CoChat
Sign Up
Cited by 463D Printing in Biomedical ResearchTissue Engineering and Regenerative MedicineElectrospun Nanofibers in Biomedical Applications

Vascularized 3D Human Skin Models in the Forefront of Dermatological Research

Open access
Rimal, Rahul, Muduli, Saradaprasan, Desai, Prachi, Marquez, Andrea Bonnin, Möller, Martin, Platzman, Ilia, Spatz, Joachim, Singh, Smriti·2024·Advanced Healthcare Materials
DOI 10.1002/adhm.202303351PMC PMC11468127
Open this paper in CoChat — free accountOpen PDF

Abstract

In vitro engineered skin models are emerging as an alternative platform to reduce and replace animal testing in dermatological research. Despite the progress made in recent years, considerable challenges still exist for the inclusion of diverse cell types within skin models. Blood vessels, in particular, are essential in maintaining tissue homeostasis and are one of many primary contributors to skin disease inception and progression. Substantial efforts in the past have allowed the successful fabrication of vascularized skin models that are currently utilized for disease modeling and drugs/cosmetics testing. This review first discusses the need for vascularization within tissue‐engineered skin models, highlighting their role in skin grafting and disease pathophysiology. Second, the review spotlights the milestones and recent progress in the fabrication and utilization of vascularized skin models. Additionally, advances including the use of bioreactors, organ‐on‐a‐chip devices, and organoid systems are briefly explored. Finally, the challenges and future outlook for vascularized skin models are addressed.

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/adhm.202303351

Cites

163 of 163 references verified0 citation errors · 0 not checkable

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?

  • There has been a complete absence of an endogenously differentiating vascularized, hair-bearing human skin equivalent that contains immune cell populations.

    “While many attempts to generate complex 3D skin equivalents have achieved vascularization, hair follicle generation, and immune cell co‐cultures, there has been a complete absence of endogenously differentiating a vascularized, hair‐bearing human skin equivalent that contains immune cell populations.[ 21 , 22 , 23 , 24 , 25 , 26 , 27 ]”

    From Coordinated Development of Immune Cell Populations in Vascularized Skin Organoids from Human Induced Pluripotent Stem Cells (2025) · cites this paper as [23]

    The Skin Organoids section describes hair-bearing models derived from human iPSCs but identifies vascularization and immune competence as challenges. Challenges and Outlook also notes a lack of immune cells and blood vessels in skin organoids, while Resemblance with Native Human Skin says a complete functional model is lacking. These passages support the combination as an unmet challenge, but do not establish the categorical claim that no endogenously differentiating model with all three features exists. (LLM, conf=0.82)

    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.

Cites

Flagged first, then by citations

1 of the 164 references couldn’t be matched to a known paper.

Research works printed but not linked: 158

  1. [1]R. L. Giesey, S. Mehrmal, P. Uppal, G. Delost, SKIN J. Cutan. Med. 2021, 5, 125.
  2. [2]L. M. Hollestein, T. Nijsten, J. Invest. Dermatol. 2014, 134, 1499. 24825057
  3. [3]H. W. Lim, S. A. Collins, J. S. Resneck Jr, J. L. Bolognia, J. A. Hodge, T. A. Rohrer, M. J. Van Beek, D. J. Margolis, A. J. Sober, M. A. Weinstock, J. Am. Acad. Dermatol. 2017, 76, 958. 28259441
  4. [4]A. M. Wojtowicz, S. Oliveira, M. W. Carlson, A. Zawadzka, C. F. Rousseau, D. Baksh, Wound Repair Regener. 2014, 22, 246. PMC4211362 24635175
  5. [5]M. Jevtić, A. Loewa, A. Nováčková, A. Kováčik, S. Kaessmeyer, G. Erdmann, K. Vávrová, S. Hedtrich, Biochim. Biophys. Acta 2020, 1867, 118722. 32302667
  6. [6]R. K. Jain, P. Au, J. Tam, D. G. Duda, D. Fukumura, Nat. Biotechnol. 2005, 23, 821. 16003365
  7. [7]C. Jensen, Y. Teng, Front. Mol. Biosci. 2020, 7, 33. 32211418 PMC7067892
  8. [8]M. Kapałczyńska, T. Kolenda, W. Przybyła, M. Zajączkowska, A. Teresiak, V. Filas, M. Ibbs, R. Bliźniak, Ł. Łuczewski, K. Lamperska, Arch. Med. Sci. 2018, 14, 910. 30002710 PMC6040128
  9. [9]T. Gura, Science 1997, 278, 1041. 9381203
  10. [10]S. Gallagher, U. Kruger, K. Josyula, A. Gong, A. Song, R. Sweet, B. Makled, C. Parsey, J. Norfleet, S. De, Sci. Rep. 2022, 12, 4565. 35296755 PMC8927453
  11. [11]C. Choe, J. Schleusener, J. Lademann, M. E. Darvin, J. Biophotonics 2018, 11, 201700355. 29460347
  12. [12]A. C. Sintov, Eur. J. Pharm. Sci. 2017, 102, 261. 28323119
  13. [13]P. A. Gerber, B. A. Buhren, H. Schrumpf, B. Homey, A. Zlotnik, P. Hevezi, Biol. Chem. 2014, 395, 577. 24497224
  14. [14]M. I. Koster, Ann. N. Y. Acad. Sci. 2009, 1170, 7. 19686098 PMC2861991
  15. [15]H. D. Zomer, A. G. Trentin, J. Dermatol. Sci. 2018, 90, 3. 29289417
  16. [16]D. A. Ewald, S. Noda, M. Oliva, T. Litman, S. Nakajima, X. Li, H. Xu, C. T. Workman, P. Scheipers, N. Svitacheva, J. Allergy Clin. Immunol. 2017, 139, 562. 27702671
  17. [17]W. R. Swindell, A. Johnston, S. Carbajal, G. Han, C. Wohn, J. Lu, X. Xing, R. P. Nair, J. J. Voorhees, J. T. Elder, PLoS One 2011, 6, e18266. 21483750 PMC3070727
  18. [18]J. R. Yu, J. Navarro, J. C. Coburn, B. Mahadik, J. Molnar, J. H. Holmes IV, A. J. Nam, J. P. Fisher, Adv. Healthcare Mater. 2019, 8, 1801471. PMC10290827 30707508
  19. [19]E. Fuchs, S. Raghavan, Nat. Rev. Genet. 2002, 3, 199. 11972157
  20. [20]E. Proksch, J. M. Brandner, J. M. Jensen, Exp. Dermatol. 2008, 17, 1063. 19043850
  21. [21]V. T. Natarajan, P. Ganju, A. Ramkumar, R. Grover, R. S. Gokhale, Nat. Chem. Biol. 2014, 10, 542. 24937072
  22. [22]C. L. Simpson, D. M. Patel, K. J. Green, Nat. Rev. Mol. Cell Biol. 2011, 12, 565. 21860392 PMC3280198
  23. [23]R. Wong, S. Geyer, W. Weninger, J. C. Guimberteau, J. K. Wong, Exp. Dermatol. 2016, 25, 92. 26284579
  24. [24]K. Vig, A. Chaudhari, S. Tripathi, S. Dixit, R. Sahu, S. Pillai, V. A. Dennis, S. R. Singh, Int. J. Mol. Sci. 2017, 18, 789. 28387714 PMC5412373
  25. [25]Y. E. Yun, Y. J. Jung, Y. J. Choi, J. S. Choi, Y. W. Cho, J. Pharm. Investig. 2018, 48, 215.
  26. [26]A. N. Dehkordi, F. M. Babaheydari, M. Chehelgerdi, S. R. Dehkordi, Stem Cell Res. Ther. 2019, 10, 111. 30922387 PMC6440165
  27. [27]M. J. Randall, A. Jüngel, M. Rimann, K. Wuertz‐Kozak, Front. Bioeng. Biotechnol. 2018, 6, 154. 30430109 PMC6220074
  28. [29]I. M. Braverman, J. Investig. Dermatol. Sympos. Proc. 2000, 5, 3. 11147672
  29. [30]I. M. Braverman, A. Yen, J. Invest. Dermatol. 1977, 68, 44. 830769
  30. [31]E. M. Landis, J. Invest. Dermatol. 1938, 1, 295.
  31. [32]R. A. Swerlick, J. Dermatol. 1997, 24, 734. 9433032
  32. [33]J. G. Rheinwald, Int. Rev. Cytol. 1979, 10, 25. 391745
  33. [34]J. G. Rheinwald, H. Green, Cell 1975, 6, 317. 1052770
  34. [35]G. J. Todaro, H. Green, J. Cell Biol. 1963, 17, 299. 13985244 PMC2106200
  35. [36]J. G. Rheinwatd, H. Green, Cell 1975, 6, 331. 1052771
  36. [37]H. Green, Cell 1977, 11, 405. 302145
  37. [38]H. Green, O. Kehinde, J. Thomas, Proc. Natl. Acad. Sci. USA 1979, 76, 5665. 293669 PMC411710
  38. [39]T. J. Phillips, O. Kehinde, H. Green, B. A. Gilchrest, J. Am. Acad. Dermatol. 1989, 21, 191. 2768568
  39. [40]M. Koga, Arch. Dermatol. 1988, 124, 1656. 3178247
  40. [41]H. Mizutani, Y. Shirakata, A. Adachi, K. Hashimoto, M. Shimizu, Lancet 1998, 352, 709. 9728996
  41. [42]C. Cuono, R. Langdon, J. McGuire, Lancet 1986, 327, 1123. 2422513
  42. [43]E. Bell, H. P. Ehrlich, D. J. Buttle, T. Nakatsuji, Science 1981, 211, 1052. 7008197
  43. [44]E. Bell, N. Parenteau, R. Gay, C. Nolte, P. Kemp, P. Bilbo, B. Ekstein, E. Johnson, Toxicol. In Vitro 1991, 5, 591. 20732083
  44. [45]N. Richarz, A. Boada, J. Carrascosa, Actas Dermosifiliogr. 2017, 108, 515. 28162227
  45. [46]L. Chen, H. Deng, H. Cui, J. Fang, Z. Zuo, J. Deng, Y. Li, X. Wang, L. Zhao, OncoTargets Ther. 2018, 9, 7204. PMC5805548 29467962
  46. [47]P. Libby, Nutr. Rev. 2007, 65, 140. 18240538
  47. [48]W.‐H. Boehncke, M. P. Schön, Lancet 2015, 386, 983. 26025581
  48. [49]R. Heidenreich, M. Röcken, K. Ghoreschi, Int. J. Exp. Pathol. 2009, 90, 232. 19563608 PMC2697548
  49. [50]P. Telner, Z. Fekete, J. Invest. Dermatol. 1961, 36, 225. 13775806
  50. [51]R. Huggenberger, M. Detmar, J. Investig. Dermatol. Sympos. Proc. 2011, 15, 24. PMC3398151 22076324
  51. [52]L. Sankar, D. Arumugam, S. Boj, P. Pradeep, J. Clin. Diagn. Res. 2017, 11, EC23. 28511390 PMC5427316
  52. [53]A. L. Bressan, B. L. Picciani, L. Azulay‐Abulafia, A. K. Fausto‐Silva, P. N. Almeida, K. S. Cunha, E. P. Dias, S. Carneiro, Int. J. Dermatol. 2018, 57, 209. 29318579
  53. [54]S.‐C. Liew, E. Das‐Gupta, S. Chakravarthi, S.‐F. Wong, N. Lee, N. Safdar, A. Jamil, BMC Res. Notes 2012, 5, 201. 22537619 PMC3392727
  54. [55]S. Hanssen, C. van der Vleuten, P. van Erp, M. Seyger, P. van de Kerkhof, J. Dermatolog. Treat. 2019, 30, 221. 30074865
  55. [56]H. J. Lee, Y. J. Hong, M. Kim, Int. J. Mol. Sci. 2021, 22, 12035. 34769465 PMC8584589
  56. [57]Y. Zhang, H. Matsuo, E. Morita, Arch. Dermatol. Res. 2006, 297, 425. 16456664
  57. [59]R. Agha‐Majzoub, R. P. Becker, D. E. Schraufnagel, L. S. Chan, Microcirculation 2005, 12, 455. 16147464
  58. [60]Q. Peng, K. Sha, Y. Liu, M. Chen, S. Xu, H. Xie, Z. Deng, J. Li, Front. Cell Dev. Biol. 2021, 9, 722904. 34993194 PMC8724421
  59. [61]K. Yamasaki, R. L. Gallo, J. Dermatol. Sci. 2009, 55, 77. 19481425 PMC2745268
  60. [62]A. H. Gomaa, M. Yaar, M. M. Eyada, J. Bhawan, J. Cutan. Pathol. 2007, 34, 748. 17880579
  61. [63]K. Aroni, E. Tsagroni, N. Kavantzas, E. Patsouris, E. Ioannidis, Arch. Dermatol. Res. 2008, 300, 125. 18071725
  62. [64]L. F. Brown, T. J. Harrist, K.‐T. Yeo, M. Ståhle‐Bäckdahl, R. W. Jackman, B. Berse, K. Tognazzi, H. F. Dvorak, M. Detmar, J. Invest. Dermatol. 1995, 104, 744. 7738351
  63. [65]V. Martins, M. Caley, K. Moore, Z. Szentpetery, S. Marsh, D. Murrell, M. Kim, M. Avari, J. McGrath, R. Cerio, JNCI 2016, 108, djv293. 26476432
  64. [66]M. Carleton, M. Zhou, O. De Henau, P. Phillips, T. Chen, Y. Feng, S.‐P. Huang, A. Walsh, T. P. Reilly, I. Melero Bermejo, Am. Soc. Clin. Oncol. 2018, 36, 3025.
  65. [67]M. Kashani‐Sabet, R. W. Sagebiel, C. M. Ferreira, M. Nosrati, J. R. Miller, III, Arch. Dermatol. 2001, 137, 1169. 11559212
  66. [68]J. Welzel, S. Schuh, N. De Carvalho, L. Themstrup, M. Ulrich, G. Jemec, J. Holmes, G. Pellacani, J. Eur. Acad. Dermatol. Venereol. 2021, 35, 1087. 33300200
  67. [69]B. J. Nickoloff, R. S. Mitra, J. Varani, V. M. Dixit, P. J. Polverini, Am. J. Pathol. 1994, 144, 820. 7512793 PMC1887235
  68. [70]M. Bhushan, B. McLaughlin, J. Weiss, C. Griffiths, Br. J. Dermatol. 1999, 141, 1054. 10606852
  69. [71]J. Creamer, J. Barker, Clin. Exp. Dermatol. 1995, 20, 6. 8857336
  70. [72]P. H. Prose, E. Sedlis, J. Invest. Dermatol. 1960, 34, 149. 14435075
  71. [73]V. D. Schwab, M. Sulk, S. Seeliger, P. Nowak, J. Aubert, C. Mess, M. Rivier, I. Carlavan, P. Rossio, D. Metze, J. Investig. Dermatol. Sympos. Proc. 2011, 15, 53. PMC3704331 22076328
  72. [74]W. C. Cho, G. Jour, P. P. Aung, in Seminars in Cancer Biology, Vol. 59, Elsevier, Amsterdam, 2019.
  73. [75]A. Smith, T. Watkins, G. Theocharidis, I. Lang, M. Leschinsky, A. Maione, O. Kashpur, T. Raimondo, S. Rahmani, J. Baskin, Tissue Eng., Part C 2021, 27, 49. PMC8349718 33280487
  74. [76]A. Abedin‐Do, Z. Zhang, Y. Douville, M. Méthot, J. Bernatchez, M. Rouabhia, Front. Bioeng. Biotechnol. 2022, 10, 989888. 36246377 PMC9561872
  75. [77]C. Y. Ozdogan, H. Kenar, K. E. Davun, D. Yucel, E. Doger, S. Alagoz, Biomed. Mater. 2020, 16, 015027. 33331294
  76. [78]B. S. Kim, M. Ahn, W.‐W. Cho, G. Gao, J. Jang, D.‐W. Cho, Biomaterials 2021, 272, 120776. 33798956
  77. [79]T. Markham, R. Mullan, L. Golden‐Mason, S. Rogers, B. Bresnihan, O. FitzGerald, U. Fearon, D. J. Veale, J. Am. Acad. Dermatol. 2006, 54, 1003. 16713454
  78. [80]D. N. Sauder, J. DeKoven, P. Champagne, D. Croteau, É. Dupontb, J. Am. Acad. Dermatol. 2002, 47, 535. 12271297
  79. [81]H. Shahin, M. Elmasry, I. Steinvall, F. Söberg, A. El‐Serafi, Int. J. Burns Trauma 2020, 8, tkaa022. PMC7396265 32766342
  80. [82]S. Dixit, D. R. Baganizi, R. Sahu, E. Dosunmu, A. Chaudhari, K. Vig, S. R. Pillai, S. R. Singh, V. A. Dennis, J. Biol. Eng. 2017, 11, 49. 29255480 PMC5729423
  81. [83]Q. H. Phua, H. A. Han, B.‐S. Soh, J. Transl. Med. 2021, 19, 83. 33602284 PMC7891016
  82. [84]C. K. Griffith, C. Miller, R. C. Sainson, J. W. Calvert, N. L. Jeon, C. C. Hughes, S. C. George, Tissue Eng. 2005, 11, 257. 15738680
  83. [85]D. M. Young, K. M. Greulich, H. G. Weier, J. Burn Care Rehabil. 1996, 17, 305. 8844350
  84. [86]D. Ausprunk, D. Knighton, J. Folkman, Am. J. Pathol. 1975, 79, 597. 1094838 PMC1913018
  85. [87]L. Chen, Q. Xing, Q. Zhai, M. Tahtinen, F. Zhou, L. Chen, Y. Xu, S. Qi, F. Zhao, Theranostics 2017, 7, 117. 28042321 PMC5196890
  86. [88]H. E. Abaci, Z. Guo, A. Coffman, B. Gillette, W. h. Lee, S. K. Sia, A. M. Christiano, Adv. Healthcare Mater. 2016, 5, 1800. PMC5031081 27333469
  87. [89]T. Baltazar, J. Merola, C. Catarino, C. B. Xie, N. C. Kirkiles‐Smith, V. Lee, S. Hotta, G. Dai, X. Xu, F. C. Ferreira, Tissue Eng., Part A 2020, 26, 227. 31672103 PMC7476394
  88. [90]A. S. Klar, S. Güven, T. Biedermann, J. Luginbühl, S. Böttcher‐Haberzeth, C. Meuli‐Simmen, M. Meuli, I. Martin, A. Scherberich, E. Reichmann, Biomaterials 2014, 35, 5065. 24680190
  89. [91]H. Miyazaki, Y. Tsunoi, T. Akagi, S. Sato, M. Akashi, D. Saitoh, Sci. Rep. 2019, 9, 1. 31127144 PMC6534548
  90. [92]M. I. Echeverria Molina, K. G. Malollari, K. Komvopoulos, Front. Bioeng. Biotechnol. 2021, 9, 617141. 34195178 PMC8236583
  91. [93]B. Kinikoglu, Altern. Lab. Anim. 2017, 45, 309. 29313702
  92. [94]A. F. Black, F. Berthod, N. L'Heureux, L. Germain, F. A. Auger, FASEB J. 1998, 12, 1331. 9761776
  93. [95]V. Hudon, F. Berthod, A. F. Black, O. Damour, L. Germain, F. A. Auger, Br. J. Dermatol. 2003, 148, 1094. 12828735
  94. [96]D. M. Supp, A. P. Supp, S. T. Boyce, S. M. Bell, J. Invest. Dermatol. 2000, 114, 5. 10620108
  95. [97]D. M. Supp, K. Wilson‐Landy, S. T. Boyce, FASEB J. 2002, 16, 797. 12039861 PMC1820617
  96. [98]P. L. Tremblay, V. Hudon, F. Berthod, L. Germain, F. A. Auger, Am. J. Transplant. 2005, 5, 1002. 15816880
  97. [99]C. Auxenfans, C. Lequeux, E. Perrusel, A. Mojallal, B. Kinikoglu, O. Damour, J. Tissue Eng. Regen. Med. 2012, 6, 512. 21755603
  98. [100]S. Sun, L. Jin, Y. Zheng, J. Zhu, Nat. Commun. 2022, 13, 5481. 36123328 PMC9485166
  99. [101]A. Pappalardo, D. Alvarez Cespedes, S. Fang, A. R. Herschman, E. Y. Jeon, K. M. Myers, J. W. Kysar, H. E. Abaci, Sci. Adv. 2023, 9, eade2514. 36706190 PMC9882972
  100. [102]L. J. Meyer, R. Stern, J. Invest. Dermatol. 1994, 102, 385. 8120424
  101. [103]G. Galassi, P. Brun, M. Radice, R. Cortivo, G. F. Zanon, P. Genovese, G. Abatangelo, Biomaterials 2000, 21, 2183. 10985492
  102. [104]C. Tonello, B. Zavan, R. Cortivo, P. Brun, S. Panfilo, G. Abatangelo, Biomaterials 2003, 24, 1205. 12527261
  103. [105]M. T. Cerqueira, L. P. da Silva, T. C. Santos, R. R. P. Pirraco, V. M. Correlo, R. L. Reis, A. P. Marques, ACS Appl. Mater. Interfaces 2014, 6, 19668. 25361388
  104. [106]C. Tonello, V. Vindigni, B. Zavan, S. Abatangelo, G. Abatangelo, P. Brun, R. Cortivo, FASEB J. 2005, 19, 1546. 15972294
  105. [107]A. Montero, C. Atienza, C. Elvira, J. L. Jorcano, D. Velasco, Mater. Sci. Eng., C 2021, 128, 112352. 34474900
  106. [108]S. Bencherif, O. Gsib, C. Egles, J. Mol. Biol. 2017, 2, 1.
  107. [109]F. M. Shaikh, A. Callanan, E. G. Kavanagh, P. E. Burke, P. A. Grace, T. M. McGloughlin, Cells Tissues Organs 2008, 188, 333. 18552484
  108. [110]X. Chen, A. S. Aledia, C. M. Ghajar, C. K. Griffith, A. J. Putnam, C. C. Hughes, S. C. George, Tissue Eng Part A 2009, 15, 1363. 18976155 PMC2792096
  109. [111]R. K. Chan, D. O. Zamora, N. L. Wrice, D. G. Baer, E. M. Renz, R. J. Christy, S. Natesan, Stem Cells Int. 2012, 2012, 1. PMC3399490 22848228
  110. [112]X. Liu, S. Michael, K. Bharti, M. Ferrer, M. J. Song, Biofabrication 2020, 12, 035002. 32059197 PMC7457159
  111. [113]J. S. Schechner, S. K. Crane, F. Wang, A. M. Szeglin, G. Tellides, M. I. Lorber, A. L. M. Bothwell, J. S. Pober, FASEB J. 2003, 17, 2250. 14656987
  112. [114]P. S. Sahota, J. L. Burn, M. Heaton, E. Freedlander, S. K. Suvarna, N. J. Brown, S. M. Neil, Wound Repair Regener. 2003, 11, 275. 12846915
  113. [115]A. M. Sarmin, J. T. Connelly, Curr. Protoc. 2022, 2, e393. 35263039 PMC9310708
  114. [116]A. M. Jorgensen, Z. Chou, G. Gillispie, S. J. Lee, J. J. Yoo, S. Soker, A. Atala, Nanomaterials 2020, 10, 1484. 32751101 PMC7466410
  115. [117]H. Fu, D. Zhang, J. Zeng, Q. Fu, Z. Chen, X. Sun, Y. Yang, S. Li, M. Chen, Int. J. Bioprint. 2023, 9, 674. 37065662 PMC10090812
  116. [118]B. S. Kim, Y. W. Kwon, J.‐S. Kong, G. T. Park, G. Gao, W. Han, M.‐B. Kim, H. Lee, J. H. Kim, D.‐W. Cho, Biomaterials 2018, 168, 38. 29614431
  117. [119]N. Khoshnood, A. Zamanian, Int. J. Bioprint. 2020, 20, e00095.
  118. [120]S. Singh, Y. Marquardt, R. Rimal, A. Nishiguchi, S. Huth, M. Akashi, M. Moeller, J. M. Baron, ACS Appl. Bio Mater. 2020, 3, 6639. PMC9062876 35019390
  119. [121]A. Nishiguchi, H. Yoshida, M. Matsusaki, M. Akashi, Adv. Mater. 2011, 23, 3506. 21728193
  120. [122]M. Matsusaki, K. Fujimoto, Y. Shirakata, S. Hirakawa, K. Hashimoto, M. Akashi, J. Biomed. Mater. Res. A 2015, 103, 3386. 25850823
  121. [123]R. Rimal, Y. Marquardt, T. Nevolianis, S. Djeljadini, A. B. Marquez, S. Huth, D. N. Chigrin, M. Wessling, J. M. Baron, M. Möller, Appl. Mater. Today 2021, 25, 101213.
  122. [124]M. Cerqueira, R. P. Pirraco, A. Martins, T. Santos, R. Reis, A. Marques, Acta Biomater. 2014, 10, 3145. 24650971
  123. [125]J. Bourland, J. Fradette, F. A. Auger, Sci. Rep. 2018, 8, 13191. 30181613 PMC6123405
  124. [126]N. Gallo, H. Nasser, L. Salvatore, M. L. Natali, L. Campa, M. Mahmoud, L. Capobianco, A. Sannino, M. Madaghiele, Eur. Polym. J. 2019, 117, 134.
  125. [127]B. M. Lee, S. J. Park, I. Noh, C.‐H. Kim, Biomater. Res. 2021, 25, 1. 34462017 PMC8404285
  126. [128]J. Lee, K. R. Koehler, Exp Dermatol 2021, 30, 613. 33507537 PMC8265774
  127. [129]J. Lee, C. C. Rabbani, H. Gao, M. R. Steinhart, B. M. Woodruff, Z. E. Pflum, A. Kim, S. Heller, Y. Liu, T. Z. Shipchandler, Nature 2020, 582, 399. 32494013 PMC7593871
  128. [130]A. De Pieri, Y. Rochev, D. I. Zeugolis, NPJ Regen. Med. 2021, 6, 18. 33782415 PMC8007731
  129. [131]S. Jiang, Y. Zhuang, M. Cai, X. Wang, K. Lin, Eng. Regen. 2023, 4, 357.
  130. [132]J. E. Neil, M. B. Brown, A. C. Williams, Sci. Rep. 2020, 10, 21192. 33273665 PMC7712775
  131. [133]S. Eberlin, G. Facchini, G. H. da Silva, S. Eberlin, A. R. Bragatto, A. L. T. A. Pinheiro, A. da Silva Pinheiro, Altern. Lab. Anim. 2021, 49, 137. 34399588
  132. [134]D. B. Kolesky, K. A. Homan, M. A. Skylar‐Scott, J. A. Lewis, Proc. Natl. Acad. Sci. USA 2016, 113, 3179. 26951646 PMC4812707
  133. [135]N. Mori, Y. Morimoto, S. Takeuchi, Biomaterials 2017, 116, 48. 27914266
  134. [136]B. S. Kim, G. Gao, J. Y. Kim, D. W. Cho, Adv. Healthcare Mater. 2019, 8, 1801019.
  135. [137]M. J. Helmedag, S. Weinandy, Y. Marquardt, J. M. Baron, N. Pallua, C. V. Suschek, S. Jockenhoevel, Tissue Eng., Part A 2015, 21, 343. 25159286 PMC4293133
  136. [138]N. Jusoh, J. Ko, N. L. Jeon, APL Bioeng. 2019, 3, 036101. 31431937 PMC6697035
  137. [139]F. Groeber, L. Engelhardt, J. Lange, S. Kurdyn, F. F. Schmid, C. Rucker, S. Mielke, H. Walles, J. Hansmann 2016, 33, 415. 27180196
  138. [140]A.‐E. Matei, C.‐W. Chen, L. Kiesewetter, A.‐H. Györfi, Y.‐N. Li, T. Trinh‐Minh, X. Xu, C. T. Manh, T. van Kuppevelt, J. Hansmann, Ann. Rheum. Dis. 2019, 78, 1686. 31540936
  139. [141]D. Marino, J. Luginbühl, S. Scola, M. Meuli, E. Reichmann, Sci. Transl. Med. 2014, 6, 221ra14. 24477001
  140. [142]F. Kreimendahl, Y. Marquardt, C. Apel, M. Bartneck, G. Zwadlo‐Klarwasser, J. Hepp, S. Jockenhoevel, J. M. Baron, J. Biomed. Mater. Res., Part A 2019, 107, 1340. 30724457
  141. [143]B. Kwak, S. Jin, S. Kim, E. Kim, J. Chung, J. Sung, Biotechnol. Bioeng. 2020, 117, 1853. 32100875
  142. [144]E. Attiogbe, S. Larochelle, Y. Chaib, C. Mainzer, A. Mauroux, S. Bordes, B. Closs, C. Gilbert, V. J. Moulin, Acta Biomater. 2023, 168, 361. 37419164
  143. [145]I. Wagner, E.‐M. Materne, S. Brincker, U. Süßbier, C. Frädrich, M. Busek, F. Sonntag, D. A. Sakharov, E. V. Trushkin, A. G. Tonevitsky, Lab Chip 2013, 13, 3538. 23648632
  144. [146]I. Maschmeyer, T. Hasenberg, A. Jaenicke, M. Lindner, A. K. Lorenz, J. Zech, L.‐A. Garbe, F. Sonntag, P. Hayden, S. Ayehunie, Eur. J. Pharm. Biopharm. 2015, 95, 77. 25857839 PMC6574126
  145. [147]Z. Guo, C. A. Higgins, B. M. Gillette, M. Itoh, N. Umegaki, K. Gledhill, S. K. Sia, A. M. Christiano, Stem Cell Res. Ther. 2013, 4, S2. 24564920 PMC4029476
  146. [148]S. Girardeau‐Hubert, C. Deneuville, H. Pageon, K. Abed, C. Tacheau, N. Cavusoglu, M. Donovan, D. Bernard, D. Asselineau, Sci. Rep. 2019, 9, 7456. 31092846 PMC6520399
  147. [149]S.‐Y. Jung, H. J. You, M.‐J. Kim, G. Ko, S. Lee, K.‐S. Kang, iScience 2022, 25. PMC9526179 36193049
  148. [150]J. Lee, W. H. van der Valk, S. A. Serdy, C. Deakin, J. Kim, A. P. Le, K. R. Koehler, Nat. Protoc. 2022, 17, 1266. 35322210 PMC10461778
  149. [151]M.‐A. Bolzinger, S. Briançon, J. Pelletier, Y. Chevalier, Curr. Opin. Colloid Interface Sci. 2012, 17, 156.
  150. [152]B. Illel, H. Schaefer, J. Wepierre, O. Doucet, J. Pharm. Sci. 1991, 80, 424. 1880719
  151. [153]E. Roig‐Rosello, P. Rousselle, Biomolecules 2020, 10, 1607. 33260936 PMC7760980
  152. [154]C. O'Connor, E. Brady, Y. Zheng, E. Moore, K. R. Stevens, Nat. Rev. Mater. 2022, 7, 702. 35669037 PMC9154041
  153. [155]S. M. White, R. Hingorani, R. P. Arora, C. C. Hughes, S. C. George, B. Choi, Tissue Eng., Part C 2012, 18, 697. PMC3427639 22435776
  154. [156]J. A. Bouwstra, R. W. Helder, A. El Ghalbzouri, Adv. Drug Delivery Rev. 2021, 175, 113802. 34015420
  155. [157]B. R. Shepherd, D. R. Enis, F. Wang, Y. Suarez, J. S. Pober, J. S. Schechner, FASEB J. 2006, 20, 1739. 16807367
  156. [158]A. Pappalardo, L. Herron, D. E. Alvarez Cespedes, H. E. Abaci, Adv. Wound Care 2021, 10, 490. PMC8260893 32870778
  157. [159]C. Korn, H. G. Augustin, Am. Heart Assoc. 2012, 125, 3063. 22661515
  158. [161]G. Chen, R. Levin, S. Landau, M. Kaduri, O. Adir, I. Ianovici, N. Krinsky, O. Doppelt‐Flikshtain, J. Shklover, J. Shainsky‐Roitman, Proc. Natl. Acad. Sci. USA 2022, 119, e2207525119. 36095208 PMC9499519

Cited by

Sorted by citations

Related

Authors
Rimal, R., Muduli, S., Desai, P., Marquez, A. B., Möller, M., Platzman, I., Spatz, J., & Singh, S.
Affiliations
  • Max Planck Institute for Medical Research (DE)
  • DWI – Leibniz Institute for Interactive Materials (DE)
  • DWI Leibniz Institute for Interactive Materials e.V RWTH Aachen University Forckenbeckstrasse 50 52074 Aachen Germany
  • Heidelberg University (DE)
Corresponding author
Singh, Smriti
ORCID
Venue
Advanced Healthcare Materials
Publisher
Wiley
Published
2024-02
Volume
13
Issue
9
Pages
e2303351-e2303351
ISSN
  • 2192-2640 (ISSN-L)
  • 2192-2659
DOI
10.1002/adhm.202303351
PMC
PMC11468127
OpenAlex
W4391246670
Cited by
46
References
164
Citations by year
2026: 18 · 2025: 26 · 2024: 2
FWCI
1.65
Type
journal article
Language
en
Open access
Licence
Locations
  • Advanced Healthcare Materials (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • RWTH Publications (RWTH Aachen) (submittedVersion, other-oa)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
  • RWTH Publications (RWTH Aachen)
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Physical Sciences › Materials Science › Biomaterials › Electrospun Nanofibers in Biomedical Applications
Keywords
tissue-engineered skin, skin grafting, bioreactors, organ-on-a-chip, organoids, alternatives to animal testing
MeSH terms
Animals, Humans, Neovascularization, Pathologic, Organoids, Skin, Skin Diseases, Tissue Engineering

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