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Adipose Cells Induce Escape from an Engineered Human Breast Microtumor Independently of their Obesity Status

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Abstract

Introduction

Obesity is associated with increased breast cancer incidence, recurrence, and mortality. Adipocytes and adipose-derived stem cells (ASCs), two resident cell types in adipose tissue, accelerate the early stages of breast cancer progression. It remains unclear whether obesity plays a role in the subsequent escape of malignant breast cancer cells into the local circulation.

Methods

We engineered models of human breast tumors with adipose stroma that exhibited different obesity-specific alterations. We used these models to assess the invasion and escape of breast cancer cells into an empty, blind-ended cavity (as a mimic of a lymphatic vessel) for up to sixteen days.

Results

Lean and obese donor-derived adipose stroma hastened escape to similar extents. Moreover, a hypertrophic adipose stroma did not affect the rate of adipose-induced escape. When admixed directly into the model tumors, lean and obese donor-derived ASCs hastened escape similarly.

Conclusions

This study demonstrates that the presence of adipose cells, independently of the obesity status of the adipose tissue donor, hastens the escape of human breast cancer cells in multiple models of obesity-associated breast cancer.

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Abbreviations

ASC:

Adipose-derived stem cell

BMI:

Body mass index

CM:

Conditioned medium

ECM:

Extracellular matrix

FFA:

Free fatty acid

IFP:

Interstitial fluid pressure

SMA:

Smooth muscle actin

SVF:

Stromal-vascular fraction

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Acknowledgments

This work was supported by award U01 CA214292 from the National Cancer Institute and by award P30 DK046200 (Boston Nutrition Obesity Research Center; BNORC) from the National Institute of Diabetes and Digestive and Kidney Diseases. Y.W.D. was funded through the CURE Diversity Research Supplements Program at the National Cancer Institute, and M.C.O. was funded through the Undergraduate Research Opportunities Program at Boston University. Human breast-derived ASCs were provided by the Mayo Clinic Comprehensive Cancer Center and BNORC. We thank Miguel L. Batista, Jr. and Nabil Rabhi for insightful discussions.

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Authors and Affiliations

  1. Department of Biomedical Engineering, Boston University, 44 Cummington Mall, Boston, MA, 02215, USA

    Yoseph W. Dance, Mackenzie C. Obenreder, Alex J. Seibel, Nikhil Lahiri & Joe Tien

  2. Boston Nutrition Obesity Research Center, Boston University School of Medicine, Boston, MA, USA

    Tova Meshulam & Stephen R. Farmer

  3. Department of Biochemistry, Boston University School of Medicine, Boston, MA, USA

    Tova Meshulam, Matthew D. Layne & Stephen R. Farmer

  4. Department of Cancer Biology, Mayo Clinic Comprehensive Cancer Center, Jacksonville, FL, USA

    Joshua W. Ogony & Derek C. Radisky

  5. Department of Quantitative Health Sciences, Mayo Clinic Comprehensive Cancer Center, Jacksonville, FL, USA

    Laura Pacheco-Spann

  6. Department of Chemical and Biological Engineering, Princeton University, 303 Hoyt Laboratory, 25 William Street, Princeton, NJ, 08544, USA

    Celeste M. Nelson

  7. Department of Molecular Biology, Princeton University, Princeton, NJ, USA

    Celeste M. Nelson

  8. Division of Materials Science and Engineering, Boston University, Boston, MA, USA

    Joe Tien

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  1. Yoseph W. Dance
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Yoseph W. Dance, Mackenzie C. Obenreder, Alex J. Seibel, Tova Meshulam, Joshua W. Ogony, Nikhil Lahiri, Laura Pacheco-Spann, Derek C. Radisky, Matthew D. Layne, Stephen R. Farmer, Celeste M. Nelson, and Joe Tien declare that they have no conflict of interest.

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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients for being included in the study.

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Dance, Y.W., Obenreder, M.C., Seibel, A.J. et al. Adipose Cells Induce Escape from an Engineered Human Breast Microtumor Independently of their Obesity Status. Cel. Mol. Bioeng. 16, 23–39 (2023). https://doi.org/10.1007/s12195-022-00750-y

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