrations elicits a strong umami taste. This
remarkable synergism was not seen in rats or cats. In rats, the
synergism was seen in sucrose-sensitive fibers (Sato et al. 1967
). Thus the responses to umami substances were related to
responses to both NaCl and sucrose; the umami substances did not elicit
unique responses independently of the four basic tastes in rats or
cats.
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Canine taste nerve responses to umami substances |
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TOPABSTRACTHistory of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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, Kumazawa et al. 1991
, Nakamura and Kurihara 1991
)
(Fig. 1
). GMP (0.5 mmol/L) alone induced only a small response, which reverted
to a spontaneous level during stimulation. After adaptation of the
response, solutions containing MSG of varying concentrations and 0.5
mmol/L GMP were applied to the tongue. Hence, the responses to the
mixture of MSG and GMP did not contain the response to GMP itself. The
response was observed to rise with increasing concentrations of MSG. In
the presence of 0.5 mmol/L GMP, the response was much greater than that
observed in the absence of GMP. This increase due to the presence of
GMP resulted from a synergism between MSG and GMP. The synergism was
remarkable at lower concentrations of MSG and attenuated at high
concentrations.
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The effects of 0.2 mmol/L GMP on responses to various stimuli were also
examined (Fig. 2
). GMP (0.2 mmol/L) showed practically no effect on responses to 0.1
mol/L NaCl, HCl (pH, 3), 500 mmol/L sucrose, 10 mmol/L quinine and 100
mmol/L glycine. Thus, the umami substance (GMP) had no ability to
enhance the responses to the four basic taste stimuli. The synergism
between MSG and the nucleotides was ultimately explained in terms of an
allosteric effect (Fig. 1)
(Kumazawa et al. 1991
).
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) (Nakamura and Kurihara 1990
). Amiloride also inhibits the
response to MSG. On the other hand, the response to 3 mmol/L GMP alone
or the response induced by the synergism between 0.5 mmol/L GMP and 100
mmol/L MSG was practically unaffected by amiloride (over the range of
concentrations examined) (Nakamura and Kurihara 1991
).
These results suggest that the response to MSG alone contains a
component derived from the sodium ion, but that the response to GMP
alone or to MSG and GMP together is independent of the sodium
component. In other words, the response to GMP alone or to MSG and GMP
together reflects purely a umami component.
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Umami taste as a basic taste |
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TOPABSTRACTHistory of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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The umami taste fulfills criteria 1, 2 and 3. The fact that the umami
taste is independent of the salt response in dogs speaks in part to
criterion 4. In addition, Ninomiya and Funakoshi (1989)
showed that in the glossopharyngeal nerve of certain species of mice,
there were single fibers that were sensitive only to MSG or mixtures of
MSG and the nucleotides, and insensitive to the other basic taste
stimuli. Baylis and Rolls (1991)
showed that in the
taste cortex and adjoining orbitofrontal cortex of the macaque monkey,
single neurons were observed that were tuned to respond best to MSG.
Thus, the umami taste clearly fulfills criterion 4, and we can conclude
that the umami taste is a fifth basic taste.
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Agonist and modulator properties of umami substances |
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TOPABSTRACTHistory of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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). The synergism between MSG and the nucleotides is
not robust in monkeys. In mice, MSG alone induced a large umami
response in the glossopharyngeal nerve (Ninomiya and Funakoshi 1989
), and therefore MSG is considered an agonist in this
species. In dogs, GMP or IMP alone induces a large response
(Kumazawa and Kurihara 1990
, Kumazawa et al. 1991
, Nakamura and Kurihara 1991
), indicating
that the nucleotides are the primary agonists, whereas MSG is a
modulator. Thus the function of MSG as a modulator or agonist varies
with the species of animal. |
Comparison of glutamate receptors in brain with umami receptors |
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TOPABSTRACTHistory of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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). Stimulation of group I
receptors with agonists activates adenylyl cyclase, protein kinase C
and phospholipase C. mGluR1 and mGluR5 are thus excitatory receptors.
On the other hand, stimulation of group II or III receptors with
agonists inhibits adenylyl cyclase; they are thus classed as inhibitory
receptors.
Chaudhari et al. (1996)
reported that mGluR4 is
expressed in rat papillae-bearing taste buds and suggested that
mGluR4 may be a chemosensory receptor responsible for umami taste.
Bigiani et al. (1997)
examined the actions of glutamate
on the membrane properties of rat taste cells using whole-cell
patch-clamp techniques. In the majority of taste cells, application of
glutamate induced "sustained" glutamate responses, which consisted
of an outward current (reduction of the maintained inward current).
L(+)-2-Amino-4-phosphonobutyric acid (L-AP4), a
specific agonist of mGluR4 receptors, mimicked the sustained glutamate
responses.
In psychometric studies in humans, we have evaluated the intensity of
the umami taste induced by various glutamate agonists (Kurihara
and Kashiwayanagi 1999>). A solution containing 0.5 mmol/L GMP
and 1.5 mmol/L MSG together elicited a umami taste that was much
stronger than that of 20 mmol/L MSG alone. The intensity of the umami
taste induced by a solution containing 0.5 mmol/L GMP and 1.5 mmol/L of
each of several glutamate receptor agonists was also evaluated and
compared with the response to MSG alone at each of several
concentrations. In combination with GMP, ibotenate induced a rather
strong umami taste, whereas L-AP4 and
(±)1-aminocyclopentane-trans-1,3-dicarboxylic acid
(ACPD) induced a weak umami taste; kainate, NMDA and AMPA induced no
umami taste (Table 1
). The results suggest that the umami receptor is not a subtype of an
ionotropic receptor. L-AP4 in the presence of GMP elicited
umami taste, although AP4 is an agonist at mGluR4, an inhibitory
receptor. Because MSG induces a large response in the taste nerve, a
receptor for umami taste should be an excitatory receptor. Thus, it is
unlikely that the mGluR4 receptor is a receptor for umami taste,
although AP4 has an umami taste. The agonist specificity of the mGluR1
and mGluR5 receptors, which are excitatory, is different from that of
the umami receptor. It is concluded that the receptor for umami taste
is not identical to any known glutamate receptors, and thus there seems
to be a unique receptor mediating the umami taste.
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Great contribution of amino acids, umami substances and salts to taste of foods |
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TOPABSTRACTHistory of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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showed that the
characteristic tastes of many natural foods are reproduced by mixing
amino acids, umami substances and salts in appropriate ratios.
Regarding amino acids, although various species are contained in foods,
only a small number are required to produce the characteristic tastes
of foods. As described above, umami substances are also essential to
produce the characteristic tastes of many foods.
Salts also are essential for producing the characteristic tastes
of many foods. Thus, a mixture of amino acids and umami substances in
the absence of salts can impart a weak taste, and one that is quite
different from that of the parent foods. To confirm the effects of
salts on the taste of amino acids, psychometric studies were conducted
using a solution containing alanine, glycine or serine (which have a
sweet taste) (Ugawa et al. 1992
). The sweetness of these
amino acids was greatly enhanced by the addition of NaCl. The addition
of sodium phosphate also enhanced the sweetness of the amino acids, but
its enhancing effect was much less than that of NaCl.
The effects of salts on the taste of amino acids were also examined in
animals. The enhancing effects of salts were not observed in rats, but
were observed in dogs (Ugawa and Kurihara 1993
). The
responses to most amino acids examined were greatly enhanced by the
presence of salts, but the degree of enhancement varied with the
species of amino acids. The enhancing effects were dependent on the
species of both cations and anions. That is, the responses to most
amino acids were enhanced by sodium, potassium and calcium salts, but
not magnesium salts. NaCl was much more effective than sodium
phosphate.
The canine taste nerve responses to umami substances were also enhanced
by the presence of salts (Ugawa and Kurihara 1994
). That
is, the responses to MSG, GMP or the combination of MSG and GMP were
enhanced by salts. Similar to the effects of salts on the responses to
amino acids, the effects of the salts on the umami responses depended
on the species of both cation and anion. It should be noted that the
canine taste nerve responses to sugars were also enhanced by the
presence of salts (Kumazawa and Kurihara 1990a
). In
humans as well, the sweetness of sugars is enhanced by NaCl.
Salts carrying organic cations such as choline and N-methyl-D-glucosamine (which are impermeable to taste cell membranes) were also found to be effective in enhancing the responses of chemical stimuli. Hence, the enhancing effects of salts were not explained simply in terms of ion permeability at the apical membranes of taste cells. We hypothesize that the binding of both cations and anions to taste receptor membranes may induce exposure of the receptor sites for amino acids, umami substances and sugars.
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FOOTNOTES |
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3 Abbreviations used: ACPD,
(±)1-aminocyclopentane-trans-1,3-dicarboxylic acid;
AMPA, (RS)–amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid;
L-AP4, L(+)-2-amino-4-phosphonobutyric acid;
GMP, disodium guanylate; IMP, disodium inosinate; MSG, monosodium
glutamate; NMDA, N-methyl-D-aspartic acid.
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REFERENCES |
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TOPABSTRACTHistory of physiological studies...Canine taste nerve responses...Umami taste as a...Agonist and modulator properties...Comparison of glutamate...Great contribution of amino...REFERENCES |
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1. Adachi A., Funakoshi M., Kawamura Y. Neurophysiological studies on taste effectiveness of chemical taste enhancers. Hayashi T. eds. Olfaction and Taste 1967;Vol. II:411-413 Pergamon Press Oxford, UK.
2. Baylis L. L., Rolls E. T. Responses of neurons in the primate taste cortex to glutamate. Physiol. Behav. 1991;49:973-979[Medline]
3.
Bigiani A., Delay R. J., Chaudhari N., Kinnamon S. C., Roper S. D. Responses to glutamate in rat taste cells. J. Neurophysiol. 1997;77:3048-3059
4.
Chaudhari N., Yang H., Lamp C., Delay E., Cartford C., Than T., Roper S. J. Neurosci 1996;16:3817-3826
5. Konosu S., Hayashi T., Yamaguchi K. Role of extractive components of boiled crab in producing the characteristic flavor. Kawamura Y. Kare M. R. eds. Umami: A Basic Taste 1987:235-253 Marcel Dekker New York, NY.
6.
Kumazawa T., Kurihara K. Large enhancement of canine taste responses to sugars by salts, J. Gen. Physiol. 1990a;95:1007-1018
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Kumazawa T., Kurihara K. Large synergism between monosodium glutamate and 5'-nucleotides in canine taste nerve responses. Am. J. Physiol. 1990b;259:R420-R426
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9. Kuninaka A. A flavor potentiator. Schults H. W. Day E. A. Libbey L. M. eds. The Chemistry and Physiology of Flavors 1967:517-535 AVI Publ Westport, CT.
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11. Nakamura M., Kurihara K. Non-specific inhibition by amiloride of canine chorda tympani nerve responses to various salts: do Na+-specific channels exist in canine taste receptor membranes?. Brain Res 1990;524:42-48[Medline]
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13. Ninomiya Y., Funakoshi M. Qualitative discrimination among "umami" and the four basic taste substances in mice. Kawamura Y. Kare M. R. eds. Umami: A Basic Taste 1989:365-385 Marcel Dekker New York, NY.
14. Sato M., Yamasita S., Ogawa H. Patterns of impulses produced by MSG and 5'-ribonucleotides in taste units of the rat. Hayashi T. eds. Olfaction and Taste 1967;Vol. II:399-410 Pergamon Press Oxford, UK.
15. Tanabe Y., Nomura A., Masu M., Shigetomo R., Mizuno N., Nakanishi S. Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J. Neurosci. 1993;13:1372-1378[Abstract]
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Ugawa T., Konosu S., Kurihara K. Enhancing effects of NaCl and Na phosphate on human gustatory responses to amino acids. Chem. Senses 1992;17:811-815
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) and presence (
) of 0.5 mmol/L
disodium guanylate (GMP). Right panel: A schematic
allosteric model for synergism between MSG and GMP.
) as a function of the logarithmic
concentration of amiloride, where Ro and R represent the magnitude of
the response before and after treatment with amiloride, respectively.