Ultrastructural and biochemical evidence of glycogen in the developing lung of the chick embryo: Possible contribution to surfactant

doi:10.1016/0300-9629(89)90483-0

Comparative Biochemistry and Physiology Part A: Physiology

Volume 93, Issue 4, 1989, Pages 677-683

Comparative Biochemi...

https://doi.org/10.1016/0300-9629(89)90483-0 Get rights and content

Abstract

1.
1. Glycogen was identified ultrastructurally in undifferentiated type-II cells of the lung of the day 16 chick embryo.
2.
2. By 4 days after hatching, glycogen in type-II cells could not be observed, although lungs were actively secreting surfactant.
3.
3. Biochemical measurements of pulmonary glycogen revealed a depletion during days 14–20 of incubation, corroborating ultrastructural data.
4.
4. Using lung slices, ¹⁴C-glucose was incorporated in vitro into pulmonary surfactant phospholipids at a high rate in day 14 embryos, and a significantly lower rate on day 19.
5.
5. Hypophysectomy resulted in sub-normal initial accumulation of pulmonary glycogen on day 14 of development, but did not alter the depletion pattern after day 16.
6.
6. Thus, glycogen stores may contribute to avian embryonic pulmonary surfactant, and accumulation of early stores may be under hormonal control.

References (29)

J.R. Bourbon et al.
Utilization of glycogen for phospholipid synthesis in fetal rat lung
Biochem. biophys. Acta
(1982)
B.A. Doneen
Effects of hypophysectomy and corticosterone acetate treatment on hepatic lipid composition in the chick (Gallus domesticus) embryo
Gen. comp. Endocrinol.
(1981)
J. Folch et al.
A simple method for the isolation and purification of total lipides from animal tissues
J. biol. Chem.
(1957)
V.W. Hylka et al.
Ontogeny of the embryonic chicken lung: effects of pituitary gland, corticosterone, and other hormones upon pulmonary growth and synthesis of surfactant phospholipids
Gen. comp. Endocrinol.
(1983)
O.H. Lowry et al.
Protein measurement with the folin phenol reagent
J. biol. Chem.
(1951)
W.M. Maniscalco et al.
Development of glycogen and phospholipid metabolism in fetal and newborn rat lung
Biochim. biophys. Acta
(1978)
R.J. Mason et al.
Isolation of disaturated phosphatidylcholine with osmium tetroxide
J. Lipid Res.
(1976)
R.C. Thommes et al.
The effects of hypophysectomy by means of surgical decapitation on thyroid function in the developing chick embryo. I. Plasma thyroxine
Gen. comp. Endocrinol.
(1977)
T. Alescio et al.
Hydrocortisone increased glycogen deposition and its dependence on tissue interactions in mouse embryonic lung developing in vitro
Embryol, exp. Morphol.
(1972)
P.L. Ballard
Hormonal regulation of the surfactant system

T.A. Bancroft

Topics in Intermediate Statistical Methods

(1968)

N. Bandstrup et al.

The metabolism of glycogen in the lungs of the fetal rabbit

Devl Biol.

(1965)

W.R. Blackburn

Hormonal influences in fetal lung development

F. Dameron et al.

Mode de formation des inclusions lamellaires dans le poumon embryonnaire de poulet

Z. Zellforsch.

(1970)

Cited by (5)

Clutch formation and nest activities by the setting hen synchronize chick emergence with intestinal development to foster viability
2019, Animal Feed Science and Technology
Citation Excerpt :
Change from chorio-allantois to pulmonary respiration occurs in concert with internal to external pipping (Vince, 1976; Burton and Tullet, 1985; Chiba et al., 2002; Menna and Mortola, 2002) which depends on closures of the umbilical vein together with the heart’s intra-atrial opening (White, 1974, 1975; Tazawa et al., 1991; Moriya et al., 2000). Emergence places considerable demands on all muscular systems, particularly those associated with pipping, heart, lungs, and thigh; thus, intracellular glycogen of these parts becomes immediately important along with complimentary glucose released from liver glycogen (Bakhuis, 1974; Murakami et al., 1980: Hylka, 1989; Pulikanti et al., 2010). Use of glycogen is a necessity through this period because of reduced access to oxygen and ability to use fatty acids as an energy source.
The fertile hen collects eggs in a nest to form her clutch. The egg’s asymmetrical ellipsoid shape encourages placement blunt end up. Chalaza formation centralizes ovum in the egg while its high lipid favors upward positioning as early rotations interface germ with outer thin and access its glucose. Repetitive heating during successive ovipositions together with glucose recovery sustain blastodisc viability. Further turning of eggs upon formal incubation distributes the chorio-allantois over the blunt end while consolidating albumen in its sac at the sharp end. Rupture of the sero-amnionic connection mixes albumen with amnion which the embryo consumes over the next several days. During consumption certain of the proteins directly enter the vascular system while most pass through the jejunum to enter the yolk sac and foster embryonic nutrition. Mineralization of the skeleton, pipping muscle enlargement, multiple fortifications of glycogen, and deposition of subcutaneous fat subsequently occur as liver cholesterol becomes exaggerated. Minimal oxygen during transition from chorio-allantois to pulmonary respiration necessitates umbilical closure together with the heart’s intra-auricle septum as inner to outer shell pipping proceeds. Abdominal pressures during yolk sac retraction force a portion of yolk contents back into the jejunum while bile and pancreatic enzymes initiate its digestion to enhance early mucosal maturation. Concurrently, glycogen is sourced for energy in support of emergence. A narrow hatch window exists for the clutch because of egg uniformity while intermittent pre-incubation heating enabled similar germ development. Hen confinement of emergents to the nest provides insulation and heat sharing to extend body reserves through completion of hatch. Confinement also exposes hatchlings to a mature microbial population from hen excreta that colonize the gastrointestinal tract (GIT). Microbe composition in concert with the hen’s environment advantages digestion of hatchling feedstuffs outside the nest while concurrent mucosal failures generate permanent immunoglobins to commensals as passive ones dissipate. Inherent delays to feed with commercial chicks and absence of a favorable microflora impair early intestinal maturation prior to initial feed access. A pre-starting feed providing high protein that assures amino acids favoring mucin is thought to resist lumen microbes while aiding recovery of delayed development. Concurrent dietary enzyme supplementation and a source of nucleic acids are believed to partially substitute for digestive and nutritional complementation expected from commensals.
The comparative biology of pulmonary surfactant: Past, present and future
2001, Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology
Richard E. Pattle contributed enormously to the biology of the pulmonary surfactant system. However, Pattle can also be regarded as the founding father of comparative and evolutionary research of the surfactant system. He contributed eight seminal papers of the 167 publications we have located on this topic. In particular, Pattle produced a synthesis interpreting the evolution of the surfactant system that formed the foundation for the area. Prepared 25 years ago this synthesis spawned the three great discoveries in the comparative biology of the surfactant system: (1) that the surfactant system has been highly conserved throughout the enormous radiation of the air breathing vertebrates; (2) that temperature is the major selective condition that influences surfactant composition; (3) that acting as an anti-adhesive is one primitive and ubiquitous function of vertebrate surfactant. Here we review the literature and history of the comparative and evolutionary biology of the surfactant system and highlight the areas of comparative physiology that will contribute to our understanding of the surfactant system in the future. In our view the surfactant system is a neatly packaged system, located in a single cell and highly conserved, yet spectacularly complex. The surfactant system is one of the best systems we know to examine evolutionary processes in physiology as well as gain important insights into gas transfer by complex organisms.
Molecular aspects of avian lung development
2017, The Biology of the Avian Respiratory System: Evolution, Development, Structure and Function
Dexamethasone and epinephrine stimulate surfactant secretion in type II cells of embryonic chickens
2001, American Journal of Physiology - Regulatory Integrative and Comparative Physiology
Thyroid transcription factor-1, hepatocyte nuclear factor-3β and surfactant protein A and B in the developing chick lung
1998, Journal of Anatomy

View full text

Article preview

Comparative Biochemistry and Physiology Part A: Physiology

Abstract

References (29)

Utilization of glycogen for phospholipid synthesis in fetal rat lung

Biochem. biophys. Acta

Effects of hypophysectomy and corticosterone acetate treatment on hepatic lipid composition in the chick (Gallus domesticus) embryo

Gen. comp. Endocrinol.

A simple method for the isolation and purification of total lipides from animal tissues

J. biol. Chem.

Ontogeny of the embryonic chicken lung: effects of pituitary gland, corticosterone, and other hormones upon pulmonary growth and synthesis of surfactant phospholipids

Gen. comp. Endocrinol.

Protein measurement with the folin phenol reagent

J. biol. Chem.

Development of glycogen and phospholipid metabolism in fetal and newborn rat lung

Biochim. biophys. Acta

Isolation of disaturated phosphatidylcholine with osmium tetroxide

J. Lipid Res.

The effects of hypophysectomy by means of surgical decapitation on thyroid function in the developing chick embryo. I. Plasma thyroxine

Gen. comp. Endocrinol.

Hydrocortisone increased glycogen deposition and its dependence on tissue interactions in mouse embryonic lung developing in vitro

Embryol, exp. Morphol.

Hormonal regulation of the surfactant system

Topics in Intermediate Statistical Methods

The metabolism of glycogen in the lungs of the fetal rabbit

Devl Biol.

Hormonal influences in fetal lung development

Mode de formation des inclusions lamellaires dans le poumon embryonnaire de poulet

Z. Zellforsch.

Cited by (5)

Clutch formation and nest activities by the setting hen synchronize chick emergence with intestinal development to foster viability

The comparative biology of pulmonary surfactant: Past, present and future

Molecular aspects of avian lung development

Dexamethasone and epinephrine stimulate surfactant secretion in type II cells of embryonic chickens

Thyroid transcription factor-1, hepatocyte nuclear factor-3β and surfactant protein A and B in the developing chick lung