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Department of Molecular Biosciences, School of Veterinary Medicine, University of California, Davis, CA 95616–8741; a Department of Pharmacological Sciences, Health Sciences Center, State University of New York at Stony Brook, Stony Brook, NY 11794–8651; and b Cardiovascular Research Institute and c Department of Anatomy, University of California, San Francisco, CA 94143–0130
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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KEY WORDS: • apolipoproteinB100 • liver • kidney • ultrastructure • yolk deposition
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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).
The 200–220 mg of cholesterol contained in the typical egg yolk
represents only ~3% of yolk lipids and it is largely unesterified
(Kuksis 1992
). Yolk cholesteryl ester content can be varied somewhat
under experimental settings (Naber 1983
) but is typically low (Kuksis 1992
). Thus, triacylglycerols are the dominant nonpolar lipid in egg
yolk and represent 189 kJ of energy, or 75% of the embryo's
total requirement for hatching. |
TRIGLYCERIDE DEPOSITION INTO OVARIAN YOLK FOLLICLES |
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TOPABSTRACTINTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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, Clifford and Bensadoun 1975
). Later, ultrastructural studies
documented that intact lipoprotein particles were endocytosed via
coated pits located on the oolemma of the oocyte of developing yolk
follicles (Perry et al. 1978
). A decade later, Schneider's group
published the first evidence detailing avian oocyte receptor biology
(Nimpf et al. 1988
). They established the molecular mechanisms of
oocyte triacylglycerol deposition as receptor-mediated endocytosis of
intact VLDL particles via the ligand apolipoprotein (apo)B100 (apoB100) (Bujo et al. 1997
).
Yolk deposition is continuous, and yolk follicles increase in size from
7 to 35 mm in diameter and in weight from 0.2 to 17 g in the 7–10
d preceding ovulation (Etches 1996
). Interestingly, ultrastructural
studies of the granulosa basal lamina surrounding the oocyte indicated
that this membrane acts as a selective mechanical sieve to circulating
generic VLDL (Griffin and Perry 1985
). Only those apoB-lipoproteins
(apoB-LP) with diameters of 25–44 nm were observed distal to the
granulosa basal lamina. These results suggest that only a select size
subclass of apoB-LP can access oocytic receptors.
During classical apoB-LP metabolism, lipoprotein lipase (LPL) hydrolysis and other intravascular remodeling processes rapidly convert VLDL into intermediate (IDL) and low density lipoproteins containing substantial cholesteryl esters and reduced fractional triacylglycerol content. Thus, under typical VLDL metabolic conditions, apoB-LP with diameters sufficiently small to pass through the granulosa basal lamina (i.e., IDL and LDL) are unable to provide sufficient energy for embryonic growth and development (Table 1 ).These findings indicate that significant changes in generic VLDL assembly and metabolism must have evolved to permit small energy-laden VLDLy to deposit nutritionally adequate egg yolk.
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VLDLy, A SPECIAL CLASS OF VLDL FOR YOLK DEPOSITION |
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TOPABSTRACTINTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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). The remarkable reduction in mean VLDL particle diameter during
egg production is apparent in direct comparisons between VLDL diameter
distributions of roosters and laying hens (Fig. 1
).Studies of large numbers of hens showed that VLDL with particle
diameters of 25–44 nm were highly correlated with successful egg
production (Walzem 1996
). Hens with increased amounts of VLDL particles
<25 nm or >50 nm were poor egg producers. Separation of laying hen
plasma VLDL by size-exclusion chromatography into three subfractions
with mean particle diameters of 48, 30 and 21 nm showed that the 30-nm
fraction was comparatively enriched in triacylglycerol (Table 2
).Among genetically selected quail hens with comparably sized VLDL
particles, but whose plasma VLDL cholesteryl ester:triacylglycerol
varied from 1.8 to 2.9 and 4.3, yolk cholesteryl ester:triacylglycerol
was more uniform, varying from 1.8 to 1.8 and 2.4 (Chen et al. 1997
).
These results suggest that a small-diameter triacylglycerol-rich
subclass of plasma VLDL is "targeted" for yolk deposition. We
recently proposed the term "VLDLy" to describe this
reproduction-specific class of VLDL, and proposed that impaired VLDLy
assembly process(es) may underlie some reproductive dysfunction in hens
(Walzem 1996
).
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) and in vivo (Bacon et al. 1978
). This LPL
resistance prevents IDL or LDL formation from VLDLy, thereby securing a
high triacylglycerol content for the egg yolk. The degree of
LPL-resistance appears to vary somewhat among individual birds, but
wholesale loss of VLDLy size characteristics is associated with
reappearance of generic VLDL particles arising from the VLDL/LPL
lipolytic cascade and subsequent reproductive failure (Walzem et al. 1994
). The specific VLDLy properties associated with a high degree of
yolk targeting are as follows: 1) particle diameter of
25–44 nm; 2) high apoVLDL-II to apoB ratio; 3)
resistance to LPL; and 4) high triacylglycerol to very low
cholesteryl ester content. Factors that are known currently to
influence the fraction of VLDLy present in hens include genetic
background and energy intake (Chen et al. 1997
, Walzem et al. 1994
). |
HOW DOES VLDLy GET SMALL? |
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TOPABSTRACTINTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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). Estrogen
stimulates bird hepatic triacylglycerol and phospholipid biosynthetic
rates several-fold, whereas cholesterol synthesis remarkably remains
unchanged (Dashti et al. 1983
, Kudzma et al. 1975
). Estrogen also
dramatically stimulates hepatic synthesis of apoB in birds four- to
sixfold (Capony and Williams 1980
, Kirchgessner et al. 1987
, Williams 1979
) and induces the de novo synthesis of the reproduction specific
apolipoprotein, apoVLDL-II (Chan et al. 1976
, Lin and Chan 1980,
Williams 1979
).
Apolipoprotein VLDL-II and apoB are rapidly induced by exogenous
estrogen in the rooster liver and accumulate within the VLDL fraction
in an approximately equal mass ratio (Williams 1979
). On the basis of
the known molecular weights of apoB and apoVLDL-II, the VLDL fraction
contains ~46 apoVLDL-II molecules per apoB. Each VLDL particle
contains a single apoB and most of the apoVLDL-II is recovered as a
disulfide-linked dimer. Hence, the VLDLy particles that accumulate in
response to estrogen appear to contain 1 apoB and 23 apoVLDL-II. To
test directly that apoB and apoVLDL-II are present on the same VLDL
particles, an estrogen-treated rooster was injected with
3H-leucine, and 3H-VLDL was isolated. The
isolated VLDL underwent reaction with antibodies to apoB and to
apoVLDL-II to determine how much of the apoVLDL-II was
co-immunoprecipitated by anti-apoB and, conversely, how much of the
apoB was co-immunoprecipitated by anti-apoVLDL-II. The antibodies were
shown to be free of reactivity toward the other apolipoprotein (Blue and Williams 1981
, Williams 1979
) but would be expected to precipitate
the other apolipoprotein if it were present in the same VLDL particle.
The results in Table 3
show that each antibody was able to precipitate 86–100% of the other
apolipoprotein in native VLDLy. Furthermore, the distribution of
radioactivity between apoB and apoVLDL-II in the immunoprecipitate
formed with either antibody was the same as in native VLDL. This latter
result confirms that apoB or apoVLDL-II is co-immunoprecipitated by
virtue of residence in the same VLDLy particle. These results indicate
that the great majority of VLDL particles present in blood plasma after
estrogen treatment contain both apoVLDL-II and apoB in the same VLDLy
particle.
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, Schneider et al. 1990
),
perhaps by competitively excluding other exchangeable apoproteins from
the surface of VLDLy (Miller and Lane 1984
). Like apoB, apoVLDL-II does
not exchange between lipoprotein surfaces; because of this
characteristic and its induction by estrogen in hepatocytes, the
presence of apoVLDL-II on nascent VLDLy may limit the expansion of the
VLDL particle during the assembly process, giving rise to the smaller
VLDLy.
The reduced particle diameter of VLDLy could result from a
relatively greater estrogen-induced increase in apoB synthesis compared
with triacylglycerol synthesis. With less core lipid available for each
molecule of apoB protein, particle size could be expected to decline.
However, this is not an adequate explanation because VLDLy particle
diameter continued to be a highly regulated physical property in hens
sufficiently overfed to produce a fatty liver (Walzem et al. 1993
).
Overfed egg-laying hens allowed only a 22% increase in VLDLy particle
diameter, from 27 to 33 nm (Walzem et al. 1994
). How VLDLy particle
diameter is downsized in the setting of surplus lipid substrates is
under active investigation because it is contrary to a major paradigm
of apoB biology.
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WHY DOES AVIAN KIDNEY SECRETE GENERIC VLDL? |
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TOPABSTRACTINTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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). Subsequently, this tissue was
shown to express apoB RNA at high levels, comparable to liver and
intestine (Kirchgessner et al. 1987
). ApoVLDL-II and apoB gene
expression are estrogen-responsive in both adult and embryonic bird
livers, whereas only apoB is made in adult kidney, and it is not
responsive to estrogen (Lazier et al. 1994
). We observed recently that
lipid-staining nascent VLDL particles of primarily 60 nm diameter were
assembled within the endoplasmic reticulum (ER) of some proximal
tubular cells of the rooster kidney. These kidney nascent VLDL were
concentrated in clusters within Golgi secretory vesicles and were
exocytosed into the basal extracellular spaces adjacent to peritubular
capillaries where they could readily access the blood stream
(Fig. 2
).We discovered, however, that some proximal tubule cells of the rooster
kidney had fewer and often smaller lipid-staining particles within the
secretory pathway than those shown in Figure 2
, and that many proximal
tubule cells contained no detectable lipoprotein particles. In the same
rooster kidneys used for ultrastructural analyses, microsomal
triglyceride transfer protein (MTP) levels and MTP-mediated
triacylglycerol transfer activity were 40% of that measured in liver
(David A. Gordon, Bristol Meyers Squibb, personal communication). Other
investigators very recently published biochemical evidence consistent
with our ultrastructural analyses, i.e., male chick kidney slices
incubated with 35S amino acids for 3 h in the absence
of added lipid substrates secreted newly synthesized apoB100 in VLDL,
IDL, LDL and even in HDL (Tarugi et al. 1998
). We interpret our
electron microscopic and their biochemical findings as follows: the
proximal tubule may be considered analogous to the small intestine.
Thus, although apoB is synthesized throughout the entire length of the
tube, lipid substrates driving triacylglycerol-rich particle assembly
and apoB secretion are likely to be in highest concentration at the
upper end nearest the urinary pole, lowest in the mid-region and
virtually absent in lower portions of the proximal tubule. This would
be reflected in the numbers and diameters of apoB-LP being assembled.
Proximal tubule cells closest to the urinary pole absorb most of the
glomerular filtered lipids (probably albumin-bound free fatty acids).
These cells appear to assemble more and larger particles compared with
mid- and terminal proximal tubule cells, which may be "starved" for
lipid substrate and consequently may assemble fewer and smaller
particles or even none at all. This hypothesis is testable and may
explain our morphologic observations and the biochemical finding of
substantial apoB in a "Light" HDL fraction in the medium of bird
kidney slices after a 3-h incubation without added free fatty acid
substrate (Tarugi et al. 1998
).
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, Griffin and Mitchell 1984
, Heald and Badman 1963
),
which in turn would increase the flux of free fatty acids into the
urinary filtrate, stimulating the production (both size and number) of
proximal tubule generic VLDL secretion. Second, LPL expression in
laying hen cardiac muscle may be increased to ensure the supply of
adequate triacylglycerol calories from generic kidney VLDL (Fig. 3)
,
whereas LPL expression may be down-regulated in laying hen adipose
tissue, safeguarding kidney generic VLDL for heart muscle.
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HOW ARE VLDLy ASSEMBLED? |
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TOPABSTRACTINTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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). Subsequently,
small apoB-containing particles of HDL/LDL size and density were
observed by different investigators in several experimental settings,
contributing to the hypothesis that apoB may become core-lipidated by a
two-step mechanism (Borén et al. 1994
, Hamilton and Havel 1993
,
Hamilton 1994
, Hamilton et al. 1995
, Rustaeus et al. 1995
, 1998
, and
1999
, Spring et al. 1992
).
A basic tenet of our hypothesis of the two-step process of apoB
core-lipidation is that a second-step triacylglycerol-rich particle of
nascent VLDL size is formed independently of apoB within the lumen of
the ER (Hamilton 1994
). To further test this hypothesis in a different
but well-defined setting, we examined absorptive enterocytes of the
duodenum of mice at 19 d gestation (i.e., before intestinal
exposure to food) and during the first hours of sucking mother's milk.
The novelty of this experiment is that we characterized the
ultrastructural appearance of these cells that normally secrete
chylomicrons in mice that were genetically engineered to be deficient
in apoB expression in the intestine. In the virtual absence of apoB
expression in the intestines, triacylglycerol-rich particles of nascent
VLDL size (19-d gestational) and of chylomicron size (first fatty meal)
continued to be assembled within the lumen of the enterocyte ER, but
very few triacylglycerol-rich particles entered the Golgi apparatus and
even fewer reached the extracellular space (Hamilton et al. 1998
).
Thus, the ability of an absorptive enterocyte to assemble a
triacylglycerol-rich particle of VLDL or chylomicron size within the ER
lumen without the requirement for apoB is a compelling argument
supporting the two-step hypothesis.
We have biochemically addressed the question of whether second-step triacylglycerol-rich particles of VLDL size that lack apoB can be isolated from the ER. We developed a novel technique to rapidly recover large amounts of mainly uncontaminated rough ER membranes to determine the biochemical properties of both first-step (small apoB-containing particles) and second-step particles (lacking apoB) isolated from the lumen of the ER (Hamilton, R. L., unpublished ). We compared the putative first- and second-step particles that were isolated from rat liver rough ER fractions (mainly apoB48) to similar particles from rough ER fractions of the liver of the laying hen (apoB100 only). The first-step apoB-containing particles from rat liver rough ER consisted mainly of apoB48 together with lesser amounts of apoB100 and contained both of the core lipids. In contrast, the first-step particle fraction from the rough ER of the laying hen liver consisted only of apoB100, and the core lipids were almost exclusively triacylglycerol, consistent with the lipid profile of the laying hen's liver Golgi nascent VLDLy and plasma VLDLy compositions. The most interesting finding of these preliminary studies was the isolation of putative second-step triacylglycerol-rich particles that were biochemically shown to lack apoB in both rat and hen. Those particles lacking apoB48 from the rat liver rough ER matched the size distribution (~35–85 nm) of rat liver Golgi nascent VLDL containing mainly apoB48, whereas those lacking apoB100 from the laying hen liver matched the size distribution (~25–45 nm) of laying hen Golgi nascent VLDLy containing only apoB100.
These results strongly suggest that both apoB48 and apoB100 isoforms obtain most of their core lipids during VLDL assembly from a second-step mechanism by synthesizing a triacylglycerol-rich particle of nascent VLDL diameter within the lumen of the ER independent of apoB. We also hypothesize that the two-step mechanism of apoB-core lipidation is an ancient feature of apoB biology because oviparous species preceded mammals in evolution.
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FOOTNOTES |
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1 Presented at the symposium "Assembly and
Physiology of Apolipoprotein B-Containing Lipoproteins It's Not Just
for Heart Disease Anymore!" as part of Experimental Biology 98, April
18–22, 1998, San Francisco, CA. The symposium was sponsored by the
Energy and Macronutrient Research Interest Section of the American
Society for Nutritional Sciences, the Egg Nutrition Center, the
American Heart Association-Western States Affiliate, Merck Research
Laboratories, Bristol-Meyers Squibb Pharmaceutical Research Institute
and Parke-Davis Pharmaceutical Research. Published as a supplement to
The Journal of Nutrition. Guest editors for this supplement
were Rosemary L. Walzem, University of California, Davis, and Robert L.
Hamilton, University of California, San Francisco, CA.
2 Supported by American Heart
Association-Grant-in-Aid #97–218 (R.L.H. and R.L.W.), U.S. Department
of Agriculture Formula Funds provided through the School of Veterinary
Medicine (R.J.H. and R.L.W.), UCSF-ASFRG (R.L.H.) and National
Institiutes of Health grant HL32868 (D.L.W.).
3 Abbreviations used: apo, apolipoprotein;
apoB-LP, apolipoprotein B–containing lipoproteins; apoVLDL-II,
apolipoprotein VLDL-II; ER, endoplasmic reticulum; IDL, intermediate
density lipoprotein; LPL, lipoprotein lipase; MTP, microsomal
triglyceride transfer protein; VLDLy, yolk targeted VLDL.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONTRIGLYCERIDE DEPOSITION INTO...VLDLy, A SPECIAL CLASS...HOW DOES VLDLy GET...WHY DOES AVIAN KIDNEY...HOW ARE VLDLy ASSEMBLED?REFERENCES |
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