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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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Suppression of effector but not regulatory T cells by omentum cells.(a) Immunosuppressive functions of omentum cells on effector T cells. Naïve CD4+ T cells were induced to differentiate into Th1, Th2, Th17, or iTregs. 5 days after induction, omentum cells were added to each group of cells. T cells were maintained further with the same culture medium for 2 days, harvested, and were stimulated with PMA and ionomycin for 4 hours to induce cytokine production. (b) Cells were cultured with (+) or without (−) omentum cells and treated as in (a). Cell numbers that are expressing IFNγ, IL-4, IL-17, or Foxp3 were determined after intracellular cytokine stain. For nTregs, CD4+CD25+ from spleen were expanded prior to co-culture for 2 weeks, then cultured with omentum cells for 2 days. (c) Effect of iNOS inhibitor on Th1 and Th17 inhibition by omentum cells. Differentiated Th1 or Th17 cells were cultured with omentum cells in the presence/absence of an iNOS inhibitor for 2 days as in (a). (d) Omentum cells were sorted into CD45− and CD45+ cells, then co-cultured with CD4+T cell differentiated into Th1 (upper panels) or Th17 (lower panels) cells for 5 days. After 2 days of co-culture, cells were harvested and cytokine profiles were determined as in (a).
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pone-0038368-g004: Suppression of effector but not regulatory T cells by omentum cells.(a) Immunosuppressive functions of omentum cells on effector T cells. Naïve CD4+ T cells were induced to differentiate into Th1, Th2, Th17, or iTregs. 5 days after induction, omentum cells were added to each group of cells. T cells were maintained further with the same culture medium for 2 days, harvested, and were stimulated with PMA and ionomycin for 4 hours to induce cytokine production. (b) Cells were cultured with (+) or without (−) omentum cells and treated as in (a). Cell numbers that are expressing IFNγ, IL-4, IL-17, or Foxp3 were determined after intracellular cytokine stain. For nTregs, CD4+CD25+ from spleen were expanded prior to co-culture for 2 weeks, then cultured with omentum cells for 2 days. (c) Effect of iNOS inhibitor on Th1 and Th17 inhibition by omentum cells. Differentiated Th1 or Th17 cells were cultured with omentum cells in the presence/absence of an iNOS inhibitor for 2 days as in (a). (d) Omentum cells were sorted into CD45− and CD45+ cells, then co-cultured with CD4+T cell differentiated into Th1 (upper panels) or Th17 (lower panels) cells for 5 days. After 2 days of co-culture, cells were harvested and cytokine profiles were determined as in (a).

Mentions: Adoptive transfer of omentum cells imposed a profound effect on bleomycin-induced lung inflammation. Recent studies revealed the significance of Th17 cells in this disease model [38]. Thus, we tested if omentum cells also inhibit activation/proliferation of already differentiated effector/regulatory T cells. When naive CD4+ T cells were differentiated into effector/regulatory T cells in vitro, and then co-cultured with omentum cells for 5 days, a significant reduction in cell numbers and expression of IFNγ (Th1 cells) and IL-17 (Th17 cells) was found (Fig. 4a, b). Little effect on Th2 cells was observed. Importantly, no effect on Foxp3 expression or numbers of Foxp3+ iTreg cells was detectable. Spleen-derived nTregs showed a mild increase in cell number when co-cultured with omentum cells. Together, the data show that omentum cells have cell type specific inhibition on effector type T cells.


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)

Suppression of effector but not regulatory T cells by omentum cells.(a) Immunosuppressive functions of omentum cells on effector T cells. Naïve CD4+ T cells were induced to differentiate into Th1, Th2, Th17, or iTregs. 5 days after induction, omentum cells were added to each group of cells. T cells were maintained further with the same culture medium for 2 days, harvested, and were stimulated with PMA and ionomycin for 4 hours to induce cytokine production. (b) Cells were cultured with (+) or without (−) omentum cells and treated as in (a). Cell numbers that are expressing IFNγ, IL-4, IL-17, or Foxp3 were determined after intracellular cytokine stain. For nTregs, CD4+CD25+ from spleen were expanded prior to co-culture for 2 weeks, then cultured with omentum cells for 2 days. (c) Effect of iNOS inhibitor on Th1 and Th17 inhibition by omentum cells. Differentiated Th1 or Th17 cells were cultured with omentum cells in the presence/absence of an iNOS inhibitor for 2 days as in (a). (d) Omentum cells were sorted into CD45− and CD45+ cells, then co-cultured with CD4+T cell differentiated into Th1 (upper panels) or Th17 (lower panels) cells for 5 days. After 2 days of co-culture, cells were harvested and cytokine profiles were determined as in (a).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3368844&req=5

pone-0038368-g004: Suppression of effector but not regulatory T cells by omentum cells.(a) Immunosuppressive functions of omentum cells on effector T cells. Naïve CD4+ T cells were induced to differentiate into Th1, Th2, Th17, or iTregs. 5 days after induction, omentum cells were added to each group of cells. T cells were maintained further with the same culture medium for 2 days, harvested, and were stimulated with PMA and ionomycin for 4 hours to induce cytokine production. (b) Cells were cultured with (+) or without (−) omentum cells and treated as in (a). Cell numbers that are expressing IFNγ, IL-4, IL-17, or Foxp3 were determined after intracellular cytokine stain. For nTregs, CD4+CD25+ from spleen were expanded prior to co-culture for 2 weeks, then cultured with omentum cells for 2 days. (c) Effect of iNOS inhibitor on Th1 and Th17 inhibition by omentum cells. Differentiated Th1 or Th17 cells were cultured with omentum cells in the presence/absence of an iNOS inhibitor for 2 days as in (a). (d) Omentum cells were sorted into CD45− and CD45+ cells, then co-cultured with CD4+T cell differentiated into Th1 (upper panels) or Th17 (lower panels) cells for 5 days. After 2 days of co-culture, cells were harvested and cytokine profiles were determined as in (a).
Mentions: Adoptive transfer of omentum cells imposed a profound effect on bleomycin-induced lung inflammation. Recent studies revealed the significance of Th17 cells in this disease model [38]. Thus, we tested if omentum cells also inhibit activation/proliferation of already differentiated effector/regulatory T cells. When naive CD4+ T cells were differentiated into effector/regulatory T cells in vitro, and then co-cultured with omentum cells for 5 days, a significant reduction in cell numbers and expression of IFNγ (Th1 cells) and IL-17 (Th17 cells) was found (Fig. 4a, b). Little effect on Th2 cells was observed. Importantly, no effect on Foxp3 expression or numbers of Foxp3+ iTreg cells was detectable. Spleen-derived nTregs showed a mild increase in cell number when co-cultured with omentum cells. Together, the data show that omentum cells have cell type specific inhibition on effector type T cells.

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