Functions of Thrombospondin-1 in the Tumor Microenvironment

The identification of thrombospondin-1 as an angiogenesis inhibitor in 1990 prompted interest in its role in cancer biology and potential as a therapeutic target. Decreased thrombospondin-1 mRNA and protein expression are associated with progression in several cancers, while expression by nonmaligna...

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Published inInternational journal of molecular sciences Vol. 22; no. 9; p. 4570
Main Authors Kaur, Sukhbir, Bronson, Steven M, Pal-Nath, Dipasmita, Miller, Thomas W, Soto-Pantoja, David R, Roberts, David D
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 01.05.2021
MDPI
Subjects
Adhesion
Angiogenesis
Angiogenesis inhibitors
Animals
Autophagy
Binding sites
Breast cancer
Cancer
Carcinogenesis
Carcinogens
CD36
CD47
Cell Adhesion
Cell Movement
Cell surface
Chemotherapy
cytotoxic T cells
Extracellular vesicles
Fibroblasts
Gene expression
Genotoxicity
Growth factors
Humans
Immune system
integrins
Integrins - metabolism
Ischemia
Life Sciences
Low density lipoprotein receptors
Lymphocytes
Melanoma
Metabolic response
Metastases
Metastasis
Mice
Motility
mRNA
natural killer cells
Neoplasms - blood supply
Neoplasms - immunology
Neoplasms - pathology
Neovascularization, Pathologic - metabolism
Neovascularization, Physiologic - genetics
Peptides
Perfusion
Phagocytosis
Proteins
Radiation therapy
Review
Senescence
Stem cells
T-Lymphocytes - immunology
Therapeutic targets
Thrombospondin
Thrombospondin 1 - genetics
Thrombospondin 1 - metabolism
Thrombospondin 1 - physiology
Tumor microenvironment
Tumor Microenvironment - physiology
Tumor suppressor genes
natural killer cells
integrins
nitric oxide
autophagy
angiogenesis
transforming growth factor-β1
tumor-initiating cells
CD36
CD47
cytotoxic T cells
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Abstract The identification of thrombospondin-1 as an angiogenesis inhibitor in 1990 prompted interest in its role in cancer biology and potential as a therapeutic target. Decreased thrombospondin-1 mRNA and protein expression are associated with progression in several cancers, while expression by nonmalignant cells in the tumor microenvironment and circulating levels in cancer patients can be elevated. is not a tumor suppressor gene, but the regulation of its expression in malignant cells by oncogenes and tumor suppressor genes mediates some of their effects on carcinogenesis, tumor progression, and metastasis. In addition to regulating angiogenesis and perfusion of the tumor vasculature, thrombospondin-1 limits antitumor immunity by CD47-dependent regulation of innate and adaptive immune cells. Conversely, thrombospondin-1 is a component of particles released by immune cells that mediate tumor cell killing. Thrombospondin-1 differentially regulates the sensitivity of malignant and nonmalignant cells to genotoxic stress caused by radiotherapy and chemotherapy. The diverse activities of thrombospondin-1 to regulate autophagy, senescence, stem cell maintenance, extracellular vesicle function, and metabolic responses to ischemic and genotoxic stress are mediated by several cell surface receptors and by regulating the functions of several secreted proteins. This review highlights progress in understanding thrombospondin-1 functions in cancer and the challenges that remain in harnessing its therapeutic potential.
AbstractList The identification of thrombospondin-1 as an angiogenesis inhibitor in 1990 prompted interest in its role in cancer biology and potential as a therapeutic target. Decreased thrombospondin-1 mRNA and protein expression are associated with progression in several cancers, while expression by nonmalignant cells in the tumor microenvironment and circulating levels in cancer patients can be elevated. THBS1 is not a tumor suppressor gene, but the regulation of its expression in malignant cells by oncogenes and tumor suppressor genes mediates some of their effects on carcinogenesis, tumor progression, and metastasis. In addition to regulating angiogenesis and perfusion of the tumor vasculature, thrombospondin-1 limits antitumor immunity by CD47-dependent regulation of innate and adaptive immune cells. Conversely, thrombospondin-1 is a component of particles released by immune cells that mediate tumor cell killing. Thrombospondin-1 differentially regulates the sensitivity of malignant and nonmalignant cells to genotoxic stress caused by radiotherapy and chemotherapy. The diverse activities of thrombospondin-1 to regulate autophagy, senescence, stem cell maintenance, extracellular vesicle function, and metabolic responses to ischemic and genotoxic stress are mediated by several cell surface receptors and by regulating the functions of several secreted proteins. This review highlights progress in understanding thrombospondin-1 functions in cancer and the challenges that remain in harnessing its therapeutic potential.
The identification of thrombospondin-1 as an angiogenesis inhibitor in 1990 prompted interest in its role in cancer biology and potential as a therapeutic target. Decreased thrombospondin-1 mRNA and protein expression are associated with progression in several cancers, while expression by nonmalignant cells in the tumor microenvironment and circulating levels in cancer patients can be elevated. is not a tumor suppressor gene, but the regulation of its expression in malignant cells by oncogenes and tumor suppressor genes mediates some of their effects on carcinogenesis, tumor progression, and metastasis. In addition to regulating angiogenesis and perfusion of the tumor vasculature, thrombospondin-1 limits antitumor immunity by CD47-dependent regulation of innate and adaptive immune cells. Conversely, thrombospondin-1 is a component of particles released by immune cells that mediate tumor cell killing. Thrombospondin-1 differentially regulates the sensitivity of malignant and nonmalignant cells to genotoxic stress caused by radiotherapy and chemotherapy. The diverse activities of thrombospondin-1 to regulate autophagy, senescence, stem cell maintenance, extracellular vesicle function, and metabolic responses to ischemic and genotoxic stress are mediated by several cell surface receptors and by regulating the functions of several secreted proteins. This review highlights progress in understanding thrombospondin-1 functions in cancer and the challenges that remain in harnessing its therapeutic potential.
The identification of thrombospondin-1 as an angiogenesis inhibitor in 1990 prompted interest in its role in cancer biology and potential as a therapeutic target. Decreased thrombospondin-1 mRNA and protein expression are associated with progression in several cancers, while expression by nonmalignant cells in the tumor microenvironment and circulating levels in cancer patients can be elevated. THBS1 is not a tumor suppressor gene, but the regulation of its expression in malignant cells by oncogenes and tumor suppressor genes mediates some of their effects on carcinogenesis, tumor progression, and metastasis. In addition to regulating angiogenesis and perfusion of the tumor vasculature, thrombospondin-1 limits antitumor immunity by CD47-dependent regulation of innate and adaptive immune cells. Conversely, thrombospondin-1 is a component of particles released by immune cells that mediate tumor cell killing. Thrombospondin-1 differentially regulates the sensitivity of malignant and nonmalignant cells to genotoxic stress caused by radiotherapy and chemotherapy. The diverse activities of thrombospondin-1 to regulate autophagy, senescence, stem cell maintenance, extracellular vesicle function, and metabolic responses to ischemic and genotoxic stress are mediated by several cell surface receptors and by regulating the functions of several secreted proteins. This review highlights progress in understanding thrombospondin-1 functions in cancer and the challenges that remain in harnessing its therapeutic potential.
Author Kaur, Sukhbir
Miller, Thomas W
Soto-Pantoja, David R
Roberts, David D
Pal-Nath, Dipasmita
Bronson, Steven M
AuthorAffiliation 1 Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, MD 20892, USA; Sukhbir.Kaur@nih.gov (S.K.); dipasmita.palnath@nih.gov (D.P.-N.)
4 Department of Surgery and Department of Cancer Biology, Comprehensive Cancer Center, Wake Forest School of Medicine, Winston-Salem, NC 27101, USA
2 Department of Internal Medicine, Section of Molecular Medicine, Comprehensive Cancer Center, Wake Forest School of Medicine, Winston-Salem, NC 27101, USA; sbronson@wakehealth.edu
3 Centre de Recherche en Cancérologie de Marseille, Institut Paoli-Calmettes, 13273 Marseille, France
AuthorAffiliation_xml – name: 1 Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, MD 20892, USA; Sukhbir.Kaur@nih.gov (S.K.); dipasmita.palnath@nih.gov (D.P.-N.)
– name: 4 Department of Surgery and Department of Cancer Biology, Comprehensive Cancer Center, Wake Forest School of Medicine, Winston-Salem, NC 27101, USA
– name: 3 Centre de Recherche en Cancérologie de Marseille, Institut Paoli-Calmettes, 13273 Marseille, France
– name: 2 Department of Internal Medicine, Section of Molecular Medicine, Comprehensive Cancer Center, Wake Forest School of Medicine, Winston-Salem, NC 27101, USA; sbronson@wakehealth.edu
Author_xml – sequence: 1
  givenname: Sukhbir
  surname: Kaur
  fullname: Kaur, Sukhbir
  organization: Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, MD 20892, USA
– sequence: 2
  givenname: Steven M
  surname: Bronson
  fullname: Bronson, Steven M
  organization: Department of Internal Medicine, Section of Molecular Medicine, Comprehensive Cancer Center, Wake Forest School of Medicine, Winston-Salem, NC 27101, USA
– sequence: 3
  givenname: Dipasmita
  surname: Pal-Nath
  fullname: Pal-Nath, Dipasmita
  organization: Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, MD 20892, USA
– sequence: 4
  givenname: Thomas W
  orcidid: 0000-0001-8645-2785
  surname: Miller
  fullname: Miller, Thomas W
  organization: Centre de Recherche en Cancérologie de Marseille, Institut Paoli-Calmettes, 13273 Marseille, France
– sequence: 5
  givenname: David R
  surname: Soto-Pantoja
  fullname: Soto-Pantoja, David R
  organization: Department of Surgery and Department of Cancer Biology, Comprehensive Cancer Center, Wake Forest School of Medicine, Winston-Salem, NC 27101, USA
– sequence: 6
  givenname: David D
  orcidid: 0000-0002-2481-2981
  surname: Roberts
  fullname: Roberts, David D
  organization: Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, MD 20892, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33925464$$D View this record in MEDLINE/PubMed
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Issue 9
Keywords natural killer cells
integrins
nitric oxide
autophagy
angiogenesis
transforming growth factor-β1
tumor-initiating cells
CD36
CD47
cytotoxic T cells
Language English
License Attribution: http://creativecommons.org/licenses/by
Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
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Snippet The identification of thrombospondin-1 as an angiogenesis inhibitor in 1990 prompted interest in its role in cancer biology and potential as a therapeutic...
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SubjectTerms Adhesion
Angiogenesis
Angiogenesis inhibitors
Animals
Autophagy
Binding sites
Breast cancer
Cancer
Carcinogenesis
Carcinogens
CD36
CD47
Cell Adhesion
Cell Movement
Cell surface
Chemotherapy
cytotoxic T cells
Extracellular vesicles
Fibroblasts
Gene expression
Genotoxicity
Growth factors
Humans
Immune system
integrins
Integrins - metabolism
Ischemia
Life Sciences
Low density lipoprotein receptors
Lymphocytes
Melanoma
Metabolic response
Metastases
Metastasis
Mice
Motility
mRNA
natural killer cells
Neoplasms - blood supply
Neoplasms - immunology
Neoplasms - pathology
Neovascularization, Pathologic - metabolism
Neovascularization, Physiologic - genetics
Peptides
Perfusion
Phagocytosis
Proteins
Radiation therapy
Review
Senescence
Stem cells
T-Lymphocytes - immunology
Therapeutic targets
Thrombospondin
Thrombospondin 1 - genetics
Thrombospondin 1 - metabolism
Thrombospondin 1 - physiology
Tumor microenvironment
Tumor Microenvironment - physiology
Tumor suppressor genes
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Title Functions of Thrombospondin-1 in the Tumor Microenvironment
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Volume 22
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