Engineering the Cellular Microenvironment: Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior

Einollah Sarikhani; Dhivya Pushpa Meganathan; Anne Kathrine Kure Larsen; Keivan Rahmani; Ching Ting Tsai; Chih Hao Lu; Abel Marquez-Serrano; Leah Sadr; Xiao Li; Mingdong Dong; Francesca Santoro; Bianxiao Cui; Lasse Hyldgaard Klausen; Zeinab Jahed

doi:10.1021/acsnano.4c03743

Engineering the Cellular Microenvironment: Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior

Einollah Sarikhani, Dhivya Pushpa Meganathan, Anne Kathrine Kure Larsen, Keivan Rahmani, Ching Ting Tsai, Chih Hao Lu, Abel Marquez-Serrano, Leah Sadr, Xiao Li, Mingdong Dong, Francesca Santoro, Bianxiao Cui, Lasse Hyldgaard Klausen^*, Zeinab Jahed^*

^*Corresponding author af dette arbejde

Interdisciplinary Nanoscience Center

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

Abstract

The development of biomaterials capable of regulating cellular processes and guiding cell fate decisions has broad implications in tissue engineering, regenerative medicine, and cell-based assays for drug development and disease modeling. Recent studies have shown that three-dimensional (3D) nanoscale physical cues such as nanotopography can modulate various cellular processes like adhesion and endocytosis by inducing nanoscale curvature on the plasma and nuclear membranes. Two-dimensional (2D) biochemical cues such as protein micropatterns can also regulate cell function and fate by controlling cellular geometries. Development of biomaterials with precise control over nanoscale physical and biochemical cues can significantly influence programming cell function and fate. In this study, we utilized a laser-assisted micropatterning technique to manipulate the 2D architectures of cells on 3D nanopillar platforms. We performed a comprehensive analysis of cellular and nuclear morphology and deformation on both nanopillar and flat substrates. Our findings demonstrate the precise engineering of single cell architectures through 2D micropatterning on nanopillar platforms. We show that the coupling between the nuclear and cell shape is disrupted on nanopillar surfaces compared to flat surfaces. Furthermore, our results suggest that cell elongation on nanopillars enhances nanopillar-induced endocytosis. We believe our platform serves as a versatile tool for further explorations into programming cell function and fate through combined physical cues that create nanoscale curvature on cell membranes and biochemical cues that control the geometry of the cell.

Originalsprog	Engelsk
Tidsskrift	ACS Nano
Vol/bind	18
Nummer	29
Sider (fra-til)	19064-19076
Antal sider	13
ISSN	1936-0851
DOI	https://doi.org/10.1021/acsnano.4c03743
Status	Udgivet - jul. 2024

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10.1021/acsnano.4c03743Licens: CC BY-NC-ND

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Sarikhani, E., Meganathan, D. P., Larsen, A. K. K., Rahmani, K., Tsai, C. T., Lu, C. H., Marquez-Serrano, A., Sadr, L., Li, X., Dong, M., Santoro, F., Cui, B., Klausen, L. H., & Jahed, Z. (2024). Engineering the Cellular Microenvironment: Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior. ACS Nano, 18(29), 19064-19076. https://doi.org/10.1021/acsnano.4c03743

@article{0e24d348fc41435fa787b61dfdd69e00,

title = "Engineering the Cellular Microenvironment: Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior",

abstract = "The development of biomaterials capable of regulating cellular processes and guiding cell fate decisions has broad implications in tissue engineering, regenerative medicine, and cell-based assays for drug development and disease modeling. Recent studies have shown that three-dimensional (3D) nanoscale physical cues such as nanotopography can modulate various cellular processes like adhesion and endocytosis by inducing nanoscale curvature on the plasma and nuclear membranes. Two-dimensional (2D) biochemical cues such as protein micropatterns can also regulate cell function and fate by controlling cellular geometries. Development of biomaterials with precise control over nanoscale physical and biochemical cues can significantly influence programming cell function and fate. In this study, we utilized a laser-assisted micropatterning technique to manipulate the 2D architectures of cells on 3D nanopillar platforms. We performed a comprehensive analysis of cellular and nuclear morphology and deformation on both nanopillar and flat substrates. Our findings demonstrate the precise engineering of single cell architectures through 2D micropatterning on nanopillar platforms. We show that the coupling between the nuclear and cell shape is disrupted on nanopillar surfaces compared to flat surfaces. Furthermore, our results suggest that cell elongation on nanopillars enhances nanopillar-induced endocytosis. We believe our platform serves as a versatile tool for further explorations into programming cell function and fate through combined physical cues that create nanoscale curvature on cell membranes and biochemical cues that control the geometry of the cell.",

keywords = "cell and nuclear deformation, cell and nuclear mechanics, cell and nuclear morphology, mechanobiology, micropatterning, nanopillar, nanostructures",

author = "Einollah Sarikhani and Meganathan, {Dhivya Pushpa} and Larsen, {Anne Kathrine Kure} and Keivan Rahmani and Tsai, {Ching Ting} and Lu, {Chih Hao} and Abel Marquez-Serrano and Leah Sadr and Xiao Li and Mingdong Dong and Francesca Santoro and Bianxiao Cui and Klausen, {Lasse Hyldgaard} and Zeinab Jahed",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors. Published by American Chemical Society.",

year = "2024",

month = jul,

doi = "10.1021/acsnano.4c03743",

language = "English",

volume = "18",

pages = "19064--19076",

journal = "ACS Nano",

issn = "1936-0851",

publisher = "American Chemical Society",

number = "29",

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Sarikhani, E, Meganathan, DP, Larsen, AKK, Rahmani, K, Tsai, CT, Lu, CH, Marquez-Serrano, A, Sadr, L, Li, X, Dong, M, Santoro, F, Cui, B, Klausen, LH & Jahed, Z 2024, 'Engineering the Cellular Microenvironment: Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior', ACS Nano, bind 18, nr. 29, s. 19064-19076. https://doi.org/10.1021/acsnano.4c03743

Engineering the Cellular Microenvironment: Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior. / Sarikhani, Einollah; Meganathan, Dhivya Pushpa; Larsen, Anne Kathrine Kure et al.
I: ACS Nano, Bind 18, Nr. 29, 07.2024, s. 19064-19076.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

TY - JOUR

T1 - Engineering the Cellular Microenvironment

T2 - Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior

AU - Sarikhani, Einollah

AU - Meganathan, Dhivya Pushpa

AU - Larsen, Anne Kathrine Kure

AU - Rahmani, Keivan

AU - Tsai, Ching Ting

AU - Lu, Chih Hao

AU - Marquez-Serrano, Abel

AU - Sadr, Leah

AU - Li, Xiao

AU - Dong, Mingdong

AU - Santoro, Francesca

AU - Cui, Bianxiao

AU - Klausen, Lasse Hyldgaard

AU - Jahed, Zeinab

PY - 2024/7

Y1 - 2024/7

N2 - The development of biomaterials capable of regulating cellular processes and guiding cell fate decisions has broad implications in tissue engineering, regenerative medicine, and cell-based assays for drug development and disease modeling. Recent studies have shown that three-dimensional (3D) nanoscale physical cues such as nanotopography can modulate various cellular processes like adhesion and endocytosis by inducing nanoscale curvature on the plasma and nuclear membranes. Two-dimensional (2D) biochemical cues such as protein micropatterns can also regulate cell function and fate by controlling cellular geometries. Development of biomaterials with precise control over nanoscale physical and biochemical cues can significantly influence programming cell function and fate. In this study, we utilized a laser-assisted micropatterning technique to manipulate the 2D architectures of cells on 3D nanopillar platforms. We performed a comprehensive analysis of cellular and nuclear morphology and deformation on both nanopillar and flat substrates. Our findings demonstrate the precise engineering of single cell architectures through 2D micropatterning on nanopillar platforms. We show that the coupling between the nuclear and cell shape is disrupted on nanopillar surfaces compared to flat surfaces. Furthermore, our results suggest that cell elongation on nanopillars enhances nanopillar-induced endocytosis. We believe our platform serves as a versatile tool for further explorations into programming cell function and fate through combined physical cues that create nanoscale curvature on cell membranes and biochemical cues that control the geometry of the cell.

AB - The development of biomaterials capable of regulating cellular processes and guiding cell fate decisions has broad implications in tissue engineering, regenerative medicine, and cell-based assays for drug development and disease modeling. Recent studies have shown that three-dimensional (3D) nanoscale physical cues such as nanotopography can modulate various cellular processes like adhesion and endocytosis by inducing nanoscale curvature on the plasma and nuclear membranes. Two-dimensional (2D) biochemical cues such as protein micropatterns can also regulate cell function and fate by controlling cellular geometries. Development of biomaterials with precise control over nanoscale physical and biochemical cues can significantly influence programming cell function and fate. In this study, we utilized a laser-assisted micropatterning technique to manipulate the 2D architectures of cells on 3D nanopillar platforms. We performed a comprehensive analysis of cellular and nuclear morphology and deformation on both nanopillar and flat substrates. Our findings demonstrate the precise engineering of single cell architectures through 2D micropatterning on nanopillar platforms. We show that the coupling between the nuclear and cell shape is disrupted on nanopillar surfaces compared to flat surfaces. Furthermore, our results suggest that cell elongation on nanopillars enhances nanopillar-induced endocytosis. We believe our platform serves as a versatile tool for further explorations into programming cell function and fate through combined physical cues that create nanoscale curvature on cell membranes and biochemical cues that control the geometry of the cell.

KW - cell and nuclear deformation

KW - cell and nuclear mechanics

KW - cell and nuclear morphology

KW - mechanobiology

KW - micropatterning

KW - nanopillar

KW - nanostructures

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U2 - 10.1021/acsnano.4c03743

DO - 10.1021/acsnano.4c03743

M3 - Journal article

C2 - 38978500

AN - SCOPUS:85198076629

SN - 1936-0851

VL - 18

SP - 19064

EP - 19076

JO - ACS Nano

JF - ACS Nano

IS - 29

ER -

Engineering the Cellular Microenvironment: Integrating Three-Dimensional Nontopographical and Two-Dimensional Biochemical Cues for Precise Control of Cellular Behavior

Abstract

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