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Volume 15
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10.3390/genes15020199
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Article

The Impact of 3D Nichoids and Matrix Stiffness on Primary Malignant Mesothelioma Cells

by
Stefania Oliveto
1,2,
Paolo Ritter
2,3,
Giorgia Deroma
1,2,
Annarita Miluzio
2,
Chiara Cordiglieri
2,
Mauro Roberto Benvenuti
4,
Luciano Mutti
5,6,
Manuela Teresa Raimondi
3 and
Stefano Biffo
1,2,*
1
Department of Biosciences, University of Milan, 20133 Milan, Italy
2
National Institute of Molecular Genetics, Fondazione Romeo ed Enrica Invernizzi, INGM, 20122 Milan, Italy
3
Department of Chemistry, Materials and Chemical Engineering “Giulio Natta”, Politecnico di Milano, 20133 Milano, Italy
4
Thoracic Surgery Unit, Department of Medical and Surgical Specialties Radiological Sciences and Public Health, Medical Oncology, University of Brescia, ASST Spedali Civili of Brescia, 25123 Brescia, Italy
5
Department of Applied Clinical Sciences and Biotechnology, DISCAB, Aquila University, 67100 L’ Aquila, Italy
6
Department of Biotechnology, SHRO, Temple University, Philadelphia, PA 19122, USA
*
Author to whom correspondence should be addressed.
Genes 2024, 15(2), 199; https://doi.org/10.3390/genes15020199
Submission received: 24 December 2023 / Revised: 23 January 2024 / Accepted: 25 January 2024 / Published: 1 February 2024
(This article belongs to the Section Molecular Genetics and Genomics)
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Abstract

Malignant mesothelioma is a type of cancer that affects the mesothelium. It is an aggressive and deadly form of cancer that is often caused by exposure to asbestos. At the molecular level, it is characterized by a low number of genetic mutations and high heterogeneity among patients. In this work, we analyzed the plasticity of gene expression of primary mesothelial cancer cells by comparing their properties on 2D versus 3D surfaces. First, we derived from primary human samples four independent primary cancer cells. Then, we used Nichoids, which are micro-engineered 3D substrates, as three-dimensional structures. Nichoids limit the dimension of adhering cells during expansion by counteracting cell migration between adjacent units of a substrate with their microarchitecture. Tumor cells grow effectively on Nichoids, where they show enhanced proliferation. We performed RNAseq analyses on all the samples and compared the gene expression pattern of Nichoid-grown tumor cells to that of cells grown in a 2D culture. The PCA analysis showed that 3D samples were more transcriptionally similar compared to the 2D ones. The 3D Nichoids induced a transcriptional remodeling that affected mainly genes involved in extracellular matrix assembly. Among these genes responsible for collagen formation, COL1A1 and COL5A1 exhibited elevated expression, suggesting changes in matrix stiffness. Overall, our data show that primary mesothelioma cells can be effectively expanded in Nichoids and that 3D growth affects the cells’ tensegrity or the mechanical stability of their structure.
Keywords: NFATC1; epithelioid; organoids; malignant pleural mesothelioma; extracellular matrix NFATC1; epithelioid; organoids; malignant pleural mesothelioma; extracellular matrix

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MDPI and ACS Style

Oliveto, S.; Ritter, P.; Deroma, G.; Miluzio, A.; Cordiglieri, C.; Benvenuti, M.R.; Mutti, L.; Raimondi, M.T.; Biffo, S. The Impact of 3D Nichoids and Matrix Stiffness on Primary Malignant Mesothelioma Cells. Genes 2024, 15, 199. https://doi.org/10.3390/genes15020199

AMA Style

Oliveto S, Ritter P, Deroma G, Miluzio A, Cordiglieri C, Benvenuti MR, Mutti L, Raimondi MT, Biffo S. The Impact of 3D Nichoids and Matrix Stiffness on Primary Malignant Mesothelioma Cells. Genes. 2024; 15(2):199. https://doi.org/10.3390/genes15020199

Chicago/Turabian Style

Oliveto, Stefania, Paolo Ritter, Giorgia Deroma, Annarita Miluzio, Chiara Cordiglieri, Mauro Roberto Benvenuti, Luciano Mutti, Manuela Teresa Raimondi, and Stefano Biffo. 2024. "The Impact of 3D Nichoids and Matrix Stiffness on Primary Malignant Mesothelioma Cells" Genes 15, no. 2: 199. https://doi.org/10.3390/genes15020199

APA Style

Oliveto, S., Ritter, P., Deroma, G., Miluzio, A., Cordiglieri, C., Benvenuti, M. R., Mutti, L., Raimondi, M. T., & Biffo, S. (2024). The Impact of 3D Nichoids and Matrix Stiffness on Primary Malignant Mesothelioma Cells. Genes, 15(2), 199. https://doi.org/10.3390/genes15020199

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