Cited by 83D Printing in Biomedical ResearchSilk-based biomaterials and applicationsTissue Engineering and Regenerative Medicine

Cell-laden constructs with anisotropic pores fabricated by collagen/silk-fibroin for muscle tissue regeneration

Open access
Koo, YoungWon, Kim, WonJin, Hwangbo, Hanjun, Ryu, Dongryeol, Kim, GeunHyung·2026·Advanced Functional Materials

Abstract

Advancements in bioprinting technology, driven by innovations in bioink formulations, have made it possible to create tissue‐engineered constructs that closely replicate the intricate structures of native tissues. Despite the development of numerous cell‐laden bioinks, three critical challenges remain: (1) achieving adequate porosity, (2) mimicking the anisotropic morphology of native tissues, and (3) maintaining mechanical properties sufficient for structural integrity. Although previous studies using collagen‐based foam bioinks have addressed the issue of porosity, the enhancement of mechanical properties and anisotropic physical structure remains limited. In this study, silk fibroin (S‐F) is integrated with collagen to form an interpenetrating polymer network with improved mechanical strength. In addition, a stretching technique is applied to generate anisotropic morphological features, producing biocomposites with enhanced mechanical and structural properties suitable for muscle tissue regeneration. The resulting cell‐laden constructs demonstrated significantly improved cellular activities, including myogenic differentiation, which are attributed to their anisotropic oval shapes, aligned collagen fibrils, and mechanical stimulation. These properties are assessed using in vitro and in vivo experiments. The findings suggest that anisotropically porous collagen/S‐F constructs offer a versatile platform for anisotropic tissue regeneration, effectively bridging the gap between physical structure and biological function in tissue engineering.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1002/adfm.202503933

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Methacrylation of collagen (ColMA) is an effective strategy to address collagen's drawbacks by introducing photocrosslinkable methacrylate groups, enabling rapid photopolymerization and improving structural stability while preserving the inherent bioactivity of collagen.

    “Methacrylation of collagen (ColMA) has emerged as an effective strategy to address these drawbacks by introducing photocrosslinkable methacrylate groups, enabling rapid photopolymerization and improving structural stability while preserving the inherent bioactivity of collagen [12,13,14].”

    From Montmorillonite-reinforced methacrylated collagen/methacrylated silk fibroin hydrogel-based inks: rheological and physicochemical characterization for bone scaffold applications (2026) · cites this paper as [12]

    The Results and Discussion section describes collagen’s biocompatibility and low mechanical strength, supporting the background about its benefits and drawbacks. It addresses those drawbacks by adding silk fibroin, not by methacrylating collagen; the fabrication section uses genipin crosslinking. Our copy does not support the claims about ColMA, rapid photopolymerization, or preservation of bioactivity through methacrylation. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 78 · Cited by 8

Research works printed but not linked: 80

  1. N. Ashammakhi, S. Ahadian, C. Xu, H. Montazerian, H. Ko, R. Nasiri, N. Barros, A. Khademhosseini, Mater. Today Bio 2019, 1, 100008;
  2. W. Aljohani, M. W. Ullah, X. Zhang, G. Yang, Int. J. Biol. Macromol. 2018, 107, 261;
  3. I. T. Ozbolat, Trends Biotechnol. 2015, 33, 395.
  4. M. Mirzaei, O. V. Okoro, L. Nie, D. F. S. Petri, A. Shavandi, Bioeng. 2021, 8, 48;
  5. N. Davari, N. Bakhtiary, M. Khajehmohammadi, S. Sarkari, H. Tolabi, F. Ghorbani, B. Ghalandari, Polymers 2022, 14, 986.
  6. Y. Koo, E.-J. Choi, J. Lee, H.-J. Kim, G. Kim, S. H. Do, J. Ind. Eng. Chem. 2018, 66, 343.
  7. X. Cui, J. Li, Y. Hartanto, M. Durham, J. Tang, H.u Zhang, G. Hooper, K. Lim, T. Woodfield, Adv. Healthcare Mater. 2020, 9, 1901648;
  8. J. Yang, H. He, D. Li, Q. Zhang, L. Xu, C. Ruan, Bio-Des. Manuf. 2023, 6, 586.
  9. J. M. Lee, S. K. Q. Suen, W. L. Ng, W. C. Ma, W. Y. Yeong, Macro- mol. Biosci. 2021, 21, 2000280;
  10. E. O. Osidak, V. I. Kozhukhov, M. S. Osidak, S. P. Domogatsky, Int. J. Bioprint. 2020, 6, 270;
  11. J. Stepanovska, M. Supova, K. Hanzalek, A. Broz, R. Matejka, Biomedicines 2021, 9, 1137;
  12. C. Marques, G. Diogo, S. Pina, J. M. Oliveira, T. Silva, R. Reis, J. Mater. Sci.: Mater. Med. 2019, 30, 1;
  13. W. W. Chan, D. C. L. Yeo, V. Tan, S. Singh, D. Choudhury, M. W. Naing, Bioengineering 2020, 7, 66.
  14. S. Lee, W. Kim, G. Kim, Biomacromolecules 2023, 24, 5219;
  15. H. Hwangbo, S. Chae, D. Ryu, G. Kim, Bioact. Mater. 2025, 45, 417;
  16. M. Samandari, J. Quint, A. Rodríguez- delaRosa, I. Sinha, O. Pourquié, A. Tamayol, Adv. Mater. 2022, 34, 2105883.
  17. S. Sabetkish, P. Currie, L. Meagher, Acta Biomater. 2024, 181, 46.
  18. Y. Koo, G. H. Kim, Bioeng. Transl. Med. 2022, 7, 10330;
  19. Y. Koo, H. Lee, C. S. Lim, S. Y. Kwon, I. Han, G. H. Kim, Int. J. Biol. Macromol. 2022, 222, 1264.
  20. X. H. Tan, L. Liu, A. Mitryashkin, Y. Wang, J. C. H. Goh, ACS Bio- mater. Sci. Eng. 2022, 8, 3242;
  21. B. B. Mandal, A. Grinberg, E. Seok Gil, B. Panilaitis, D. L. Kaplan, Proc. Natl. Acad. Sci. USA 2012, 109, 7699;
  22. Y.u Qi, H. Wang, K. Wei, Y.a Yang, R.u-Y. Zheng, I. Kim, K.e-Q. Zhang, Int. J. Mol. Sci. 2017, 18, 237;
  23. Z. Yin, F. Wu, T. Xing, V. K. Yadavalli, S. C. Kundu, S. Lu, RSC Adv. 2017, 7, 24085;
  24. W. Zhang, Y.u Li, D. Jiang, S. Xie, M. Zeng, J. Chen, L. Chen, H. Ouyang, X. Zou, ACS Biomater. Sci. Eng. 2017, 4, 2067;
  25. V. A. Deshpande, A. Kore, B. Kandasubramanian, Eur. Polym. J. 2023, 196, 112255.
  26. V. Chaturvedi, D. Naskar, B. F. Kinnear, E. Grenik, D. E. Dye, M. D. Grounds, S. C. Kundu, D. R. Coombe, J. Tissue Eng. Regener. Med. 2017, 11, 3178.
  27. M. Kamaraj, N. Moghimi, J. Chen, R. Morales, S. Chen, A. Khademhosseini, J. V. John, Trends Biotechnol. 2024, 42, 631.
  28. G. H. Yang, W. Kim, J. Kim, G. Kim, Theranostics 2021, 11, 48;
  29. A. Pardo, S. M. Bakht, M. Gomez-Florit, R. Rial, R. F. Monteiro, S. P. B. Teixeira, P. Taboada, R. L. Reis, R. M. A. Domingues, M. E. Gomes, Adv. Funct. Mater. 2022, 32, 2208940;
  30. W. Kim, H. Lee, C. K. Lee, J. W. Kyung, S. B. An, I.n-B.o Han, G. H. Kim, Adv. Funct. Mater. 2021, 31, 2105170.
  31. H. Hwangbo, H. Lee, E.-J. Jin, J. Y. Lee, Y. Jo, D. Ryu, G. H. Kim, Bioact. Mater. 2022, 8, 57.
  32. W. Kim, G. Kim, Appl. Mater. Today 2020, 19, 100588;
  33. W. Kim, G. Kim, Chem. Eng. J. 2019, 366, 150;
  34. W. Kim, C. H. Jang, G. H. Kim, Nano Lett. 2019, 19, 8612;
  35. L. Frese, P. E. Dijkman, S. P. Hoerstrup, Transfus. Med. Hemother. 2016, 43, 268.
  36. W. Kim, H. Hwangbo, G. Heo, D. Ryu, G. Kim, Adv. Funct. Mater. 2025, 35, 2406591;
  37. A. Augello, C. De Bari, Hum. Gene Ther. 2010, 21, 1226.
  38. G. Huang, F. Li, X. Zhao, Y. Ma, Y. Li, M. Lin, G. Jin, T. J. Lu, G. M. Genin, F. Xu, Chem. Rev. 2017, 117, 12764.
  39. R. Wu, Y. Li, M. Shen, X. Yang, L. Zhang, X. Ke, G. Yang, C. Gao, Z. Gou, S. Xu, Bioact. Mater. 2021, 6, 1242;
  40. H. Tetik, Y. Wang, X. Sun, D. Cao, N. Shah, H. Zhu, F. Qian, D. Lin, Adv. Funct. Mater. 2021, 31, 2103410.
  41. W. Friess, Eur. J. Pharm. Biopharm. 1998, 45, 113;
  42. C. H. Lee, A. Singla, Y. Lee, Int. J. Pharm. 2001, 221, 1.
  43. K. Lin, D. Zhang, M. H. Macedo, W. Cui, B. Sarmento, G. Shen, Adv. Funct. Mater. 2019, 29, 1804943.
  44. J. O. Buitrago, K. D. Patel, A. El-Fiqi, J.-H. Lee, B. Kundu, H.-H. Lee, H.-W. Kim, Acta Biomater. 2018, 69, 218.
  45. M. Farokhi, M. Aleemardani, A. Solouk, H. Mirzadeh, A. H. Teuschl, H. Redl, Biomed. Mater. 2021, 16, 022004.
  46. K. Bischof, S. Stafilidis, L. Bundschuh, S. Oesser, A. Baca, D. König, Front. Nutr. 2024, 11, 1384112;
  47. J. Park, M. Kim, H. Shin, H. Ahn, Y. K. Park, Clin. Nutr. Res. 2023, 12, 245;
  48. M. S. Zafar, K. H. Al- Samadani, J. Taibah Univ. Med. Soc. 2014, 9, 171;
  49. E. Sashina, A. Y. Golubikhin, A. Susanin, Fibre Chem. 2015, 47, 253;
  50. S.-G. Do, J.- H. Park, H. Nam, J.-B. Kim, J.-Y. Lee, Y.-S. Oh, J.-G. Suh, J. Vet. Sci. 2012, 13, 339.
  51. W. Xiao, J. He, J. W. Nichol, L. Wang, C. B. Hutson, B. Wang, Y. Du, H. Fan, A. Khademhosseini, Acta Biomater. 2011, 7, 2384;
  52. K. Ziv, H. Nuhn, Y. Ben-Haim, L. S. Sasportas, P. J. Kempen, T. P. Niedringhaus, M. Hrynyk, R. Sinclair, A. E. Barron, S. S. Gambhir, Biomaterials 2014, 35, 3736;
  53. X. Hu, K. Shmelev, L. Sun, E.-S. Gil, S.-H. Park, P. Cebe, D. L. Kaplan, Biomacromolecules 2011, 12, 1686.
  54. N. Paxton, W. Smolan, T. Böck, F. Melchels, J. Groll, T. Jungst, Bio- fabrication 2017, 9, 044107;
  55. S. C. Lee, G. Gillispie, P. Prim, S. J. Lee, Chem. Rev. 2020, 120, 10834.
  56. X. Wan, Z. Liu, L. Li, Adv. Funct. Mater. 2021, 31, 2010626;
  57. X. Wang, N. Rivera-Bolanos, B. Jiang, G. A. Ameer, Adv. Funct. Mater. 2019, 29, 1809009;
  58. A. S. Vaziri, E. Vasheghani-Farahani, S. Hosseinzadeh, F. Bagheri, M. Büchner, D. W. Schubert, A. R. Boccaccini, Biomacromolecules 2024, 25, 2323.
  59. Y. B. Kim, H. Lee, G. H. Kim, ACS Appl. Mater. Interfaces 2016, 8, 32230.
  60. S. Jana, S. K. L. Levengood, M. Zhang, Adv. Mater. 2016, 28, 10588.
  61. S. Choi, J. Kim, J. Mat. Chem. B 2015, 3, 1479;
  62. D. R. King, R. Takahashi, T. Ikai, K. Fukao, T. Kurokawa, J. P. Gong, ACS Appl. Polym. Mater. 2020, 2, 2350;
  63. S. Choi, Y. Choi, J. Kim, Adv. Funct. Mater. 2019, 29, 1904342;
  64. P. M. Gilbert, K. L. Havenstrite, K. E. G. Magnusson, A. Sacco, N. A. Leonardi, P. Kraft, N. K. Nguyen, S. Thrun, M. P. Lutolf, H. M. Blau, Science 2010, 329, 1078;
  65. A. J. Engler, M. A. Griffin, S. Sen, C. G. Bönnemann, H. L. Sweeney, D. E. Discher, J. Cell Biol. 2004, 166, 877.
  66. X.-Z. Fang, T. Zhou, J.i-Q. Xu, Y.a-X. Wang, M.-M. Sun, Y.a-J. He, S.-W. Pan, W. Xiong, Z.-K. Peng, X.-H. Gao, Y. Shang, Cell Biosci. 2021, 11, 13.
  67. P. Atherton, B. Stutchbury, D. Jethwa, C. Ballestrem, Exp. Cell Res. 2016, 343, 21.
  68. S. Dupont, L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, N. Elvassore, S. Piccolo, Nature 2011, 474, 179;
  69. D. E. Jaalouk, J. Lammerding, Nat. Rev. Mol. Cell Biol. 2009, 10, 63;
  70. L. A. Olsen, J. X. Nicoll, A. C. Fry, Eur. J. Appl. Physiol. 2019, 119, 333.
  71. F. Sachs, Physiology 2010, 25, 50;
  72. R. G. O 'Neil, S. Heller, Pflügers Archiv 2005, 451, 193;
  73. B. C. Coutiño, R. Mayor, Cells Dev. 2021, 168, 203730.
  74. F. Martino, A. R. Perestrelo, V. Vinarský, S. Pagliari, G. Forte, Front. Physiol. 2018, 9, 824.
  75. H. Hwangbo, H. Lee, E.-J. Jin, Y. Jo, J. Son, H. M. Woo, D. Ryu, G. H. Kim, Adv. Funct. Mater. 2023, 33, 2209157;
  76. J. Gilbert-Honick, W. Grayson, Adv. Healthcare Mater. 2020, 9, 1900626.
  77. S. H. Kim, H. Hong, O. Ajiteru, M. D. T. Sultan, Y. J. Lee, J. S. Lee, O. J. Lee, H. Lee, H. S. Park, K. Y. Choi, J. S. Lee, H. W. Ju, I.-S. Hong, C. H. Park, Nat. Protoc. 2021, 16, 5484.
  78. J. Kim, H. Lee, G. Lee, D. Ryu, G. Kim, Bioact. Mater. 2024, 36, 14.
  79. S. Jo, J. Lee, H. Lee, D. Ryu, G. Kim, npj Regener. Med. 2023, 8, 30;
  80. J. Lee, H. Lee, E.-J. Jin, D. Ryu, G. H. Kim, npj Regener. Med. 2023, 8, 18.

Authors
Koo, Y., Kim, W., Hwangbo, H., Ryu, D., & Kim, G.
Affiliations
  • Sungkyunkwan University (KR)
  • Department of Precision Medicine Sungkyunkwan University School of Medicine (SKKU‐SOM) Suwon 16419 Republic of Korea
  • Gwangju Institute of Science and Technology (KR)
Corresponding author
  • Ryu, Dongryeol
  • Kim, GeunHyung
Venue
Advanced Functional Materials
Publisher
Wiley
Published
2025-07-10
Volume
36
Issue
2
ISSN
  • 1616-301X (ISSN-L)
  • 1616-3028
OpenAlex
W4412187276
Cited by
8
References
78
Citations by year
2026: 6 · 2025: 2
FWCI
1.96
Type
journal article
Language
en
Open access
Locations
Advanced Functional Materials (publishedVersion)
Funders
  • National Research Foundation
  • National Research Foundation of Korea
  • Ministry of Science and ICT, South Korea
  • Korea National Institute of Health (2022ER130500)
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
  • Physical Sciences › Materials Science › Biomaterials › Silk-based biomaterials and applications
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
Keywords
muscle regeneration, interpenetrating polymer networks, mechanical properties, myogenesis, cell-laden constructs, collagen fibril alignment, mechanical stimulation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review