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Cellular basis of tissue regeneration by omentum.

Shah S, Lowery E, Braun RK, Martin A, Huang N, Medina M, Sethupathi P, Seki Y, Takami M, Byrne K, Wigfield C, Love RB, Iwashima M - PLoS ONE (2012)

Bottom Line: To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses.Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells.Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Chicago, Illinois, United States of America.

ABSTRACT
The omentum is a sheet-like tissue attached to the greater curvature of the stomach and contains secondary lymphoid organs called milky spots. The omentum has been used for its healing potential for over 100 years by transposing the omental pedicle to injured organs (omental transposition), but the mechanism by which omentum helps the healing process of damaged tissues is not well understood. Omental transposition promotes expansion of pancreatic islets, hepatocytes, embryonic kidney, and neurons. Omental cells (OCs) can be activated by foreign bodies in vivo. Once activated, they become a rich source for growth factors and express pluripotent stem cell markers. Moreover, OCs become engrafted in injured tissues suggesting that they might function as stem cells.Omentum consists of a variety of phenotypically and functionally distinctive cells. To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses. Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells. Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

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Differentiation of omentum cells into lung epithelium or osteoblasts.Omentum cells were cultured in the medium conditioned to induce (a, b, d) lung epithelium or (c) osteoblast. (a) After 5 weeks of culture, cells were stained for expression of CCSP. (×10) (b) Cells cultured as in (a) were used to determine the expression of ccsp mRNA by semi-quantitative RT-PCR. gapdh mRNA level was examined to determine the amount of mRNA in each sample. (c) Omentum cells cultured in the basal (lower panels) or medium conditioned for osteoblast induction (upper panels) for 2 weeks. Cells were stained by DAPI (middle) or with anti-osteopontin antibody. (d) Omentum cells were separated into CD45+, CD45−CD34+, or CD45−CD34− cells, and were cultured in the medium conditioned for lung epithelium cell induction. Only CD45−CD34+ cells survived and expanded to the analyzable level in the conditioned medium and are shown.
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pone-0038368-g005: Differentiation of omentum cells into lung epithelium or osteoblasts.Omentum cells were cultured in the medium conditioned to induce (a, b, d) lung epithelium or (c) osteoblast. (a) After 5 weeks of culture, cells were stained for expression of CCSP. (×10) (b) Cells cultured as in (a) were used to determine the expression of ccsp mRNA by semi-quantitative RT-PCR. gapdh mRNA level was examined to determine the amount of mRNA in each sample. (c) Omentum cells cultured in the basal (lower panels) or medium conditioned for osteoblast induction (upper panels) for 2 weeks. Cells were stained by DAPI (middle) or with anti-osteopontin antibody. (d) Omentum cells were separated into CD45+, CD45−CD34+, or CD45−CD34− cells, and were cultured in the medium conditioned for lung epithelium cell induction. Only CD45−CD34+ cells survived and expanded to the analyzable level in the conditioned medium and are shown.

Mentions: Amelioration of bleomycin-induced lung injury by adoptive transfer of omentum cells could also be promoted by potentiating tissue regeneration processes. Previous reports suggest that rat omentum contains cells that have stem cell functions to differentiate into nerve cells, adipocytes, and hepatocytes [39]–[41]. To determine if mouse omentum contains stem cells, we cultured omentum cells in medium conditioned to induce differentiation into lung epithelial cells [42], [43]. After 28 days, we determined expression of a lung specific antigen, clara cell secretory protein (CCSP). Cells maintained in the lung epithelial-inducing medium clearly expressed CCSP detected both by immunofluorescent analysis and by RT-PCR (Fig. 5a, b). We also cultured omentum cells in medium inducing differentiation into osteoblasts [44]. 2 weeks after the start of culture, we observed a high level of osteopontin expression (Fig. 5c). The data show that a subset of omentum cells is omnipotent in differentiation. To determine the phenotype of the stem cell subset, we separated omentum cells into CD45+ and CD45− subsets. A previous report showed that bone marrow derived MSCs from C57BL/6 mice are CD45−CD34+, although CD34+ cells are considered to be hematopoietic stem cells in other strains of mice and in humans [32]. Thus, we further separated CD45− cells into CD34+ and CD34− subset. In the lung epithelial-inducing medium or in basal medium, CD45+ cells died within 2 weeks of culture. CD45−CD34− cells survived the culture but showed no expansion. Cells derived from CD45−CD34+ cells expanded under these conditions and differentiated into CCSP+ cells (Fig. 6, Fig. 5d). Together, the data show that CD45−CD34+ cells are the major source of stem cells from activated omentum.


Cellular basis of tissue regeneration by omentum.

Shah S, Lowery E, Braun RK, Martin A, Huang N, Medina M, Sethupathi P, Seki Y, Takami M, Byrne K, Wigfield C, Love RB, Iwashima M - PLoS ONE (2012)

Differentiation of omentum cells into lung epithelium or osteoblasts.Omentum cells were cultured in the medium conditioned to induce (a, b, d) lung epithelium or (c) osteoblast. (a) After 5 weeks of culture, cells were stained for expression of CCSP. (×10) (b) Cells cultured as in (a) were used to determine the expression of ccsp mRNA by semi-quantitative RT-PCR. gapdh mRNA level was examined to determine the amount of mRNA in each sample. (c) Omentum cells cultured in the basal (lower panels) or medium conditioned for osteoblast induction (upper panels) for 2 weeks. Cells were stained by DAPI (middle) or with anti-osteopontin antibody. (d) Omentum cells were separated into CD45+, CD45−CD34+, or CD45−CD34− cells, and were cultured in the medium conditioned for lung epithelium cell induction. Only CD45−CD34+ cells survived and expanded to the analyzable level in the conditioned medium and are shown.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3368844&req=5

pone-0038368-g005: Differentiation of omentum cells into lung epithelium or osteoblasts.Omentum cells were cultured in the medium conditioned to induce (a, b, d) lung epithelium or (c) osteoblast. (a) After 5 weeks of culture, cells were stained for expression of CCSP. (×10) (b) Cells cultured as in (a) were used to determine the expression of ccsp mRNA by semi-quantitative RT-PCR. gapdh mRNA level was examined to determine the amount of mRNA in each sample. (c) Omentum cells cultured in the basal (lower panels) or medium conditioned for osteoblast induction (upper panels) for 2 weeks. Cells were stained by DAPI (middle) or with anti-osteopontin antibody. (d) Omentum cells were separated into CD45+, CD45−CD34+, or CD45−CD34− cells, and were cultured in the medium conditioned for lung epithelium cell induction. Only CD45−CD34+ cells survived and expanded to the analyzable level in the conditioned medium and are shown.
Mentions: Amelioration of bleomycin-induced lung injury by adoptive transfer of omentum cells could also be promoted by potentiating tissue regeneration processes. Previous reports suggest that rat omentum contains cells that have stem cell functions to differentiate into nerve cells, adipocytes, and hepatocytes [39]–[41]. To determine if mouse omentum contains stem cells, we cultured omentum cells in medium conditioned to induce differentiation into lung epithelial cells [42], [43]. After 28 days, we determined expression of a lung specific antigen, clara cell secretory protein (CCSP). Cells maintained in the lung epithelial-inducing medium clearly expressed CCSP detected both by immunofluorescent analysis and by RT-PCR (Fig. 5a, b). We also cultured omentum cells in medium inducing differentiation into osteoblasts [44]. 2 weeks after the start of culture, we observed a high level of osteopontin expression (Fig. 5c). The data show that a subset of omentum cells is omnipotent in differentiation. To determine the phenotype of the stem cell subset, we separated omentum cells into CD45+ and CD45− subsets. A previous report showed that bone marrow derived MSCs from C57BL/6 mice are CD45−CD34+, although CD34+ cells are considered to be hematopoietic stem cells in other strains of mice and in humans [32]. Thus, we further separated CD45− cells into CD34+ and CD34− subset. In the lung epithelial-inducing medium or in basal medium, CD45+ cells died within 2 weeks of culture. CD45−CD34− cells survived the culture but showed no expansion. Cells derived from CD45−CD34+ cells expanded under these conditions and differentiated into CCSP+ cells (Fig. 6, Fig. 5d). Together, the data show that CD45−CD34+ cells are the major source of stem cells from activated omentum.

Bottom Line: To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses.Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells.Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Chicago, Illinois, United States of America.

ABSTRACT
The omentum is a sheet-like tissue attached to the greater curvature of the stomach and contains secondary lymphoid organs called milky spots. The omentum has been used for its healing potential for over 100 years by transposing the omental pedicle to injured organs (omental transposition), but the mechanism by which omentum helps the healing process of damaged tissues is not well understood. Omental transposition promotes expansion of pancreatic islets, hepatocytes, embryonic kidney, and neurons. Omental cells (OCs) can be activated by foreign bodies in vivo. Once activated, they become a rich source for growth factors and express pluripotent stem cell markers. Moreover, OCs become engrafted in injured tissues suggesting that they might function as stem cells.Omentum consists of a variety of phenotypically and functionally distinctive cells. To understand the mechanism of tissue repair support by the omentum in more detail, we analyzed the cell subsets derived from the omentum on immune and inflammatory responses. Our data demonstrate that the omentum contains at least two groups of cells that support tissue repair, immunomodulatory myeloid derived suppressor cells and omnipotent stem cells that are indistinguishable from mesenchymal stem cells. Based on these data, we propose that the omentum is a designated organ for tissue repair and healing in response to foreign invasion and tissue damage.

Show MeSH
Related in: MedlinePlus