Complement Component 3 Adapts the Cerebrospinal Fluid for Leptomeningeal Metastasis

We molecularly dissected leptomeningeal metastasis, or spread of cancer to the cerebrospinal fluid (CSF), which is a frequent and fatal condition mediated by unknown mechanisms. We selected lung and breast cancer cell lines for the ability to infiltrate and grow in CSF, a remarkably acellular, mitog...

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Veröffentlicht in:	Cell Jg. 168; H. 6; S. 1101 - 1113.e13
Hauptverfasser:	Boire, Adrienne, Zou, Yilong, Shieh, Jason, Macalinao, Danilo G, Pentsova, Elena, Massagué, Joan
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States 09.03.2017
Schlagworte:	Animals Breast Neoplasms - pathology Cerebrospinal Fluid Choroid Plexus - blood supply Complement C3 - genetics Complement C3 - metabolism Humans Intercellular Signaling Peptides and Proteins - metabolism Lung Neoplasms - pathology Macrophage-1 Antigen - metabolism Meningeal Neoplasms - secondary Mice Neoplasm Metastasis - pathology Signal Transduction Tumor Microenvironment Up-Regulation amphiregulin lung cancer leptomeningeal metastasis GDNF carcinomatous meningitis PDGF cerebrospinal fluid breast cancer complement C3 brain metastasis choroid plexus
ISSN:	1097-4172
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Abstract	We molecularly dissected leptomeningeal metastasis, or spread of cancer to the cerebrospinal fluid (CSF), which is a frequent and fatal condition mediated by unknown mechanisms. We selected lung and breast cancer cell lines for the ability to infiltrate and grow in CSF, a remarkably acellular, mitogen-poor metastasis microenvironment. Complement component 3 (C3) was upregulated in four leptomeningeal metastatic models and proved necessary for cancer growth within the leptomeningeal space. In human disease, cancer cells within the CSF produced C3 in correlation with clinical course. C3 expression in primary tumors was predictive of leptomeningeal relapse. Mechanistically, we found that cancer-cell-derived C3 activates the C3a receptor in the choroid plexus epithelium to disrupt the blood-CSF barrier. This effect allows plasma components, including amphiregulin, and other mitogens to enter the CSF and promote cancer cell growth. Pharmacologic interference with C3 signaling proved therapeutically beneficial in suppressing leptomeningeal metastasis in these preclinical models.
AbstractList	We molecularly dissected leptomeningeal metastasis, or spread of cancer to the cerebrospinal fluid (CSF), which is a frequent and fatal condition mediated by unknown mechanisms. We selected lung and breast cancer cell lines for the ability to infiltrate and grow in CSF, a remarkably acellular, mitogen-poor metastasis microenvironment. Complement component 3 (C3) was upregulated in four leptomeningeal metastatic models and proved necessary for cancer growth within the leptomeningeal space. In human disease, cancer cells within the CSF produced C3 in correlation with clinical course. C3 expression in primary tumors was predictive of leptomeningeal relapse. Mechanistically, we found that cancer-cell-derived C3 activates the C3a receptor in the choroid plexus epithelium to disrupt the blood-CSF barrier. This effect allows plasma components, including amphiregulin, and other mitogens to enter the CSF and promote cancer cell growth. Pharmacologic interference with C3 signaling proved therapeutically beneficial in suppressing leptomeningeal metastasis in these preclinical models. We molecularly dissected leptomeningeal metastasis, or spread of cancer to the cerebrospinal fluid (CSF), which is a frequent and fatal condition mediated by unknown mechanisms. We selected lung and breast cancer cell lines for the ability to infiltrate and grow in CSF, a remarkably acellular, mitogen-poor metastasis microenvironment. Complement component 3 (C3) was upregulated in four leptomeningeal metastatic models and proved necessary for cancer growth within the leptomeningeal space. In human disease, cancer cells within the CSF produced C3 in correlation with clinical course. C3 expression in primary tumors was predictive of leptomeningeal relapse. Mechanistically, we found that cancer-cell-derived C3 activates the C3a receptor in the choroid plexus epithelium to disrupt the blood-CSF barrier. This effect allows plasma components, including amphiregulin, and other mitogens to enter the CSF and promote cancer cell growth. Pharmacologic interference with C3 signaling proved therapeutically beneficial in suppressing leptomeningeal metastasis in these preclinical models.
Author	Macalinao, Danilo G Pentsova, Elena Shieh, Jason Zou, Yilong Boire, Adrienne Massagué, Joan
Author_xml	– sequence: 1 givenname: Adrienne surname: Boire fullname: Boire, Adrienne organization: Department of Neurology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA; Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA – sequence: 2 givenname: Yilong surname: Zou fullname: Zou, Yilong organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA – sequence: 3 givenname: Jason surname: Shieh fullname: Shieh, Jason organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA – sequence: 4 givenname: Danilo G surname: Macalinao fullname: Macalinao, Danilo G organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA – sequence: 5 givenname: Elena surname: Pentsova fullname: Pentsova, Elena organization: Department of Neurology, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA – sequence: 6 givenname: Joan surname: Massagué fullname: Massagué, Joan email: j-massague@ski.mskcc.org organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA. Electronic address: j-massague@ski.mskcc.org
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28283064$$D View this record in MEDLINE/PubMed
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Keywords	amphiregulin lung cancer leptomeningeal metastasis GDNF carcinomatous meningitis PDGF cerebrospinal fluid breast cancer complement C3 brain metastasis choroid plexus
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Snippet	We molecularly dissected leptomeningeal metastasis, or spread of cancer to the cerebrospinal fluid (CSF), which is a frequent and fatal condition mediated by...
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SubjectTerms	Animals Breast Neoplasms - pathology Cerebrospinal Fluid Choroid Plexus - blood supply Complement C3 - genetics Complement C3 - metabolism Humans Intercellular Signaling Peptides and Proteins - metabolism Lung Neoplasms - pathology Macrophage-1 Antigen - metabolism Meningeal Neoplasms - secondary Mice Neoplasm Metastasis - pathology Signal Transduction Tumor Microenvironment Up-Regulation
Title	Complement Component 3 Adapts the Cerebrospinal Fluid for Leptomeningeal Metastasis
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