Modularity-based mathematical modeling of ligand inter-nanocluster connectivity for unraveling reversible stem cell regulation

Chowon Kim, Nayeon Kang, Sunhong Min, Ramar Thangam, Sungkyu Lee, Hyunsik Hong, Kanghyeon Kim, Seong Yeol Kim, Dahee Kim, Hyunji Rha, Kyong-Ryol Tag, Hyun-Jeong Lee, Nem Singh, Daun Jeong, Jangsun Hwang, Yuri Kim, Sangwoo Park, Hyesung Lee, Taeeon Kim, Sang Wook Son, Steve Park, Solmaz Karamikamkar, Yangzhi Zhu, Alireza Hassani Najafabadi, Zhiqin Chu, Wujin Sun, Pengchao Zhao, Kunyu Zhang, Liming Bian, Hyun-Cheol Song, Sung-Gyu Park, Jong Seung Kim, Sang-Yup Lee, Jae-Pyoung Ahn, Hong-Kyu Kim, Yu Shrike Zhang () and Heemin Kang ()
Additional contact information
Chowon Kim: Korea University
Nayeon Kang: Korea University
Sunhong Min: Korea University
Ramar Thangam: Korea University
Sungkyu Lee: Korea University
Hyunsik Hong: Korea University
Kanghyeon Kim: Korea University
Seong Yeol Kim: Korea University
Dahee Kim: Korea University
Hyunji Rha: Korea University
Kyong-Ryol Tag: Korea University
Hyun-Jeong Lee: Korea University
Nem Singh: Korea University
Daun Jeong: Korea University Anam Hospital
Jangsun Hwang: Korea University Anam Hospital
Yuri Kim: Korea University
Sangwoo Park: Korea University
Hyesung Lee: Yonsei University
Taeeon Kim: Korea Institute of Materials Science (KIMS)
Sang Wook Son: Korea University College of Medicine
Steve Park: Korea Advanced Institute of Science and Technology (KAIST)
Solmaz Karamikamkar: Terasaki Institute for Biomedical Innovation
Yangzhi Zhu: Terasaki Institute for Biomedical Innovation
Alireza Hassani Najafabadi: Terasaki Institute for Biomedical Innovation
Zhiqin Chu: The University of Hong Kong
Wujin Sun: Virginia Tech
Pengchao Zhao: South China University of Technology
Kunyu Zhang: South China University of Technology
Liming Bian: South China University of Technology
Hyun-Cheol Song: Korea Institute of Science and Technology (KIST)
Sung-Gyu Park: Korea Institute of Materials Science (KIMS)
Jong Seung Kim: Korea University
Sang-Yup Lee: Korea Institute of Materials Science (KIMS)
Jae-Pyoung Ahn: Korea Institute of Science and Technology (KIST)
Hong-Kyu Kim: Korea Institute of Science and Technology (KIST)
Yu Shrike Zhang: Brigham and Women’s Hospital Harvard Medical School
Heemin Kang: Korea University

Nature Communications, 2024, vol. 15, issue 1, 1-22

Abstract: Abstract The native extracellular matrix is continuously remodeled to form complex interconnected network structures that reversibly regulate stem cell behaviors. Both regulation and understanding of its intricate dynamicity can help to modulate numerous cell behaviors. However, neither of these has yet been achieved due to the lack of designing and modeling such complex structures with dynamic controllability. Here we report modularity-based mathematical modeling of extracellular matrix-emulating ligand inter-cluster connectivity using the graph theory. Increasing anisotropy of magnetic nano-blockers proportionately disconnects arginine-glycine-aspartic acid ligand-to-ligand interconnections and decreases the number of ligand inter-cluster edges. This phenomenon deactivates stem cells, which can be partly activated by linearizing the nano-blockers. Remote cyclic elevation of high-anisotropy nano-blockers flexibly generates nano-gaps under the nano-blockers and augments the number of ligand inter-cluster edges. Subsequently, integrin-presenting stem cell infiltration is stimulated, which reversibly intensifies focal adhesion and mechanotransduction-driven differentiation both in vitro and in vivo. Designing and systemically modeling extracellular matrix-mimetic geometries opens avenues for unraveling dynamic cell-material interactions for tissue regeneration.

Date: 2024
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DOI: 10.1038/s41467-024-54557-8

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