Are Vacuoles In Animal And Plant Cells
Bioarchitecture. 2013 January 1; 3(1): 13–19.
Vacuoles in mammals
A subcellular structure indispensable for early embryogenesis
Abstruse
A vacuole is a membrane-bound subcellular structure involved in intracellular digestion. Instead of the large "vacuolar" organelles that are institute in plants and fungi, brute cells possess lysosomes that are smaller in size and are enriched with hydrolytic enzymes similar to those found in the vacuoles. Large vacuolar structures are often observed in highly differentiated mammalian tissues such equally embryonic visceral endoderm and absorbing epithelium. Vacuoles/lysosomes share a conserved machinery of biogenesis, and they are at the terminal of the endocytic pathways, Recent genetic studies of the mammalian orthologs of Vam/Vps genes, which accept essential functions for vacuole assembly, revealed that the dynamics of vacuoles/lysosomes are important for tissue differentiation and patterning through regulation of various molecular signaling events in mammals.
Keywords: vacuole, endocytosis, embryogenesis, rab7, Vam2/Vps41
Introduction
Eukaryotic cells develop membrane-jump organelles that provide specialized environments for biochemical and biophysical processes essential for cellular functions. Vacuoles are one member of the organelles. The term "vacuole" originates from the transparent morphology of this organelle, implying that the structure is "empty," being devoid of the cytoplasmic materials. Lite microscopy studies have revealed that a typical establish cell vacuole frequently occupies more than 90% of the cellular volume (Fig. 1). Vacuoles besides prominently occur in fungal cells: they occupy approximately a quarter of the cell volume in Saccharomyces cerevisiae.1 Filamentous fungi also possess well-developed vacuoles.2 Fission yeasts such as Schizosaccharomyces exhibit smaller but numerous vacuoles within the cells.three
Figure ane. Compages of lysosomes and vacuoles in plant, yeast, and beast cells. (A) Foliage of a flowering aqueous plant, Egeria densa. The vacuoles occupy approximately xc% of the cell volume and push the cytoplasmic greenish chloroplasts toward the cell wall. (B) Yeast cells in stationary phase testify a single large vacuole accumulating reddish ade pigment (cherry-red). (C) Mouse embryonic fibroblasts bear witness numerous pocket-size compartments with lysosome associated membrane protein 2 (lamp2; green).
Creature vacuoles are ordinarily far less morphologically developed than those in plants and fungi. Beast cells possess hydrolytic enzyme enriched lysosomes, which are commonly much smaller than plant and fungal vacuoles. In this regard, the vacuolar/lysosomal architecture in brute cells is similar to that in fission yeast. However, recent studies have revealed that some animal cells possess well-developed prominent vacuoles. In this article, I describe creature cells that develop "vacuoles" with morphological signatures and the role of these organelles in cell and tissue physiology.
Membrane Flow Toward Vacuoles: A Conserved Mechanism in Different Species
Cells take up extracellular material by invagination of a small portion of the cell membrane, which and so pinches off to form a vesicle that travels through the cytoplasm and interacts with a series of membrane compartments. This process is known as endocytosis (Fig. ii). The yeast vacuole is at the terminal of the endocytic pathways, where the endocytosed materials are accumulated.iv In animal cells, the endocytic pathways are well characterized. Plant cells also exhibit endocytic activities and deliver the extracellular molecules to the vacuoles.five
Figure ii. Endocytic and exocytic membrane dynamics composed of various membrane organelles. The early on endosomes, which receive the internalized materials, gradually mature, removing some components to be recycled dorsum to the cell surface/extracellular spaces, and become late endosomes. The tardily endosomes, and then acquire a digestive nature including an acidic interior environment and lytic enzymes, and develop into fully matured lysosomes. The endocytic pathway is highly regulated and provides membrane every bit well every bit luminal contents to the lysosomes and vacuoles. The vacuolar proteins are synthesized on ribosomes on the endoplasmic reticulum (ER), translocated into the ER lumen, and transported to the Golgi apparatus. This intracellular trafficking route constitutes the early on stages of exocytosis. In the Golgi apparatus, the proteins destined for endosomes and vacuoles are sorted out from those to exist directed to the cell surface and/or to exist secreted. Therefore, the early secretory and vacuolar pathways are the essential processes for vacuole assembly. In addition, the protein sorting in the Golgi apparatus is indispensable for establishing organelle identities and office.
The intracellular membrane compartments actively exchange their membranes and contents, yet keeping their identities. The bones logics for intracellular transport take been evolutionarily conserved in diverse species of fungi, plant, and the brute kingdom. The dynamic exchange processes among organelle membranes are tightly regulated by cellular machinery equanimous of small GTP-binding proteins like arf and rab proteins, v- and t-SNARE molecules, and tethering complexes.6 , 7
Yeast genetic studies take revealed that more than than l genes, known as VPS ( vacuolar protein sorting) genes, are involved in vacuolar protein transport and localization. Orthologs of VPS are found in plants and mammals. Thus, the basic mechanisms for vacuole- and lysosome assembly are similar in fungi and animals. In improver to VPS, many yeast genes, including PEP ( peptidase) and VAM ( vacuolar chiliadorphology), take been identified. The orthologs of VPS, PEP, and VAM genes are nowadays in plants likewise as animals and some of these genes can functionally substitute the endogenous yeast genes.8 - 10 Mammalian VPS homologs are implicated in lysosome-related hereditary complications.xi
Endocytic Pathway in Visceral Endoderm, an Embryonic Epithelium
The endocytic pathway is thought to downregulate various signal transduction pathways by compartmentalizing and degrading the signaling molecules. Although this view has been well established at the cellular level, the significance of vacuolar/lysosomal signal regulation is poorly understood at the level of tissues. This article reviews the physiological relevance of endocytosis in the mammalian system, peculiarly in the context of prison cell differentiation and tissue system that is directly regulated by both activation and silencing of various betoken cascades.
Yeast Vam/Vps41 protein is a subunit of the HOPS (homotypic fusion and vacuole protein sorting) tethering circuitous involved in vacuolar assembly.12 - 14 Along with Ypt7, a small GTP-binding poly peptide, the HOPS tethering complex mediates specific membrane recognition between vacuole and both homotypic vacuole as well as endosome. Deletion of either the VAM2 or YPT7 genes in yeast results in fragmentation of large vacuoles and partially aberrant localization of vacuolar proteins,12 , xv - 18 indicating that the HOPS circuitous and its regulators are required for vacuolar assembly in yeast cells (Fig. 3).
Figure 3. Vacuolar morphology in yeast and mouse visceral endoderm. (Upper panels) Saccharomyces cerevisiae harbouring the vam mutations were labeled with a fluid-phase endocytic mark, lucifer xanthous CH (for vacuoles) and aniline blue WS (for cell wall) and viewed under a fluorescence microscope. The wild blazon yeast cells showroom a few large vacuoles (Five), however, loss of VAM genes causes fragmentation of the vacuoles, where the endocytic markers are accumulated. (Lower panels) Wild-type mouse visceral endoderm (VE) cells show large apical vacuoles (AV) at the upmost side of the nucleus. Upon loss of mVam2 or rab7 gene function, the apical vacuoles bear witness fragmented morphology.
The HOPS subunit orthologs and its regulator (Ypt7) are widely distributed in various organisms, including animals and plants.19 - 21 The Vam2/Vps41 poly peptide is implicated in the maintenance of nervous organization integrity in nematodes, and in fruit wing eye pigmentation. A mutation in rab7, a factor encoding the ortholog for YPT7, was shown to be responsible for the pathogenesis of Charcot-Marie-Tooth affliction type 2B (CMT2B): degeneration of peripheral neurons in humans.22 These observations suggested that the HOPS proteins influence the physiology of multicellular organisms past controlling endosome/lysosome function. However, the relationship between the cell and tissue phenotypes remains to be established.
Our opposite-genetic studies showed that either mVam2 or rab7 functions are required for early embryogenesis in the mouse. The targeted deletion of either cistron leads to early embryonic expiry at peri-gastrulation stages.23 , 24 Notably, mutant cells actively proliferate with no obvious degeneration. However, at the systemic level, the embryo morphology is severely afflicted. In the rab7-deficient embryos, the embryonic mesoderm initially differentiates, but fails to migrate distally to form a archaic streak, a structure essential for establishing the three germ layers. In addition, the embryos lose the extraembryonic mesoderm components such as the allantois and amnion.24 In contrast, mVam2-mutant embryos tin organize the extraembryonic mesoderm structures in a normal fashion, but the mutant embryos are defective in differentiation/maintenance of the embryonic mesoderm and the neural ectoderm, showing a severe inductive-truncation phenotype.23 Although mVam2- and rab7-mutants bear witness the contrasting phenotypes, these studies showed that gastrulation, a key upshot of mammalian embryogenesis, requires the function of the organelle assembly factors.
Embryonic fibroblasts defective either mVam2 or rab7 functions show severe defects in endocytic transport from early on endosome to late endosome, yet internalization of cell surface and extracellular molecules remains largely unaffected. These cellular phenotypes correspond well to those of the yeast mutants (Fig. 3). In addition, the lysosome compartments of the mutant fibroblasts are smaller than those of wild-types. The reduced lysosome size is also observed in yeast with VAM deletion.15 However, every bit described before, animal cells exhibit smaller lysosomal compartments; therefore, the morphological phenotype is not apparent in the fibroblasts.
"Vacuole" in Embryonic Tissue and its Function During Gastrulation
Large vacuolar structures in visceral endoderm (VE), an embryonic tissue of pregastrulae, have been described in previous electron microscopic studies.25 , 26 The big vacuoles (apical vacuoles) participate in the endocytic pathway equally they are labeled by tracer molecules27 , 28. The apical vacuoles are the terminal organelles of the fluid-phase endocytosis, and accumulate lysosomal membrane proteins, including lysosomal associated membrane proteins (lamps), syntaxin-seven, and lysosomal proteinases cathepsins. Thus, apical vacuoles and lysosomes have like characteristics in creature cells.23 , 24 , 29
Both mVam2 and rab7 are required for the assembly of apical vacuoles. In the mutant embryos, the VE cells lack the apical vacuoles merely accrue numerous fragmented membrane compartments which are positive for endosomal markers. The mutant cells are capable of taking up prison cell-surface and extracellular materials and transporting them to the endocytic compartments positive for an early endosome marker sorting nexin ane (SNX1). Notwithstanding, the mutant cells fail to deliver the engulfed material to lamp2-positive, belatedly endosomal compartments. In addition, endosome-endosome fusion in the mutant cells is severely impaired. Thus, the materials endocytosed at dissimilar time points are well separated inside the cytoplasm, indicating that the accumulated fragmented vesicles are derivatives of those endosomes.23 , 24 These morphological phenotypes associated with the loss of mammalian vam −/− function is similar to that constitute in the yeast vacuolar assembly.
Endocytosis Controls Molecular Signaling and Developmental Patterning
VE is an absorbing epithelium overlying the epiblast (embryo proper) and extraembryonic ectoderm. Rodent embryos obtain nutrition from uterus fluid and the maternal circulation that are separated from the embryo proper by the VE epithelial layer. Early embryogenesis is regulated by multiple cytokines provided from maternal tissues, and transcellular signaling occurs across the VE cells. Obviously, these functions are critically dependent upon endocytosis. Indeed, the VE actively endocytoses diverse materials from the maternal circulation, and develops big vacuoles between the apical plasma membrane and the nucleus.
The mVam2-mutant embryos show severe defects in tissue patterning at the peri-gastrulation phase, as well as defective subcellular morphogenesis. Various signaling cascades such equally TGF-β, BMP, Wnt, and FGF signaling, command the spatial arrangement of embryos. In the mVam2-deficient embryos, the spatial and temporal patterns for TGF- β and Fgf activities remain unaffected; however, the BMP signaling is ectopically activated. Mouse embryos plant a specific repertoire of VE at the distal end of the egg cylinder (referred to as distal visceral endoderm; DVE) at embryonic day 5.two (E5.2). In the subsequent developmental stages, the DVE moves toward the future anterior side to form the anterior visceral endoderm (AVE), which defines the anterior-posterior centrality earlier gastrulation. This axial determination is one of the paramount events of mammalian patterning,30 and information technology is regulated by a residual between BMP and TGF-β signaling activity.31 The BMP signaling components (activated receptors and ligands) are endocytosed and delivered to the lysosomes and apical vacuoles, in fibroblasts and visceral endoderm, respectively, to terminate the signaling. However, in the absence of mVam2, the BMP signaling complex remains activated, leading to excessive BMP signaling, which ultimately results in defective embryo patterning.23
Assembly of the Apical Vacuoles: Microautophagy
Delivery of endocytosed materials to the large apical vacuoles involves quite unique membrane dynamics. In nearly cases, so far studied, the mixing of contents of ii distinct membrane compartments occurs via a fusion of the ii distinct membranes to class a continuous membrane. However, the big upmost vacuoles can exist assembled past another scenario, wherein the large upmost vacuoles eat the smaller, pre-vacuolar endosomes entirely, without forming a continuous membrane, then assimilate the endosomes within the vacuole.24 This rather unique membrane process is known as microautophagy, by which peroxisomes and the nucleus are delivered to the vacuoles in yeast cells. In mammalian cells, microautophagy has been less frequently reported, and its relevance has not been elucidated. Rab7 and mVam2 are required for microautophagy in the VE cells, and the loss of either protein results in defective gastrulation. Therefore, the microautophagic delivery of endosomes is pertinent for early embryogenesis.32
Large vacuolar structures are often observed in highly differentiated mammalian tissues. The newborn rodent ileum, which is the absorbing epithelium facing the digestive tract, develops large compartments at the apical side of the cytoplasm.33 - 35 The ileum of neonates is specialized to absorb milk nutrients, and information technology develops an intracellular compartment known as the supranuclear vacuole.36 The supranuclear vacuoles possess several lysosomal proteins and digest the milk endocytosed from the lumen of the digestive tract. These features imply that large subcellular compartments are components of the endocytic pathway, and are most likely involved at the terminal of the pathway.37 , 38
Microautophagy in the ileum has not been well characterized. Because the ileal and visceral endoderm are the arresting epithelia with high activity for endocytosis, they may share a similar machinery for vacuolar assembly. Farther studies on endocytic membrane dynamics in the ileal cells as well as other epithelium are required to identify the cellular mechanisms that sustain the nutritional and barrier functions of absorbing epithelial tissues. Avian hypoblast cells and germ wall cells often exhibit large vacuolar structures known equally the yolk sphere, which contain materials of varying electron density.39 , 40 However, membrane dynamics accept not been well studied in these tissues. The hypoblast, the equivalent of rodent visceral endoderm in human being and chick, plays of import regulatory roles in early embryogenesis through active regulation of multiple bespeak transduction cascades and supplying nutrients.41 Like microautophagic membrane dynamics may occur in the hypoblasts for fulfilling the endocytic tasks.
Interest of Early on Endocytic Stages for Embryogenesis
In addition to the protein machinery, lipids also play a central role in determining the organelle identity. Phosphoinositides (PtdIns), enriched in the cytosolic leaflets of organelle membranes, show an organelle-specific distribution and provide the location cue. PtdIns are characterized on the basis of the number and position of phosphate moieties in the inositol ring. Phosphorylation and de-phosphorylation of PtdIns are catalyzed by specific enzymes which reside in the distinct subcellular compartments, therefore, PtdIns function as specific markers for each subcellular compartment.42
Phosphatidyl inositol 3-phosphate [PtdIns(3)P] plays a function in the early stages of the endocytic pathway. PtdIns derived from the Golgi and plasma membrane reach the endosomes via the synthetic and endocytic pathways, respectively, and are modified by the class 3 PtdIns kinase, Vps34, resulting in the accumulation of PtdIns(3)P in the early on endosome. PtdIns(3)P shows high analogousness for a Zinc-finger motif known equally a FYVE domain and recruits a set of proteins containing the FYVE motif, which include Fab1, YOTB, Vac1, and EEA1 ("FYVE" is an acronym for the names of these proteins). These FYVE containing proteins are indeed involved in the associates and dynamics of endosomes through interacting with the endosomal membranes.
The role of Vps34 PtdIns 3-kinase is required for mouse development at pregastrulation,43 implicating PtdIns-mediated membrane dynamics in an essential function in this critical developmental phase. In add-on, the Vps52 gene is required for embryonic growth and organization at the perigastrulation stage.44 These findings suggest a regulatory link between cellular architecture and global embryonic patterning. In the later on developmental stages, proper embryogenesis is dependent on the functions of multiple Vps-related proteins, including SNX13,45 Hβ58/Vps26,46 , 47 CHMP5/Vps60,48 and Hgs,49 , fifty further demonstrating that regulation of membrane trafficking is involved in tissue morphogenesis.
The PtdIns(iii)P associated with the early endosomes is modified further by a PtdIns kinase, which adds another phosphate moiety at the five-position of PtdIns(iii)P. This enzymatic reaction leads to consumption of PtdIns(3)P on the endosomes, and accumulation of PtdIns(3,5)P2, which crusade loss of EEA1 and rab5 proteins from the transient endosomes. And so by an undetermined mechanism, the tardily-endosomal rab7 is recruited to the nascent belatedly endosomes. This endosome conversion is dependent on the switch of PtdIns(three)P to PtdIns(3,5)P2 and subsequent replacement of rab5 with rab7. It is an intriguing possibility that rab7 itself, or its binding partners, specifically recognize PtdIns(3,5)P2 on the membrane, although this mechanism has not been fully substantiated yet.
Conversion of PtsIns(3)P to PtdIns(3,five)P2 is mediated by PIPKIII and Fab1, in mammalian and yeast cells, respectively. Loss of this key enzyme results in severe defects in the endosome/vacuole part, including acidification, endocytic and biosynthetic trafficking. One of the most apparent phenotypes is that the lysosome/vacuole shows enlarged morphology. PtdIns(iii,5)P2 is required for membrane budding, without which the vacuole/lysosome continue to overstate in size due to an imbalance of arrival and outflow of the membranes. Alternatively, inward invagination of membranes, known as multivesicular body formation, requires the presence of PtdIns(3,5)P2. Indeed, proteins involved in the MVB formation contain the PtdIns(3,5)P2 recognition motif. In either state of affairs, the product of PtdIns(3,five)P2 or consumption of PtdIns(iii)P is essential for maintaining lysosomal/vacuolar integrity.
Again, the importance of PIPKIII and its orthologs is well conserved amidst the 3 kingdoms. Yeast fab1 mutants exhibit giant vacuoles.51 In Arabidopsis, 2 PIPKIII enzymes with a PtdIns(three)P recognition motif are encoded past two genes, and double mutants show accumulation of aberrantly huge vacuoles in pollen.52 Alteration of PIPKIII function in somatic cells results in defective endocytosis and vacuolar acidification.53 PIPKIII is required for the proper associates of the apical vacuoles in the VE cells of the mouse embryo.54 PIPKIII mutant embryos develop a gigantic vacuole in the visceral endoderm cells. The abnormally enlarged vacuoles carry lysosomal proteins, including lamp1, suggesting that the biosynthetic pathway from the Golgi apparatus proceeds ordinarily. Withal, an endocytic tracer like FITC-dextran is not efficiently delivered from the extracellular medium to the abnormally large vacuoles. Importantly, the PIPKIII mutant embryos are lacking in gastrulation: they are able to initiate mesoderm differentiation; yet, they fail to extend the primitive streak and organize the extraembryonic mesoderm structures, thus the mutant embryos are lacking in the progression of the subsequent developmental plan.54 An intestine-specific deletion of the PIKIII function in mouse results in malnutrition subsequently birth and pathological appearance of an ileum that resembles the human Crohn's disease morphology. These findings suggest that the 2 distinct polarized absorbent epithelia, visceral endoderm and intestine, have similar molecular mechanisms for assembling endomembrane systems.54
Decision
Vacuoles are considered to be rather specific for plants and fungi, however, fifty-fifty animate being cells often showroom lysosomal compartments with a prominent appearance. The physiological and molecular roles of mammalian vacuoles are described in this commodity. There is increasing testify that the pregnant vacuolar/lysosomal architecture is directly reflecting the importance of their office, especially in cell differentiation and tissue-modeling in the early stages of embryogenesis. Cell signaling regulates multiple critical events in all the developmental stages and organogenesis. In the adult animals, tissue regeneration and maintenance are regulated by proper doses of signaling and underlying controlling mechanisms may exist involved in pathological complications such every bit carcinogenesis, immune function, and neural manual. Time to come studies on vacuole function and endocytic compartment architecture in highly differentiated and specialized cells in mammals would offer additional insight.
Acknowledgments
I thank my colleagues from both developmental and cell biological fields for exchanging ideas and for valuable comments and discussion. The writer's laboratory has been supported by CREST, JST, and MEXT, Nippon.
Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed.
Footnotes
References
1. Wickner W. Membrane fusion: five lipids, iv SNAREs, three chaperones, ii nucleotides, and a Rab, all dancing in a band on yeast vacuoles. Annu Rev Cell Dev Biol. 2010;26:115–36. doi: 10.1146/annurev-cellbio-100109-104131. [PubMed] [CrossRef] [Google Scholar]
ii. Shoji JY, Arioka Yard, Kitamoto K. Vacuolar membrane dynamics in the filamentous fungus Aspergillus oryzae. Eukaryot Jail cell. 2006;five:411–21. doi: 10.1128/EC.five.2.411-421.2006. [PMC gratuitous article] [PubMed] [CrossRef] [Google Scholar]
3. Kashiwazaki J, Iwaki T, Takegawa K, Shimoda C, Nakamura T. Two fission yeast rab7 homologs, ypt7 and ypt71, play antagonistic roles in the regulation of vacuolar morphology. Traffic. 2009;10:912–24. doi: 10.1111/j.1600-0854.2009.00907.x. [PubMed] [CrossRef] [Google Scholar]
4. Riezman H. Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis. Cell. 1985;40:1001–9. doi: 10.1016/0092-8674(85)90360-5. [PubMed] [CrossRef] [Google Scholar]
5. Contento AL, Bassham DC. Structure and function of endosomes in plant cells. J Cell Sci. 2012;125:3511–8. doi: 10.1242/jcs.093559. [PubMed] [CrossRef] [Google Scholar]
6. Schmitt HD, Jahn R. A tethering complex recruits SNAREs and grabs vesicles. Cell. 2009;139:1053–5. doi: 10.1016/j.jail cell.2009.eleven.041. [PubMed] [CrossRef] [Google Scholar]
7. Peplowska K, Markgraf DF, Ostrowicz CW, Bange G, Ungermann C. The CORVET tethering circuitous interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev Prison cell. 2007;12:739–50. doi: 10.1016/j.devcel.2007.03.006. [PubMed] [CrossRef] [Google Scholar]
8. Sato MH, Nakamura N, Ohsumi Y, Kouchi H, Kondo 1000, Hara-Nishimura I, et al. The AtVAM3 encodes a syntaxin-related molecule implicated in the vacuolar assembly in Arabidopsis thaliana. J Biol Chem. 1997;272:24530–5. doi: x.1074/jbc.272.39.24530. [PubMed] [CrossRef] [Google Scholar]
ix. Nakamura N, Yamamoto A, Wada Y, Futai M. Syntaxin 7 mediates endocytic trafficking to late endosomes. J Biol Chem. 2000;275:6523–9. doi: ten.1074/jbc.275.9.6523. [PubMed] [CrossRef] [Google Scholar]
10. Nakamura N, Sun-Wada GH, Yamamoto A, Wada Y, Futai M. Association of mouse sorting nexin one with early endosomes. J Biochem. 2001;130:765–71. doi: ten.1093/oxfordjournals.jbchem.a003047. [PubMed] [CrossRef] [Google Scholar]
11. Di Pietro SM, Dell'Angelica EC. The prison cell biology of Hermansky-Pudlak syndrome: recent advances. Traffic. 2005;6:525–33. doi: 10.1111/j.1600-0854.2005.00299.x. [PubMed] [CrossRef] [Google Scholar]
12. Nakamura North, Hirata A, Ohsumi Y, Wada Y. Vam2/Vps41p and Vam6/Vps39p are components of a poly peptide complex on the vacuolar membranes and involved in the vacuolar assembly in the yeast Saccharomyces cerevisiae. J Biol Chem. 1997;272:11344–nine. doi: 10.1074/jbc.272.17.11344. [PubMed] [CrossRef] [Google Scholar]
13. Wurmser AE, Sato TK, Emr SD. New component of the vacuolar course C-Vps circuitous couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J Jail cell Biol. 2000;151:551–62. doi: 10.1083/jcb.151.3.551. [PMC gratuitous article] [PubMed] [CrossRef] [Google Scholar]
xiv. Bröcker C, Kuhlee A, Gatsogiannis C, Balderhaar HJ, Hönscher C, Engelbrecht-Vandré S, et al. Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering circuitous. Proc Natl Acad Sci U S A. 2012;109:1991–6. doi: x.1073/pnas.1117797109. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
15. Wada Y, Ohsumi Y, Anraku Y. Genes for directing vacuolar morphogenesis in Saccharomyces cerevisiae. I. Isolation and characterization of two classes of vam mutants. J Biol Chem. 1992;267:18665–lxx. [PubMed] [Google Scholar]
16. Wichmann H, Hengst L, Gallwitz D. Endocytosis in yeast: evidence for the involvement of a modest GTP-binding protein (Ypt7p) Jail cell. 1992;71:1131–42. doi: x.1016/S0092-8674(05)80062-5. [PubMed] [CrossRef] [Google Scholar]
17. Wada Y, Ohsumi Y, Kawai Due east, Ohsumi M. Mutational analysis of Vam4/Ypt7p function in the vacuolar biogenesis and morphogenesis in the yeast, Saccharomyces cerevisiae. Protoplasma. 1996;191:126–35. doi: x.1007/BF01281810. [CrossRef] [Google Scholar]
18. Haas A, Scheglmann D, Lazar T, Gallwitz D, Wickner Westward. The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance. EMBO J. 1995;14:5258–70. [PMC gratuitous article] [PubMed] [Google Scholar]
19. Radisky DC, Snyder WB, Emr SD, Kaplan J. Characterization of VPS41, a gene required for vacuolar trafficking and loftier-affinity iron send in yeast. Proc Natl Acad Sci U Southward A. 1997;94:5662–half-dozen. doi: 10.1073/pnas.94.11.5662. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
twenty. Saito C, Ueda T, Abe H, Wada Y, Kuroiwa T, Hisada A, et al. A complex and mobile structure forms a distinct subregion inside the continuous vacuolar membrane in young cotyledons of Arabidopsis. Institute J. 2002;29:245–55. doi: ten.1046/j.0960-7412.2001.01189.x. [PubMed] [CrossRef] [Google Scholar]
21. Bottanelli F, Gershlick DC, Denecke J. Evidence for sequential activity of Rab5 and Rab7 GTPases in prevacuolar organelle partitioning. Traffic. 2012;thirteen:338–54. doi: 10.1111/j.1600-0854.2011.01303.x. [PubMed] [CrossRef] [Google Scholar]
22. Verhoeven 1000, De Jonghe P, Coen K, Verpoorten Due north, Auer-Grumbach M, Kwon JM, et al. Mutations in the minor GTP-ase late endosomal protein RAB7 crusade Charcot-Marie-Tooth type 2B neuropathy. Am J Hum Genet. 2003;72:722–7. doi: x.1086/367847. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
23. Aoyama M, Dominicus-Wada G-H, Yamamoto A, Yamamoto M, Hamada H, Wada Y. Spatial restriction of os morphogenetic protein signaling in mouse gastrula through the mVam2-dependent endocytic pathway. Dev Cell. 2012;22:1163–75. doi: 10.1016/j.devcel.2012.05.009. [PubMed] [CrossRef] [Google Scholar]
24. Kawamura N, Sun-Wada Thousand-H, Aoyama M, Harada A, Takasuga S, Sasaki T, et al. Delivery of endosomes to lysosomes via microautophagy in the visceral endoderm of mouse embryos. Nat Commun. 2012;iii:1071. doi: x.1038/ncomms2069. [PubMed] [CrossRef] [Google Scholar]
25. Solter D, Damjanov I, Skreb N. Ultrastructure of mouse egg-cylinder. Z Anat Entwicklungsgesch. 1970;132:291–8. doi: ten.1007/BF00569266. [PubMed] [CrossRef] [Google Scholar]
26. Enders Air conditioning, Given RL, Schlafke Due south. Differentiation and migration of endoderm in the rat and mouse at implantation. Anat Rec. 1978;190:65–77. doi: 10.1002/ar.1091900107. [PubMed] [CrossRef] [Google Scholar]
27. Kugler P, Miki A. Study on membrane recycling in the rat visceral yolk-sac endoderm using concanavalin-A conjugates. Histochemistry. 1985;83:359–67. doi: 10.1007/BF00684383. [PubMed] [CrossRef] [Google Scholar]
28. Miki A, Kugler P. Effects of leupeptin on endocytosis and membrane recycling in rat visceral yolk-sac endoderm. Histochemistry. 1986;85:169–75. doi: 10.1007/BF00491765. [PubMed] [CrossRef] [Google Scholar]
29. Nada S, Hondo A, Kasai A, Koike G, Saito K, Uchiyama Y, et al. The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J. 2009;28:477–89. doi: 10.1038/emboj.2008.308. [PMC gratuitous article] [PubMed] [CrossRef] [Google Scholar]
xxx. Takaoka Thou, Yamamoto Yard, Hamada H. Origin and office of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat Cell Biol. 2011;thirteen:743–52. doi: 10.1038/ncb2251. [PubMed] [CrossRef] [Google Scholar]
31. Yamamoto M, Beppu H, Takaoka K, Meno C, Li Due east, Miyazono K, et al. Animosity between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo. J Jail cell Biol. 2009;184:323–34. doi: 10.1083/jcb.200808044. [PMC free commodity] [PubMed] [CrossRef] [Google Scholar]
32. Wada Y, Dominicus-Wada GH, Kawamura N. Microautophagy in the visceral endoderm is essential for mouse early development. Autophagy. 2013;9:252–four. doi: 10.4161/auto.22585. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
33. Wissig SL, Graney Do. Membrane modifications in the upmost endocytic circuitous of ileal epithelial cells. J Cell Biol. 1968;39:564–79. doi: x.1083/jcb.39.3.564. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
34. Knutton S, Limbrick AR, Robertson JD. Regular structures in membranes. I. Membranes in the endocytic complex of ileal epithelial cells. J Cell Biol. 1974;62:679–94. doi: 10.1083/jcb.62.three.679. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
35. Baba R, Fujita M, Tein CE, Miyoshi K. Endocytosis by absorptive cells in the middle segment of the suckling rat small intestine. Anat Sci Int. 2002;77:117–23. doi: 10.1046/j.0022-7722.2002.00017.x. [PubMed] [CrossRef] [Google Scholar]
36. Gonnella PA, Neutra MR. Membrane-leap and fluid-phase macromolecules enter dissever prelysosomal compartments in absorbent cells of suckling rat ileum. J Prison cell Biol. 1984;99:909–17. doi: x.1083/jcb.99.iii.909. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
37. Gonnella PA, Siminoski K, White potato RA, Neutra MR. Transepithelial send of epidermal growth factor by absorptive cells of suckling rat ileum. J Clin Invest. 1987;80:22–32. doi: ten.1172/JCI113051. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
38. Fujita K, Reinhart F, Neutra M. Convergence of apical and basolateral endocytic pathways at apical late endosomes in absorbent cells of suckling rat ileum in vivo. J Cell Sci. 1990;97:385–94. [PubMed] [Google Scholar]
39. Al-Nassar NA, Bellairs R. An electron-microscopical analysis of embryonic chick tissues explanted in culture. Jail cell Tissue Res. 1982;225:415–26. doi: 10.1007/BF00214692. [PubMed] [CrossRef] [Google Scholar]
forty. Sanders EJ, Bellairs R, Portch PA. In vivo and in vitro studies on the hypoblast and definitive endoblast of avian embryos. J Embryol Exp Morphol. 1978;46:187–205. [PubMed] [Google Scholar]
41. Stern CD, Downs KM. The hypoblast (visceral endoderm): an evo-devo perspective. Development. 2012;139:1059–69. doi: 10.1242/dev.070730. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
42. Sasaki T, Takasuga S, Sasaki J, Kofuji S, Eguchi S, Yamazaki One thousand, et al. Mammalian phosphoinositide kinases and phosphatases. Prog Lipid Res. 2009;48:307–43. doi: ten.1016/j.plipres.2009.06.001. [PubMed] [CrossRef] [Google Scholar]
43. Zhou X, Takatoh J, Wang F. The mammalian class iii PI3K (PIK3C3) is required for early embryogenesis and cell proliferation. PLoS 1. 2011;half-dozen:e16358. doi: x.1371/journal.pone.0016358. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
44. Sugimoto M, Kondo Grand, Hirose M, Suzuki M, Mekada Thou, Abe T, et al. Molecular identification of t(w5): Vps52 promotes pluripotential jail cell differentiation through prison cell-cell interactions. Cell reports 2012; 2:1363-74. [PubMed]
45. Zheng B, Tang T, Tang N, Kudlicka K, Ohtsubo Grand, Ma P, et al. Essential role of RGS-PX1/sorting nexin 13 in mouse development and regulation of endocytosis dynamics. Proc Natl Acad Sci U Due south A. 2006;103:16776–81. doi: ten.1073/pnas.0607974103. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
46. Lee JJ, Radice Thousand, Perkins CP, Costantini F. Identification and label of a novel, evolutionarily conserved gene disrupted by the murine H beta 58 embryonic lethal transgene insertion. Development. 1992;115:277–88. [PubMed] [Google Scholar]
47. Radice G, Lee JJ, Costantini FH. H beta 58, an insertional mutation affecting early postimplantation development of the mouse embryo. Development. 1991;111:801–eleven. [PubMed] [Google Scholar]
48. Shim JH, Xiao C, Hayden MS, Lee KY, Trombetta ES, Pypaert G, et al. CHMP5 is essential for belatedly endosome function and down-regulation of receptor signaling during mouse embryogenesis. J Jail cell Biol. 2006;172:1045–56. doi: ten.1083/jcb.200509041. [PMC gratuitous commodity] [PubMed] [CrossRef] [Google Scholar]
49. Komada M, Soriano P. Hrs, a FYVE finger poly peptide localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis. Genes Dev. 1999;13:1475–85. doi: 10.1101/gad.13.11.1475. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
50. Miura S, Takeshita T, Asao H, Kimura Y, Murata K, Sasaki Y, et al. Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol Cell Biol. 2000;xx:9346–55. doi: 10.1128/MCB.20.24.9346-9355.2000. [PMC complimentary commodity] [PubMed] [CrossRef] [Google Scholar]
51. Yamamoto A, DeWald DB, Boronenkov Iv, Anderson RA, Emr SD, Koshland D. Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole office and morphology in yeast. Mol Biol Prison cell. 1995;6:525–39. [PMC free article] [PubMed] [Google Scholar]
52. Whitley P, Hinz Southward, Doughty J. Arabidopsis FAB1/PIKfyve proteins are essential for development of viable pollen. Plant Physiol. 2009;151:1812–22. doi: 10.1104/pp.109.146159. [PMC free commodity] [PubMed] [CrossRef] [Google Scholar]
53. Hirano T, Matsuzawa T, Takegawa K, Sato MH. Loss-of-office and gain-of-part mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis. Plant Physiol. 2011;155:797–807. doi: 10.1104/pp.110.167981. [PMC costless commodity] [PubMed] [CrossRef] [Google Scholar]
54. Takasuga Due south, Horie Y, Sasaki J, Sunday-Wada GH, Kawamura N, Iizuka R, et al. Critical roles of type Three phosphatidylinositol phosphate kinase in murine embryonic visceral endoderm and adult intestine. Proc Natl Acad Sci U South A. 2013;110:1726–31. doi: 10.1073/pnas.1213212110. [PMC complimentary article] [PubMed] [CrossRef] [Google Scholar]
Articles from BioArchitecture are provided here courtesy of Taylor & Francis
Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3639239/
Posted by: brittpreal1963.blogspot.com
0 Response to "Are Vacuoles In Animal And Plant Cells"
Post a Comment