Comparative Biochemistry and Physiology Part B 129 Ž2001.

243᎐249

Review

Glucose intolerance in teleost fish: fact or fiction?

Thomas W. MoonU
Department of Biology, Uni¨ ersity of Ottawa, P.O. Box 450, Stn A, Ottawa, ON, Canada K1N 6N5

Received 28 August 2000; received in revised form 30 November 2000; accepted 8 December 2000

Abstract

Teleost fish are generally considered to be glucose intolerant. This mini-review examines some of the background and
the possible mechanistic bases for this statement. Glucose intolerance is a clinical mammalian term meaning that a
glucose load results in persistent hyperglycemia. Teleost fish show persistent hyperglycemia that is generally coincident
with transient hyperinsulinemia. The fact that teleost generally have high plasma insulin compared with mammals
implies insulin-deficiency is not a suitable explanation for this persistent hyperglycemia. Instead, peripheral utilization of
glucose is probably the principle cause of hyperglycemia. Recent evidence for muscle insulin receptors, glucose
transporters and hexokinaserglucokinase is reviewed and future experimental directions are suggested. If by altering
peripheral glucose utilization fish could become more glucose tolerant, costs to the aquaculture industry may be
substantially reduced. 䊚 2001 Elsevier Science Inc. All rights reserved.

Keywords: Fish; Glucose intolerance; Glucose utilization; Insulin; Insulin receptors; GLUT; Hexokinase; Glucokinase; Glucose-6-
phosphatase; Diet

1. Introduction cussed some of these issues ŽMommsen and

Teleost fishes are generally considered to be
glucose intolerant. The purpose of this short re-
view is to examine glucose tolerance in fish, dis-
cuss potential explanations that may account for
intolerance, and finally present some ideas that
may direct our further study within this area. The
reader is directed towards reviews that have dis-
U
Corresponding author. Tel.: q1-613-562-5800, ext. 6002;
fax: q1-613-562-5486.
E-mail address: tmoon@science.uottawa.ca ŽT.W. Moon..
Plisetskaya, 1991; Wilson, 1994..
2. Glucose intolerance
Glucose intolerance is a term that refers to the
inability of an organism to rapidly deal with a
glucose load. The consequences are persistent
hyperglycemia and in many cases, reduced growth.
Glucose intolerance is a clinical term used in the
diagnosis of insulin-dependent diabetes mellitus
ŽIDDM. and is assessed by the use of a glucose
tolerance test ŽGTT.. A GTT involves administer-

1096-4959r01r$ - see front matter 䊚 2001 Elsevier Science Inc. All rights reserved.
PII: S 1 0 9 6 - 4 9 5 9 Ž 0 1 . 0 0 3 1 6 - 5
244 T.W. Moon r Comparati¨ e Biochemistry and Physiology Part B 129 (2001) 243᎐249

ing a bolus of glucose either orally or intra-
venously, and if plasma glucose values do not
return to baseline within 1᎐2 h, the subject
Žs human. is considered to have impaired glu-
cose tolerance. The GTT has been used in many
fish studies to test glucose tolerance and in most
cases, hyperglycemia is persistent.
Table 1 provides a partial list of fish species
where GTT have been performed. Since the early
observations of Phillips et al. Ž1948. and Falkmer
Ž1961., the data consistently show that teleost
fishes show persistent hyperglycemia after a glu-
cose load. The important point noted on Table 1,
however, is that the time period of hyperglycemia
is species- and condition-dependent. Furuichi and
Yone Ž1981. using the same glucose dose, demon-
strated that the most severe hyperglycemia oc-
curred in the carnivorous yellow tail, and the least
in the omnivorous carp. In general, the more
carnivorous is the species, the longer time needed
to clear a glucose load. Wilson Ž1994. has sug-
gested that marine species are more tolerant of a
glucose load than freshwater species, although
other data dispute this observation ŽGarcia-Riera
and Hemre, 1996a,b.. Finally, there are differ-
ences in tolerance observed between chinook sal-
mon strains ŽMazur et al., 1992..
The conditions of the test species are also key
to its glucose tolerance. Again, Furuichi and Yone
Ž1981. fed a 0, 10 and 40% dextrin diet to carp,

Table 1
A partial list of teleost fish species where glucose tolerance tests have been performedc

Species Routea Dose Insulin change Comments

Žmgrkg.
b
Palmer and Ryman, 1972 O ND Hyperglycemia at least to 7 h
Rainbow trout Pre-spawning females ᎏ mild hyperglycemia
Insulin injection ᎏ mild hyperglycemia

Harmon et al., 1991 IP 300 x Hyperglycemia at least to 18 h

Rainbow trout

Blasco et al., 1996 IV 500 ­Ž; 2.5. Hyperglycemia corrected by 8 h fasting

Brown trout Increased hyperglycemic response

Mazur et al., 1992 O 1670 ­Ž; 2. Hyperglycemia at least to 36 h

Chinook salmon Strain and diet differences observed

Wilson and Poe, 1987 O 1670 ND Hyperglycemia corrected by 6 h

Channel catfish Hyperglycemia also to fructose, maltose, sucrose and dextrin

Ottolenghi et al., 1995 IV 250 ND Hyperglycemia corrected by 11 h

Channel catfish

Falkmer, 1961 IM 500 ND Hyperglycemia at least to 9 h

Daddy sculphin

Furuichi and Yone, 1981

Carp O 167 ­Ž; 3. Hyperglycemia related to diet Žapprox. 5 h for carp;
longer for other species.
Red sea bream ­Ž; 2. Hyperglycemia dependent upon prior feeding with dextrin
Yellow tail ­Ž; 2.

Wright et al., 1998

Tilapia IP 2000 ND Hyperglycemia exceeded 6 h

Ince and Thorpe, 1974 IV 500 ND IV ᎏ hyperglycemia corrected by 9 h

Silver European eels O O ᎏ minor hyperglycemia
a
Route indicates the method used to increase glucose content: O, oral; IV, intravenous; IM, intramuscular; IP, intraperitoneal.
b
A dose of 1 g glucose given orally, but fish weights were not reported.
c
ND, not done.
 T.W. Moon r Comparati¨ e Biochemistry and Physiology Part B 129 (2001) 243᎐249
red sea bream and yellow tail; the highest dextrin
content resulted in the highest hyperglycemia and
lowest insulin levels. Glucose tolerance is im-
proved in chinook salmon strains previously fed a
high starch diet ŽMazur et al., 1992.. Pre-spawn-
ing female rainbow trout show a mild hyper-
glycemia that is short lived and pre-injecting
insulin always lead to a decrease in the hyper-
glycemic response ŽPalmer and Ryman, 1972..
Also the route of glucose dosing alters the hyper-
glycemic response, at least in the European eel
ŽInce and Thorpe, 1974., and the glucose concen-
tration used in the test ŽTable 1.. Prolonged
food-deprivation compared with feeding will gen-
erally extend the period of hyperglycemia ŽBlasco
et al., 1996; Legate et al., 2001.. And finally, the
source of starch can also affect the hyperglycemic
response to a glucose load ŽHemre and Hansen,
1998..
Certainly these studies and many others indi-
cate teleost fish clear a glucose load more slowly
than mammals. This has lead a number of investi-
gators to suggest that teleost fish are an adequate
IDDM model Žsee Kelley, 1993 and below.. This
idea was strengthened by the early observations
of Palmer and Ryman Ž1972. that insulin injection
promoted hypoglycemia in fasted rainbow trout
and improved glucose tolerance when given
together with glucose. As with IDDM in humans,
insulin seemed to be the reason for glucose in-
tolerance in fish.
There are a number of possible explanations
for glucose intolerance in fish. A simple cartoon
ŽFig. 1. demonstrates these various possibilities.
Basically two major possibilities exist. One is at
the level of insulin concentrations in the blood.
Two is the peripheral utilization of glucose which
in mammals, at least, is linked to the existence of
insulin receptors and glucose transporters.
3. Insulin in the blood of teleost fish
The simplest explanation for the lack of glu-
cose clearance would be a low level of blood
insulin. This 51᎐58 amino acid peptide is ar-
ranged in A and B chains, linked through critical
disulfide bridges. The biochemistry and physi-
ology of this peptide in fishes has been extensively
reviewed ŽMommsen and Plisetskaya, 1991;
Plisetskaya, 1995.. Suffice it to say that the struc-
ture of this hormone and its receptor are well
245
Fig. 1. Cartoon showing the interactions thought to occur in
mammals between blood glucose and glucose uptake in the
two most significant glucose-sensitive tissues Žskeletal muscle
and adipose tissue. and liver. Question marks are components
of the pathway that have not been confirmed in fish. Dotted
lines represent the mammalian pathway between the IR and
GLUT, while the dashed line is a more direct pathway that
may involve changes in GLUT transcription. Neither pathway
has been shown to exist in fish. GLUT, Naq-independent
facilitative glucose transporter; IR-RTK, insulin receptor-re-
ceptor tyrosine kinase; GK, glucokinase; HK, hexokinase; Glu,
glucose; G6-P, glucose 6-phosphate.
conserved across the vertebrates. Importantly, al-
though glucose-stimulated insulin release has
been reported in vivo and in vitro in some fish
species, amino acids Žespecially arginine. are a
more potent insulin secretagogue in most species
Žsee Mommsen and Plisetskaya, 1991.. But even
more importantly, insulin levels are in the 0.2᎐5
nM range, values that tend to be higher than
found in mammals ŽMommsen and Plisetskaya,
1991.. As noted by Plisetskaya Ž1998., however,
the radioimmunoassay of insulin may also detect
pro-insulin, and it is not clear whether this pre-
cursor peptide has any specific physiological role
in fish.
Until such time that pro-insulin can be mea-
sured in a fish, all that can be said is that gener-
ally insulin levels in fish are comparable with
those of mammals where blood glucose is more
precisely controlled. Certainly the potency of glu-
cose as an insulin secretagogue could be impor-
tant, but as noted on Table 1, hyperglycemia
generally does result in hyperinsulinemia where
the hormone has been studied. The one exception
is the study of Harmon et al. Ž1991. where insulin
levels transiently fell. The authors showed that
sommatostatin-25 levels rose with glucose chal-
lenge, and this hormone is known to decrease
insulin release. Glucose does activate glucokinase
246 T.W. Moon r Comparati¨ e Biochemistry and Physiology Part B 129 (2001) 243᎐249
in catfish Brockmann bodies, implicating this en-
zyme as a glucose sensor, just as in mammals
ŽRonner, 1991.. These studies imply that fish may
be a good model of non-insulin-dependent dia-
betes ŽWilson, 1994. rather than IDDM as previ-
ously suggested ŽKelley, 1993..
Obviously other hormones may alter plasma
glucose levels in fish. This could include glucagon,
glucagon-like peptide ŽGLP., insulin-like growth
factor ŽIGF., growth hormone, the somatostatins,
cortisol and even catecholamines. It was not the
purpose of this review to examine these other
hormones, but reference to them can be found in
Harmon et al. Ž1991., Mommsen and Plisetskaya
Ž1991., Plisetskaya Ž1995. and Navarro et al.
Ž1999.. Certainly the relationship between insulin
and glucagon and GLP is not as well defined as it
is in mammals and in fact there may be a dissoci-
ation between these hormones ŽMommsen and
Plisetskaya, 1991.. It is critical, however, that any
study examining glucose tolerance must also in-
clude these other hormones.
If plasma insulin levels are not critically impor-
tant to plasma glucose levels, what of peripheral
glucose utilization?
4. Peripheral utilization of glucose by teleost fish
Resting glucose turnover rates for fish species
are in general 20᎐100 times lower than values
reported in mammals of equivalent body mass,
consistent with their lower body temperatures
and metabolic rates Žsee Weber and Zwingelstein,
1995.. Blasco et al. Ž1996. have reported that
brown trout increased the rate of glucose disap-
pearance by only 1.3-fold after an IV glucose load
of 500 mgrkg that raised plasma glucose four- to
five-fold and insulin levels by approximately 2.5-
fold. Even so, in this experiment glucose uptake
by red and white muscles increased by four- and
three-fold, respectively. Exercise is also known to
increase glucose utilization by red skeletal muscle
of trout Žsee Weber and Zwingelstein, 1995.. On
a total tissue weight basis, muscle represents ap-
proximately 50% of total body weight, and must
be considered to be key to the disposal of glucose
from the blood in fish. Certainly it is both muscle
and adipose tissue in mammals that are uniquely
designed to dispose of a glucose load ŽKlip et al.,
1996; Zierler, 1999..
Glucose crosses tissue membranes by carrier-
facilitative transport. There are at least five Naq-
independent glucose transport isoforms in mam-
mals, collectively called GLUT, with GLUT-1 and
-4 found in skeletal muscle and adipose tissue
ŽKlip et al., 1996; Zierler, 1999.. When insulin
binds to its membrane receptor, GLUT-4 moves
from an intracellular to a membrane position,
enhancing the movement of glucose into the mus-
cle cell Žsee Fig. 1.; GLUT-1 is thought to be
constitutively expressed. Whether such a system
exists in fish is not clear.
Wright et al. Ž1998. were unable to detect
either GLUT-1 or -4 mRNA or protein in skeletal
muscle of tilapia using mammalian probes. Using
the identical techniques, Legate et al. Ž2001. were
also unable to demonstrate any mammalian
GLUT homologue in muscle of rainbow trout,
brown bullhead or American eel, even though
glucose uptake into skeletal muscle membrane
vesicles followed hyperbolic kinetics. However, at
this conference, Planas et al. Ž2000. presented
phylogenetic evidence for a GLUT-4 homologue
in brown trout muscle. Whether this homologue
is an insulin-dependent GLUT awaits further in-
vestigation.
Insulin receptors do exist on skeletal muscle
from a number of fish species. Gutierrez ´ and
colleagues Žreviewed by Navarro et al., 1999. re-
port fewer muscle insulin receptors in fish than
mammals and higher receptor numbers in herbiv-
orous than carnivorous fish species. In addition,
fasting decreases and hyperinsulinemia down-
regulates receptor numbers Žsee Navarro et al.,
1999.. Insulin binding to its receptors activates
receptor tyrosine kinase, but it may be that the
signaling pathway beyond the receptor differs
between fish and mammals; this has yet to be
studied. Certainly one of the most intriguing is-
sues with fish is that the number of IGF-I Žin-
sulin-like growth factor-I. receptors exceeds those
of insulin in all species examined to date ŽNavarro
et al., 1999.. IGF-I receptors are linked to devel-
opmental changes, but whether IGF-I has a
metabolic role is not clear.
These studies demonstrate that fish skeletal
muscle does express facilitative glucose trans-
porters, possibly a mammalian GLUT homo-
logue, and insulin receptors but whether these
two systems are coupled as in mammals is un-
known. GLUT-4 in null mice do show higher
blood glucose and insulin values, but these dif-
ferences were gender-dependent and did not
 T.W. Moon r Comparati¨ e Biochemistry and Physiology Part B 129 (2001) 243᎐249
clearly demonstrate a dysfunction in glucose
homeostasis ŽKatz et al., 1995.. Glucose intoler-
ance in fish may at least partly be explained by
either low activity or numbers of these
transporters andror receptors, as previously sug-
gested Žsee Navarro et al., 1999., but there are
other possibilities ŽFig. 1..
Once inside the cells, glucose must be phos-
phorylated to glucose-6-phosphate by a hexoki-
nase ŽHK. to ensure favorable glucose gradients
for transport. Hexokinases are a family of en-
zymes designated HK I᎐IV or A᎐D in mammals
ŽIynedjian, 1993.. These are either high ŽHK I᎐III;
K m ( 0.1 mM glucose. or low ŽHK IV or glucoki-
nase, GK; K m ) 5 mM. affinity enzymes, with GK
being present in the liver and endocrine pancreas
of mammals. Glucokinase expression is required
for normal plasma glucose levels and insulin-
secretion rates in mammals as demonstrated in a
GK-transgenic mice model ŽNiswender et al.,
1997.. This requirement reflects the key role that
glucose plays in the mammalian liver regulating
enzymes of glycolysis, gluconeogenesis and li-
pogenesis. Fish tissues, including muscle, express
a high affinity HK ŽMoon and Foster, 1995..
Tranulis et al. Ž1996. did report hepatic GK activ-
ities in Atlantic salmon and recent studies de-
monstrate a carbohydrate-induced GK mRNA ex-
pression and GK activity in rainbow trout, gilt-
head seabream and common carp ŽPanserat et al.,
2000a.. Induction is linked to increased plasma
glucose values in these species, although all
changes were much reduced for the omnivorous
carp. Minor alterations were noted in HK activi-
ties in this study.
The role of the liver in glucose tolerance is not
as clear in fish as in mammals. Insulin receptors
are present Žsee Navarro et al., 1999. but the
existence of a GLUT has not been shown. Blasco
et al. Ž1996. did report 2-deoxyglucose uptake and
phosphorylation in the liver of brown trout, but
rates were low reflecting what the authors as-
sumed to be high glucose-6-phosphatase ŽG6Pase.
activities. Whether brown trout have an inducible
hepatic GK is not known, but this report did show
that uptake and phosphorylation of glucose are
well coupled. High plasma glucose should reduce
hepatic glucose output in an insulin-dependent
manner ŽZierler, 1999., but if not, this could
exaggerate plasma glucose levels in fish receiving
a glucose load. The contrary enzyme to HKrGK
is G6Pase, and there is agreement in the mam-
247
malian literature that the glucose-repression of
this enzyme is required for normal glycemia. In-
terestingly, Panserat et al. Ž2000b. were unable to
show glucose repression of rainbow trout G6Pase
mRNA. Further studies are needed to clarify the
role of the liver in teleost glucose homeostasis.
Panserat et al. Ž2000a. do conclude that things
other than GK must be involved as levels of this
enzyme and its induction were lowest in the om-
nivorous carp compared with the more carnivo-
rous species of trout and seabream, a result con-
trary to expectations.
5. Perspectives
This short review can not answer the question
‘are teleost fish glucose intolerant’? Certainly the
long held view that they are must be tempered by
new data that are noted here, including species-
specific sensitivities, existence of hepatic carbohy-
drate-inducible GK activities, and existence of
skeletal muscle GLUT. So what research ques-
tions need to be addressed?
1. The issue of metabolic rate is overlooked in
all studies of glucose intolerance. The aver-
age fish has an oxygen consumption rate
one-tenth that of mammals. The implication
is that blood flows, nutrient uptake, nutrient
demands, etc. will scale accordingly. Certainly
this is the case for glucose turnover ŽWeber
and Zwingelstein, 1995., so why should teleost
fish clear a glucose load as quickly as a simi-
lar sized mammal? In fact, if they did one
might question why they do! Looking at tuna
with their high glucose turnover and metabolic
rates compared with other teleosts ŽWeber
and Zwingelstein, 1995. might address this
issue; a very difficult experiment indeed.
2. The presence of a muscle GLUT in fish must
be confirmed. As noted above, a GLUT ho-
mologue has been identified ŽPlanas et al.,
2000., but is this GLUT coupled to the in-
sulin receptors known to exist in fish muscle?
The signaling pathway between the insulin
receptor and the GLUT needs to be es-
tablished. There is some evidence that the
linkage of GLUT to specific hexokinase iso-
forms in mammalian skeletal muscle may lead
to insulin resistance ŽEbeling et al., 1998.,
and this possibility must be considered in fish.
248 T.W. Moon r Comparati¨ e Biochemistry and Physiology Part B 129 (2001) 243᎐249
3. It is unlikely that insulin-deficiency is respon-
sible for glucose intolerance, but the biologi-
cally-active insulin levels in blood need to be
determined. Does pro-insulin contribute sig-
nificantly to the content of insulin measured
in the radioimmunoassay ŽPlisetskaya, 1998.?
If so, does pro-insulin play any metabolic
role?
4. Obviously other hormones may impact upon
glucose tolerance. Glucagon, GLP, IGF,
growth hormone, the somatostatins, cortisol
and the catecholamines may all be important.
As noted in the paper by Kelley et al. Ž2001.,
islectomy in the goby results in a diabetic-like
condition after 15᎐20 days. This delay may be
due to an absence of glucagon and possibly
directed by cortisol. Few studies have looked
at multiple hormones as the key to glucose
utilization.
5. Given that hormones other than insulin may
be involved, the use of glucose may also be
affected by other nutrients within a diet.
Diets high in carbohydrate are generally de-
signed to be isocaloric by modifying levels of
lipids and protein; might such changes affect
the use of carbohydrates especially if these
‘other’ hormones alter the handling of lipids
or proteins? Obviously total diet composition
must to be examined to estimate nutrient
interactions.
6. Does the liver play any role in fish glucose
utilization? In mammals the presence of GK
is key to normal glucose homeostasis
ŽNiswender et al., 1997.. Is this the case for
fish? Transient expression of trout embryos
with human GLUT-1 and rat hexokinase II
increased 3-O-methylglucose uptake and oxi-
dation of glucose ŽKrasnov et al., 1999.. Such
studies are a start to potentially addressing
this issue. The issue of G6Pase also needs to
be addressed to see whether the hepatic
GKrG6Pase cycle is a key component to
glucose intolerance.
It is clear that more work is necessary espe-
cially with regards to the differences between
those teleost species that can utilize high car-
bohydrate diets effectively compared with the car-
nivorous salmonids that seem to be preferred by
the aquaculture industry. Molecular biology tools
will greatly assist in these efforts. Enhancing the
carbohydrate tolerance of species under aquacul-
ture will decrease food costs, decrease demand
for fish mealroil and reduce environmental pollu-
tion resulting from high nitrogenrphosphorous
meals. Each of these will have a positive impact
upon the aquaculture industry and the perception
of the industry by the general public.
Acknowledgements
I would like to acknowledge discussions with
Tom Mommsen, Kevin Kelley and Josep Planas
at the 4th International Symposium on Fish En-
docrinology in Seattle, WA. These discussions
helped focus some of my thinking on these issues.
Also, thanks to the Natural Sciences and Engi-
neering Research Council of Canada for support-
ing my research program.
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