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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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CAIX expression in bronchial trees and genital organs: In the bronchial trees high expression of CAIX was seen in the peribronchial immature mesenchymal cells and cartilage (designated C) (A1) but progressively diminished when the tissues became mature (A2, A3). CAIX positivity was persistently seen in peritoneal lining cells as shown in B (insert) and G1, G2 (surface epithelium [SE], arrow). As early as the 13th week of gestation, CAIX positive cells were seen in the flat SE of the ovary, the outer muscular layer and rare epithelial cells of the uterus and fallopian tubes (B). Around 26 to 27 weeks, high levels of CAIX expression were transiently seen in the epithelium of fallopian tubes (C1), endometrium (D1), and the cervix (E1). After birth, there was either no CAIX expression (C3) or expression was limited to occasional endometrial cells (D2), reserve cells of the cervix (E2, and corresponding H&E stain in insert, and F1, F2). In the ovary, CAIX expression was observed in SE migrating into the stroma and forming the primordial follicle (PF) (G1, G2). Persistent expression of CAIX was observed in the coelomic remnants: rete testis (H1) and tubule reti (H2). W = gestational age in weeks; D, M = postnatal age in days and months, respectively. Original magnifications: A1, A2, A3, C1, C2, C3, E1, E2 and F2 (20×); B (4×); H1 and H2 (10×); D1, D2, F1, G1 and G2 (40×).
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Figure 3: CAIX expression in bronchial trees and genital organs: In the bronchial trees high expression of CAIX was seen in the peribronchial immature mesenchymal cells and cartilage (designated C) (A1) but progressively diminished when the tissues became mature (A2, A3). CAIX positivity was persistently seen in peritoneal lining cells as shown in B (insert) and G1, G2 (surface epithelium [SE], arrow). As early as the 13th week of gestation, CAIX positive cells were seen in the flat SE of the ovary, the outer muscular layer and rare epithelial cells of the uterus and fallopian tubes (B). Around 26 to 27 weeks, high levels of CAIX expression were transiently seen in the epithelium of fallopian tubes (C1), endometrium (D1), and the cervix (E1). After birth, there was either no CAIX expression (C3) or expression was limited to occasional endometrial cells (D2), reserve cells of the cervix (E2, and corresponding H&E stain in insert, and F1, F2). In the ovary, CAIX expression was observed in SE migrating into the stroma and forming the primordial follicle (PF) (G1, G2). Persistent expression of CAIX was observed in the coelomic remnants: rete testis (H1) and tubule reti (H2). W = gestational age in weeks; D, M = postnatal age in days and months, respectively. Original magnifications: A1, A2, A3, C1, C2, C3, E1, E2 and F2 (20×); B (4×); H1 and H2 (10×); D1, D2, F1, G1 and G2 (40×).

Mentions: The mesothelial cells lining the body cavities and the surfaces of visceral organ system showed high levels of CAIX expression throughout the developmental stages of the fetus and continued into adulthood [7]. Representative examples are shown in figs 1F, 1G, 3B, 3G1, and 3G2.


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

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

CAIX expression in bronchial trees and genital organs: In the bronchial trees high expression of CAIX was seen in the peribronchial immature mesenchymal cells and cartilage (designated C) (A1) but progressively diminished when the tissues became mature (A2, A3). CAIX positivity was persistently seen in peritoneal lining cells as shown in B (insert) and G1, G2 (surface epithelium [SE], arrow). As early as the 13th week of gestation, CAIX positive cells were seen in the flat SE of the ovary, the outer muscular layer and rare epithelial cells of the uterus and fallopian tubes (B). Around 26 to 27 weeks, high levels of CAIX expression were transiently seen in the epithelium of fallopian tubes (C1), endometrium (D1), and the cervix (E1). After birth, there was either no CAIX expression (C3) or expression was limited to occasional endometrial cells (D2), reserve cells of the cervix (E2, and corresponding H&E stain in insert, and F1, F2). In the ovary, CAIX expression was observed in SE migrating into the stroma and forming the primordial follicle (PF) (G1, G2). Persistent expression of CAIX was observed in the coelomic remnants: rete testis (H1) and tubule reti (H2). W = gestational age in weeks; D, M = postnatal age in days and months, respectively. Original magnifications: A1, A2, A3, C1, C2, C3, E1, E2 and F2 (20×); B (4×); H1 and H2 (10×); D1, D2, F1, G1 and G2 (40×).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 3: CAIX expression in bronchial trees and genital organs: In the bronchial trees high expression of CAIX was seen in the peribronchial immature mesenchymal cells and cartilage (designated C) (A1) but progressively diminished when the tissues became mature (A2, A3). CAIX positivity was persistently seen in peritoneal lining cells as shown in B (insert) and G1, G2 (surface epithelium [SE], arrow). As early as the 13th week of gestation, CAIX positive cells were seen in the flat SE of the ovary, the outer muscular layer and rare epithelial cells of the uterus and fallopian tubes (B). Around 26 to 27 weeks, high levels of CAIX expression were transiently seen in the epithelium of fallopian tubes (C1), endometrium (D1), and the cervix (E1). After birth, there was either no CAIX expression (C3) or expression was limited to occasional endometrial cells (D2), reserve cells of the cervix (E2, and corresponding H&E stain in insert, and F1, F2). In the ovary, CAIX expression was observed in SE migrating into the stroma and forming the primordial follicle (PF) (G1, G2). Persistent expression of CAIX was observed in the coelomic remnants: rete testis (H1) and tubule reti (H2). W = gestational age in weeks; D, M = postnatal age in days and months, respectively. Original magnifications: A1, A2, A3, C1, C2, C3, E1, E2 and F2 (20×); B (4×); H1 and H2 (10×); D1, D2, F1, G1 and G2 (40×).
Mentions: The mesothelial cells lining the body cavities and the surfaces of visceral organ system showed high levels of CAIX expression throughout the developmental stages of the fetus and continued into adulthood [7]. Representative examples are shown in figs 1F, 1G, 3B, 3G1, and 3G2.

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