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Journal ArticleDOI

Histamine treatment induces rearrangements of orthogonal arrays of particles (OAPs) in human AQP4-expressing gastric cells

17 Sep 2001-Journal of Cell Biology (The Rockefeller University Press)-Vol. 154, Iss: 6, pp 1235-1243
TL;DR: Cell surface biotinylation experiments confirmed that AQP4 is internalized after 20 min of histamine exposure, which may account for the downregulation of water transport, the first evidence for short term rearrangement of OAPs in an established AQP 4-expressing cell line.
Abstract: To test the involvement of the water channel aquaporin (AQP)-4 in gastric acid physiology, the human gastric cell line (HGT)-1 was stably transfected with rat AQP4. AQP4 was immunolocalized to the basolateral membrane of transfected HGT-1 cells, like in native parietal cells. Expression of AQP4 in transfected cells increased the osmotic water permeability coefficient (Pf) from 2.02 +/- 0.3 x 10-4 to 16.37 +/- 0.5 x 10-4 cm/s at 20 degrees C. Freeze-fracture EM showed distinct orthogonal arrays of particles (OAPs), the morphological signature of AQP4, on the plasma membrane of AQP4-expressing cells. Quantitative morphometry showed that the density of OAPs was 2.5 +/- 0.3% under basal condition and decreased by 50% to 1.2 +/- 0.3% after 20 min of histamine stimulation, mainly due to a significant decrease of the OAPs number. Concomitantly, Pf decreased by approximately 35% in 20-min histamine-stimulated cells. Both Pf and OAPs density were not modified after 10 min of histamine exposure, time at which the maximal hormonal response is observed. Cell surface biotinylation experiments confirmed that AQP4 is internalized after 20 min of histamine exposure, which may account for the downregulation of water transport. This is the first evidence for short term rearrangement of OAPs in an established AQP4-expressing cell line.
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Journal ArticleDOI
TL;DR: Light is shed on the molecular basis for brain water transport and a class of specialized water channels in the brain that might be crucial to the physiological and pathophysiological handling of water are identified.
Abstract: Brain function is inextricably coupled to water homeostasis. The fact that most of the volume between neurons is occupied by glial cells, leaving only a narrow extracellular space, represents an important challenge, as even small extracellular volume changes will affect ion concentrations and therefore neuronal excitability. Further, the ionic transmembrane shifts that are required to maintain ion homeostasis during neuronal activity must be accompanied by water. It follows that the mechanisms for water transport across plasma membranes must have a central part in brain physiology. These mechanisms are also likely to be of pathophysiological importance in brain oedema, which represents a net accumulation of water in brain tissue. Recent studies have shed light on the molecular basis for brain water transport and have identified a class of specialized water channels in the brain that might be crucial to the physiological and pathophysiological handling of water.

684 citations


Cites background from "Histamine treatment induces rearran..."

  • ...If the mode of expression does affect water permeability it will be important to resolve how array formation is controlle...

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Journal ArticleDOI
TL;DR: The diverse and characteristic distribution of aquaporins in the body suggests their important and specific roles in each organ.

371 citations


Cites background from "Histamine treatment induces rearran..."

  • ...AQP4 in the stomach 45 9.6....

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  • ...Non-glycosylated form as well as glycosylated form of apparently high molecular weight are usually detected ARTICLE IN PRESS K. Takata et al. / Progress in Histochemistry and Cytochemistry 39 (2004) 1–83 5 ARTICLE IN PRESS K. Takata et al. / Progress in Histochemistry and Cytochemistry 39 (2004) 1–836 ARTICLE IN PRESS Table 1 (continued) AQP Organ Tissue/cell References Ear Organ of Corti Stankovic et al. (1995), Sawada et al. (2003) Vestibule Stankovic et al. (1995), Sawada et al. (2003) AQP2 Kidney Collecting duct (principal cell) Fushimi et al. (1993), Nielsen et al. (1993a), Nielsen et al. (1995a), Sasaki et al. (1994) Vas deferens Epithelium (principal cell) Stevens et al. (2000) Ear Organ of Corti Mhatre et al. (2002a) AQP3 Kidney Collecting duct (principal cell) Ishibashi et al. (1994), Ma et al. (1994), Echevarria et al. (1994), Ecelbarger et al. (1995) Renal pelvis Matsuzaki et al. (1999a) Ureter Epithelium (basal and intermediate cells) Matsuzaki et al. (1999a) Urinary bladder Epithelium (basal and intermediate cells) Matsuzaki et al. (1999a) Urethra Epithelium (basal and intermediate cells) Matsuzaki et al. (1999a) Oral cavity Epithelium (basal and intermediate cells) Matsuzaki et al. (1999a) Esophagus Epithelium (basal and intermediate cells) Matsuzaki et al. (1999a) Stomach Matsuzaki et al. (1999a) Ileum Matsuzaki et al. (1999a) Colon Matsuzaki et al. (1999a) Nasal cavity Epithelium (basal and intermediate cells) Matsuzaki et al. (1999a) Trachea Epithelium (basal cell) King et al. (1997), Nielsen et al. (1997a), Matsuzaki et al. (1999a) Lung Bronchus King et al. (1997), Nielsen et al. (1997a), Matsuzaki et al. (1999a) Skin Epidermis (basal and intermediate cells) Matsuzaki et al. (1999a) Hair follicle Matsuzaki et al. (1999a) Brain Ependyma Ma et al. (1994) Eye Conjunctiva Hamann et al. (1998) K. Takata et al. / Progress in Histochemistry and Cytochemistry 39 (2004) 1–83 7 ARTICLE IN PRESS Table 1 (continued) AQP Organ Tissue/cell References Ear Organ of Corti (spiral ligament, inner spiral tunnel) Huang et al. (2002) Vestibules Huang et al. (2002) AQP4 Kidney Collecting duct (principal cell) Frigeri et al. (1995a, b) Skeletal muscle Fast-twitch muscle Frigeri et al. (1998) Stomach Parietal cell Misaka et al. (1996), Koyama et al. (1999) Nasal cavity Ciliated cell Nielsen et al. (1997a) Trachea Nielsen et al. (1997a) Lung Bronchus Nielsen et al. (1997a), Kreda et al. (2001) Brain Astrocyte Nielsen et al. (1997b) Eye Retina (M .uller cell) Nagelhus et al. (1998), Hamann et al. (1998) Ciliary body (non-Pigmented epithelial cell) Hamann et al. (1998) Ear Organ of Corti (supporting cell) Minami et al. (1998), Takumi et al. (1998), Li et al. (2001) Vestibules (ciliated cell) Mhatre et al. (2002b) Minami et al. (2001) AQP5 Salivary gland Secretory cell Nielsen et al. (1997a), He et al. (1997), Funaki et al. (1998), Matsuzaki et al. (1999b) Stomach Pyrolic gland Matsuzaki et al. (2003) Duodenum Duodenal gland Matsuzaki et al. (2003) Pancreas Intercalated duct cell Burghardt et al. (2003) Airway Glandular cell Lung Type I pneumocyte Nielsen et al. (1997a) Sweat gland Nejsum et al. (2002) Eye Cornea Raina et al. (1995), Hamann et al. (1998) Lacrimal gland Glandular cell Ishida et al. (1997), Matsuzaki et al. (1999b) Ear Organ of Corti Mhatre et al. (1999) AQP6 Kidney Collecting duct (intercalated cell) Yasui et al. (1999a), Yasui et al. (1999b) K. Takata et al. / Progress in Histochemistry and Cytochemistry 39 (2004) 1–838 ARTICLE IN PRESS Table 1 (continued) AQP Organ Tissue/cell References AQP7 Kidney Proximal tubule (S3) Ishibashi et al. (2000a), Nejsum et al. (2000) Adipose tissue Adipocyte Kishida et al. (2000) Immune system Dendritic cell Testis Seminiferous tubules (spermatid) Ishibashi et al. (1997b), Suzuki-Toyota et al. (1999) Ear Organ of Corti (supporting cells) Huang et al. (2002) Vestibule Huang et al. (2002) AQP8 Kidney Proximal tubule Collecting duct Elkjaer et al. (2001) Salivary gland Glandular cell Koyama et al. (1997), Wellner et al. (2000) Myoepithelial cell Elkjaer et al. (2001) Duct cell Elkjaer et al. (2001) Liver Hepatocyte Ishibasi et al. (1997a), Koyama et al. (1997), Calamita et al. (2001a), Tani et al. (2001) Pancreas Glandular cell Hurley et al. (2001), Tani et al. (2001) Intestine Epithelial cell Elkjaer et al. (2001), Tani et al. (2001) Airway Myoepithelial cell Elkjaer et al. (2001) Testis Seminiferous tubules (spermatogenic cells, Sertoli cell) Ishibasi et al. (1997a), Elkjaer et al. (2001), Calamita et al. (2001b) AQP9 Liver Hepatocyte Tsukaguchi et al. (1998) Testis Seminiferous tubule Leydig cells Tsukaguchi et al. (1998), Nicchia et al. (2001) Epididymis Pastor-Soler et al. (2001) Vas deferens Pastor-Soler et al. (2001) Brain Astrocytes Tsukaguchi et al. (1998) Circumventricular organs Nicchia et al. (2001) Leukocyte Tsukaguchi et al. (1998) Ovary Oocyte Ford et al. (2000) Digestive tract Goblet cell Okada et al. (2003) Ear Organ of Corti Huang et al. (2002) Vestibule Huang et al. (2002) Placenta Syncytiotrophoblast Damiano et al. (2001) AQP10 Intestine Epithelial cell Hatakeyama et al. (2001), Morinaga et al. (2002) K. Takata et al. / Progress in Histochemistry and Cytochemistry 39 (2004) 1–83 9 by immunoblotting (Fig....

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  • ...This observation indicates that AQP4 may undergo acute rearrangement by endocytosis (Carmosino et al., 2001)....

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  • ...with H/K-ATPase clearly showed that AQP4 is expressed only in the parietal cells (Fujita et al., 1999; Wang et al., 2000; Carmosino et al., 2001) (Fig....

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  • ...AQP4 in the eye 50 9.10....

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Journal ArticleDOI
TL;DR: It is concluded that in a range of situations at the cellular, subcellular and tissue levels the SPH cannot satisfactorily account for the presence of AQPs and suggested that this sensor hypothesis can provide an explanation of many basic processes in which AQPs are already implicated.
Abstract: The prime function of aquaporins (AQPs) is generally believed to be that of increasing water flow rates across membranes by raising their osmotic or hydraulic permeability. In addition, this applies to other small solutes of physiological importance. Notable applications of this 'simple permeability hypothesis' (SPH) have been epithelial fluid transport in animals, water exchanges associated with transpiration, growth and stress in plants, and osmoregulation in microbes. We first analyze the need for such increased permeabilities and conclude that in a range of situations at the cellular, subcellular and tissue levels the SPH cannot satisfactorily account for the presence of AQPs. The analysis includes an examination of the effects of the genetic elimination or reduction of AQPs (knockouts, antisense transgenics and null mutants). These either have no effect, or a partial effect that is difficult to explain, and we argue that they do not support the hypothesis beyond showing that AQPs are involved in the process under examination. We assume that since AQPs are ubiquitous, they must have an important function and suggest that this is the detection of osmotic and turgor pressure gradients. A mechanistic model is proposed--in terms of monomer structure and changes in the tetrameric configuration of AQPs in the membrane--for how AQPs might function as sensors. Sensors then signal within the cell to control diverse processes, probably as part of feedback loops. Finally, we examine how AQPs as sensors may serve animal, plant and microbial cells and show that this sensor hypothesis can provide an explanation of many basic processes in which AQPs are already implicated. Aquaporins are molecules in search of a function; osmotic and turgor sensors are functions in search of a molecule.

212 citations


Cites background from "Histamine treatment induces rearran..."

  • ...One of the earliest is that water transport is porecontrolled, based on transport in the red cell [133, 150–152, 174] although the function of pore-mediated water flow in this system is unclear; another is the long-standing research on vasopressin-modulated water antidiuresis [24, 35, 91] where a clear function exists for water permeability modulation by channels; another is water transport in epithelia, where the proximal tubule received the earliest attention [134, 142] and where there already existed a significant argument about the magnitude of Pos required to achieve isotonic flow (see below)....

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  • ...An additional relation is Pos ¼ rLp ð2Þ where r is the osmotic reflexion coefficient....

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  • ...The osmotic permeability Pos and the hydraulic conductance Lp are related to the volume flow Jv by Jv ¼ LpDPþ PosDp ð1Þ where DP and Dp are the pressure and osmotic pressure....

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  • ...In human gastric cell lines transfected with rat AQP4 it appears on the basolateral membranes (as in native parietal cells) and has been shown there to contribute 2 substantially (88%) to Pos [22] when on this parietal membrane....

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Journal ArticleDOI
TL;DR: It is shown that two independent C‐terminal signals determine AQP4 basolateral membrane targeting in epithelial MDCK cells, and stress‐induced kinase casein kinase (CK)II phosphorylates the Ser276 immediately preceding the tyrosine motif, increasing AQp4–μ3A interaction and enhancing AQP 4–lysosomal targeting and degradation.
Abstract: Aquaporin 4 (AQP4) is the predominant water channel in the brain. It is targeted to specific membrane domains of astrocytes and plays a crucial role in cerebral water balance in response to brain edema formation. AQP4 is also specifically expressed in the basolateral membranes of epithelial cells. However, the molecular mechanisms involved in its polarized targeting and membrane trafficking remain largely unknown. Here, we show that two independent C-terminal signals determine AQP4 basolateral membrane targeting in epithelial MDCK cells. One signal involves a tyrosine-based motif; the other is encoded by a di-leucine-like motif. We found that the tyrosine-based basolateral sorting signal also determines AQP4 clathrin-dependent endocytosis through direct interaction with the mu subunit of AP2 adaptor complex. Once endocytosed, a regulated switch in mu subunit interaction changes AP2 adaptor association to AP3. We found that the stress-induced kinase casein kinase (CK)II phosphorylates the Ser276 immediately preceding the tyrosine motif, increasing AQP4-mu 3A interaction and enhancing AQP4-lysosomal targeting and degradation. AQP4 phosphorylation by CKII may thus provide a mechanism that regulates AQP4 cell surface expression.

157 citations

Journal ArticleDOI
TL;DR: The future therapies will have to address not only the forces driving the water and solute transport (e.g. as mannitol infusion does in the treatment of brain edema), but also the regulation of AQPs, which provide the means for water entry to the brain, for water exit from thebrain, and for redistribution of water andsolutes within the brain compartments.

155 citations

References
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Journal ArticleDOI
TL;DR: The tissue-specific expression of MIWC suggests a role in fluid transport and/or cell volume regulation in stomach and glandular epithelia, and orthogonal arrays of particles have been visualized by freeze-fracture electron microscopy, suggesting that MIWC may be the OAP protein.
Abstract: It was shown recently that water channel homologs MIWC (mercurial insensitive water channel) and GLIP (glycerol intrinsic protein) colocalized in basolateral membranes of kidney collecting duct, tracheal and colonic epithelia, and in brain pia mater. We report here an extensive immunolocalization study of MIWC and GLIP in non-epithelial and glandular epithelial tissues in rat. Immunogold electron microscopy confirmed colocalization of MIWC and GLIP in basolateral membrane of principal cells in kidney collecting duct. However, in other epithelia, MIWC but not GLIP was expressed in basolateral membrane of parietal cells in stomach, and in excretory tubules of salivary and lacrimal glands; GLIP but not MIWC was expressed in transitional epithelium of urinary bladder and skin epidermis. In the central nervous system, MIWC was strongly expressed in the ependymal layer lining the aqueductal system, and in astrocytes throughout the spinal cord and in selected regions of brain. MIWC was also expressed in a plasma membrane pattern in skeletal, but not smooth or cardiac muscle. Neither protein was expressed in small intestine, testis, liver, spleen and nerve. The tissue-specific expression of MIWC suggests a role in fluid transport and/or cell volume regulation in stomach and glandular epithelia. The functional role of MIWC expression in the neuromuscular system and of GLIP expression in skin and urinary bladder is uncertain. The specific cellular sites of MIWC expression (astrocytes, trachea, sarcolemma, gastric parietal cells and kidney principal cells) correspond exactly to sites where orthogonal arrays of particles (OAPs) have been visualized by freeze-fracture electron microscopy, suggesting that MIWC may be the OAP protein.

378 citations


"Histamine treatment induces rearran..." refers background in this paper

  • ...AQP4 have been detected only in parietal cells located at the base of the gastric pit in human, mouse, and rat stomach (Frigeri et al., 1995; Misaka et al., 1996; Wang et al., 2000)....

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  • ...Rat AQP4 was immunolocalized to the basolateral membranes of gastric parietal cells (Frigeri et al., 1995)....

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  • ...…stomach; water channel; histamine; H /K -ATPase 1236 The Journal of Cell Biology | Volume 154, Number 6, 2001 AQP4 have been detected only in parietal cells located at the base of the gastric pit in human, mouse, and rat stomach (Frigeri et al., 1995; Misaka et al., 1996; Wang et al., 2000)....

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Journal ArticleDOI
TL;DR: Evidence that aquaporin‐type water channels are involved in GI fluid transport is evaluated and preliminary evaluation of GI function suggests a role for AQP1 in dietary fat processing and AQP4 in colonic fluid absorption.
Abstract: Fluid transport is a major function of the gastrointestinal (GI) tract with more than 9 litres of fluid being absorbed or secreted across epithelia in human salivary gland, stomach, the hepatobiliary tract, pancreas, small intestine and colon. This review evaluates the evidence that aquaporin-type water channels are involved in GI fluid transport. The aquaporins are a family of small (≈30 kDa) integral membrane proteins that function as water channels. At least seven aquaporins are expressed in various tissues in the GI tract: AQP1 in intrahepatic cholangiocytes, AQP4 in gastric parietal cells, AQP3 and AQP4 in colonic surface epithelium, AQP5 in salivary gland, AQP7 in small intestine, AQP8 in liver, pancreas and colon, and AQP9 in liver. There are functional data suggesting that some GI cell types expressing aquaporins have high or regulated water permeability; however, there has been no direct evidence for a role of aquaporins in GI physiology. Recently, transgenic mice have been generated with selective deletions of various aquaporins. Preliminary evaluation of GI function suggests a role for AQP1 in dietary fat processing and AQP4 in colonic fluid absorption. Further study of aquaporin function in the GI tract should provide new insights into normal GI physiology and disease mechanisms, and may yield novel therapies to regulate fluid movement in GI diseases.

267 citations

Journal ArticleDOI
TL;DR: Results provide direct evidence that a molecular water channel can spontaneously assemble in regular arrays.

264 citations


"Histamine treatment induces rearran..." refers background in this paper

  • ...The center-to-center spacing of the P-face grooves was 8 nm, as also reported in other heterologous systems expressing AQP4 water channels (Yang et al., 1996)....

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  • ...Freeze-fracture EM revealed the presence of orthogonal arrays of particles (OAPs),* the morphological feature of AQP4 (Yang et al., 1996), in the basolateral plasma membrane of transfected cells....

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  • ...4, CTR) typical of AQP4 (Yang et al., 1996)....

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Journal ArticleDOI
TL;DR: It is suggested MIP may behave as an intercellular adhesion protein which can also act as a volume-regulating channel to collapse the lens extracellular space and, in these junctions, MIP is unlikely to form gap junction-like channels.
Abstract: The structural organization and protein composition of lens fiber junctions isolated from adult bovine and calf lenses were studied using combined electron microscopy, immunolocalization with monoclonal and polyclonal anti-MIP and anti-MP70 (two putative gap junction-forming proteins), and freeze-fracture and label-fracture methods. The major intrinsic protein of lens plasma membranes (MIP) was localized in single membranes and in an extensive network of junctions having flat and undulating surface topologies. In wavy junctions, polyclonal and monoclonal anti-MIPs labeled only the cytoplasmic surface of the convex membrane of the junction. Label-fracture experiments demonstrated that the convex membrane contained MIP arranged in tetragonal arrays 6-7 nm in unit cell dimension. The apposing concave membrane of the junction displayed fracture faces without intramembrane particles or pits. Therefore, wavy junctions are asymmetric structures composed of MIP crystals abutted against particle-free membranes. In thin junctions, anti-MIP labeled the cytoplasmic surfaces of both apposing membranes with varying degrees of asymmetry. In thin junctions, MIP was found organized in both small clusters and single membranes. These small clusters also abut against particle-free apposing membranes, probably in a staggered or checkerboard pattern. Thus, the structure of thin and wavy junctions differed only in the extent of crystallization of MIP, a property that can explain why this protein can produce two different antibody-labeling patterns. A conclusion of this study is that wavy and thin junctions do not contain coaxially aligned channels, and, in these junctions, MIP is unlikely to form gap junction-like channels. We suggest MIP may behave as an intercellular adhesion protein which can also act as a volume-regulating channel to collapse the lens extracellular space. Junctions constructed of MP70 have a wider overall thickness (18-20 nm) and are abundant in the cortical regions of the lens. A monoclonal antibody raised against this protein labeled these thicker junctions on the cytoplasmic surfaces of both apposing membranes. Thick junctions also contained isolated clusters of MIP inside the plaques of MP70. The role of thick junctions in lens physiology remains to be determined.

213 citations


"Histamine treatment induces rearran..." refers background in this paper

  • ...The OAPs visible in AQP4-transfected cells were morphologically undistinguable from those observed in other tissues (Rash et al., 1974; Orci et al., 1981; Hatton and Ellisman, 1982; Hirsch et al., 1988; Zampighi et al., 1989)....

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Journal ArticleDOI
TL;DR: The life story of parietal cells has been investigated in the corpus of the mouse stomach using electron microscopy and 3H‐thymidine radioautography, which indicates that the transformation of granule‐free cells into pre‐parietal cells takes at least one day.
Abstract: The life story of parietal cells has been investigated in the corpus of the mouse stomach using electron microscopy and 3H-thymidine radioautography. Parietal cells are scattered in the four regions of the unit. On the average 3.6 cells are in the pit, 6.2 in the isthmus, 5.6 in the neck, and 10.6 in the base. Parietal cells do not divide. They arise from partially differentiated pre-parietal cells, which are believed to be derived in the isthmus from the three subtypes of granule-free cells: undifferentiated cells, pre-pit cell precursors, and pre-neck cell precursors. Radioautography indicates that the transformation of granule-free cells into pre-parietal cells takes at least one day. The pre-parietal cells, of which there are 0.6 per unit on the average, develop into parietal cells through three successive stages. Stage 1 is characterized by small immature cells that are identified by long apical microvilli. Stage 2 is characterized by larger cells, about one-third the size of parietal cells, and by an incipient canaliculus and a few apical tubulovesicles. Stage 3 is characterized by the expansion of the canalicular and tubulovesicular systems as well as mitochondrial enlargement, which cause the pre-parietal cell to gradually approach the size of, and eventually become, a parietal cell. This cell sequence mainly takes place in the isthmus, but may extend to the neck region. Continuous infusion of 3H-thymidine confirms that parietal cells originate in the isthmus and that they migrate in two directions: some go outward to the pit and the others migrate inward to the neck and eventually to the base. It has been estimated that for every six parietal cells produced per month in the isthmus, three migrate to the pit and three migrate to the neck to eventually reach the base. While almost all parietal cells in the isthmus and neck appear normal, a large proportion of those reaching the pit (21%) and base (23%) undergo gradual alteration and degeneration. After the ensuing death, parietal cells are eliminated in one of two major ways: 1) extrusion into the gastric lumen, if they appear necrotic, or 2) phagocytosis by a neighboring cell or even by an invading connective tissue macrophage, if they are apoptotic. The overall turnover time of parietal cells averages 54 days.(ABSTRACT TRUNCATED AT 400 WORDS)

200 citations

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