- anterior endoderm produces Wnt inhibitors (e.g. Cerberus, Dickkopf, Crescent); prevent Wnts from binding to their receptors
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1 Biology 4361 Developmental Biology Gilbert Chapter 15. Lateral Plate Mesoderm and Endoderm December 12, 2006 LATERAL PLATE MESODERM Two bands of lateral plate mesoderm lie peripheral to the intermediate mesoderm - each plate is split into two horizontal layers: - dorsal - somatic (parietal) mesoderm - underlies ectoderm - together with ectoderm forms the somatopleure - ventral - splanchnic (visceral) mesoderm - the space in between the two layers forms the body cavities - coeloms - later in development the right and left coeloms fuse - tissue extends from the somatic mesoderm to split the coelom: - pleural cavity - pericardial cavity - peritoneal cavity - evolutionary similarity between vertebrates The Heart The circulatory system is the first functioning unit of the developing embryo Specification of heart tissue - presumptive heart cells originate in the early primitive streak, just posterior to Hensen s node; extending about half its length - cells migrate through the streak and form two groups of mesodermal cells lateral to and at the same level as Hensen s node - referred to as cardiogenic mesoderm (cardiac crescent) Specification of cardiac precursor cells - induced by endoderm adjacent to the heart through BMP (esp. BMP2) and FGF signals - also, inhibitory signals prevent heart formation where it should not occur - notochord secretes Noggin and chordin; blocks BMP signal at center of embryo - Wnts from neural tube inhibit heart formation, but promote blood formation - anterior endoderm produces Wnt inhibitors (e.g. Cerberus, Dickkopf, Crescent); prevent Wnts from binding to their receptors - cardiac precursor cells specified in the places where BMPs (lateral mesoderm and endoderm) and Wnt antagonists (anterior endoderm) coincide Migration of the cardiac precursor cells 1
2 - chick, h; cardiac precursor cells move anteriorly between ectoderm and endoderm toward middle - reach lateral walls of anterior gut tube - directionality provided by foregut endoderm (fibronectin) - foregut formed by inward folding of spanchnopleure - movement brings two cardiac tubes together - tubes fuse; endocardia fuse Establishment of anterior and posterior cardiac domains - as cardiac precursor cells migrate, posterior region becomes exposed to increasingly higher retinoic acid concentrations (produced by posterior mesoderm) - RA critical in specifying posterior cardiac cells to become inflow (venous) portions; e.g. sinus venosus and atria Initial cell differentiation - early heart differentiation: GATA4 gene (transcription factor) - activates numerous heart-specific genes; e.g. atrial natriuretic factor and cardiacspecific troponin-1 and troponin-c; N-cadherin (critical for fusion of the two heart rudiments into one tube) - cell differentiation occurs independently in the two heart-forming primordia - as they migrate toward each other, central mesoderm cells of the primordia begin to express N-cadherin at their apices; sort out from the dorsal mesodermal cells; join together to form an epithelium -joining leads to formation of the pericardial cavity - sac in which heart is formed - small population of these cells downregulates N-cadherin and delaminates from the epithelium to form the endocardium; lining of the heart (continuous with the blood vessels) - epithelial cells form the myocardium; gives rise to the heart muscle - endocardial cells produce many of the heart valves, secrete proteins that regulate myocardial growth, regulate placement of nervous tissue in the heart Fusion of the heart rudiments and initial heartbeats - fusion of the two heart primordia occurs at about 29 hours in the chick; 3 wks in humans - myocardia unite to form single tube - endocardia stay separate for a while, but then also fuse - unfused posterior portions of the endocardium become the opening of the vitelline veins into the heart - veins carry nutrients from the yolk sac into the sinus venosus; posterior region where 2
3 major veins fuse - blood goes through valve-like flap into the atrial region - contractions of the truncus arteriosus push blood into aorta - pulsations start while paired primordia are fusing - heart muscles have an inherent ability to contract pulsations caused by Na /Ca exchange pump in the muscle cell membrane Looping and formation of heart chambers In 3-day chick and 5 wk human embryos, heart is a two-chambered tube, one atrium and one ventricle - looping converts the original anterior-posterior polarity of the heart tube into the right-left polarity seen in the adult - looping is dependent on left-right patterning proteins (Nodal, Lefty-2) - within the heart primordium, Nkx2-5 regulates the Hand1 and Hand2 transcription factors - both Hand proteins synthesized throughout early heart tube, as looping commences, Hand1 becomes restricted to the future left ventricle and Hand2 to the right - lack of Hand proteins produces abnormal looping; ventricles fail to form properly - extracellular matrices are also important for looping; regulate physical tension of the heart tissues on the different sides - transcription factors Nkx2-5 andcef2c activate the Xin gene; product may mediate cytoskeletal changes essential for heart looping - metalloproteases; e.g. metalloprotease-2 (MMP2)) are critical for remodeling the cytoskeleton - if blocked, ECM fails to change; asymmetric cell divisions (cause left side to grow faster than right) fail to occur; looping stops - formation of the four heart valves - not well understood - in mammals an endocardial cushion forms from the endocardium; divides the tube into right and left atrioventricular channels - primitive atria is partitioned by two septa that grow ventrally toward the endocardial cushion - septa have opening to allow maternal blood to cross to embryonic circulation - atrial opening is closed at first breath Redirecting Blood Flow in the Newborn Mammal chick blood circulation - blood pumped through he dorsal aorta passes over the aortic arches and down the embryo - some blood leave the embryo through the vitelline arteries and enters the yolk sac - nutrients and oxygen are adsorbed from the yolk - blood returns through vitelline veins to reenter the heart through th sinus venosus 3
4 human blood circulation - mammalian embryos obtain food and oxygen through the placenta; vessel analogous to the vitelline veins supply food and oxygen from the umbilical vein - umbilical artery caries wastes to the placenta - derived from what would be the allantoic artery in birds - specialized fetal hemoglobin is the key to obtaining oxygen from the maternal blood - fetal hemoglobins have a higher affinity for oxygen than adult; therefore exchange in the O2 -poor placenta is toward the fetus - also, fetal myoglobin has higher affinity for O than fetal hemoglobin, so O is passed on during fetal development an opening (ductus arteriosus) diverts blood from the pulmonary artery into the aorta (and thus to the placenta) - blood does not return from the lungs through the pulmonary vein; an opening is formed between the right and left ventricle - foramen ovale - blood enters the tight atrium, passes through the foramen ovale into the left atrium, then enters the left ventricle - at the first breath, blood pressure in the left side of the heart increases; pressure closes the septa over the foramen ovale; separates pulmonary and systemic circulation - prostaglandins in the newborn cause muscle surrounding the ductus arteriosus to close Formation of Blood Vessels Blood vessels form independently from the heart - link with the heart soon after forming - heart does not start to beat until after first circulatory loop is established - genome cannot encode the intricate series of connections between all of the arteries and veins; therefore, every individual circulatory system is unique - however, within a given species, most look basically the same - constrained by physiological, evolutionary, and physical parameters Constraints on the construction of blood vessels Physiological constraints: - embryos need to function as they develop; even with the lack of lungs, digestive system, etc. - therefore, embryonic circulatory physiology is different from adult - food absorbed from yolk or placenta - respiration through chorionic or allantoic membrane - major blood vessels must be constructed to serve these extraembryonic structures Evolutionary constraints - mammalian embryo extends blood vessels to the yolk sac even though there is no yolk - blood leaving the heart via the truncus arteriosus passes through vessels that loop over the 4
5 foregut to reach the dorsal aorta - six pairs of aortic arches - each loops over the pharynx (anterior foregut) - in primitive fish, arches persist; enable gills to oxygenate the blood - in birds and mammals all six pairs of aortic arches are formed - system eventually becomes simplified into a single aortic arch Physical constraints: - laws of fluid movement produce paradoxical situation regarding blood flow and nutrient/gas diffusion - most effective transport of fluids is performed by large tubes -4 - as the radius of a vessel gets smaller, resistance to flow increases as r ; therefore, a blood vessel that is half as wide as another has a resistance to flow 16 times greater - however, diffusion of nutrients can take place only when flow is slow and has access to cell membranes - the solution is to create a hierarchy of vessel size and number - large delivery vessel provide blood to very small vessels for distribution to tissues Vasculogenesis: The initial formation of blood vessels Formation of blood vessels takes place in two temporally-separate process: - vasculogenesis - network of blood vessels created de novo from the lateral plate mesoderm - angiogenesis - this primary network in remodeled and pruned into a distinct capillary bed, arteries, and veins - first phase - cells leaving the primitive streak in the posterior become hemangioblasts - precursors of both blood cells and blood vessels - reside in splanchnic mesoderm - condense into aggregations - blood islands - inner cells become blood progenitor cells - outer cells become angioblasts - blood vessel progenitors - second phase - angioblasts multiply; differentiate into endothelial cells - endothelial cells line the blood vessels - third phase - endothelial cells form tubes and connect - form primary capillary plexus The sites of vasculogenesis: two distinct and independent regions Region one - extraembryonic vasculogenesis occurs in the blood islands of the yolk sac - formed by hemangioblasts - give rise to early vasculature needed to feed the embryo - also create primitive red blood cells that function in early embryo (not found in later 5
6 embryo or adult) - blood islands produce the veins that supply nutrients and remove wastes - birds - vitelline veins - mammals - omphalomesenteric (umbilical) veins - chick - blood islands first seen in area opaca - form cords of hemangioblasts - cords become hollow - outer cells become flat endothelial cells lining the vessels - central cells differentiate into the embryonic blood cells - as blood island grow, they merge to form capillary network, which drains the vitelline veins Region two - intraembryonic vasculogenesis occurs within each organ - vessels arise from individual angioblast progenitor cells in the mesoderm surrounding a developing organ - cells not otherwise associated with blood cell formation Growth factors and vasculogenesis requires three growth factors - basic fibroblast growth factor (Fgf2) - required for generation of hemangioblasts from the splanchnic mesoderm - vascular endothelial growth factor (VEGF) - enables differentiation of angioblasts and their multiplication to form endothelial tubes - secreted by mesenchymal cells near blood islands [NOTE - regulation of VEGF production in the adult may correspond to several disease states; green tea consumption prevents angiogenesis; active ingredient - epigallocatechin-3-gallate (EGCG) inhibits VEGF; also, red wine reduces VEGF production in adults by inhibiting endothelin-1, which induces VEGF and is crucial for the formation of atherosclerotic plaques] - angiopoietins mediate interactions between endothelial cells and pericytes (smooth musclelike cells; cover endothelial cells; have something to do with patterning Angiogenesis: Sprouting of blood vessels and remodeling of vascular beds - primary capillary networks are remodeled and veins and arteries are made - extracellular matrix involved - VEGF acts of newly formed capillaries; causes loosening of cell-cell contacts; degradation of ECM - exposed endothelial cell proliferate and sprout from these regions; form new vessels - new vessel also formed in primary capillary bed by spitting existing vessel in two - eventually mature capillary network forms and is stabilized by TGF-â; strengthens ECM 6
7 and platelet-derived growth factor (PDGF); necessary for the recruitment of pericyte cells, which contribute to the mechanical flexibility of capillary walls - metalloprotease involvement: - metalloproteases digest ECM - developing blood vessels contain powerful metalloprotease inhibitors - angiogenesis occurs only where metalloproteases are active; e.g. - collagen XVIII stabilizes capillaries structurally - defends blood vessels chemically against external metalloproteases - when cleaved by metalloproteases, C-terminal forms endostatin - prevents angiogenesis by inhibiting cyclin expression and by interfering with VEGF binding - endostatin production is downregulated when new blood vessels are formed - endostatin may prevent tumor growth and spread by inhibiting blood vessel formation Arterial and venous differentiation - veins and arteries contain two types of endothelial cells - artery precursors contain ephrin-b2 - knockouts - vasculogenesis, but no angiogenesis - veins contain ephrin receptor - EphB4 tyrosine kinase - during angiogenesis EphB4 and ephrin interactions: - at the borders of the venose and arterial capillaries, it ensures that arterial capillaries connect only to venous ones - in non-border areas ensures that fusion of capillaries to make larger vessels occurs only between the same type of vessel - each angioblast is specified early - controlled by Notch pathway - activation of Notch suppressed venous development - Notch activates Gridlock (transcription factor); Gridlock activities expression of Ephrin-B2 - vessels with low amounts of Gridlock become EphB4-expressing vein cells - Notch expression controlled by VEGF Organ-specific angiogenesis factors Several organs (e.g. placenta) make their own angiogenesis factors; e.g. - leptin; can act locally to induce angiogenesis and cause endothelial cells to organize into tubes - kidney vasculature mainly derived from sprouting endothelial cells froth the dorsal aorta during initial nephrogenesis 7
8 - developing nephrons secrete VEGF; allow blood vessels to enter kidney - peripheral nerves; blood vessels follow peripheral nerves - nerves secrete an angiongenesis factor; blood vessels secrete nerve growth factor The lymphatic vessels Lymphatic vasculature forms separate system of vessels which is essential for draining fluid and transporting lymphocytes - subset of endothelial cells from the jugular vein sprout to form lymphatic sacs - peripheral lymphatic vessels are generated by further sprouting - Prox1 transcription factor downregulates blood vessel-specific genes; upregulates lymphatic vessel genes - VEGFR-3; encodes receptor for VEGF-C paracrine factor The Development of Blood Cells The stem cell concept 11 - about 10 RBCs replaced daily (old cells killed in the spleen); replaced through stem cells - pluripotential hematopoietic stem cells (a.k.a. hematopoietic stem cell; HSC) capable of generating all blood and lymph cells - generates series of intermediate stem cells; potency restricted to certain lineages Sites of hematopoiesis Hematopoiesis occurs in two stages: 1. embryonic ( primitive ) - provides the embryo with its initial blood cells and capillary network to the endoderm or yolk 2. definitive ( adult ) - generates more cell types - provides stem cells - embryonic hematopoiesis is associated with the blood islands in the ventral mesoderm near the yolk sac - hematopoietic stem cells seem capable of generating all blood cell lineages (but not lymphocytes) - but these cells usually just produce RBCs - BMPs are crucial for inducing blood forming cells in all vertebrates - definitive hematopoietic cells are derived from mesodermal area surrounding the aorta - formed within nodes of mesoderm the at line the mesentery and major blood vessels - e.g. in 4-day chick, aortic walls most important source of new blood cells - contain numerous hematopoietic stem cells - in fish, chicks, mammal, frogs definitive hematopoietic stem cells formed in the visceral (splanchnic) lateral plate mesoderm near the aorta 8
9 - aorta-gonad-mesonephros (AGM) region - hematopoietic stem cell later colonize the fetal liver - at around birth, seem cells from the liver populate the bone marrow - major source thereon - the placenta also contributes blood stem cells - pluripotential hematopoietic stem cells appear to be generated along with the endothelium of the placental blood vessels - the hematopoietic stem cell formed in the embryo are those that populate the bone marrow and spleen of adults - adult HSC niches in bone and spleen make chemoattractant proteins that attract circulating stem cells into them - pluripotent HSC in the marrow is thus descended from stem cell that had populated the embryonic liver, and probably the AGM or placenta Committed stem cells and their fates The bone marrow HSC is the common precursors for RBCs, white blood cells (granulocytes, neutrophils, platelets), and lymphocytes - estimates - 1:10,000 blood cells is a pluripotential HSC - pluripotential HSC appears to be dependant on the SCL transcription factor - SCL specifies blood cell fate in mesoderm cells - continues to be expressed in HSCs - pluripotential HSCs also dependent on osteoblasts in the bone marrow - osteoblasts that have finished making bone form endosteal osteoblasts - endosteal osteoblasts line the bone marrow - responsible for providing the niche that attracts HSCs; prevent apoptosis; keep HSCs in state of plasticity - osteoblasts bind HSCs; probably through N-cadherin; provide other signals, including: - Jagged protein - activates Notch protein on the HSC surface - angiopoietin-1 ; activates receptor tyrosine kinase Tie2 on HSC surface - Wnt pathway, localizing â-catenin into nucleus - critical for HSC self-renewal - HSC cells give rise to lineage-restricted stem cells that produce blood - e.g. HSC can give rise to the blood cell precursor (common myeloid precursor cell; CMP) or the lymphocyte stem cell (CLP) - these cells may also be stem cells; uncertain - CMP produce megakaryocyte / erythroid precursor cells (MEP) - MEPs generate red blood cell (erythrocyte) lineage or platelet lineage 9
10 - CMPs also produce granulocyte / monocyte precursor cells (GMP) - GMPs generate basophils, eosinophils, neutrophils, monocytes - eventually all of these cells produce progenitor cells that can divide but produce only one type of cell in addition to renewing itself Hematopoietic inductive microenvironments - cytokines - paracrine factors involved in blood cell and lymphocyte formation - made by several cell types - collected and concentrated by the ECM of stromal (mesenchymal) cells at the sites of hematopoiesis - e.g. granulocyte-macrophage colony-stimulating factor (GM-CSF) and the multilineage growth factor interleukin-3 (IL3) bind to heparan sulfate glycosaminoglycan of the bone marrow stroma - ECM presents paracrine factors to stem cells - high concentration - developmental pathway of pluripotential HSC descendants depends on which growth factors it meets - therefore, the pathway is determined by the stroma ENDODERM Endoderm has two functions: 1. Critical for instructing the formation of notochord, heart, blood vessels, and the mesodermal germ layer 2. Construction of the linings of the digestive tube (including liver, gall bladder, pancreas) and respiratory tube - pharynx - portion of the digestive tube anterior to the point of branching of the respiratory tube - pharyngeal outpocketings give rise to the thyroid, thymus, parathyroid glands - both the respiratory and digestive tubes are products of the primitive gut - the endoderm pinches in toward the center of the embryo; foregut and hindgut are formed - the oral end is initially blocked by oral plate ectoderm - the stomodeum - stomodeum breaks (in humans - 22 d); creates oral opening, lined with ectoderm - oral plate ectoderm comes in contact with brain ectoderm - roof of the oral region forms Rathke s pouch; becomes the glandular portion of the pituitary gland - diencephalon floor gives rise to the infundibulum - neural portion of the pituitary - this dual origin of the pituitary is reflected in its adult functions 10
11 The Pharynx - pharyngeal pouches - outpocketings between the pharyngeal arches - 4 pairs of pharyngeal pouches in mammals st 1 - form the auditory cavities of the middle ear; associated eustachian tubes nd 2 - walls of the tonsils rd 3 - thymus; directs differentiation of T lymphocytes during later development - one pair of parathyroid glands th 4 - second pair of parathyroid glands nd - thyroid gland formation: a small, central diverticulum forms between the 2 pouch and the floor of the pharynx - pocket buds off; migrates down the neck to become the thyroid gland th - the respiratory tube sprouts from the pharyngeal floor between the 4 pouches - forms lungs - endoderm meets ectoderm in the pharynx - endoderm plays a critical role in determining which pouches develop - Shh is a cell survival factor, prevents apoptosis of neural crest cells - FGFs from ectoderm and mesoderm are important for migration and survival of n NC cells,; also for formation of pouches The Digestive Tube and its Derivatives Posterior to the pharynx, the digestive tube forms the esophagus, stomach, small intestine, and large intestine - endodermal cells line the digestive tube and its glands - mesenchymal cells form splanchnic lateral plate mesoderm surround the tube; form muscles Specification of the gut tissue - endodermal epithelium responds differently to regionally specific mesodermal mesenchymes - differentiates into esophagus, stomach, small intestine, colon - the gut is regionally specified at a very early stage - in chicks, endoderm appears to be regionally specified even before it forms a tube - the endoderm expresses regionally-specific transcription factors - this specific expression is retained throughout gut development - however, regional specificity is labile; boundaries between regions are uncertain - boundaries stabilize after interaction with mesoderm - the gut induces splanchnic mesoderm to become regionally specific - Shh plays a role - Shh target - mesoderm surrounding the gut tube - induces a nested pattern of posterior Hox gene expression in the mesoderm 11
12 - anterior borders of Hox gene expression delineates the morphological boundaries of the regions that will form cloaca, large intestine, cecum, mid-cecum and the posterior portion of the midgut - Hox genes are thought to specify the mesoderm so that it can interact with the endodermal tube and specify its regions - once the boundaries of transcription factors are established, differentiation occurs - regional differentiation of the mesoderm into smooth muscle types is synchronized with the regional differentiation of the endoderm into different fuctional units (e.g. stomach, duodenum, small intestine) Liver, pancreas, and gallbladder - endoderm forms the lining of liver, pancreas, and gallbladder - the hepatic diverticulum is a bud of endoderm that extends out from the foregut into the surrounding mesenchyme - mesenchyme induces endoderm to proliferate & branch; forms the glandular epithelium of the liver - a portion of the hepatic diverticulum continues to function as the liver drainage duct - a second portion produces the gallbladder - the pancreas develops from the fusion of dorsal and ventral diverticula - in humans, only the ventral duct survives The Respiratory Tube Lungs and trachea are derived from the digestive tube. th - the laryngotracheal groove occurs at the center of the pharyngeal floor, between the 4 pair of pharyngeal pouches - groove extends ventrally, then bifurcates into branches - forms paired bronchi and lungs - laryngotracheal endoderm becomes lining of the trachea, the two bronchi, and alveoli (air sacs) of the lungs - if separation between digestive and respiratory tubes is not complete, baby is born with a tracheal-esophageal fistula - production of laryngotracheal groove correlated with retinoic acid in the ventral mesoderm (Note - may be same wave of RA that induces posterior region of heart) - RA probably induces Fgf10 by activating Tbx4 in splanchnic mesoderm adjacent to the ventral foregut 12
13 - regional specificity of the mesenchyme determines differentiation of the respiratory tube - in neck region, respiratory epithelium grows straight; forms trachea - in thorax, respiratory epithelium branches, forms two bronchi, then lungs - in addition, differentiation of respiratory epithelia into trachea cells or lung cells depends on the mesenchyme it encounters - lungs are among the last mammalian organs to fully differentiate - alveolar cells secrete a surfactant into the fluid bathing the lungs - surfactant consists of protein, phospholipids (e.g. sphingomyelin, lecithin) - enables cells to touch one another without sticking together - necessary of inflation of lungs - secreted late in gestation; ~ wk 34 (humans) - premature birth - must be placed on respirators until surfactant secretion matures - mammalian birth occurs soon after lung maturation - embryonic lung may signal mother to start delivery - mouse surfactant-a; one of final products produced by embryonic lung activates macrophages in amnionic fluid - macrophages migrate from amnion into uterine muscle - produce immune system proteins; e.g. interleukin-1â (IL-1â) - IL-1â initiates contraction of labor - activates cyclooxygenase-2 (stimulates production of prostaglandins) - antagonizes progesterone receptor The Extraembryonic Membranes Reptiles, birds, mammals - amniotes - amniote egg - evolutionary adaptation that allowed development on dry land - four sets of extraembryonic membranes mediate between the embryo and environment (evolution of the placenta and internal development displaced the hard shell in mammals) - initially, no distinction between embryonic and extraembryonic domains - later, epithelia at the border between the embryo and extraembryonic domain divide unequally; create body folds that isolate the embryo from the yolk - folds created by extension of ectodermal and endodermal epithelium underlain with lateral plate mesoderm - ectoderm and mesoderm (somatopleure) forms the amnion and chorion - endoderm and mesoderm (splanchnopleure) forms the yolk sac and allantois - endoderm and ectoderm provide the epithelial cells for membranes - mesoderm provides the essential blood supply The amnion and chorion 13
14 Problems for land-dwelling species (and eggs) include - desiccation - amnion supplies and aqueous environment for the embryo - cells secrete amnionic fluid (embryogenesis occurs in water in all amniotes) - gas exchange - chorion - outermost membrane; - in birds and reptiles chorion adheres to shell; allows gas exchange between egg and environment - in mammals, the chorion develops into the placenta; evolved endocrine, immune, nutritive functions in addition to respiration The allantois and yolk sac Additional problems: - waste disposal - allantois stores urinary wastes - also helps mediate gas exchange - in reptiles and birds, allantois becomes a large sac - in chickens, mesodermal layers of allantois and chorion fuse to create chorioallantoic membrane - extremely vascularized - responsible for transporting calcium from the shell to the embryo for bone formation - in mammals, allantois size depends on efficiency of nitrogenous waste clearance; e.g. - humans - very efficient clearance; allantois is vestigial sac - pigs - allantois is a large and very important organ - nutrition - yolk sac mediates nutrition - derived from splanchnopleural cells that grow over the yolk to enclose it - connected to the midgut by an open tube - the yolk duct - thus, the walls of the yolk sac and walls of the gut are continuous - note - blood vessels within the mesoderm of the splanchnopleure transport nutrients from the yolk into the body; yolk is not taken directly into the body through the yolk duct - endodermal cells digest yolk protein; transport amino acids - additional nutrients (i.e. vitamins, ions, fatty acids) also move from yolk to body through vessels 14
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