Robust tumor immunity to melanoma mediated by interleukin-9–producing T cells
In this issue, Thomas Kupper and colleagues report that mice deficient for ROR-γ or interleukin-23 (IL-23) receptor showed impaired melanoma growth. Tumor growth inhibition was dependent in part on IL-9 and T helper type 9 (T H 9) cells. Moreover, the authors showed that IL-9 acts on mast cells rath...
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| Published in | Nature medicine Vol. 18; no. 8; pp. 1248 - 1253 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.08.2012
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | In this issue, Thomas Kupper and colleagues report that mice deficient for ROR-γ or interleukin-23 (IL-23) receptor showed impaired melanoma growth. Tumor growth inhibition was dependent in part on IL-9 and T helper type 9 (T
H
9) cells. Moreover, the authors showed that IL-9 acts on mast cells rather than T or B cells to mediate its antitumor effects and that T
H
9 cells are present in human blood and skin, suggesting that a role for T
H
9 cells in human tumor immunity should be explored.
Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (T
H
17) pathway genes encoding retinoid-related orphan receptor γ (ROR-γ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9–blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice.
Il9r
−/−
mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and
Rag1
−/−
mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen–specific T
H
9 cells into both WT and
Rag1
−/−
mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in
Rag1
−/−
mice but not in mast-cell–deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of T
H
9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies. |
|---|---|
| AbstractList | In this issue, Thomas Kupper and colleagues report that mice deficient for ROR-γ or interleukin-23 (IL-23) receptor showed impaired melanoma growth. Tumor growth inhibition was dependent in part on IL-9 and T helper type 9 (T
H
9) cells. Moreover, the authors showed that IL-9 acts on mast cells rather than T or B cells to mediate its antitumor effects and that T
H
9 cells are present in human blood and skin, suggesting that a role for T
H
9 cells in human tumor immunity should be explored.
Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (T
H
17) pathway genes encoding retinoid-related orphan receptor γ (ROR-γ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9–blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice.
Il9r
−/−
mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and
Rag1
−/−
mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen–specific T
H
9 cells into both WT and
Rag1
−/−
mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in
Rag1
−/−
mice but not in mast-cell–deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of T
H
9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies. Interleukin-9 (IL-9) is a T cell cytokine that acts through a gamma C-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (T sub(H)17) pathway genes encoding retinoid-related orphan receptor gamma (ROR- gamma ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9-blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice. Il9r super(-/-) mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and Rag1 super(-/-) mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen-specific T sub(H)9 cells into both WT and Rag1 super(-/-) mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in Rag1 super(-/-) mice but not in mast-cell-deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of T sub(H)9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies. Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (TH17) pathway genes encoding retinoid-related orphan receptor γ (ROR-γ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9-blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice. Il9r-/- mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and Rag1-/- mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen-specific TH9 cells into both WT and Rag1-/- mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in Rag1-/- mice but not in mast-cell-deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of TH9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies. [PUBLICATION ABSTRACT] Interleukin-9 (IL-9) is a T cell cytokine that acts through a γ C-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 ([T.sub.H] 17) pathway genes encoding retinoid-related orphan receptor g (ROR-g) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9-blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice. [Il9r.sup.-/-] mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and [Rag1.sup.-/-] mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen-specific [T.sub.H] 9 cells into both WT and [Rag1.sup.-/-] mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in [Rag1.sup.-/-] mice but not in mast-cell-deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of [T.sub.H] 9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies. Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (T(H)17) pathway genes encoding retinoid-related orphan receptor γ (ROR-γ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9-blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice. Il9r(-/-) mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and Rag1(-/-) mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen-specific T(H)9 cells into both WT and Rag1(-/-) mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in Rag1(-/-) mice but not in mast-cell-deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of T(H)9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies.Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (T(H)17) pathway genes encoding retinoid-related orphan receptor γ (ROR-γ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9-blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice. Il9r(-/-) mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and Rag1(-/-) mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen-specific T(H)9 cells into both WT and Rag1(-/-) mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in Rag1(-/-) mice but not in mast-cell-deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of T(H)9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies. Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (T(H)17) pathway genes encoding retinoid-related orphan receptor γ (ROR-γ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9-blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice. Il9r(-/-) mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and Rag1(-/-) mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen-specific T(H)9 cells into both WT and Rag1(-/-) mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in Rag1(-/-) mice but not in mast-cell-deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of T(H)9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies. |
| Audience | Academic |
| Author | Purwar, Rahul Kuchroo, Vijay K Clark, Rachael A Schlapbach, Christoph Jiang, Xiaodong Fuhlbrigge, Robert C Elyaman, Wassim Jetten, Anton M Khoury, Samia J Kang, Hong Soon Xiao, Sheng Kupper, Thomas S |
| Author_xml | – sequence: 1 givenname: Rahul surname: Purwar fullname: Purwar, Rahul organization: Department of Dermatology, Brigham and Women's Hospital, Harvard Medical School – sequence: 2 givenname: Christoph surname: Schlapbach fullname: Schlapbach, Christoph organization: Department of Dermatology, Brigham and Women's Hospital, Harvard Medical School – sequence: 3 givenname: Sheng surname: Xiao fullname: Xiao, Sheng organization: Department of Neurology, Brigham and Women's Hospital, Harvard Medical School – sequence: 4 givenname: Hong Soon surname: Kang fullname: Kang, Hong Soon organization: Cell Biology Section, National Institute of Environmental Health Science, National Institutes of Health – sequence: 5 givenname: Wassim surname: Elyaman fullname: Elyaman, Wassim organization: Department of Neurology, Brigham and Women's Hospital, Harvard Medical School – sequence: 6 givenname: Xiaodong surname: Jiang fullname: Jiang, Xiaodong organization: Department of Dermatology, Brigham and Women's Hospital, Harvard Medical School – sequence: 7 givenname: Anton M surname: Jetten fullname: Jetten, Anton M organization: Cell Biology Section, National Institute of Environmental Health Science, National Institutes of Health – sequence: 8 givenname: Samia J surname: Khoury fullname: Khoury, Samia J organization: Department of Neurology, Brigham and Women's Hospital, Harvard Medical School – sequence: 9 givenname: Robert C surname: Fuhlbrigge fullname: Fuhlbrigge, Robert C organization: Department of Dermatology, Brigham and Women's Hospital, Harvard Medical School – sequence: 10 givenname: Vijay K surname: Kuchroo fullname: Kuchroo, Vijay K organization: Department of Neurology, Brigham and Women's Hospital, Harvard Medical School – sequence: 11 givenname: Rachael A surname: Clark fullname: Clark, Rachael A organization: Department of Dermatology, Brigham and Women's Hospital, Harvard Medical School – sequence: 12 givenname: Thomas S surname: Kupper fullname: Kupper, Thomas S email: tkupper@partners.org, tskupper@rics.bwh.harvard.edu organization: Department of Dermatology, Brigham and Women's Hospital, Harvard Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22772464$$D View this record in MEDLINE/PubMed |
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| Snippet | In this issue, Thomas Kupper and colleagues report that mice deficient for ROR-γ or interleukin-23 (IL-23) receptor showed impaired melanoma growth. Tumor... Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined... Interleukin-9 (IL-9) is a T cell cytokine that acts through a γ C-family receptor on target cells and is associated with inflammation and allergy. We... Interleukin-9 (IL-9) is a T cell cytokine that acts through a gamma C-family receptor on target cells and is associated with inflammation and allergy. We... |
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| SubjectTerms | 631/250/127/1213 692/699/67/1813/1634 692/699/67/580 Allergies Animals Biomedical and Life Sciences Biomedicine Blood Cancer Research Cancer Vaccines Carcinoma, Lewis Lung - immunology Carcinoma, Lewis Lung - pathology Care and treatment Cellular immunity Cytokines Diagnosis Disease Progression Gene expression Gene Expression Profiling Genetic aspects Health aspects Homeodomain Proteins - genetics Humans Immune system Immunotherapy, Adoptive Infectious Diseases Interleukin-9 Interleukin-9 - analysis Interleukin-9 - biosynthesis Interleukin-9 - genetics Interleukin-9 - physiology Lesions Lymphatic Metastasis Lymphocytes Lymphocytes, Tumor-Infiltrating - immunology Mast Cells - drug effects Mast Cells - immunology Melanoma Melanoma - chemistry Melanoma - immunology Melanoma - pathology Melanoma - secondary Melanoma, Experimental - immunology Melanoma, Experimental - pathology Melanoma, Experimental - therapy Metabolic Diseases Metastasis Mice Mice, Inbred C57BL Mice, Knockout Molecular Medicine Neoplasm Proteins - analysis Neoplasm Proteins - biosynthesis Neoplasm Proteins - genetics Neoplasm Proteins - physiology Neurosciences Nuclear Receptor Subfamily 1, Group F, Member 3 - deficiency Nuclear Receptor Subfamily 1, Group F, Member 3 - genetics Radiation Chimera Receptors, Interleukin - deficiency Receptors, Interleukin - genetics Recombinant Fusion Proteins - physiology Skin - immunology Skin cancer Skin Neoplasms - chemistry Skin Neoplasms - immunology Skin Neoplasms - pathology T cells T-Lymphocyte Subsets - immunology T-Lymphocyte Subsets - metabolism Tumor Burden Tumors Vaccination |
| Title | Robust tumor immunity to melanoma mediated by interleukin-9–producing T cells |
| URI | https://link.springer.com/article/10.1038/nm.2856 https://www.ncbi.nlm.nih.gov/pubmed/22772464 https://www.proquest.com/docview/1040232504 https://www.proquest.com/docview/1221142166 https://www.proquest.com/docview/1413162695 |
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