Transgenic silkworm expressing bioactive human ciliary neurotrophic factor for biomedical application.
human ciliary neurotrophic factor
silk materials
silkworm
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
01 Sep 2024
01 Sep 2024
Historique:
revised:
29
07
2024
received:
26
05
2024
accepted:
31
07
2024
medline:
2
9
2024
pubmed:
2
9
2024
entrez:
2
9
2024
Statut:
aheadofprint
Résumé
Ciliary neurotrophic factor (CNTF) acts as a potent neuroprotective agent in neuronal survival and regeneration, and can also induce the differentiation of several stem cells into neurons, which highlights the broad application of CNTF in biomedicine. However, large-scale production of bioactive recombinant human CNTF protein remains to be explored. Herein, this study aims to express a bioactive human CNTF protein on a large scale by genetically engineering a silk gland bioreactor of silkworm. Our results showed that CNTF protein was successfully expressed in the middle silk gland (MSG) of silkworm, which can be secreted into the silks with the amount of 3.2 mg/g cocoons. The fabrication of human CNTF-functionalized silk material was able to promote proliferation and migration of neural cells when compared to the natural silk protein. Importantly, this functional silk material could also facilitate neurite outgrowth of mouse retinal ganglion cell (RGC-5) cells. All these data demonstrated a high bioactivity of the recombinant human CNTF protein expressed in the MSG of silkworm. The further fabrication of different silk materials with CNTF bioactivity will give biomedical applications in tissue engineering and neuroregeneration.
Identifiants
pubmed: 39219303
doi: 10.1111/1744-7917.13442
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Key Research and Development Program of China
ID : 2022YFD1201600
Organisme : National Natural Science Foundation of China
ID : 32030103
Organisme : National Natural Science Foundation of China
ID : 32172798
Organisme : Natural Science Foundation of Chongqing Municipality
ID : CSTB2023NSCQ-MSX0814
Organisme : Natural Science Foundation of Chongqing Municipality
ID : cstc2020jcyj-cxttX0001
Informations de copyright
© 2024 Institute of Zoology, Chinese Academy of Sciences.
Références
ALS CNTF Treatment Study Group (1996) A double‐blind placebo‐controlled clinical trial of subcutaneous recombinant human ciliary neurotrophic factor (rHCNTF) in amyotrophic lateral sclerosis. Neurology, 46, 1244–1249.
Benowitz, L.I. and Routtenberg, A. (1997) GAP‐43: an intrinsic determinant of neuronal development and plasticity. Trends in Neurosciences, 20, 84–91.
Chato‐Astrain, J., Roda, O., Sanchez‐Porras, D., Miralles, E., Alaminos, M., Campos, F. et al. (2023) Peripheral nerve regeneration through nerve conduits evokes differential expression of growth‐associated protein‐43 in the spinal cord. Neural Regeneration Research, 18, 1852–1856.
Chen, K., Li, Y., Li, Y., Pan, W. and Tan, G. (2023) Silk fibroin combined with electrospinning as a promising strategy for tissue regeneration. Macromolecular Bioscience, 23, 2200380.
Chen, S., Matsumoto, H., Moro‐Oka, Y., Tanaka, M., Miyahara, Y., Suganami, T. et al. (2019) Smart microneedle fabricated with silk fibroin combined semi‐interpenetrating network hydrogel for glucose‐responsive insulin delivery. ACS Biomaterials Science & Engineering, 5, 5781–5789.
Chen, W., Wang, F., Tian, C., Wang, Y., Xu, S., Wang, R. et al. (2018) Transgenic silkworm‐based silk gland bioreactor for large scale production of bioactive human platelet‐derived growth factor (PDGF‐BB) in silk cocoons. International Journal of Molecular Sciences, 19, 2533.
Do Rhee, K., Wang, Y., Ten Hoeve, J., Stiles, L., Nguyen, T.T.T., Zhang, X. et al. (2022) Ciliary neurotrophic factor‐mediated neuroprotection involves enhanced glycolysis and anabolism in degenerating mouse retinas. Nature Communications, 13, 7037.
Korshunova, I. and Mosevitsky, M. (2010) Role of the growth‐associated protein GAP‐43 in NCAM‐mediated neurite outgrowth. Advances in Experimental Medicine and Biology, 663, 169–182.
Kundu, B., Rajkhowa, R., Kundu, S.C. and Wang, X. (2013) Silk fibroin biomaterials for tissue regenerations. Advanced Drug Delivery Reviews, 65, 457–470.
Lavail, M.M., Unoki, K., Yasumura, D., Matthes, M.T., Yancopoulos, G.D. and Steinberg, R.H. (1992) Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proceedings of the National Academy of Sciences USA, 89, 11249–11253.
Lee, N., Batt, M.K., Cronier, B.A., Jackson, M.C., Bruno Garza, J.L., Trinh, D.S. et al. (2013) Ciliary neurotrophic factor receptor regulation of adult forebrain neurogenesis. Journal of Neuroscience, 33, 1241–1258.
Lindsley, C.W. (2010) The Akt/PKB family of protein kinases: a review of small molecule inhibitors and progress towards target validation: a 2009 update. Current Topics in Medicinal Chemistry, 10, 458–477.
Ma, L., Sun, Y., Cheng, Q., Yang, Z., Wang, J., Xu, Z. et al. (2023) Silk protein‐mediated biomineralization: from bioinspired strategies and advanced functions to biomedical applications. ACS Applied Materials & Interfaces, 15, 33191–33206.
Miller, R.G., Petajan, J.H., Bryan, W.W., Armon, C., Barohn, R.J., Goodpasture, J.C. et al. (1996) A placebo‐controlled trial of recombinant human ciliary neurotrophic (rhCNTF) factor in amyotrophic lateral sclerosis. Annals of Neurology, 39, 256–360.
Mittoux, V., Joseph, J.M., Conde, F., Palfi, S., Dautry, C., Poyot, T. et al. (2000) Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease. Human Gene Therapy, 11, 1177–1187.
Ogawa, S., Tomita, M., Shimizu, K. and Yoshizato, K. (2007) Generation of a transgenic silkworm that secretes recombinant proteins in the sericin layer of cocoon: production of recombinant human serum albumin. Journal of Biotechnology, 128, 531–544.
Sango, K., Yanagisawa, H. and Takaku, S. (2007) Expression and histochemical localization of ciliary neurotrophic factor in cultured adult rat dorsal root ganglion neurons. Histochemistry and Cell Biology, 128, 35–43.
Stockli, K.A., Lillien, L.E., Naher‐Noe, M., Breitfeld, G., Hughes, R.A., Raff, M.C. et al. (1991) Regional distribution, developmental changes, and cellular localization of CNTF‐mRNA and protein in the rat brain. Journal of Cell Biology, 115, 447–459.
Talukdar, S., Mandal, M., Hutmacher, D.W., Russell, P.J., Soekmadji, C. and Kundu, S.C. (2011) Engineered silk fibroin protein 3D matrices for in vitro tumor model. Biomaterials, 32, 2149–2159.
Tamura, T., Thibert, C., Royer, C., Kanda, T., Abraham, E., Kamba, M. et al. (2000) Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon‐derived vector. Nature Biotechnology, 18, 81–84.
Tomita, M. (2011) Transgenic silkworms that weave recombinant proteins into silk cocoons. Biotechnology Letters, 33, 645–654.
Tomita, M., Munetsuna, H., Sato, T., Adachi, T., Hino, R., Hayashi, M. et al. (2003) Transgenic silkworms produce recombinant human type III procollagen in cocoons. Nature Biotechnology, 21, 52–56.
Vepari, C. and Kaplan, D.L. (2007) Silk as a biomaterial. Progress in Polymer Science, 32, 991–1007.
Wang, F., Guo, C., Yang, Q., Li, C., Zhao, P., Xia, Q. et al. (2021) Protein composites from silkworm cocoons as versatile biomaterials. Acta Biomaterialia, 121, 180–192.
Wang, F., Wang, R., Wang, Y., Zhao, P. and Xia, Q. (2015) Large‐scale production of bioactive recombinant human acidic fibroblast growth factor in transgenic silkworm cocoons. Scientific Reports, 5, 16323.
Wang, F., Xu, H., Yuan, L., Ma, S., Wang, Y., Duan, X. et al. (2013) An optimized sericin‐1 expression system for mass‐producing recombinant proteins in the middle silk glands of transgenic silkworms. Transgenic Research, 22, 925–938.
Wang, H.Y., Zhang, Y., Zhang, M. and Zhang, Y.Q. (2024) Functional modification of silk fibroin from silkworms and its application to medical biomaterials: a review. International Journal of Biological Macromolecules, 259, 129099.
Wen, R., Tao, W., Li, Y. and Sieving, P.A. (2012) CNTF and retina. Progress in Retinal and Eye Research, 31, 136–151.
Winter, C.G., Saotome, Y., Levison, S.W. and Hirsh, D. (1995) A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proceedings of the National Academy of Sciences USA, 92, 5865–5869.
Xia, Q., Li, S. and Feng, Q. (2014) Advances in silkworm studies accelerated by the genome sequencing of Bombyx mori. Annual Review of Entomology, 59, 513–536.
Xia, Q., Zhou, Z., Lu, C., Cheng, D., Dai, F., Li, B. et al. (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science, 306, 1937–1940.
Xu, L., Zhang, C., Liu, L., Zhang, Y., Wang, Q., Wang, J. et al. (2017) Purification and characterization of a long‐acting ciliary neurotrophic factor via genetically fused with an albumin‐binding domain. Protein Expression and Purification, 139, 14–20.
Xu, S., Tan, H., Yang, Q., Wang, R., Tian, C., Ji, Y. et al. (2021) Fabrication of a silk sericin hydrogel system delivering human lactoferrin using genetically engineered silk with improved bioavailability to alleviate chemotherapy‐induced immunosuppression. ACS Applied Materials & Interfaces, 13, 45175–45190.
Zeng, S., Zhao, X., Zhang, L., Pathak, J.L., Huang, W., Li, Y. et al. (2020) Effect of ciliary neurotrophic factor on neural differentiation of stem cells of human exfoliated deciduous teeth. Journal of Biological Engineering, 14, 29.
Zhang, K., Hopkins, J.J., Heier, J.S., Birch, D.G., Halperin, L.S., Albini, T.A. et al. (2011) Ciliary neurotrophic factor delivered by encapsulated cell intraocular implants for treatment of geographic atrophy in age‐related macular degeneration. Proceedings of the National Academy of Sciences USA, 108, 6241–6245.
Zhang, W., Li, Z., Lan, W., Guo, H., Chen, F., Wang, F. et al. (2022) Bioengineered silkworm model for expressing human neurotrophin‐4 with potential biomedical application. Frontiers in Physiology, 13, 1104929.
Zhang, Y., Liu, J., Huang, L., Wang, Z. and Wang, L. (2015) Design and performance of a sericin‐alginate interpenetrating network hydrogel for cell and drug delivery. Scientific Reports, 5, 12374.
Zheng, J., Feng, X., Hou, L., Cui, Y., Zhu, L., Ma, J. et al. (2011) Latanoprost promotes neurite outgrowth in differentiated RGC‐5 cells via the PI3K‐Akt‐mTOR signaling pathway. Cellular and Molecular Neurobiology, 31, 597–604.