Académique Documents
Professionnel Documents
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679-690, 1988
Printed in Great Britain
MINI-REVIEW
LIPID DYNAMICS IN FISH: ASPECTS OF
ABSORPTION, TRANSPORTATION, DEPOSITION
AND MOBILIZATION
MARK A. SHERIDAN
Department of Zoology, North Dakota State University, Fargo, ND 58105, USA (Tel.: 701-237-81I0)
(Received 2 September 1987)
Al~raet--1. Aspects of lipid metabolism, including absorption and depositional processes, appear quite
different in fish as compared to homeothcrrnic vertebrates.
2. Dietary lipids in fish arc absorbed as fatty acids and as triacylglycerois aggregated into chylomicra
particles.
3. Interorgan transport of lipids, like that of mammals, consists of an exogenous (dietary) loop and
an endogenous loop.
4. Fish store lipids among several depot organs, including mesenteric membranes, liver and muscle.
5. Several fast-acting and slow-acting agents modulate depot lipid mobilization.
6. Mobilized lipids may be transported in the serum as free fatty acids bound to specific carrier proteins.
INTRODUCTION
680
MARK A. SHR]DAN
DIETARY
UPID
I.
digestion
2o absorption
LIPID DEPOTS
INTESTINE
3. de novo
TTpo-'~esi s
from CHU
7. de novo
4. Assembly of
transport
]ipoproteins
8. Mobilization
of stored
]ipid by TG
lipase
PERIPHERY
I0. B-oxidation
TTpo--g-~'esis
from CHO
5. Transport of lipid
via lipoproteins
to storage and
utilizing tissues
II. Packaging of
export lipids
(yolk, milk,
etc.)
9o Transport of
mobilized lipid
as albumin-bound
FA
6. Clearance of lipid
from ECF by
lipoprotein lipase
Oh
lh
2h
oe
4h
8h
pe
Do~
16h
J,,
human
pee
0
m
D D,
DQ,
D~L
D~L
ii
m
m
limb
$2
MM
me
--
!. . . . . . . . . . . . . . . . . . . .
a
e{
Fig. 2. Effects of lipid load on serum lipoprotein distribution in steelhead trout, Salmo gairdnerii. 10 #1
of serum was incubated with 5/~l of Sudan Black B-ethylene glycol for 24 hr prior to electrophoresis.
Dotted lines indicate boundary between stacking gel and separation gel, and the location of tracking dye;
solid lines indicate major components; dashed lines indicate minor components. Number indicates hours
after feeding; human serum reference I hr postprandial. (Reprinted with permission from Sheridan et al.,
1985a, Pergamon Press Journals).
681
SLOW COMPONENT
PERIPHERAL TISSUES
PERIPHERAL TISSUES
Fig. 3. Two-steplipid absorption model. Fast component is a fatty acid deliverysystem. Slow component
represents a TO delivery system wherein TG are aggregated into chylomicra particles. NEFA,
nonestefified fatty acids; TG, triacylglycerols.(Reprinted with permission from Sheridan et al., 1985a,
Pergamon Press.)
approximately 80% triacylglycerol (Sheridan et al.,
1985a). Rapid appearance (within 30 rain) of FFA
(Robinson and Mead, 1973; Kayama and Iijima,
1976) followed by the subsequent appearance of TG
and chylomicra, lead Vernier and Sire (1983) and
Sheridan et al. (1985a) to independently postulate a
two-step lipid absorption model for fish (Fig. 3). The
model consists of a fast component and a slow
component. The fast component represents an FFA
delivery system that consists of short-chain FFA that
are soluble in plasma and longer-chain FFA that are
presumably bound to carrier proteins. This component explains the radiolabel data of Robinson and
Mead (1973) and of Kayama and Iijima (1976). The
slower component represents a TG delivery system
that consists of the aggregation, extrusion and transport of TG-rich particles, a mechanism similar to that
used by mammals.
Transport
EXOGENOUG PATHWAY
DIETARY LIPID
BILE COMPONENTS
FA
LPL
A"t
TG
A-I
TG
A-I
A-II
Fig. 4. Exogenousand endogenous lipid transport pathways in fish. (Adopted after mammalian model
from Goldstein et al., 1983.)
MARK A. SI-IF.R~AN
682
*OSOS*g
A
B
D
,,E
~F
/a
.
4Fig. 5. Trout (Salmo gairdneri) serum lipoprotein components prestained with Sudan Black B as in Fig. 2 and
separated by polyacrylamide gel electrophoresis (7.5%
monomere concentration). The electrophoretic pattern depicted represents a typical 2 hr postprandial profile. Dotted
fines indicate boundary betweenstacking gel and separation
gel, and the location of tracking dye. A, chylomicra;B, very
low density lipoprotein; C and D, low density lipoprotein
components. C and D may also contain slow high density
lipoprotein components. E and F, high density lipoprotein
components, G-I, fatty acid binding proteins.
Table I. Lipid and protein composition of rainbow trout Salmo gaird~terU lipoproteins (%)
Lipoprotein
Component
Triacyiglycerol
Cholesterol
Chole~-ryl ester
Phospholipid
Protein
Major apoproteins
Chylomicra
74.6*
2.2*
5.9*
10.4"
6.7*
A-l, B~
VLDLt
41.9/38.5
6.9/I 1.5
15.1/26.7
26.5/16.1
9.6/7.2
n/B, C
LDLt
26.9/12.5
6.7/9.5
15.6/27.9
27.1/14.9
24.7/35.2
It/it
HDLt
1.5/5.7
3.4/4.1
7.7/20.1
26.5/27.9
46.9/42.2
A-l, A-II/
A-I, A-If
683
Lipid c~u
Species
PL
TG
CHOL
FA
6.2
26
20
22
7.5
529
113
46
17
11
5.5
3
1.2
2.3
5.8
39
21
25
5.2
535
10
10
5
7
0.2
0.2
0.6
1. I
0.03
0.5
5
2
6.2
2
1.5
4.4
CE
WE
Total
1.23
2.2
527
137
62
46
25
0.10
0.66
54O
47
27
3O
14
Trout
gairdnerii *
(Juvenile; FW parr)
MF
DM
LM
L
S
S. gairdnerii ]
(Juvenile; FW smolt)
MF
DM
LM
L
S
S. goirdherii 2
(Adult FW resident)
DM
LM
L
Salmon
Oncorhynchus kisutch 3
(Juvenile; F%V parr)
MF
DM
L
O. kisutch 3
(Juvenile; FW smolt)
MF
DM
L
Whitefish4`b
Coregonus albula
(Adult)
MF
Roe
Tilapias
Oreochromis mossambicus
LM
L
Gill
Brain
Bogue 6.b
Boops hoops
LM
L
head
skin
Haddock 7,b
Gadus aeglefinus
LM
CodS,b
Gadus callarias
LM
10
4
9.6
34
16
2.9
19
37
19.5
590
53
22
17
11
13
17
27
12
525
41
10
18
9
7.5
10
25.5
~62.7
3.3
31.6
3.8
80.4
5.3
28.2
12
8
12.1
48.7
144
169.3
0.06
1.5
0.72
1.6
0.08
0.26
3.1
51
23
26
tr
tr
625
107
6O
tr
580
62
41
tr
1.4
20c
0.02
1.7r
15.6f
3.5 t
25.5f
17.8
47.6
8.5
35
66.5
164.4
76.9
212.3
0.3
0.9
2
I
tr
tr
tr
tr
17.7
77.8
158
178
*------ 1.7 - - - *
3O
98
2.9
0.13
0.33
0.33
0.18
0.58~
5.50s
2.58
0.16
0.49
0.32
0.31
0.77e
6.04s
tSheridan et aL (1983).
2Robinson and Mead (1973).
3Sheridan (1986).
4Kaitaranta (1980).
SRao and Rao (1984).
6Kapoulas and Miniadis-Meimarogiou (1985).
7Garcia et al. (1956).
SOIley and Lovern (1954).
alncludes serum.
bCalculated from authors' original % composition data.
CData for all neutral lipids combined.
dData for CE and WE fractions combined.
CData for WE and alcohols.
fData for total cholesterol; includes both cholesterol and cholesteryl esters.
qncludes unidentified components and hydrocarbons.
Abbreviations: PL--phospholipid, TG---triac34giycerol, Chol---cholesterol, FA--fatty acid, CE---cholesteryl ester,
WE--wax ester, MF--mesenteric fat, DM--dark muscle, LM---light muscle, L---liver, S--serum, FW--fresh water,
tr--trace amounts.
M A R K A. SHERIDAN
684
the case with mammals. The primary storage molecule in higher bony fish (teleosts) is TG, however,
giyceryi ether analogs (long-chain alcohols bound to
glycerol via ether bonds) have been reported in
certain tissues of some species (Kapoulas and
Miniadis-Meimaroglou, 1985; Table 2). Some elasmobranchs use alkoxydiacylgiycerols as depot lipids
exclusively or in combination with other lipid classes,
including TG (Lovern, 1962).
The major storage sites of fish are mesenteric fat,
muscle and liver. Compositional data of various
organs in several teleostean species are listed in
Table 2. Braekken (1959) has suggested that the liver
serves a major role in sluggish, bottom-dwelling fish,
whereas skeletal muscle is important in more active
groups. Such ecological correlates are difficult to
support. For example, cod, which are deep-water
feeders but hardly sluggish, have little lipid stored in
the skeletal muscle and considerable amounts stored
in the liver. Rainbow trout, which are active surface
feeders, on the other hand, have substantial amounts
of lipid stored in skeletal muscle and support Braekken's contention. Of the two skeletal muscle types,
dark muscle appears to store more lipid than light
muscle (Robinson and Mead, 1973; Sheridan et al.,
1983; Sheridan, 1986; Table 2). Robinson and Mead,
(1973) showed that trout force-fed 14C-palmitic acid
incorporated radioactivity into dark muscle lipids
5-fold higher than into light muscle lipids.
Compositional data alone, however, do not indicate the dynamic nature of depot organs. Additional
criteria, such as possession of lipid uptake and lipid
breakdown systems reveal the physiological usefulness of the store. Lipoprotein lipase (the enzyme
controlling lipid uptake in mammals) activity has
been observed in the several depots (dark muscle,
liver and mesenteric fat) of salmonids (Black et al.,
1982; Sheridan and Allen, 1984). Mobilization of
iipids from depots is accomplished by activation of
the lipolytic enzyme, TG lipase. Lipase activity has
been observed in the liver, dark muscle and mesenteric fat of coho salmon, O. kisutch (Sheridan et al.,
1985b).
MOBILIZATION
The majority of the work on lipid mobilization has
been done on mammalian and avian adipose tissue,
the primary storage site for these animal groups. The
hydrolysis of depot fat in the rat (Rizack, 1961;
Vaughan et al., 1964; Huttunen and Steinberg, 1971;
Arnaud and Boyer, 1974; Pittman et al., 1975;
Fredrikson et al., 1981) and the chicken (Khoo
et al., 1976) is catalyzed by "hormone-sensitive"
triacylglycerol (TG) lipase, diacylglycerol hydrolase,
monoacylglycerol hydrolase and cholesteryl ester
hydrolase. The lipolytic action of these enzymes
results in the mobilization of FFA (Fredrickson and
Gordon, 1958; Vaughan and Steinberg, 1965) and the
subsequent transport of these acyl acids to peripheral
tissues (Allen, 1976). Therefore, experimental criteria
for lipid mobilization are (1) depletion of tissue total
lipid, (2) depletion of tissue triacylglycerol, (3) enhanced lipase activity, (4) increased in vitro FFA
release, and (5) elevated plasma FFA. The hormone-
685
686
MARK A. SI-~gIDAN
Agent
Epinephrine
Norepinephrine
ACTH
seconds
increases FA release2
increases lipase activity2
increases plasma FA 3
mGlucagon
?
in vivo effect in 3 hr
sGlucagon
?
in vivo effect in 3 hr
seconds
increases FA release6
increases lipase activity6
Somatostatin-14
sSomatostatin-25
?
in vivo effect in 3 hr
Urotensin II*
Arginine vasotocin
seconds
Thyroxin
Cortisol
?
in vivo effect in 24hr
?
in vivo effect in 10 days
Diethylstilbestrol
increases plasma FA ~
bGrowth hormone
oGrowth hormone
increases plasma FA 3
oProlactin
?
in vivo effect in 3-8 hr
dbcAMP
seconds
3-isobutyl- l-methylxanthine
seconds
(IBMX)
ILanson (1973).
2Sheridan (1987).
3Minick and Chavin (1970).
4Ince and Thorpe (1975).
5Sheridan (unpublished).
~heridan and Bern (1986).
7Sheridan et al. (1987).
SMcKeown et al. (1976).
9John et al. (1977).
JOMurat and Serfaty (1970).
nBarrinston et aL (1961).
nNarayansingh and Eales (1975).
t3Sinsh (1979).
i~Sheridan (1986).
ISButler (1973).
JeTakashima et al. (1972).
17Leatherland et aL (1974).
ISMeier (1972).
Species designations: m--mammalian (mixture of bovine and porcine), s--salmon, b---bovine,
o--ovine, *--synthetic Gillichthys.
Abbreviations: TG--triacylglycerols, FA--fatty acid(s).
F F A f r o m c o h o s a l m o n liver i n c u b a t e d in v i t r o
( S h e r i d a n a n d Bern, 1986).
U r o t e n s i n - I I ( U I I ) is a d o d e c a p e p t i d e s e c r e t e d by
t h e c a u d a l n e u r o s e c r e t o r y s y s t e m o f teleost fish a n d
h a s p a r t i a l a n a l o g y a n d p a r t i a l h o m o l o g y to S R I F . I n
v i v o a d m i n i s t r a t i o n o f U I I , like sSS-25, s t i m u l a t e d a
d o s e - d e p e n d e n t i n c r e a s e in p l a s m a F F A o f c o h o
s a l m o n ( S h e r i d a n e t al., 1987). I n j e c t i o n o f U I I also
r e s u l t e d in e n h a n c e d d e p o t (liver a n d a d i p o s e tissue)
lipase activity. U I I also s t i m u l a t e s fatty acid release
f r o m , a n d lipase activity in, c o h o s a l m o n liver incub a t e d / n v i t r o ( S h e r i d a n a n d Bern, 1986).
Arginine vasotocin (AVT), a neurohypophysial
h o r m o n e , is f o u n d in m o s t classes o f n o n - m a m m a l i a n
v e r t e b r a t e s . A V T injected into e i t h e r j u v e n i l e c o h o
s a l m o n (15 m U / f i s h ; M c K e o w n e t al., 1976) o r lam-
687
prey (1000mU/fish; John et a/., 1977) significantly are often subject to rhythmicity and interactions with
elevated plasma FFA 30 and 90 rain after injection, other factors (d. Meier, 1972). Ovine PRL has been
respectively. AVT injected at a dose of 150 mU/fish reported to increase plasma FFA in goldfish (Minick
decreased plasma FFA levels in salmon within 30 rain and Chavin, 1970). Leatherland etal. (1974) observed
a circadian rhythmicity in kokanee salmon plasma
(McKeown etal., 1976).
Thyroid hormones tend to reduce stored body fat PRL was followed by a rhythmicity in plasma FFA.
(Barrington et al., 1961; Narayansingh and Eales, The metabolic response to PRL appears to vary with
1975 and Singh, 1979) in fish. Radiothyroidectomy time of injection. Prolactin injections given early in
causes an increase in mesenteric fat content in rain- the day stimulate lipolysis, whereas injections given
bow trout (Norris, 1969). Injection of thyroxin (T4) later in the day favor fattening (deVlaming and Sage,
into carp results in elevated plasma FFA 24 hr after 1972). Results from our laboratory contribute further
injection (Murat and Scrfaty, 1970). Takashima et al. to the concept of rhythmicity of PRL action on lipid
(1972) reported, however, that mammalian thyroid metabolism. In vivo implantation of PRL into juvepowder (500 rag/fish) decreased plasma FFA in rain- nile coho salmon parr for 14 days strongly stimulates
bow trout by half. Chronic exposure of juvenile lipid mobilization (Sheridan, 1986). The mobilization
coho salmon parr to 1"4 for 14 days results in lipid pattern generally consisted of reduced triacylglycerol
mobilization from several storage sites: mesenteric content and enhanced lipase activity in the several
fat, dark muscle and liver (Sheridan, 1986). Although depots (liver, dark muscle and mesenteric fat). In
the mobilization scheme varies among tissues, gener- salmon smolts, however, PRL treatment, like GH,
ally, total lipids were depleted primarily from the thyroid and cortisol, had little effect on lipid mobitriacylglycerol fraction and the depletion was accom- lization. Such developmental variation in PRL effects
panied by enhanced lipase activity. Coho salmon on lipid mobilization were also observed in kokanee
smolts appeared refractory to T4 treatment (Sheridan, salmon where PRL injection into smolts failed to
1986).
increase plasma FFA (McKeown etal., 1975). The
Cortisol injections increase plasma FA in the effects of PRL on lipid metabolism also appears to
American eel, Anguilla rostrata (Butler, 1973), but involve a synergism with other hormones, particunot in the European eel, A. anguilla (Larsson and larly corticosteroids. Prolactin injected in killifish
Fange, 1977). Implantation of juvenile coho salmon (Fundulus grandis) 18 hr after a previous injection of
parr with cortisol results in lipid depletion, primarily cortisol promoted fat deposition, whereas PRL injecas triacylglycerols, accompanied by elevated lipase ted only 6 hr after steroid pretreatment promoted
activity in the liver, dark muscle and mesenteric fat lipid mobilization.
Lipolysis in liver slices is also stimulated by cAMP,
(Sheridan, 1986). Cortisol treatment failed to elicit
lipid mobilization in coho salmon smolts. The suggesting an adenylate cyclase mechanism of action
influence of sex steroids on plasma lipid levels was (though there may be other mechanisms operative
investigated by Takashima et al. (1972). Diethyl- also). Exogenous cAMP, administered to incubation
stilbestrol (DES; 2000~g/fish) injected into adult medium as dibutyryl cAMP (dbcAMP), stimulates
rainbow trout, Salmo gairdnerii, increased the plasma FFA release from coho salmon liver slices (Sheridan
lipid content from 2.8 g/dl to 4.0 g/dl. Methyl testos- and Bern, 1986). Elevated levels of intracellular
terone, however, had no effect on plasma lipids of cAMP, achieved by inhibition of phosphodiesterase
with 3-isobutyl-l-methylxanthine (IBMX), similarly
trout (Takashima et al., 1972).
Growth hormone (GH) has varied and conflicting stimulated lipid mobilization in salmon liver
effects upon lipid metabolism in fish and in lower (Sheridan and Bern, 1986).
vertebrates generally. Mammalian GH causes increased lipid storage in lizards (Licht and Hoyer,
SUMMARY AND C O N C L U S I O N
1968), has little effect on lipid storage in turtles
In fish, lipids are absorbed as either fatty acids or
(Nichols, 1973), and tends to decrease lipid storage
in salmon (Clarke, 1976). Length of GH exposure as triacylglycerols aggregated into chylomicra paris a complication which arises when assessing GH tides. The interorgan transport of lipid in fish is
action. Long exposure to GH results in lipolytic generally similar to that of mammals. Fish possess
effects, whereas short exposure periods usually both an exogenous and an endogenous transport
result in lipogenic (insulin=like) action (Goodman system. The ]ipoprotein complexes of the endogenous
and Schwartz, 1974). With long exposure, ovine GH transport system resemble those of other animals;
has the effect of increasing plasma FFA in goldfish certain apoprotein constituents are similar to human
(Minick and Chavin, 1970) and bovine GH enhances apoproteins. The interconversion of lipoprotein in
lipase activity in juvenile coho salmon parr depots fish is not well-defined as is the mechanism of LDL(Sheridan, 1986). The stage of development also cholesterol uptake. Lipids in fish are stored in several
appears to affect GH action. Juvenile coho salmon depot organs (liver, muscle, mesenteric fat) primarily
smolts, further along in sea water preadaptive devel- as triacylglycerol. Mobilization of lipids proceeds
opment than parr, are refractory to 14 days of GH from the activation of lipolytic enzyme activity (triexposure with regard to lipid mobilization (Sheridan, acylglycerol lipase) and results in the hydrolysis of
1986). Smolt refractoriness is further supported by stored TG and subsequent release of FA. Fatty acids
the report of McKeown et al. (1975) that GH ex- are carried in the plasma of fish by one, or perhaps
posure had no effect on plasma FFA levels in more, albumin-like binding proteins. Lipolytic enzyme activity is hormonally modulated. A variety of
smoltified kokanee salmon (O. nerka).
Prolactin (PRL), like GH, undoubtedly plays a role slow acting (thyroxin, cortisol, growth hormone,
in the lipid metabolism of fish, but the actions of PRL prolactin) and fast-acting (epinephrine, norC.B.P. 90/411--D
MARK A. SHERIDAN
688
689
690
MARK A. SHE~ID~