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Omental adipose tissue-derived stromal cells promote vascularization and growth of endometrial tumors
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Abstract
Purpose: Adipose tissue contains a population of tumor-tropic mesenchymal progenitors, termed adipose stromal cells (ASC), which engraft in neighboring tumors to form supportive tumor stroma. We hypothesized that intra-abdominal visceral adipose tissue may contain a uniquely tumor-promoting population of ASC to account for the relationship between excess visceral adipose tissue and mortality of intra-abdominal cancers. Experimental Design: To investigate this, we isolated and characterized ASC from intra-abdominal omental adipose tissue (O-ASC) and characterized their effects on endometrial cancer progression as compared with subcutaneous adipose-derived mesenchymal stromal cells (SC-ASC), bone marrow–derived mesenchymal stromal cells (BM-MSC), and lung fibroblasts. To model chronic recruitment of ASC by tumors, cells were injected metronomically into mice bearing Hec1a xenografts. Results: O-ASC expressed cell surface markers characteristic of BM-MSC and differentiated into mesenchymal lineages. Coculture with O-ASC increased endometrial cancer cell proliferation in vitro. Tumor tropism of O-ASC and SC-ASC for human Hec1a endometrial tumor xenografts was comparable, but O-ASC more potently promoted tumor growth. Compared with tumors in SC-ASC–injected mice, tumors in O-ASC–injected mice contained higher numbers of large tortuous desmin-positive blood vessels, which correlated with decreased central tumor necrosis and increased tumor cell proliferation. O-ASC exhibited enhanced motility as compared with SC-ASC in response to Hec1a-secreted factors. Conclusions: Visceral adipose tissue contains a population of multipotent MSCs that promote endometrial tumor growth more potently than MSCs from subcutaneous adipose tissue. We propose that O-ASCs recruited to tumors express specific factors that enhance tumor vascularization, promoting survival and proliferation of tumor cells. Clin Cancer Res; 18(3); 771–82. ©2011 AACR.
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“Both BM- and adipose-derived MSC display tumor tropism due to various tumor-released chemotactic factors including CCL25 [43], C-X-C motif chemokine-1 (CXCL1) [54], epidermal growth factor (EGF) [83, 84], hepatoma-derived growth factor (HDGF) [85], IL-8 [54], platelet-derived growth factor (PDGF) [84], stromal cell-derived factor-1 (SDF1, a.k.a. CXCL12) [86, 87], TGFβ [88], and VEGF [84].”
From Mesenchymal stem cell secretome and regenerative therapy after cancer (2013) · cites this paper as [54]
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“Although all MSC populations share basic similarities immunophenotypically and functionally, differences can be demonstrated using high resolution techniques [52, 53] and are reflected in variability within their secretome [7, 54].”
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“Subcutaneous adipose-derived MSC populations seem to secrete lower level of VEGF than BM-MSC [7, 54] or visceral ASC [54].”
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Citations
Cites
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590
Multilineage potential of adult human mesenchymal stem cells
Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., & Marshak, D. R. (1999) · Science · doi:10.1126/science.284.5411.143 · Cited by 21,052
Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F. C., Krause, D. S., Deans, R. J., Keating, A., Prockop, D. J., & Horwitz, E. M. (2006) · Cytotherapy · doi:10.1080/14653240600855905 · Cited by 17,766
Self-citationCoussens, L. M., & Werb, Z. (2002) · Nature · doi:10.1038/nature01322 · Cited by 15,111
Multilineage Cells from Human Adipose Tissue: Implications for Cell-Based Therapies
Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P., & Hedrick, M. H. (2001) · Tissue Engineering · doi:10.1089/107632701300062859 · Cited by 7,956
Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. Adults
Calle, E. E., Rodriguez, C., Walker-Thurmond, K., & Thun, M. J. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa021423 · Cited by 7,696
Tumors: Wounds That Do Not Heal
Flier, J. S., Underhill, L. H., & Dvorak, H. F. (1986) · New England Journal of Medicine · doi:10.1056/nejm198612253152606 · Cited by 4,391 · cited 1×
“Activation and proliferation of stromal cells recruited by tumors leads to their conversion into myofibroblasts/reactive stroma (12, 34, 35).”
Mesenchymal stem cells within tumour stroma promote breast cancer metastasis
Karnoub, A. E., Dash, A. B., Vo, A. P., Sullivan, A., Brooks, M. W., Bell, G. W., Richardson, A. L., Polyak, K., Tubo, R., & Weinberg, R. A. (2007) · Nature · doi:10.1038/nature06188 · Cited by 3,206
Bissell, M. J., & Radisky, D. (2001) · Nature Reviews Cancer · doi:10.1038/35094059 · Cited by 2,180
Germline Transmission and Tissue-Specific Expression of Transgenes Delivered by Lentiviral Vectors
Lois, C., Hong, E. J., Pease, S., Brown, E. J., & Baltimore, D. (2002) · Science · doi:10.1126/science.1067081 · Cited by 1,992
Adult mesenchymal stem cells for tissue engineering versus regenerative medicine
Caplan, A. I. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21200 · Cited by 1,956
Mesenchymal Stem Cells: Revisiting History, Concepts, and Assays
Bianco, P., Robey, P. G., & Simmons, P. J. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.03.002 · Cited by 1,618
Cause-Specific Excess Deaths Associated With Underweight, Overweight, and Obesity
Flegal, K. M., Graubard, B. I., Williamson, D. F., & Gail, M. H. (2007) · JAMA · doi:10.1001/jama.298.17.2028 · Cited by 1,542
Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals
Djouad, F., Plence, P., Bony, C., Tropel, P., Apparailly, F., Sany, J., Noël, D., & Jorgensen, C. (2003) · Blood · doi:10.1182/blood-2003-04-1193 · Cited by 1,166
Du, R., Lu, K. V., Petritsch, C. K., Liu, P., Ganß, R., Passegue, E. A., Song, H., VandenBerg, S. R., Johnson, R. S., Werb, Z., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.01.034 · Cited by 1,166
Self-citationHuman Bone Marrow–Derived Mesenchymal Stem Cells in the Treatment of Gliomas
Nakamizo, A., Marini, F. C., Amano, T., Khan, A., Studeny, M., Gumin, J., Chen, J. J., Hentschel, S. J., Vecil, G. G., Dembinski, J. L., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-1874 · Cited by 1,029
Self-citationTraktuev, D. O., Merfeld‐Clauss, S., Li, J., Kolonin, M. G., Arap, W., Pasqualini, R., Johnstone, B. H., & March, K. L. (2007) · Circulation Research · doi:10.1161/circresaha.107.159475 · Cited by 843
Self-citationStudeny, M., Marini, F. C., Dembinski, J. L., Zompetta, C., Cabreira-Hansen, M. D. G., Bekele, B. N., Champlin, R. E., & Andreeff, M. (2004) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djh299 · Cited by 841
Self-citationSpaeth, E. L., Dembinski, J. L., Sasser, A. K., Watson, K., Klopp, A., Hall, B., Andreeff, M., & Marini, F. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004992 · Cited by 807
Self-citationStromal Fibroblasts in Cancer: A Novel Tumor-Promoting Cell Type
Orimo, A., & Weinberg, R. A. (2006) · Cell Cycle · doi:10.4161/cc.5.15.3112 · Cited by 807
Kidd, S. M., Spaeth, E. L., Dembinski, J. L., Dietrich, M. F., Watson, K., Klopp, A. H., Battula, V. L., Weil, M., Andreeff, M., & Marini, F. C. (2009) · Stem Cells · doi:10.1002/stem.187 · Cited by 680
Self-citationRegulation of In Situ to Invasive Breast Carcinoma Transition
Hu, M., Yao, J., Carroll, D. K., Weremowicz, S., Chen, H., Carrasco, D. R., Richardson, A. L., Violette, S. M., Nikolskaya, T., Nikolsky, Y., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.03.007 · Cited by 513
Obesity and Cancer Risk: Recent Review and Evidence
Basen-Engquist, K., & Chang, M. (2011) · Current Oncology Reports · doi:10.1007/s11912-010-0139-7 · Cited by 439
Zhang, Y., Daquinag, A., Traktuev, D. O., Amaya-Manzanares, F., Simmons, P. J., March, K. L., Pasqualini, R., Arap, W., & Kolonin, M. G. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-3444 · Cited by 331
Self-citationKlopp, A. H., Spaeth, E. L., Dembinski, J. L., Woodward, W. A., Munshi, A., Meyn, R. E., Cox, J. D., Andreeff, M., & Marini, F. C. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-1406 · Cited by 304
Self-citationJoe, A. W., Yi, L., Even, Y., Vogl, A. W., & Rossi, F. M. V. (2009) · Stem Cells · doi:10.1002/stem.190 · Cited by 297
Clinical and Biological Significance of Vascular Endothelial Growth Factor in Endometrial Cancer
Kamat, A. A., Merritt, W. M., Coffey, D., Lin, Y. G., Patel, P. R., Broaddus, R. R., Nugent, E. K., Han, L. Y., Landen, C. N., Spannuth, W. A., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1017 · Cited by 194
Self-citationMalignant gliomas actively recruit bone marrow stromal cells by secreting angiogenic cytokines
Birnbaum, T., Roider, J., Schankin, C. J., Padovan, C. S., Schichor, C., Goldbrunner, R., & Straube, A. M. (2007) · Journal of Neuro-Oncology · doi:10.1007/s11060-007-9332-4 · Cited by 192
Friedenreich, C. M., Cust, A. E., Lahmann, P. H., Steindorf, K., Boutron‐Ruault, M., Clavel‐Chapelon, F., Mesrine, S., Linseisen, J., Rohrmann, S., Boeing, H., et al. (2007) · Cancer Causes & Control · doi:10.1007/s10552-006-0113-8 · Cited by 177
Klopp, A. H., Lacerda, L., Gupta, A., Debeb, B. G., Solley, T. N., Li, L., Spaeth, E. L., Xu, W., Zhang, X., Lewis, M. T., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012180 · Cited by 174
Self-citationMesenchymal Stem Cells in Cancer: Tumor-Associated Fibroblasts and Cell-Based Delivery Vehicles
Hall, B., Dembinski, J., Sasser, A., Studeny, M., Andreeff, M., & Marini, F. (2007) · International Journal of Hematology · doi:10.1532/ijh97.06230 · Cited by 171
Self-citationKim, S. M., Oh, J. H., Park, S. A., Ryu, C. H., Lim, J. Y., Kim, D., Chang, J. W., Oh, W., & Jeun, S. (2010) · Stem Cells · doi:10.1002/stem.543 · Cited by 140
Galiè, M., Konstantinidou, G., Peroni, D., Scambi, I., Marchini, C., Lisi, V., Krampera, M., Magnani, P., Merigo, F., Montani, M., et al. (2007) · Oncogene · doi:10.1038/sj.onc.1210920 · Cited by 130
More Than Structural Cells, Fibroblasts Create and Orchestrate the Tumor Microenvironment
Baglole, C. J., Ray, D. M., Bernstein, S. H., Feldon, S. E., Smith, T. J., Sime, P. J., & Phipps, R. P. (2006) · Immunological Investigations · doi:10.1080/08820130600754960 · Cited by 118
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Bellows, C. F., Zhang, Y., Simmons, P. J., Khalsa, A. S., & Kolonin, M. G. (2011) · Obesity · doi:10.1038/oby.2010.347 · Cited by 105
Self-citationZhu, W., Boachie-Adjei, O., Rawlins, B. A., Frenkel, B., Boskey, A. L., Ivashkiv, L. B., & Blobel, C. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m610232200 · Cited by 103
Mesenchymal stem cells promote mammary cancer cell migration in vitro via the CXCR2 receptor
Halpern, J. L., Kilbarger, A. K., & Lynch, C. C. (2011) · Cancer Letters · doi:10.1016/j.canlet.2011.04.018 · Cited by 102
Nie, J., Chang, B. H.-J., Traktuev, D. O., Sun, J. D., March, K. L., Chan, L., Sage, E. H., Pasqualini, R., Arap, W., & Kolonin, M. G. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0212 · Cited by 82
Self-citationCirculation of Progenitor Cells in Obese and Lean Colorectal Cancer Patients
Bellows, C. F., Zhang, Y., Chen, J., Frazier, M. L., & Kolonin, M. G. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0556 · Cited by 78
Self-citationEspinosa, Í., Carnicer, M. J., Catasús, L., Canet, B., D′Angelo, E., Zannoni, G. F., & Prat, J. (2010) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e3181f32168 · Cited by 77
Vascular targeting of adipose tissue as an anti-obesity approach
Daquinag, A. C., Zhang, Y., & Kolonin, M. G. (2011) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2011.01.004 · Cited by 74
Self-citationRapid expansion of human adipose-derived stromal cells preserving multipotency
D, H. S. M., Shigeura, T., Matsumoto, D., Inoue, K., D, H. K. M., D, N. A. M., Murase, S., Sato, K., Gonda, K., Koshima, I., et al. (2007) · Cytotherapy · doi:10.1080/14653240701679873 · Cited by 73
Intra-abdominal Fat Predicts Survival in Pancreatic Cancer
Balentine, C. J., Enriquez, J., Fisher, W. P., Hodges, S. E., Bansal, V., Sansgiry, S., Petersen, N. J., & Berger, D. H. (2010) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-010-1297-5 · Cited by 71
Prizment, A. E., Flood, A. P., Anderson, K. E., & Folsom, A. R. (2010) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-10-0522 · Cited by 65
Preadipocyte Number in Omental and Subcutaneous Adipose Tissue of Obese Individuals
Bakker, A. H. F., van Dielen, F. M. H., Greve, J. W. M., Adam, J. A., & Buurman, W. A. (2004) · Obesity Research · doi:10.1038/oby.2004.55 · Cited by 63
Engineered Mesenchymal Stem Cells for Cartilage Repair
Djouad, F., Mrugala, D., Noël, D., & Jørgensen, C. (2006) · Regenerative Medicine · doi:10.2217/17460751.1.4.529 · Cited by 57
Kinoshita, M., Johnson, D. L., Shatney, C. H., Lee, Y. L., & Mochizuki, H. (2001) · International Journal of Cancer · doi:10.1002/1097-0215(200002)9999:9999 · Cited by 51
Combinatorial stem cell mobilization
Kolonin, M. G., & Simmons, P. J. (2009) · Nature Biotechnology · doi:10.1038/nbt0309-252 · Cited by 40
Self-citationOmentectomy for Gynecologic Cancer: How Much Sampling Is Adequate for Microscopic Examination?
Usubutün, A., Özşeker, H. S., Himmetoğlu, Ç., Balcı, S., & Ayhan, A. (2007) · Archives of Pathology & Laboratory Medicine · doi:10.5858/2007-131-1578-ofgchm · Cited by 35
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Metadata
- Authors
- Klopp, A. H., Zhang, Y., Solley, T., Amaya-Manzanares, F., Marini, F., Andreeff, M., Debeb, B., Woodward, W., Schmandt, R., Broaddus, R., Lu, K., & Kolonin, M. G.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- Authors' Affiliations: Departments of 1Radiation Oncology, 2Leukemia, 3Gynecologic Oncology, and 4Pathology, The University of Texas MD Anderson Cancer Center; and 5The Brown Foundation Institute of Molecular Medicine, The University of Texas Health Science Center at Houston, Houston, Texas
- Corresponding author
- Kolonin, Mikhail G.
- ORCID
- Venue
- Clinical Cancer Research
- Published
- 2012-01-31
- Volume
- 18
- Issue
- 3
- Pages
- 771-782
- ISSN
- 1078-0432 (ISSN-L)
- 1557-3265
- PMC
- PMC3481843
- OpenAlex
- W2126961122
- Cited by
- 178
- References
- 49
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 5 · 2023: 19 · 2022: 6 · 2021: 13 · 2020: 7 · 2019: 11 · 2018: 13 · 2017: 17 · 2016: 12 · 2015: 21 · 2014: 16 · 2013: 22 · 2012: 8
- FWCI
- 7.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Clinical Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- U.S. Public Health Service (KG080782)
- National Cancer Institute (P50CA098258, P50CA140388, R01CA109451, RC1CA146381, P50CA083639, P30CA016672)
- National Institute of Neurological Disorders and Stroke (R01NS069964, R01NS06994)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- omental adipose tissue, adipose-derived stromal cells, endometrial cancer, tumor vascularization, tumor stroma, visceral adipose tissue, mesenchymal stem cells, tumor cell proliferation, tumor necrosis, cell motility, tumor microenvironment
- MeSH terms
- Adipose Tissue, Animals, Cell Differentiation, Female, Flow Cytometry, Humans, Neovascularization, Pathologic, Omentum, Transplantation, Heterologous, Endometrial Neoplasms, Stromal Cells, Subcutaneous Fat, Mice, Mesenchymal Stem Cells
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