journal article·2025-06-09Open access

Development of a Sensory Neuron-Integrated Skin Spheroid Model for the Evaluation of Neuropeptide-Based Topical Delivery Systems

Bianca Aparecida Martin, Juliana Viegas, Luciana Facco Dalmolin, Emerson de Souza Santos, Izabela Pereira Vatanabe, Sabrina Francesca Lisboa, Renata Fonseca Vianna Lopez, Bruno Sarmento

Abstract

The skin is a complex organ composed of multiple layers and diverse cell types, including keratinocytes, fibroblasts, adipocytes, and sensory neurons, which maintain its structural and functional integrity together. Conventional in vitro and ex vivo models help investigate drug permeation and selected biological effects. However, they are limited in replicating neural interactions critical for assessing the efficacy of neuropeptide-based therapies. To address this limitation, a sensory neuron-integrated skin spheroid (SS) model was established, incorporating key skin cell types and providing a rapid, adaptable, and physiologically relevant platform for screening the biological activity of topical delivery systems targeting neuronal pathways. The model's responsiveness was demonstrated using acetyl hexapeptide-3 (HEX-3), a neuropeptide that inhibits acetylcholine release. HEX-3 was internalized by spheroid cells, with preferential accumulation around sensory neurons, confirming targeted cellular uptake. In parallel, ex vivo human skin studies confirmed that HEX-3 can traverse the stratum corneum and accumulate in deeper layers. Treatment with this film enhanced skin hydration, reduced scaling, and improved the structural organization of the stratum corneum after 48 h. Functional assays using the SS model showed that HEX-3 treatment suppressed acetylcholine release, upregulated the antioxidant enzyme SOD2, and stimulated type I collagen synthesis. In aged skin samples, the application of HEX-3 significantly increased collagen levels. This effect was mirrored in the spheroid model, which reached collagen levels comparable to those of aged human skin upon treatment. These findings establish the SS model as a robust platform for evaluating the biological activity of neuropeptide-based topical therapies, offering valuable insights for developing advanced strategies for skin rejuvenation and repair.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Advancements in Transdermal Drug Delivery · Skin Protection and Aging · Polydiacetylene-based materials and applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Avenida do Café, s/n°, 14040-903 Ribeirão Preto, São Paulo, Brazil

i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Rua Alfredo Allen 208, 4200-135 Porto, Portugal

INEB - Instituto de Engenharia Biomédica, Universidade do Porto, Rua Alfredo Allen 208, 4200-135 Porto, Portugal

IUCS-CESPU - Instituto Universitário de Ciências da Saúde, Rua Central de Gandra 1317, 4585-116 Gandra, Portugal

Funding

H2020 Marie Sklodowska-Curie Actions · Conselho Nacional de Desenvolvimento Cient?fico e Tecnol?gico · Funda??o de Amparo ? Pesquisa do Estado de S?o Paulo

References (70)

Show source-provided references
1. 10.1016/j.mpmed.2021.03.00110.1016/j.mpmed.2021.03.001 ↗
2. 10.3390/pharmaceutics1602017610.3390/pharmaceutics16020176 ↗
3. 10.1021/acs.molpharmaceut.4c0105810.1021/acs.molpharmaceut.4c01058 ↗
4. 10.1089/ten.tec.2021.006910.1089/ten.tec.2021.0069 ↗
5. 10.1016/j.biomaterials.2021.12077610.1016/j.biomaterials.2021.120776 ↗
6. 10.1038/cddiscovery.2017.3810.1038/cddiscovery.2017.38 ↗
7. 10.1016/j.clindermatol.2019.04.00910.1016/j.clindermatol.2019.04.009 ↗
8. 10.1111/ene.1200910.1111/ene.12009 ↗
9. 10.1007/s13346-024-01526-910.1007/s13346-024-01526-9 ↗
10. 10.1016/j.ejpb.2018.04.01910.1016/j.ejpb.2018.04.019 ↗
11. 10.1016/j.colsurfb.2012.08.01410.1016/j.colsurfb.2012.08.014 ↗
12. 10.1038/s41598-017-18454-z10.1038/s41598-017-18454-z ↗
13. 10.1016/0278-6915(86)90099-210.1016/0278-6915(86)90099-2 ↗
14. 10.1016/j.ejps.2021.10576910.1016/j.ejps.2021.105769 ↗
15. 10.1016/j.biopha.2023.11584110.1016/j.biopha.2023.115841 ↗
16. 10.1089/wound.2011.035610.1089/wound.2011.0356 ↗
17. 10.1016/j.neuint.2013.03.00810.1016/j.neuint.2013.03.008 ↗
18. 10.1186/s12868-023-00808-110.1186/s12868-023-00808-1 ↗
19. 10.4161/bioa.2625910.4161/bioa.26259 ↗
20. 10.1038/8604210.1038/86042 ↗
21. 10.1038/s41598-021-87431-410.1038/s41598-021-87431-4 ↗
22. Greene L. A. · Issue Ai Dune 25 · 1981 · 256
23. Grosicki, M.; Latacz, G.; Szopa, A.; Cukier, A.; Kieć-Kononowicz, K. The Study of Cellular Cytotoxicity of Argireline®-an Anti-Aging Peptide* . www.actabp.pl.
24. 10.3390/jfb502004310.3390/jfb5020043 ↗
25. 10.1186/s12885-019-5606-410.1186/s12885-019-5606-4 ↗
26. 10.1002/jcp.2468310.1002/jcp.24683 ↗
27. 10.1002/advs.20240870710.1002/advs.202408707 ↗
28. 10.1002/jps.2181710.1002/jps.21817 ↗
29. 10.3389/fimmu.2020.0064810.3389/fimmu.2020.00648 ↗
30. 10.3389/fimmu.2020.56488710.3389/fimmu.2020.564887 ↗
31. 10.30733/std.2022.0157210.30733/std.2022.01572 ↗
32. 10.1007/s12079-018-0459-110.1007/s12079-018-0459-1 ↗
33. 10.1039/C9BM00900K10.1039/C9BM00900K ↗
34. 10.1038/cdd.2015.16810.1038/cdd.2015.168 ↗
35. 10.1080/0955300070172753110.1080/09553000701727531 ↗
36. 10.4161/cam.2313210.4161/cam.23132 ↗
37. Chang, H. Y.; Chi, J.T.; Dudoit, S.; Bondre, C.; Van De Rijn, M.; Botstein, D.; Brown, P. O. Diversity, Topographic Differentiation, and Positional Memory in Human Fibroblasts . www.ncbi.nlm.nih.gov.
38. 10.3389/fcell.2022.92949510.3389/fcell.2022.929495 ↗
39. 10.1089/ten.tea.2017.006010.1089/ten.tea.2017.0060 ↗
40. 10.1016/j.ejpb.2006.07.01510.1016/j.ejpb.2006.07.015 ↗
41. 10.1186/1479-5876-10-11710.1186/1479-5876-10-117 ↗
42. 10.1021/ma061010910.1021/ma0610109 ↗
43. 10.1016/j.carpta.2024.10042410.1016/j.carpta.2024.100424 ↗
44. 10.1080/05704928.2018.142659510.1080/05704928.2018.1426595 ↗
45. 10.1016/j.msec.2014.07.00110.1016/j.msec.2014.07.001 ↗
46. 10.1016/j.ijpharm.2012.05.04410.1016/j.ijpharm.2012.05.044 ↗
47. 10.1016/j.bbamem.2005.04.01010.1016/j.bbamem.2005.04.010 ↗
48. 10.1042/BJ2015027210.1042/BJ20150272 ↗
49. 10.1080/10717544.2019.158273010.1080/10717544.2019.1582730 ↗
50. 10.1080/1061186029003188610.1080/10611860290031886 ↗
51. 10.1007/s00403-004-0533-910.1007/s00403-004-0533-9 ↗
52. 10.3390/ijms22221248910.3390/ijms222212489 ↗
53. 10.1046/j.1365-2796.1997.00170.x10.1046/j.1365-2796.1997.00170.x ↗
54. 10.1016/j.addr.2003.10.02510.1016/j.addr.2003.10.025 ↗
55. 10.1038/s41598-017-16202-x10.1038/s41598-017-16202-x ↗
56. 10.1016/j.jep.2010.07.00610.1016/j.jep.2010.07.006 ↗
57. 10.3390/ijms2311595410.3390/ijms23115954 ↗
58. 10.1111/j.1471-4159.2005.03367.x10.1111/j.1471-4159.2005.03367.x ↗
59. 10.1046/j.1467-2494.2002.00153.x10.1046/j.1467-2494.2002.00153.x ↗
60. 10.4161/derm.2181910.4161/derm.21819 ↗
61. 10.3390/polym1607086710.3390/polym16070867 ↗
62. 10.3390/nu1408162210.3390/nu14081622 ↗
63. 10.1016/j.freeradbiomed.2011.09.03010.1016/j.freeradbiomed.2011.09.030 ↗
64. 10.3390/biom502054510.3390/biom5020545 ↗
65. Zeichner J. · J. Clin. Aesthet. Dermatol. · 2024 · 17 · 48
66. 10.3390/foods1207140010.3390/foods12071400 ↗
67. 10.1046/j.1523-1747.2000.00902.x10.1046/j.1523-1747.2000.00902.x ↗
68. 10.1093/rb/rbac11010.1093/rb/rbac110 ↗
69. 10.1007/s40257-013-0009-910.1007/s40257-013-0009-9 ↗
70. 10.1002/adma.20180165110.1002/adma.201801651 ↗