Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors
The presence of growth-induced solid stresses in tumors has been suspected for some time, but these stresses were largely estimated using mathematical models. Solid stresses can deform the surrounding tissues and compress intratumoral lymphatic and blood vessels. Compression of lymphatic vessels ele...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 109; no. 38; pp. 15101 - 15108 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
18.09.2012
National Acad Sciences |
| Series | Inaugural Article |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The presence of growth-induced solid stresses in tumors has been suspected for some time, but these stresses were largely estimated using mathematical models. Solid stresses can deform the surrounding tissues and compress intratumoral lymphatic and blood vessels. Compression of lymphatic vessels elevates interstitial fluid pressure, whereas compression of blood vessels reduces blood flow. Reduced blood flow, in turn, leads to hypoxia, which promotes tumor progression, immunosuppression, inflammation, invasion, and metastasis and lowers the efficacy of chemo-, radio-, and immunotherapies. Thus, strategies designed to alleviate solid stress have the potential to improve cancer treatment. However, a lack of methods for measuring solid stress has hindered the development of solid stress-alleviating drugs. Here, we present a simple technique to estimate the growth-induced solid stress accumulated within animal and human tumors, and we show that this stress can be reduced by depleting cancer cells, fibroblasts, collagen, and/or hyaluronan, resulting in improved tumor perfusion. Furthermore, we show that therapeutic depletion of carcinoma-associated fibroblasts with an inhibitor of the sonic hedgehog pathway reduces solid stress, decompresses blood and lymphatic vessels, and increases perfusion. In addition to providing insights into the mechanopathology of tumors, our approach can serve as a rapid screen for stress-reducing and perfusion-enhancing drugs. |
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| AbstractList | The presence of growth-induced solid stresses in tumors has been suspected for some time, but these stresses were largely estimated using mathematical models. Solid stresses can deform the surrounding tissues and compress intratumoral lymphatic and blood vessels. Compression of lymphatic vessels elevates interstitial fluid pressure, whereas compression of blood vessels reduces blood flow. Reduced blood flow, in turn, leads to hypoxia, which promotes tumor progression, immunosuppression, inflammation, invasion, and metastasis and lowers the efficacy of chemo-, radio-, and immunotherapies. Thus, strategies designed to alleviate solid stress have the potential to improve cancer treatment. However, a lack of methods for measuring solid stress has hindered the development of solid stress-alleviating drugs. Here, we present a simple technique to estimate the growth-induced solid stress accumulated within animal and human tumors, and we show that this stress can be reduced by depleting cancer cells, fibroblasts, collagen, and/or hyaluronan, resulting in improved tumor perfusion. Furthermore, we show that therapeutic depletion of carcinoma-associated fibroblasts with an inhibitor of the sonic hedgehog pathway reduces solid stress, decompresses blood and lymphatic vessels, and increases perfusion. In addition to providing insights into the mechanopathology of tumors, our approach can serve as a rapid screen for stress-reducing and perfusion-enhancing drugs. The presence of growth-induced solid stresses in tumors has been suspected for some time, but these stresses were largely estimated using mathematical models. Solid stresses can deform the surrounding tissues and compress intratumoral lymphatic and blood vessels. Compression of lymphatic vessels elevates interstitial fluid pressure, whereas compression of blood vessels reduces blood flow. Reduced blood flow, in turn, leads to hypoxia, which promotes tumor progression, immunosuppression, inflammation, invasion, and metastasis and lowers the efficacy of chemo-, radio-, and immunotherapies. Thus, strategies designed to alleviate solid stress have the potential to improve cancer treatment. However, a lack of methods for measuring solid stress has hindered the development of solid stress-alleviating drugs. Here, we present a simple technique to estimate the growth-induced solid stress accumulated within animal and human tumors, and we show that this stress can be reduced by depleting cancer cells, fibroblasts, collagen, and/or hyaluronan, resulting in improved tumor perfusion. Furthermore, we show that therapeutic depletion of carcinoma-associated fibroblasts with an inhibitor of the sonic hedgehog pathway reduces solid stress, decompresses blood and lymphatic vessels, and increases perfusion. In addition to providing insights into the mechanopathology of tumors, our approach can serve as a rapid screen for stress-reducing and perfusion-enhancing drugs.The presence of growth-induced solid stresses in tumors has been suspected for some time, but these stresses were largely estimated using mathematical models. Solid stresses can deform the surrounding tissues and compress intratumoral lymphatic and blood vessels. Compression of lymphatic vessels elevates interstitial fluid pressure, whereas compression of blood vessels reduces blood flow. Reduced blood flow, in turn, leads to hypoxia, which promotes tumor progression, immunosuppression, inflammation, invasion, and metastasis and lowers the efficacy of chemo-, radio-, and immunotherapies. Thus, strategies designed to alleviate solid stress have the potential to improve cancer treatment. However, a lack of methods for measuring solid stress has hindered the development of solid stress-alleviating drugs. Here, we present a simple technique to estimate the growth-induced solid stress accumulated within animal and human tumors, and we show that this stress can be reduced by depleting cancer cells, fibroblasts, collagen, and/or hyaluronan, resulting in improved tumor perfusion. Furthermore, we show that therapeutic depletion of carcinoma-associated fibroblasts with an inhibitor of the sonic hedgehog pathway reduces solid stress, decompresses blood and lymphatic vessels, and increases perfusion. In addition to providing insights into the mechanopathology of tumors, our approach can serve as a rapid screen for stress-reducing and perfusion-enhancing drugs. The presence of growth-induced solid stresses in tumors has been suspected for some time, but these stresses were largely estimated using mathematical models. Solid stresses can deform the surrounding tissues and compress intratumoral lymphatic and blood vessels. Compression of lymphatic vessels elevates interstitial fluid pressure, whereas compression of blood vessels reduces blood flow. Reduced blood flow, in turn, leads to hypoxia, which promotes tumor progression, immunosuppression, inflammation, invasion, and metastasis and lowers the efficacy of chemo-, radio-, and immunotherapies. Thus, strategies designed to alleviate solid stress have the potential to improve cancer treatment. However, a lack of methods for measuring solid stress has hindered the development of solid stress-alleviating drugs. Here, we present a simple technique to estimate the growth-induced solid stress accumulated within animal and human tumors, and we show that this stress can be reduced by depleting cancer cells, fibroblasts, collagen, and/or hyaluronan, resulting in improved tumor perfusion. Furthermore, we show that therapeutic depletion of carcinoma-associated fibroblasts with an inhibitor of the sonic hedgehog pathway reduces solid stress, decompresses blood and lymphatic vessels, and increases perfusion. In addition to providing insights into the mechanopathology of tumors, our approach can serve as a rapid screen for stress-reducing and perfusion-enhancing drugs. [PUBLICATION ABSTRACT] |
| Author | Stylianopoulos, Triantafyllos Jain, Saloni R. Hornicek, Francis J. Martin, John D. Ferrone, Cristina R. Munn, Lance L. Bardeesy, Nabeel Chauhan, Vikash P. Smith, Barbara L. Boucher, Yves Jain, Rakesh K. Diop-Frimpong, Benjamin |
| Author_xml | – sequence: 1 givenname: Triantafyllos surname: Stylianopoulos fullname: Stylianopoulos, Triantafyllos – sequence: 2 givenname: John D. surname: Martin fullname: Martin, John D. – sequence: 3 givenname: Vikash P. surname: Chauhan fullname: Chauhan, Vikash P. – sequence: 4 givenname: Saloni R. surname: Jain fullname: Jain, Saloni R. – sequence: 5 givenname: Benjamin surname: Diop-Frimpong fullname: Diop-Frimpong, Benjamin – sequence: 6 givenname: Nabeel surname: Bardeesy fullname: Bardeesy, Nabeel – sequence: 7 givenname: Barbara L. surname: Smith fullname: Smith, Barbara L. – sequence: 8 givenname: Cristina R. surname: Ferrone fullname: Ferrone, Cristina R. – sequence: 9 givenname: Francis J. surname: Hornicek fullname: Hornicek, Francis J. – sequence: 10 givenname: Yves surname: Boucher fullname: Boucher, Yves – sequence: 11 givenname: Lance L. surname: Munn fullname: Munn, Lance L. – sequence: 12 givenname: Rakesh K. surname: Jain fullname: Jain, Rakesh K. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22932871$$D View this record in MEDLINE/PubMed |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author contributions: T.S., J.D.M., V.P.C., and R.K.J. designed research; T.S., J.D.M., V.P.C., S.R.J., and B.D.-F. performed research; N.B., B.L.S., C.R.F., and F.J.H. contributed new reagents/analytic tools; T.S., J.D.M., V.P.C., Y.B., L.L.M., and R.K.J. analyzed data; and T.S., J.D.M., L.L.M., and R.K.J. wrote the paper. Contributed by Rakesh K. Jain, August 2, 2012 (sent for review December 5, 2011) This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2009. 1T.S. and J.D.M. contributed equally to this work. |
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| Snippet | The presence of growth-induced solid stresses in tumors has been suspected for some time, but these stresses were largely estimated using mathematical models.... |
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| SubjectTerms | Adenocarcinoma - pathology Animals Biological Sciences blood blood flow Blood vessels Blood Vessels - pathology Cancer Cell growth Cells Collagen Collagen - chemistry Collagens Compressive stress drugs Female fibroblasts Fibroblasts - pathology Human subjects Humans hyaluronic acid Hyaluronic Acid - chemistry Hypoxia immunotherapy Immunotherapy - methods inflammation Mathematical models Mechanical stress metastasis Mice Mice, SCID Models, Theoretical neoplasm cells Neoplasm Transplantation neoplasms Neoplasms - pathology Pancreatic Ducts - pathology Pancreatic Neoplasms - pathology Perfusion Physical Sciences Solids Stress Stress, Mechanical Stromal Cells - cytology Tensile stress Tumors |
| Title | Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors |
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