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Expression of transmembrane carbonic anhydrases, CAIX and CAXII, in human development.

Liao SY, Lerman MI, Stanbridge EJ - BMC Dev. Biol. (2009)

Bottom Line: Co-localization of CAXII with CAIX or HIF-1alpha was not observed.The study has showed that: 1) HIF-1alpha and CAIX expression co- localized in many, but not all, of the embryonic and early fetal tissues; 2) There is no evidence of co-localization of CAIX and CAXII; 3) CAIX and CAXII expression is closely related to cell origin and secretory activity involving proton transport, respectively.The intriguing finding of rare CAIX-expressing cells in those sites corresponding to stem cell niches requires further investigation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Pathology, St. Joseph Hospital, Orange, CA, USA. syliao@uci.edu

ABSTRACT

Background: Transmembrane CAIX and CAXII are members of the alpha carbonic anhydrase (CA) family. They play a crucial role in differentiation, proliferation, and pH regulation. Expression of CAIX and CAXII proteins in tumor tissues is primarily induced by hypoxia and this is particularly true for CAIX, which is regulated by the transcription factor, hypoxia inducible factor-1 (HIF-1). Their distributions in normal adult human tissues are restricted to highly specialized cells that are not always hypoxic. The human fetus exists in a relatively hypoxic environment. We examined expression of CAIX, CAXII and HIF-1alpha in the developing human fetus and postnatal tissues to determine whether expression of CAIX and CAXII is exclusively regulated by HIF-1.

Results: The co-localization of CAIX and HIF-1alpha was limited to certain cell types in embryonic and early fetal tissues. Those cells comprised the primitive mesenchyma or involved chondrogenesis and skin development. Transient CAIX expression was limited to immature tissues of mesodermal origin and the skin and ependymal cells. The only tissues that persistently expressed CAIX protein were coelomic epithelium (mesothelium) and its remnants, the epithelium of the stomach and biliary tree, glands and crypt cells of duodenum and small intestine, and the cells located at those sites previously identified as harboring adult stem cells in, for example, the skin and large intestine. In many instances co-localization of CAIX and HIF-1alpha was not evident. CAXII expression is restricted to cells involved in secretion and water absorption such as parietal cells of the stomach, acinar cells of the salivary glands and pancreas, epithelium of the large intestine, and renal tubules. Co-localization of CAXII with CAIX or HIF-1alpha was not observed.

Conclusion: The study has showed that: 1) HIF-1alpha and CAIX expression co- localized in many, but not all, of the embryonic and early fetal tissues; 2) There is no evidence of co-localization of CAIX and CAXII; 3) CAIX and CAXII expression is closely related to cell origin and secretory activity involving proton transport, respectively. The intriguing finding of rare CAIX-expressing cells in those sites corresponding to stem cell niches requires further investigation.

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Schema of CAIX expression in the cytotrophoblast and extra-/intra-embryonic mesoderm derivatives during human development (embryonic, fetal and postnatal periods).
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Figure 5: Schema of CAIX expression in the cytotrophoblast and extra-/intra-embryonic mesoderm derivatives during human development (embryonic, fetal and postnatal periods).

Mentions: During the postnatal period (especially after one year of age) and throughout adult life [7], CAIX expression was no longer present in the normal tissues, with the following exceptions: 1) persistent CAIX expression in mesothelial cells of the body cavity, the surface flat epithelium of all visceral organs, the rete ovarii, rete testis, tubuli reti, the hydatids of Morgagni, the appendix of the testis and efferent ductules. With the exception of efferent ductules, all of these CAIX positive organ systems are derived from coelomic epithelium; 2) persistent high levels of CAIX expression in the GI system, comprising the gastric surface epithelium, gastric glands, pyloric/Brunner's glands, crypt cells of the small intestine, and the biliary trees, including the gallbladder; 3) high levels of CAIX expression in the infundibulum and the outer sheath of hair follicles, and the sebaceous units of the skin; 4) variable degrees of CAIX expression in the primitive reserve cells or immature metaplastic squamous cells of the lining epithelium of all visceral organs and rare columnar cells in the crypts of the large intestine. Interestingly, in the reparative squamous or respiratory mucosa, not only do the numbers of basal/reserve cells expressing CAIX appear to increase, CAIX expression is also observed in rare columnar cells; and 5) the only mesenchymal tissues that retained CAIX expression after birth were the submesothelial stromal cells, the meniscus and the nucleus pulposus of the vertebrae. Schematic representations of the temporal and tissue-specific distribution of CAIX expressing cells, both pre- and postnatal, are shown in Figs 5 and 6. The patterns of expression clearly indicate that, during human development, all of the CAIX positive cells were derived from the mesoderm and were particularly related to the embryonic coelom and mesenchyme, with the exception of the skin, squamous mucosa, the upper gastrointestinal tract and the efferent ductules.


Expression of transmembrane carbonic anhydrases, CAIX and CAXII, in human development.

Liao SY, Lerman MI, Stanbridge EJ - BMC Dev. Biol. (2009)

Schema of CAIX expression in the cytotrophoblast and extra-/intra-embryonic mesoderm derivatives during human development (embryonic, fetal and postnatal periods).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2666674&req=5

Figure 5: Schema of CAIX expression in the cytotrophoblast and extra-/intra-embryonic mesoderm derivatives during human development (embryonic, fetal and postnatal periods).
Mentions: During the postnatal period (especially after one year of age) and throughout adult life [7], CAIX expression was no longer present in the normal tissues, with the following exceptions: 1) persistent CAIX expression in mesothelial cells of the body cavity, the surface flat epithelium of all visceral organs, the rete ovarii, rete testis, tubuli reti, the hydatids of Morgagni, the appendix of the testis and efferent ductules. With the exception of efferent ductules, all of these CAIX positive organ systems are derived from coelomic epithelium; 2) persistent high levels of CAIX expression in the GI system, comprising the gastric surface epithelium, gastric glands, pyloric/Brunner's glands, crypt cells of the small intestine, and the biliary trees, including the gallbladder; 3) high levels of CAIX expression in the infundibulum and the outer sheath of hair follicles, and the sebaceous units of the skin; 4) variable degrees of CAIX expression in the primitive reserve cells or immature metaplastic squamous cells of the lining epithelium of all visceral organs and rare columnar cells in the crypts of the large intestine. Interestingly, in the reparative squamous or respiratory mucosa, not only do the numbers of basal/reserve cells expressing CAIX appear to increase, CAIX expression is also observed in rare columnar cells; and 5) the only mesenchymal tissues that retained CAIX expression after birth were the submesothelial stromal cells, the meniscus and the nucleus pulposus of the vertebrae. Schematic representations of the temporal and tissue-specific distribution of CAIX expressing cells, both pre- and postnatal, are shown in Figs 5 and 6. The patterns of expression clearly indicate that, during human development, all of the CAIX positive cells were derived from the mesoderm and were particularly related to the embryonic coelom and mesenchyme, with the exception of the skin, squamous mucosa, the upper gastrointestinal tract and the efferent ductules.

Bottom Line: Co-localization of CAXII with CAIX or HIF-1alpha was not observed.The study has showed that: 1) HIF-1alpha and CAIX expression co- localized in many, but not all, of the embryonic and early fetal tissues; 2) There is no evidence of co-localization of CAIX and CAXII; 3) CAIX and CAXII expression is closely related to cell origin and secretory activity involving proton transport, respectively.The intriguing finding of rare CAIX-expressing cells in those sites corresponding to stem cell niches requires further investigation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Pathology, St. Joseph Hospital, Orange, CA, USA. syliao@uci.edu

ABSTRACT

Background: Transmembrane CAIX and CAXII are members of the alpha carbonic anhydrase (CA) family. They play a crucial role in differentiation, proliferation, and pH regulation. Expression of CAIX and CAXII proteins in tumor tissues is primarily induced by hypoxia and this is particularly true for CAIX, which is regulated by the transcription factor, hypoxia inducible factor-1 (HIF-1). Their distributions in normal adult human tissues are restricted to highly specialized cells that are not always hypoxic. The human fetus exists in a relatively hypoxic environment. We examined expression of CAIX, CAXII and HIF-1alpha in the developing human fetus and postnatal tissues to determine whether expression of CAIX and CAXII is exclusively regulated by HIF-1.

Results: The co-localization of CAIX and HIF-1alpha was limited to certain cell types in embryonic and early fetal tissues. Those cells comprised the primitive mesenchyma or involved chondrogenesis and skin development. Transient CAIX expression was limited to immature tissues of mesodermal origin and the skin and ependymal cells. The only tissues that persistently expressed CAIX protein were coelomic epithelium (mesothelium) and its remnants, the epithelium of the stomach and biliary tree, glands and crypt cells of duodenum and small intestine, and the cells located at those sites previously identified as harboring adult stem cells in, for example, the skin and large intestine. In many instances co-localization of CAIX and HIF-1alpha was not evident. CAXII expression is restricted to cells involved in secretion and water absorption such as parietal cells of the stomach, acinar cells of the salivary glands and pancreas, epithelium of the large intestine, and renal tubules. Co-localization of CAXII with CAIX or HIF-1alpha was not observed.

Conclusion: The study has showed that: 1) HIF-1alpha and CAIX expression co- localized in many, but not all, of the embryonic and early fetal tissues; 2) There is no evidence of co-localization of CAIX and CAXII; 3) CAIX and CAXII expression is closely related to cell origin and secretory activity involving proton transport, respectively. The intriguing finding of rare CAIX-expressing cells in those sites corresponding to stem cell niches requires further investigation.

Show MeSH
Related in: MedlinePlus