Fibronectin and vitronectin alleviate adipose-derived stem cells senescence during long-term culture through the AKT/MDM2/P53 pathway.

Vitronectin / metabolism Cellular Senescence Proto-Oncogene Proteins c-akt / metabolism Tumor Suppressor Protein p53 / metabolism Fibronectins / metabolism Proto-Oncogene Proteins c-mdm2 / metabolism Humans Signal Transduction Cells, Cultured Stem Cells / metabolism Cell Proliferation Adipose Tissue / cytology Cell Culture Techniques / methods
Adipose-derived stem cells Cell culture Cell therapy Fibronectin Good manufacturing practice Replicative senescence Vitronectin

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
20 06 2024
Historique:
received: 19 02 2024
accepted: 19 06 2024
medline: 21 6 2024
pubmed: 21 6 2024
entrez: 20 6 2024
Statut: epublish

Résumé

Cellular senescence plays a role in the development of aging-associated degenerative diseases. Cell therapy is recognized as a candidate treatment for degenerative diseases. To achieve the goal of cell therapy, the quality and good characteristics of cells are concerned. Cell expansion relies on two-dimensional culture, which leads to replicative senescence of expanded cells. This study aimed to investigate the effect of cell culture surface modification using fibronectin (FN) and vitronectin (VN) in adipose-derived stem cells (ADSCs) during long-term expansion. Our results showed that ADSCs cultured in FN and VN coatings significantly enhanced adhesion, proliferation, and slow progression of cellular senescence as indicated by lower SA-β-gal activities and decreased expression levels of genes including p16, p21, and p53. The upregulation of integrin α5 and αv genes influences phosphatidylinositol 4,5-bisphosphate 3-kinase (PI3K), and AKT proteins. FN and VN coatings upregulated AKT and MDM2 leading to p53 degradation. Additionally, MDM2 inhibition by Nutlin-3a markedly elevated p53 and p21 expression, increased cellular senescence, and induced the expression of inflammatory molecules including HMGB1 and IL-6. The understanding of FN and VN coating surface influencing ADSCs, especially senescence characteristics, offers a promising and practical point for the cultivation of ADSCs for future use in cell-based therapies.

Identifiants

DOI: 10.1038/s41598-024-65339-z PMID: 38902430
pubmed: 38902430
doi: 10.1038/s41598-024-65339-z
pii: 10.1038/s41598-024-65339-z
doi:

Substances chimiques

Vitronectin 0
Proto-Oncogene Proteins c-akt EC 2.7.11.1
Tumor Suppressor Protein p53 0
Fibronectins 0
Proto-Oncogene Proteins c-mdm2 EC 2.3.2.27
MDM2 protein, human EC 2.3.2.27
TP53 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

14242

Subventions

Organisme : Mahidol University
ID : Specific League Funds

Informations de copyright

© 2024. The Author(s).

Références

Di Micco, R., Krizhanovsky, V., Baker, D. & d’Adda di Fagagna, F. Cellular senescence in ageing: From mechanisms to therapeutic opportunities. Nat. Rev. Mol. Cell Biol. 22, 75–95 (2020).
doi: 10.1038/s41580-020-00314-w pubmed: 33328614 pmcid: 8344376
Hayflick, L. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614–636 (1965).
doi: 10.1016/0014-4827(65)90211-9 pubmed: 14315085
McHugh, D. & Gil, J. Senescence and aging: Causes, consequences, and Therapeutic Avenues. J. Cell Biol. 217, 65–77 (2017).
doi: 10.1083/jcb.201708092 pubmed: 29114066
El-Kadiry, A.E.-H., Rafei, M. & Shammaa, R. Cell therapy: Types, regulation, and clinical benefits. Front. Med. 8, 756029 (2021).
doi: 10.3389/fmed.2021.756029
Pittenger, M. F. et al. Mesenchymal stem cell perspective: Cell biology to clinical progress. npj Regen. Ther. https://doi.org/10.1038/s41536-019-0083-6 (2019).
doi: 10.1038/s41536-019-0083-6
Müller, L. et al. Immunomodulatory properties of mesenchymal stromal cells: An update. Front. Cell dev. Biol. 9, (2021).
Mazini, L., Ezzoubi, M. & Malka, G. Overview of current adipose-derived stem cell (adscs) processing involved in therapeutic advancements: Flow chart and regulation updates before and after COVID-19. Stem Cell Res. Ther. https://doi.org/10.1186/s13287-020-02006-w (2021).
doi: 10.1186/s13287-020-02006-w pubmed: 33397467 pmcid: 7781178
Pathak, R. U., Soujanya, M. & Mishra, R. K. Deterioration of nuclear morphology and architecture: A hallmark of senescence and aging. Ageing Res. Rev. 67, 101264 (2021).
doi: 10.1016/j.arr.2021.101264 pubmed: 33540043
Hernandez-Segura, A., Nehme, J. & Demaria, M. Hallmarks of cellular senescence. Trends Cell Biol. 28, 436–453 (2018).
doi: 10.1016/j.tcb.2018.02.001 pubmed: 29477613
Yao, W., Dong, H., Qi, J., Zhang, Y. & Shi, L. Safety and efficacy of mesenchymal stem cells in severe/critical patients with COVID-19: A systematic review and meta-analysis. eClinicalMedicine. 51, 101545 (2022).
doi: 10.1016/j.eclinm.2022.101545 pubmed: 35844767 pmcid: 9270852
Bhat, S., Chiew, G. G., Ng, J. X., Lin, X. & Seetharam, R. N. Optimization of culture conditions for human bone marrow-derived mesenchymal stromal cell expansion in macrocarrier-based Tide motion system. Biotechnol. J. https://doi.org/10.1002/biot.202000540 (2021).
doi: 10.1002/biot.202000540 pubmed: 33838001
López-Seijas, J. et al. Development of new non-viral systems for genetic modification of Senescent Cells. Mol. Ther. Nucleic Acids 32, 302–317 (2023).
doi: 10.1016/j.omtn.2023.03.010 pubmed: 37096164 pmcid: 10122050
Omidifar, N. et al. Trends in natural nutrients for oxidative stress and cell senescence. Oxid. Med. Cell. Longev. 2021, 1–7 (2021).
doi: 10.1155/2021/7501424
Gasek, N. S., Kuchel, G. A., Kirkland, J. L. & Xu, M. Strategies for targeting senescent cells in human disease. Nat. Aging 1, 870–879 (2021).
doi: 10.1038/s43587-021-00121-8 pubmed: 34841261 pmcid: 8612694
Jalali, M. et al. Basic Science Methods for Clinical Researchers (Elsevier Science, 2017).
Cai, S. et al. Recent advance in surface modification for regulating cell adhesion and behaviors. Nanotechnol. Rev. 9, 971–989 (2020).
doi: 10.1515/ntrev-2020-0076
Cooke, M. J. et al. Enhanced cell attachment using a novel cell culture surface presenting functional domains from extracellular matrix proteins. Cytotechnology 56, 71–79 (2008).
doi: 10.1007/s10616-007-9119-7 pubmed: 19002844 pmcid: 2259265
Li, X., Yao, J., Yang, X., Tian, W. & Liu, L. Surface modification with fibronectin or collagen to improve the cell adhesion. Appl. Surf. Sci. 255, 459–461 (2008).
doi: 10.1016/j.apsusc.2008.06.105
Li, T., Hao, L., Li, J., Du, C. & Wang, Y. Insight into vitronectin structural evolution on material surface chemistries: The mediation for cell adhesion. Bioact. Mate 5, 1044–1052 (2020).
Dalton, C. J. & Lemmon, C. A. Fibronectin: Molecular structure, fibrillar structure and mechanochemical signaling. Cells 10, 2443 (2021).
doi: 10.3390/cells10092443 pubmed: 34572092 pmcid: 8471655
Akiyama, S. K. Purification of vitronectin. Curr. Protoc. Cell. Biol. https://doi.org/10.1002/0471143030.cb1006s60 (2013).
doi: 10.1002/0471143030.cb1006s60 pubmed: 24510786
Singh, P., Carraher, C. & Schwarzbauer, J. E. Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26, 397–419 (2010).
doi: 10.1146/annurev-cellbio-100109-104020 pubmed: 20690820 pmcid: 3628685
Shen, J. et al. Vitronectin-activated αvβ3 and ΑVΒ5 integrin signalling specifies haematopoietic fate in human pluripotent stem cells. Cell Prolif. https://doi.org/10.1111/cpr.13012 (2021).
doi: 10.1111/cpr.13012 pubmed: 34888976 pmcid: 8780907
Ji, J. et al. Fibronectin 1 inhibits the apoptosis of human trophoblasts by activating the PI3K/akt signaling pathway. Int. J. Mol. Med. 46(5), 1908–22 (2020).
pubmed: 33000176 pmcid: 7521556
Cho, C., Horzempa, C., Jones, D. & McKeown-Longo, P. J. The fibronectin III-1 domain activates a PI3-kinase/Akt signaling pathway leading to αvβ5 integrin activation and trail resistance in human lung cancer cells. BMC Cancer https://doi.org/10.1186/s12885-016-2621-6 (2016).
doi: 10.1186/s12885-016-2621-6 pubmed: 27595851 pmcid: 5011927
Seger, D., Seger, R. & Shaltiel, S. The CK2 phosphorylation of vitronectin. J. Biol Chem. 276, 16998–17006 (2001).
doi: 10.1074/jbc.M003766200 pubmed: 11278271
Bera, A. et al. Functional role of vitronectin in breast cancer. PLOS ONE. 15, e0242141 (2020).
doi: 10.1371/journal.pone.0242141 pubmed: 33211735 pmcid: 7676670
Ji, S. et al. Cellular rejuvenation: molecular mechanisms and potential therapeutic interventions for diseases. Signal Transduct. Target. Ther. 8, 116 (2023).
doi: 10.1038/s41392-023-01343-5 pubmed: 36918530 pmcid: 10015098
Mylonas, A. & O’Loghlen, A. Cellular senescence and ageing: Mechanisms and interventions. Front. Aging https://doi.org/10.3389/fragi.2022.866718 (2022).
doi: 10.3389/fragi.2022.866718 pubmed: 35821824 pmcid: 9261318
Jovic, D. et al. A brief overview of global trends in MSC-based cell therapy. Stem Cell Rev. 18, 1525–1545 (2022).
doi: 10.1007/s12015-022-10369-1
Segeritz, C.-P. & Vallier, L. Cell culture. In Basic Science Methods for Clinical Researchers (ed. Segeritz, C.-P.) 151–172 (Elsevier, 2017).
doi: 10.1016/B978-0-12-803077-6.00009-6
Wuchter, P. et al. Standardization of good manufacturing practice–compliant production of bone marrow–derived human mesenchymal stromal cells for immunotherapeutic applications. Cytotherapy 17, 128–139 (2015).
doi: 10.1016/j.jcyt.2014.04.002 pubmed: 24856898
Yang, Y.-H.K., Ogando, C. R., Wang See, C., Chang, T.-Y. & Barabino, G. A. Changes in phenotype and differentiation potential of human mesenchymal stem cells aging in vitro. Stem Cell Res. Ther. https://doi.org/10.1186/s13287-018-0876-3 (2018).
doi: 10.1186/s13287-018-0876-3 pubmed: 30572947 pmcid: 6302511
Cuollo, L., Antonangeli, F., Santoni, A. & Soriani, A. The senescence-associated secretory phenotype (SASP) in the challenging future of cancer therapy and age-related diseases. Biology 9, 485 (2020).
doi: 10.3390/biology9120485 pubmed: 33371508 pmcid: 7767554
Deng, L. et al. Blockade of integrin signaling reduces chemotherapy-induced premature senescence in collagen cultured bladder cancer cells. Precis. Clin. Med. https://doi.org/10.1093/pcmedi/pbac027 (2022).
doi: 10.1093/pcmedi/pbac027 pubmed: 35694719 pmcid: 9113335
Khalili, A. & Ahmad, M. A review of cell adhesion studies for Biomedical and biological applications. Int. J. Mol. Sci. 16, 18149–18184 (2015).
doi: 10.3390/ijms160818149 pubmed: 26251901
Zhu, X.-Y. et al. Improvement of human embryonic stem cell-derived retinal pigment epithelium cell adhesion, maturation, and function through coating with truncated recombinant human vitronectin. Int. J. Ophthalmol. 14, 1160–1167 (2021).
doi: 10.18240/ijo.2021.08.04 pubmed: 34414078 pmcid: 8342289
Pattappa, G. et al. Fibronectin adherent cell populations derived from Avascular and vascular regions of the meniscus have enhanced Clonogenicity and differentiation potential under Physioxia. Front. Bioeng. Biotechnol. https://doi.org/10.3389/fbioe.2021.789621 (2022).
doi: 10.3389/fbioe.2021.789621 pubmed: 35155405 pmcid: 8831898
Kim, N.-G. & Gumbiner, B. M. Adhesion to fibronectin regulates hippo signaling via the fak–src–PI3K pathway. J. Cell Biol. 210, 503–515 (2015).
doi: 10.1083/jcb.201501025 pubmed: 26216901 pmcid: 4523609
White, E. S. et al. Control of fibroblast fibronectin expression and alternative splicing via the PI3K/AKT/mtor pathway. Exp. Cell Res. 316, 2644–2653 (2010).
doi: 10.1016/j.yexcr.2010.06.028 pubmed: 20615404 pmcid: 2924943
Juratli, M. A. et al. Integrin Α2 and β1 cross-communication with mTOR/Akt and the CDK-cyclin axis in hepatocellular carcinoma cells. Cancers 14, 2430 (2022).
doi: 10.3390/cancers14102430 pubmed: 35626034 pmcid: 9139686
Saleem, S. et al. Β1 integrin/FAK/Erk signalling pathway is essential for human fetal islet cell differentiation and survival. J. Pathol. 219, 182–192 (2009).
doi: 10.1002/path.2577 pubmed: 19544355
Yee, K. L., Weaver, V. M. & Hammer, D. A. Integrin-mediated signalling through the map-kinase pathway. IET Fnutilin Syst. Biol. 2, 8–15 (2008).
doi: 10.1049/iet-syb:20060058
Lindström, H. J. & Friedman, R. Inferring time-dependent population growth rates in cell cultures undergoing adaptation. BMC Bioinform. https://doi.org/10.1186/s12859-020-03887-7 (2020).
doi: 10.1186/s12859-020-03887-7
Chen, L. et al. 1,25-dihydroxyvitamin D exerts an antiaging role by activation of nrf2-antioxidant signaling and inactivation of p16/p53-senescence signaling. Aging Cell https://doi.org/10.1111/acel.12951 (2019).
doi: 10.1111/acel.12951 pubmed: 31880094 pmcid: 6996957
Peng, Y. et al. Mechano-signaling via piezo1 prevents activation and p53-mediated senescence of muscle stem cells. Redox Biol. 52, 102309 (2022).
doi: 10.1016/j.redox.2022.102309 pubmed: 35395625 pmcid: 9005960
Chen, C. et al. Inhibition of the p53/p21 pathway attenuates the effects of senescent nucleus pulposus cell-derived exosomes on the senescence of nucleus pulposus cells. Orthop. Surg. 13, 583–591 (2020).
doi: 10.1111/os.12886 pubmed: 33314719 pmcid: 7957423
Chibaya, L., Karim, B., Zhang, H. & Jones, S. N. MDM2 phosphorylation by Akt regulates the p53 response to oxidative stress to promote cell proliferation and tumorigenesis. Proc. Natl. Acad. Sci. https://doi.org/10.1073/pnas.2003193118 (2021).
doi: 10.1073/pnas.2003193118 pubmed: 33468664 pmcid: 7848548
Gottlieb, T. M., Leal, J. F., Seger, R., Taya, Y. & Oren, M. Cross-talk between AKT, P53 and MDM2: Possible implications for the regulation of apoptosis. Oncogene 21, 1299–1303 (2002).
doi: 10.1038/sj.onc.1205181 pubmed: 11850850
Shen, H. & Maki, C. Pharmacologic activation of p53 by small-molecule MDM2 antagonists. Curr. Pharm. Des. 17, 560–568 (2011).
doi: 10.2174/138161211795222603 pubmed: 21391906 pmcid: 3613239
Villalonga-Planells, R. et al. Activation of p53 by nutlin-3a induces apoptosis and cellular senescence in human glioblastoma multiforme. PLoS ONE 6, e18588 (2011).
doi: 10.1371/journal.pone.0018588 pubmed: 21483692 pmcid: 3071734
Manfé, V. et al. MDM2 inhibitor nutlin-3a induces apoptosis and senescence in cutaneous T-cell lymphoma: Role of p53. J. Investig. Dermatol. 132, 1487–1496 (2012).
doi: 10.1038/jid.2012.10 pubmed: 22377766
Ovadya, Y. & Krizhanovsky, V. Strategies targeting cellular senescence. J. Clin. Invest. 128, 1247–1254 (2018).
doi: 10.1172/JCI95149 pubmed: 29608140 pmcid: 5873866

Auteurs

Patcharapa Tragoonlugkana (P)

Department of Clinical Microscopy, Faculty of Medical Technology, Mahidol University, 999 Phutthamonthon Sai 4, Salaya, Phutthamonthon, Nakhon Pathom, 73170, Thailand.

Chatchai Pruksapong (C)

Department of Surgery, Phramongkutklao Hospital and Phramongkutklao College of Medicine, Bangkok, 10400, Thailand.

Pawared Ontong (P)

Department of Community Medical Technology, Faculty of Medical Technology, Mahidol University, Nakhon Pathom, 73170, Thailand.

Witchayapon Kamprom (W)

Department of Clinical Microbiology and Applied Technology, Faculty of Medical Technology, Mahidol University, Nakhon Pathom, 73170, Thailand.

Aungkura Supokawej (A)

Department of Clinical Microscopy, Faculty of Medical Technology, Mahidol University, 999 Phutthamonthon Sai 4, Salaya, Phutthamonthon, Nakhon Pathom, 73170, Thailand. aungkura.jer@mahidol.ac.th.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Scléroprotéines › Protéines de la matrice extracellulaire › Vitronectine › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Phénomènes physiologiques › Croissance et développement › Vieillissement › Vieillissement de la cellule › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines tumorales › Protéines oncogènes › Protéines proto-oncogènes › Protéines proto-oncogènes c-akt › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Phosphoprotéines › Protéine p53 suppresseur de tumeur › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Scléroprotéines › Protéines de la matrice extracellulaire › Fibronectines › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines nucléaires › Protéines proto-oncogènes c-mdm2 › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Transduction du signal › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Cellules › Cellules cultivées › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Cellules › Cellules souches › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Phénomènes physiologiques › Croissance et développement › Croissance › Processus de croissance cellulaire › Prolifération cellulaire › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Tissus › Tissu conjonctif › Tissu adipeux › Fibronectin and vitronectin alleviate...
questionsmedicales.fr › Techniques d'investigation › Techniques in vitro › Techniques de culture › Techniques de culture cellulaire › Fibronectin and vitronectin alleviate...