Preferential Attachment of Peritoneal Tumor Metastases to Omental Immune Aggregates and Possible Role of a Unique Vascular Microenvironment in Metastatic Survival and Growth
Controlling metastases remains a critical problem in cancer biology. Within the peritoneal cavity, omental tissue is a common site for metastatic disease arising from intraperitoneal tumors; however, it is unknown why this tissue is so favorable for metastatic tumor growth. Using five different tumo...
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| Veröffentlicht in: | The American journal of pathology 2006-11, Vol.169 (5), p.1739-1752 |
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| creator | Gerber, Scott A. Rybalko, Viktoriya Y. Bigelow, Chad E. Lugade, Amit A. Foster, Thomas H. Frelinger, John G. Lord, Edith M. |
| description | Controlling metastases remains a critical problem in cancer biology. Within the peritoneal cavity, omental tissue is a common site for metastatic disease arising from intraperitoneal tumors; however, it is unknown why this tissue is so favorable for metastatic tumor growth. Using five different tumor cell lines in three different strains of mice, we found that the omentum was a major site of metastases growth for intraperitoneal tumors. Furthermore, initial attachment and subsequent growth were limited to specific sites within the omentum, consisting of organized aggregates of immune cells. These immune aggregates contained a complex network of capillaries exhibiting a high vascular density, which appear to contribute to the survival of metastatic cells. We found that the vasculature within these aggregates contained CD105
+ vessels and vascular sprouts, both indicators of active angiogenesis. A subset of mesothelial cells situated atop the immune aggregates was found to be hypoxic, and a similar proportion was observed to secrete vascular endothelial growth factor-A. These data provide a physiological mechanism by which metastatic tumor cells preferentially grow at sites rich in proangiogenic vessels, apparently stimulated by angiogenic factors produced by mesothelial cells. These sites provide metastatic cells with a microenvironment highly conducive to survival and subsequent growth. |
| doi_str_mv | 10.2353/ajpath.2006.051222 |
| format | Article |
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+ vessels and vascular sprouts, both indicators of active angiogenesis. A subset of mesothelial cells situated atop the immune aggregates was found to be hypoxic, and a similar proportion was observed to secrete vascular endothelial growth factor-A. These data provide a physiological mechanism by which metastatic tumor cells preferentially grow at sites rich in proangiogenic vessels, apparently stimulated by angiogenic factors produced by mesothelial cells. These sites provide metastatic cells with a microenvironment highly conducive to survival and subsequent growth.</description><identifier>ISSN: 0002-9440</identifier><identifier>EISSN: 1525-2191</identifier><identifier>DOI: 10.2353/ajpath.2006.051222</identifier><identifier>PMID: 17071597</identifier><identifier>CODEN: AJPAA4</identifier><language>eng</language><publisher>Bethesda, MD: Elsevier Inc</publisher><subject>Animals ; Antigen-Antibody Complex - immunology ; Biological and medical sciences ; Cell Hypoxia ; Cell Line, Tumor ; Epithelium - pathology ; Investigative techniques, diagnostic techniques (general aspects) ; Macrophages - immunology ; Medical sciences ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Models, Immunological ; Neoplasm Metastasis ; Omentum - blood supply ; Omentum - cytology ; Omentum - immunology ; Omentum - pathology ; Pathology. Cytology. Biochemistry. Spectrometry. Miscellaneous investigative techniques ; Peritoneal Cavity - cytology ; Peritoneal Cavity - pathology ; Peritoneal Neoplasms - blood supply ; Peritoneal Neoplasms - pathology ; Phenotype ; Regular ; Vascular Cell Adhesion Molecule-1 - metabolism ; Vascular Endothelial Growth Factor A - biosynthesis</subject><ispartof>The American journal of pathology, 2006-11, Vol.169 (5), p.1739-1752</ispartof><rights>2006 American Society for Investigative Pathology</rights><rights>2006 INIST-CNRS</rights><rights>Copyright © American Society for Investigative Pathology 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c613t-9c6d9867b5eda273dbb070ae2a0ef0bcae26b0f46b9e77ce79bf8518fce3e5433</citedby><cites>FETCH-LOGICAL-c613t-9c6d9867b5eda273dbb070ae2a0ef0bcae26b0f46b9e77ce79bf8518fce3e5433</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1780209/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://dx.doi.org/10.2353/ajpath.2006.051222$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,315,728,781,785,886,3551,27929,27930,46000,53796,53798</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=18236912$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17071597$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gerber, Scott A.</creatorcontrib><creatorcontrib>Rybalko, Viktoriya Y.</creatorcontrib><creatorcontrib>Bigelow, Chad E.</creatorcontrib><creatorcontrib>Lugade, Amit A.</creatorcontrib><creatorcontrib>Foster, Thomas H.</creatorcontrib><creatorcontrib>Frelinger, John G.</creatorcontrib><creatorcontrib>Lord, Edith M.</creatorcontrib><title>Preferential Attachment of Peritoneal Tumor Metastases to Omental Immune Aggregates and Possible Role of a Unique Vascular Microenvironment in Metastatic Survival and Growth</title><title>The American journal of pathology</title><addtitle>Am J Pathol</addtitle><description>Controlling metastases remains a critical problem in cancer biology. Within the peritoneal cavity, omental tissue is a common site for metastatic disease arising from intraperitoneal tumors; however, it is unknown why this tissue is so favorable for metastatic tumor growth. Using five different tumor cell lines in three different strains of mice, we found that the omentum was a major site of metastases growth for intraperitoneal tumors. Furthermore, initial attachment and subsequent growth were limited to specific sites within the omentum, consisting of organized aggregates of immune cells. These immune aggregates contained a complex network of capillaries exhibiting a high vascular density, which appear to contribute to the survival of metastatic cells. We found that the vasculature within these aggregates contained CD105
+ vessels and vascular sprouts, both indicators of active angiogenesis. A subset of mesothelial cells situated atop the immune aggregates was found to be hypoxic, and a similar proportion was observed to secrete vascular endothelial growth factor-A. These data provide a physiological mechanism by which metastatic tumor cells preferentially grow at sites rich in proangiogenic vessels, apparently stimulated by angiogenic factors produced by mesothelial cells. These sites provide metastatic cells with a microenvironment highly conducive to survival and subsequent growth.</description><subject>Animals</subject><subject>Antigen-Antibody Complex - immunology</subject><subject>Biological and medical sciences</subject><subject>Cell Hypoxia</subject><subject>Cell Line, Tumor</subject><subject>Epithelium - pathology</subject><subject>Investigative techniques, diagnostic techniques (general aspects)</subject><subject>Macrophages - immunology</subject><subject>Medical sciences</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Models, Immunological</subject><subject>Neoplasm Metastasis</subject><subject>Omentum - blood supply</subject><subject>Omentum - cytology</subject><subject>Omentum - immunology</subject><subject>Omentum - pathology</subject><subject>Pathology. Cytology. Biochemistry. Spectrometry. Miscellaneous investigative techniques</subject><subject>Peritoneal Cavity - cytology</subject><subject>Peritoneal Cavity - pathology</subject><subject>Peritoneal Neoplasms - blood supply</subject><subject>Peritoneal Neoplasms - pathology</subject><subject>Phenotype</subject><subject>Regular</subject><subject>Vascular Cell Adhesion Molecule-1 - metabolism</subject><subject>Vascular Endothelial Growth Factor A - biosynthesis</subject><issn>0002-9440</issn><issn>1525-2191</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9klFv0zAQxyMEYmXwBXhAfgGeWmwnsRMJIVUTjElDq2Dj1XKcS-spsTvb6cSH4jtyoYXCy6QosXW_-99d7p9lLxld8LzM3-nbrU6bBadULGjJOOePshkreTnnrGaPsxmllM_roqAn2bMYb_Eq8oo-zU6YpJKVtZxlP1cBOgjgktU9WaakzWbAG_EdWUGwyTvAwPU4-EC-QNIRH4gkeXI1cRi7GIbRAVmu1wHWOmFQu5asfIy26YF89fhCNU1unL0bgXzX0Yy9Rjlrgge3s8G73zWt-1MiWUO-jWFnd1hgkjsP_j5tnmdPOt1HeHH4nmY3nz5en32eX16dX5wtL-dGsDzNayPauhKyKaHVXOZt01BJNXBNoaONwZNoaFeIpgYpDci66aqSVZ2BHMoiz0-zD3vd7dgM0BpsLuhebYMddPihvLbq_4izG7X2O8VkRTmtUeDtQSB4nDkmNdhooO-1Az9GJcuiEkIWBZJvHiRFTWmRU4Yg34P402LErf1th1E1-UHt_aAmP6i9HzDp1b-DHFMOBkDg9QHArei-C9oZG49cxXNRM34caGPXm3sbQMVB9z3KsqkuE7UqUTWfRn-_JwEXtLMQVDQWnIEWs0xSrbcPdfwLJFnm8g</recordid><startdate>20061101</startdate><enddate>20061101</enddate><creator>Gerber, Scott A.</creator><creator>Rybalko, Viktoriya Y.</creator><creator>Bigelow, Chad E.</creator><creator>Lugade, Amit A.</creator><creator>Foster, Thomas H.</creator><creator>Frelinger, John G.</creator><creator>Lord, Edith M.</creator><general>Elsevier Inc</general><general>ASIP</general><general>American Society for Investigative Pathology</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7T5</scope><scope>H94</scope><scope>5PM</scope></search><sort><creationdate>20061101</creationdate><title>Preferential Attachment of Peritoneal Tumor Metastases to Omental Immune Aggregates and Possible Role of a Unique Vascular Microenvironment in Metastatic Survival and Growth</title><author>Gerber, Scott A. ; Rybalko, Viktoriya Y. ; Bigelow, Chad E. ; Lugade, Amit A. ; Foster, Thomas H. ; Frelinger, John G. ; Lord, Edith M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c613t-9c6d9867b5eda273dbb070ae2a0ef0bcae26b0f46b9e77ce79bf8518fce3e5433</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Animals</topic><topic>Antigen-Antibody Complex - immunology</topic><topic>Biological and medical sciences</topic><topic>Cell Hypoxia</topic><topic>Cell Line, Tumor</topic><topic>Epithelium - pathology</topic><topic>Investigative techniques, diagnostic techniques (general aspects)</topic><topic>Macrophages - immunology</topic><topic>Medical sciences</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Models, Immunological</topic><topic>Neoplasm Metastasis</topic><topic>Omentum - blood supply</topic><topic>Omentum - cytology</topic><topic>Omentum - immunology</topic><topic>Omentum - pathology</topic><topic>Pathology. Cytology. Biochemistry. Spectrometry. Miscellaneous investigative techniques</topic><topic>Peritoneal Cavity - cytology</topic><topic>Peritoneal Cavity - pathology</topic><topic>Peritoneal Neoplasms - blood supply</topic><topic>Peritoneal Neoplasms - pathology</topic><topic>Phenotype</topic><topic>Regular</topic><topic>Vascular Cell Adhesion Molecule-1 - metabolism</topic><topic>Vascular Endothelial Growth Factor A - biosynthesis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gerber, Scott A.</creatorcontrib><creatorcontrib>Rybalko, Viktoriya Y.</creatorcontrib><creatorcontrib>Bigelow, Chad E.</creatorcontrib><creatorcontrib>Lugade, Amit A.</creatorcontrib><creatorcontrib>Foster, Thomas H.</creatorcontrib><creatorcontrib>Frelinger, John G.</creatorcontrib><creatorcontrib>Lord, Edith M.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The American journal of pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gerber, Scott A.</au><au>Rybalko, Viktoriya Y.</au><au>Bigelow, Chad E.</au><au>Lugade, Amit A.</au><au>Foster, Thomas H.</au><au>Frelinger, John G.</au><au>Lord, Edith M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Preferential Attachment of Peritoneal Tumor Metastases to Omental Immune Aggregates and Possible Role of a Unique Vascular Microenvironment in Metastatic Survival and Growth</atitle><jtitle>The American journal of pathology</jtitle><addtitle>Am J Pathol</addtitle><date>2006-11-01</date><risdate>2006</risdate><volume>169</volume><issue>5</issue><spage>1739</spage><epage>1752</epage><pages>1739-1752</pages><issn>0002-9440</issn><eissn>1525-2191</eissn><coden>AJPAA4</coden><abstract>Controlling metastases remains a critical problem in cancer biology. Within the peritoneal cavity, omental tissue is a common site for metastatic disease arising from intraperitoneal tumors; however, it is unknown why this tissue is so favorable for metastatic tumor growth. Using five different tumor cell lines in three different strains of mice, we found that the omentum was a major site of metastases growth for intraperitoneal tumors. Furthermore, initial attachment and subsequent growth were limited to specific sites within the omentum, consisting of organized aggregates of immune cells. These immune aggregates contained a complex network of capillaries exhibiting a high vascular density, which appear to contribute to the survival of metastatic cells. We found that the vasculature within these aggregates contained CD105
+ vessels and vascular sprouts, both indicators of active angiogenesis. A subset of mesothelial cells situated atop the immune aggregates was found to be hypoxic, and a similar proportion was observed to secrete vascular endothelial growth factor-A. These data provide a physiological mechanism by which metastatic tumor cells preferentially grow at sites rich in proangiogenic vessels, apparently stimulated by angiogenic factors produced by mesothelial cells. These sites provide metastatic cells with a microenvironment highly conducive to survival and subsequent growth.</abstract><cop>Bethesda, MD</cop><pub>Elsevier Inc</pub><pmid>17071597</pmid><doi>10.2353/ajpath.2006.051222</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Antigen-Antibody Complex - immunology Biological and medical sciences Cell Hypoxia Cell Line, Tumor Epithelium - pathology Investigative techniques, diagnostic techniques (general aspects) Macrophages - immunology Medical sciences Mice Mice, Inbred BALB C Mice, Inbred C57BL Models, Immunological Neoplasm Metastasis Omentum - blood supply Omentum - cytology Omentum - immunology Omentum - pathology Pathology. Cytology. Biochemistry. Spectrometry. Miscellaneous investigative techniques Peritoneal Cavity - cytology Peritoneal Cavity - pathology Peritoneal Neoplasms - blood supply Peritoneal Neoplasms - pathology Phenotype Regular Vascular Cell Adhesion Molecule-1 - metabolism Vascular Endothelial Growth Factor A - biosynthesis |
| title | Preferential Attachment of Peritoneal Tumor Metastases to Omental Immune Aggregates and Possible Role of a Unique Vascular Microenvironment in Metastatic Survival and Growth |
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