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Delivery of Endothelial Cell-Laden Microgel Elicits Angiogenesis in Self-Assembling Ultrashort Peptide Hydrogels In Vitro

  • Gustavo Ramirez-Calderon
    Gustavo Ramirez-Calderon
    Laboratory for Nanomedicine, Division of Biological & Environmental Science & Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia
  • Hepi Hari Susapto
    Hepi Hari Susapto
    Laboratory for Nanomedicine, Division of Biological & Environmental Science & Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia
  • , and 
  • Charlotte A. E. Hauser*
    Charlotte A. E. Hauser
    Laboratory for Nanomedicine, Division of Biological & Environmental Science & Engineering (BESE)  and  Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia
    *Email: [email protected]
Cite this: ACS Appl. Mater. Interfaces 2021, 13, 25, 29281–29292
Publication Date (Web):June 18, 2021
https://doi.org/10.1021/acsami.1c03787
Copyright © 2021 American Chemical Society

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    Abstract

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    Blood vessel generation is an essential process for tissue formation, regeneration, and repair. Notwithstanding, vascularized tissue fabrication in vitro remains a challenge, as current fabrication techniques and biomaterials lack translational potential in medicine. Naturally derived biomaterials harbor the risk of immunogenicity and pathogen transmission, while synthetic materials need functionalization or blending to improve their biocompatibility. In addition, the traditional top-down fabrication techniques do not recreate the native tissue microarchitecture. Self-assembling ultrashort peptides (SUPs) are promising chemically synthesized natural materials that self-assemble into three-dimensional nanofibrous hydrogels resembling the extracellular matrix (ECM). Here, we use a modular tissue-engineering approach, embedding SUP microgels loaded with human umbilical vein endothelial cells (HUVECs) into a 3D SUP hydrogel containing human dermal fibroblast neonatal (HDFn) cells to trigger angiogenesis. The SUPs IVFK and IVZK were used to fabricate microgels that gel in a water-in-oil emulsion using a microfluidic droplet generator chip. The fabricated SUP microgels are round structures that are 300–350 μm diameter in size and have ECM-like topography. In addition, they are stable enough to keep their original size and shape under cell culture conditions and long-term storage. When the SUP microgels were used as microcarriers for growing HUVECs and HDFn cells on the microgel surface, cell attachment, stretching, and proliferation could be demonstrated. Finally, we performed an angiogenesis assay in both SUP hydrogels using all SUP combinations between micro- and bulky hydrogels. Endothelial cells were able to migrate from the microgel to the surrounding area, showing angiogenesis features such as sprouting, branching, coalescence, and lumen formation. Although both SUP hydrogels support vascular network formation, IVFK outperformed IVZK in terms of vessel network extension and branching. Overall, these results demonstrated that cell-laden SUP microgels have great potential to be used as a microcarrier cell delivery system, encouraging us to study the angiogenesis process and to develop vascularized tissue-engineering therapies.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.1c03787.

    • Supplementary figures (PDF)

    • SUP droplet generation (AVI)

    • Fluorescent nanoparticles embedded in SUP microgels (AVI)

    • Fluorescent nanoparticles in SUP solution (AVI)

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    Cited By

    This article is cited by 14 publications.

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    2. Xiaochuan Liu, Jinsi Wang, Xiaoqin Xu, Hong Zhu, Kenny Man, Jingying Zhang. SDF-1 Functionalized Hydrogel Microcarriers for Skin Flap Repair. ACS Biomaterials Science & Engineering 2022, 8 (8) , 3576-3588. https://doi.org/10.1021/acsbiomaterials.2c00755
    3. Manzar Abbas, Hepi Hari Susapto, Charlotte A. E. Hauser. Synthesis and Organization of Gold-Peptide Nanoparticles for Catalytic Activities. ACS Omega 2022, 7 (2) , 2082-2090. https://doi.org/10.1021/acsomega.1c05546
    4. Kholoud A. Seferji, Hepi Hari Susapto, Babar K. Khan, Zahid U. Rehman, Manzar Abbas, Abdul-Hamid Emwas, Charlotte A. E. Hauser. Green Synthesis of Silver-Peptide Nanoparticles Generated by the Photoionization Process for Anti-Biofilm Application. ACS Applied Bio Materials 2021, 4 (12) , 8522-8535. https://doi.org/10.1021/acsabm.1c01013
    5. Congsun Li, Jie Wang, Weinan Yang, Kang Yu, Jianqiao Hong, Xiaoxiao Ji, Minjun Yao, Sihao Li, Jinwei Lu, Yazhou Chen, Shigui Yan, Haobo Wu, Chiyuan Ma, Xiaohua Yu, Guangyao Jiang, An Liu. 3D-printed hydrogel particles containing PRP laden with TDSCs promote tendon repair in a rat model of tendinopathy. Journal of Nanobiotechnology 2023, 21 (1) https://doi.org/10.1186/s12951-023-01892-5
    6. Maria Cristina Cringoli, Silvia Marchesan. Cysteine Redox Chemistry in Peptide Self-Assembly to Modulate Hydrogelation. Molecules 2023, 28 (13) , 4970. https://doi.org/10.3390/molecules28134970
    7. Lijun Cai, Ning Li, Yong Zhang, Hongcheng Gu, Yujuan Zhu. Microfluidics-derived microcarrier systems for oral delivery. Biomedical Technology 2023, 1 , 30-38. https://doi.org/10.1016/j.bmt.2022.11.001
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    9. Yang Yang, Lishan Sha, Han Zhao, Zhaojun Guo, Min Wu, Peng Lu. Recent advances in cellulose microgels: Preparations and functionalized applications. Advances in Colloid and Interface Science 2023, 311 , 102815. https://doi.org/10.1016/j.cis.2022.102815
    10. Kai Wang, Zhaoyi Wang, Haijun Hu, Changyou Gao. Supramolecular microgels/microgel scaffolds for tissue repair and regeneration. Supramolecular Materials 2022, 1 , 100006. https://doi.org/10.1016/j.supmat.2021.100006
    11. Haniyeh Najafi, Samira Sadat Abolmaali, Reza Heidari, Hadi Valizadeh, Ali Mohammad Tamaddon, Negar Azarpira. Integrin receptor-binding nanofibrous peptide hydrogel for combined mesenchymal stem cell therapy and nitric oxide delivery in renal ischemia/reperfusion injury. Stem Cell Research & Therapy 2022, 13 (1) https://doi.org/10.1186/s13287-022-03045-1
    12. Sherin Abdelrahman, Walaa F Alsanie, Zainab N Khan, Hamed I Albalawi, Raed I Felimban, Manola Moretti, Nadia Steiner, Adeel G Chaudhary, Charlotte A E Hauser. A Parkinson’s disease model composed of 3D bioprinted dopaminergic neurons within a biomimetic peptide scaffold. Biofabrication 2022, 14 (4) , 044103. https://doi.org/10.1088/1758-5090/ac7eec
    13. Peiyan Wang, Xinyue Meng, Runze Wang, Wei Yang, Lanting Yang, Jianxun Wang, Dong‐An Wang, Changjiang Fan. Biomaterial Scaffolds Made of Chemically Cross‐Linked Gelatin Microsphere Aggregates (C‐GMSs) Promote Vascularized Bone Regeneration. Advanced Healthcare Materials 2022, 11 (13) https://doi.org/10.1002/adhm.202102818
    14. Wafaa T Arab, Hepi H Susapto, Dana Alhattab, Charlotte A E Hauser. Peptide nanogels as a scaffold for fabricating dermal grafts and 3D vascularized skin models. Journal of Tissue Engineering 2022, 13 , 204173142211118. https://doi.org/10.1177/20417314221111868

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