Skip to main content
SpringerLink
Log in

Impact of micro-scale regular topography on cell and tissue behaviors

微米尺度的规则拓扑结构对细胞和组织行为的影响

  • Articles
  • Published:
Science China Materials Aims and scope Submit manuscript

Abstract

Physical cues of a biomaterial surface such as topography have received extensive attention due to their ease of engineering and reproducible bioeffects. Although many studies have been reported, the relationship between the topography of biomaterial surface and cell/tissue behaviors could not be well evaluated due to the diversified topographies and experimental environments used in these studies. Here we designed 11 patterns (triangle, rectangle, circle, etc.), and employed them to fabricate two types of topographies (micropit and microcolumn), resulting in 22 surface topographies. We conducted comparative assessments of the bioeffects of these microtopographies on cell and tissue in vitro and in vivo. Our results revealed that grooves formed by continuous micropits exhibited a greater ability to accelerate cell migration. Among them, grooves composed of triangular micropits exhibited the strongest enhancement of cell migration in vitro, reducing fibrous tissue encapsulation and promoting vascular formation in vivo.

摘要

生物材料表面的物理性质, 如拓扑结构, 由于其易于加工和稳定 的生物作用而受到广泛关注. 虽然已有许多研究报道了材料表面拓扑 结构与细胞的相互作用, 但由于不同研究中使用的微结构和实验环境的多样性, 生物材料表面不同微结构与细胞/组织行为之间的影响关系 尚未得到很好的统一评价. 在本研究中, 我们设计了11种图案(三角 形、矩形、圆形等), 这些图案包含两种类型的形貌(微坑和微柱), 这样 一共得到22种表面拓扑结构. 我们在体外和体内对这些微结构影响细 胞和组织的生物作用进行了评估. 我们的研究结果表明, 由连续微坑形 成的凹槽微结构促进细胞迁移效果相比其他微结构更强. 其中, 由三角 形微坑组成的凹槽在体外对细胞迁移的促进作用最强. 在大鼠皮下模 型中, 这种三角形微坑组成的凹槽结构减少了纤维组织的包封, 促进了 血管的形成.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Jana S. Endothelialization of cardiovascular devices. Acta BioMater, 2019, 99: 53–71

    Article  CAS  PubMed  Google Scholar 

  2. Wang Y, Li G, Yang L, et al. Development of innovative biomaterials and devices for the treatment of cardiovascular diseases. Adv Mater, 2022, 34: 2201971

    Article  CAS  Google Scholar 

  3. Huang Y, Wang J, Yu W, et al. A bioinspired hydrogel-elastomer hybrid surface for enhanced mechanical properties and lubrication. ACS Appl Mater Interfaces, 2021, 13: 50461–50469

    Article  CAS  PubMed  Google Scholar 

  4. Yu Y, Wang J, Wang X, et al. A tough, slippery, and anticoagulant double-network hydrogel coating. ACS Appl Polym Mater, 2022, 4: 5941–5951

    Article  Google Scholar 

  5. Wang X, Wang J, Yu Y, et al. A polyzwitterion-based antifouling and flexible bilayer hydrogel coating. Compos Part B-Eng, 2022, 244: 110164

    Article  CAS  Google Scholar 

  6. Hu M, Li X, Huang WP, et al. Dynamically softened substrate regulates malignancy of breast tumor cells. Sci China Mater, 2021, 64: 2580–2592

    Article  CAS  Google Scholar 

  7. Zhang T, Zhou W, Jia Z, et al. Polydopamine-assisted functionalization of heparin and vancomycin onto microarc-oxidized 3D printed porous Ti6Al4V for improved hemocompatibility, osteogenic and anti-infection potencies. Sci China Mater, 2018, 61: 579–592

    Article  CAS  Google Scholar 

  8. Ai S, Li H, Zheng H, et al. A SupraGel for efficient production of cell spheroids. Sci China Mater, 2022, 65: 1655–1661

    Article  CAS  Google Scholar 

  9. Liu Q, Zheng S, Ye K, et al. Cell migration regulated by RGD nanospacing and enhanced under moderate cell adhesion on biomaterials. Biomaterials, 2020, 263: 120327

    Article  CAS  PubMed  Google Scholar 

  10. Shen Y, Zhang W, Xie Y, et al. Surface modification to enhance cell migration on biomaterials and its combination with 3D structural design of occluders to improve interventional treatment of heart diseases. Biomaterials, 2021, 279: 121208

    Article  CAS  PubMed  Google Scholar 

  11. Jeon HJ, Simon Jr CG, Kim GH. A mini-review: Cell response to microscale, nanoscale, and hierarchical patterning of surface structure. J Biomed Mater Res, 2014, 102: 1580–1594

    Article  Google Scholar 

  12. Harrison RG. The reaction of embryonic cells to solid structures. J Exp Zool, 1914, 17: 521–544

    Article  Google Scholar 

  13. Weiss P. Experiments on cell and axon orientation in vitro: The role of colloidal exudates in tissue organization. J Exp Zool, 1945, 100: 353–386

    Article  CAS  PubMed  Google Scholar 

  14. Chen CS, Mrksich M, Huang S, et al. Geometric control of cell life and death. Science, 1997, 276: 1425–1428

    Article  CAS  PubMed  Google Scholar 

  15. Keren K, Pincus Z, Allen GM, et al. Mechanism of shape determination in motile cells. Nature, 2008, 453: 475–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. He X, Zhang J, Xie L, et al. Phytic acid-promoted rapid fabrication of natural polypeptide coatings for multifunctional applications. Chem Eng J, 2022, 440: 135917

    Article  CAS  Google Scholar 

  17. Wang K, Frey N, Garcia A, et al. Nanotopographical cues tune the therapeutic potential of extracellular vesicles for the treatment of aged skeletal muscle injuries. ACS Nano, 2023, 17: 19640–19651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Shirazi S, Huang CC, Kang M, et al. Evaluation of nanoscale versus hybrid micro/nano surface topographies for endosseous implants. Acta BioMater, 2024, 173: 199–216

    Article  CAS  PubMed  Google Scholar 

  19. Yao X, Ding J. Effects of microstripe geometry on guided cell migration. ACS Appl Mater Interfaces, 2020, 12: 27971–27983

    Article  CAS  PubMed  Google Scholar 

  20. Wang Q, Liu Q, Gao J, et al. Stereo coverage and overall stiffness of biomaterial arrays underly parts of topography effects on cell adhesion. ACS Appl Mater Interfaces, 2023, 15: 6142–6155

    Article  CAS  PubMed  Google Scholar 

  21. Robotti F, Bottan S, Fraschetti F, et al. A micron-scale surface topography design reducing cell adhesion to implanted materials. Sci Rep, 2018, 8: 10887

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lin S, Yuan X, Du X, et al. Surface microtopography construction and osteogenic properties evaluation of bulk polylactic acid implants. Colloids Surfs B-Biointerfaces, 2023, 228: 113418

    Article  CAS  Google Scholar 

  23. Wang X, Agrawal V, Dunton CL, et al. Chromatin reprogramming and bone regeneration in vitro and in vivo via the microtopography-induced constriction of cell nuclei. Nat Biomed Eng, 2023, 7: 1514–1529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhu Y, Liang H, Liu X, et al. Regulation of macrophage polarization through surface topography design to facilitate implant-to-bone osteointegration. Sci Adv, 2021, 7: eabf6654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yang Y, Xu T, Bei HP, et al. Sculpting bio-inspired surface textures: An adhesive Janus periosteum. Adv Funct Mater, 2021, 31: 2104636

    Article  CAS  Google Scholar 

  26. Wang H, Tian J, Jiang Y, et al. A 3D biomimetic optoelectronic scaffold repairs cranial defects. Sci Adv, 2023, 9: eabq7750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yi B, Zhou B, Song Z, et al. Step-wise CAG@PLys@PDA-Cu2+ modification on micropatterned nanofibers for programmed endothelial healing. Bioactive Mater, 2023, 25: 657–676

    Article  CAS  Google Scholar 

  28. Li J, Xiao L, Gao S, et al. Radial sponges facilitate wound healing by promoting cell migration and angiogenesis. Adv Healthcare Mater, 2023, 12: 2202737

    Article  CAS  Google Scholar 

  29. Jeong H, Kim D, Montagne K, et al. Differentiation-inducing effect of osteoclast microgrooves for the purpose of three-dimensional design of regenerated bone. Acta BioMater, 2023, 168: 174–184

    Article  CAS  PubMed  Google Scholar 

  30. Hosoya T. The basic repeating modules of the cerebral cortical circuit. Proc Jpn Acad Ser B, 2019, 95: 303–311

    Article  Google Scholar 

  31. Zhu L, Shao C, Chen H, et al. Hierarchical hydrogels with ordered micro-nano structures for cancer-on-a-chip construction. Research, 2021, 2021: 9845679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Zhang R, Gong Y, Cai Z, et al. A composite membrane with microtopographical morphology to regulate cellular behavior for improved tissue regeneration. Acta BioMater, 2023, 168: 125–143

    Article  CAS  PubMed  Google Scholar 

  33. Zapater V, Martinez-Costa L, Ayala G. Classifying human endothelial cells based on individual granulometric size distributions. Image Vis Comput, 2002, 20: 783–791

    Article  Google Scholar 

  34. Fauser J, Brennan M, Tsygankov D, et al. Chapter seven - Methods for assessment of membrane protrusion dynamics. Curr Top Membr, 2021, 88: 205–234

    Article  CAS  PubMed  Google Scholar 

  35. Bettinger C, Langer R, Borenstein J. Engineering substrate topography at the micro- and nanoscale to control cell function. Angew Chem Int Ed, 2009, 48: 5406–5415

    Article  CAS  Google Scholar 

  36. Driscoll MK, Sun X, Guven C, et al. Cellular contact guidance through dynamic sensing of nanotopography. ACS Nano, 2014, 8: 3546–3555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Nightingale T, Cutler D. The secretion of von Willebrand factor from endothelial cells; an increasingly complicated story. J Thrombosis Haemostasis, 2013, 11: 192–201

    Article  Google Scholar 

  38. Rusu L, Minshall RD. Endothelial cell von Willebrand factor secretion in health and cardiovascular disease. In: Lenasi H (ed). Endothelial dysfunction - Old concepts and new challenges. London: IntechOpen, 2018, Ch. 7

    Google Scholar 

  39. Dondossola E, Holzapfel BM, Alexander S, et al. Examination of the foreign body response to biomaterials by nonlinear intravital microscopy. Nat Biomed Eng, 2016, 1: 0007

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lamalice L, Le Boeuf F, Huot J. Endothelial cell migration during angiogenesis. Circ Res, 2007, 100: 782–794

    Article  CAS  PubMed  Google Scholar 

  41. Yokose S, Klokkevold PR, Takei HH, et al. Effects of surface microtopography of titanium disks on cell proliferation and differentiation of osteoblast-like cells isolated from rat calvariae. Dent Mater J, 2018, 37: 272–277

    Article  CAS  PubMed  Google Scholar 

  42. Le Maout E, Lo Vecchio S, Kumar Korla P, et al. Ratchetaxis in channels: Entry point and local asymmetry set cell directions in confinement. Biophys J, 2020, 119: 1301–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Caballero D, Comelles J, Piel M, et al. Ratchetaxis: Long-range directed cell migration by local cues. Trends Cell Biol, 2015, 25: 815–827

    Article  PubMed  Google Scholar 

  44. Vassey MJ, Figueredo GP, Scurr DJ, et al. Immune modulation by design: Using topography to control human monocyte attachment and macrophage differentiation. Adv Sci, 2020, 7: 1903392

    Article  CAS  Google Scholar 

  45. Zhang L, Cao Z, Bai T, et al. Zwitterionic hydrogels implanted in mice resist the foreign-body reaction. Nat Biotechnol, 2013, 31: 553–556

    Article  CAS  PubMed  Google Scholar 

  46. Doloff JC, Veiseh O, de Mezerville R, et al. The surface topography of silicone breast implants mediates the foreign body response in mice, rabbits and humans. Nat Biomed Eng, 2021, 5: 1115–1130

    Article  CAS  PubMed  Google Scholar 

  47. Han W, Chu Q, Li J, et al. Modulating myofibroblastic differentiation of fibroblasts through actin-MRTF signaling axis by micropatterned surfaces for suppressed implant-induced fibrosis. Research, 2023, 6: 0049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ereifej ES, Smith CS, Meade SM, et al. The neuroinflammatory response to nanopatterning parallel grooves into the surface structure of intracortical microelectrodes. Adv Funct Mater, 2018, 28: 1704420

    Article  Google Scholar 

  49. Choi J, Shin BH, Kim T, et al. Micro-textured silicone-based implant fabrication using electrospun fibers as a sacrificial template to suppress fibrous capsule formation. BioMater Adv, 2022, 135: 112687

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Zhejiang Provincial Natural Science Foundation of China (LD22E030008), National Natural Science Foundation of China (U20A20262), the Medical Health Science and Technology Project of Zhejiang Provincial Health Commission (2022483477), and the Fundamental Research Funds for the Central Universities (226-2023-00074). This work was also supported by Zhejiang University K. P. Chao’s High Technology Development Foundation.

Author information

Authors and Affiliations

  1. Key Laboratory of Cardiovascular Intervention and Regenerative Medicine of Zhejiang Province, Department of Cardiology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, 310016, China

    Xing-wang Wang  (王兴旺), Qian Tang  (唐前), Guo-sheng Fu  (傅国胜), Ke-feng Ren  (任科峰) & Lu Yu  (于路)

  2. MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310058, China

    Xing-wang Wang  (王兴旺), Han-yi Zheng  (郑晗毅), Jing Wang  (汪璟), Ke-feng Ren  (任科峰) & Jian Ji  (计剑)

  3. Department of Surgery, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, 310016, China

    Hong-mei Yu  (余红梅)

  4. Engineering Research Center for Cardiovascular Innovative Devices of Zhejiang Province, Hangzhou, 310016, China

    Qian Tang  (唐前), Ke-feng Ren  (任科峰) & Lu Yu  (于路)

Authors
  1. Xing-wang Wang  (王兴旺)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Han-yi Zheng  (郑晗毅)
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Wang  (汪璟)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong-mei Yu  (余红梅)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qian Tang  (唐前)
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guo-sheng Fu  (傅国胜)
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ke-feng Ren  (任科峰)
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jian Ji  (计剑)
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lu Yu  (于路)
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Author contributions Ren KF, Ji J, and Yu L conceived, designed, and supervised the overall project. Wang XW and Zheng HY designed and performed the experiments. All the authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Ke-feng Ren  (任科峰), Jian Ji  (计剑) or Lu Yu  (于路).

Ethics declarations

Conflict of interest The authors declare that they have no conflict of interest.

Additional information

Supplementary information Experimental details and supporting data are available in the online version of the paper.

Xing-wang Wang is a PhD candidate at Zhejiang University. His research interests are functional coatings on medical device and interaction between cell and surface topography.

Ke-feng Ren is a Full Professor at Zhejiang University. In 2015, he received the National Science Fund of Zhejiang Province for Distinguished Young Scholars. His research interests are biomaterials, medical coatings, biomimetic material surfaces, and drug/gene delivery.

Jian Ji is the Qiushi Chair Professor and the director of the Institute of Biomedical Macromolecules, the Department of Polymer Science and Engineering, Zhejiang University. His main research interest is the data-driven biomaterials research.

Lu Yu is the Professor of Cardiology in Sir Run Run Shaw Hospital, Zhejiang University. He majors in interventional diagnosis and treatment of arrhythmias, especially the catheter ablation and the left atrial appendage occlusion for patients with atrial fibrillation. His current research focuses on the optimized endothelialization of the occlusion devices.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Xw., Zheng, Hy., Wang, J. et al. Impact of micro-scale regular topography on cell and tissue behaviors. Sci. China Mater. (2024). https://doi.org/10.1007/s40843-024-2917-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s40843-024-2917-7

Keywords

Search

Navigation