Single cell, Label free Characterisation of Human Mesenchymal Stromal cell Stemness and Future Growth Potential by Autofluorescence Multispectral Imaging.

Autofluorescence Cytometry Mesenchymal stem cell Microscopy Senescence

Journal

Stem cell reviews and reports
ISSN: 2629-3277
Titre abrégé: Stem Cell Rev Rep
Pays: United States
ID NLM: 101752767

Informations de publication

Date de publication:
27 Aug 2024
Historique:
accepted: 15 08 2024
medline: 27 8 2024
pubmed: 27 8 2024
entrez: 27 8 2024
Statut: aheadofprint

Résumé

To use autofluorescence multispectral imaging (AFMI) to develop a non-invasive assay for the in-depth characterisation of human bone marrow derived mesenchymal stromal cells (hBM-MSCs). hBM-MSCs were imaged by AFMI on gridded dishes, stained for endpoints of interest (STRO-1 positivity, alkaline phosphatase, beta galactosidase, DNA content) then relocated and results correlated. Intensity, texture and morphological features were used to characterise the colour distribution of regions of interest, and canonical discriminant analysis was used to separate groups. Additionally, hBM-MSC lines were cultured to arrest, with AFMI images taken after each passage to investigate whether an assay could be developed for growth potential. STRO-1 positivity could be predicted with a receiver operator characteristic area under the curve (AUC) of 0.67. For spontaneous differentiation this was 0.66, for entry to the cell-cycle it was 0.77 and for senescence it was 0.77. Growth potential (population doublings remaining) was estimated with an RMSPE = 2.296. The Mean Absolute Error of the final prediction model indicated that growth potential could be predicted with an error of ± 1.86 doublings remaining. This non-invasive methodology enabled the in-depth characterisation of hBM-MSCs from a single assay. This approach is advantageous for clinical applications as well as research and stands out for the characterisation of both present status as well as future behaviour. The use of data from five MSC lines with heterogenous AFMI profiles supports potential generalisability.

Identifiants

pubmed: 39190057
doi: 10.1007/s12015-024-10778-4
pii: 10.1007/s12015-024-10778-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Australian Research Council Discovery project
ID : DP170101863
Organisme : Australian Research Council Discovery project
ID : DP210102960
Organisme : Cancer Council NSW
ID : 2021/ECF1291

Informations de copyright

© 2024. The Author(s).

Références

Aggarwal, S., & Pittenger, M. F. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood, 105(4), 1815–1822.
doi: 10.1182/blood-2004-04-1559 pubmed: 15494428
Ren, G., et al. (2008). Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell, 2(2), 141–150.
doi: 10.1016/j.stem.2007.11.014 pubmed: 18371435
Shammaa, R., et al. (2020). Mesenchymal stem cells beyond Regenerative Medicine. Frontiers in Cell and Developmental Biology, 8, 72.
doi: 10.3389/fcell.2020.00072 pubmed: 32133358 pmcid: 7040370
Costa, L. A., et al. (2021). Functional heterogeneity of mesenchymal stem cells from natural niches to culture conditions: Implications for further clinical uses. Cellular and Molecular Life Sciences, 78(2), 447–467.
doi: 10.1007/s00018-020-03600-0 pubmed: 32699947
Siegel, G., et al. (2013). Phenotype, donor age and gender affect function of human bone marrow-derived mesenchymal stromal cells. BMC Medicine, 11, 146.
doi: 10.1186/1741-7015-11-146 pubmed: 23758701 pmcid: 3694028
Wang, J., et al. (2013). Cell therapy with autologous mesenchymal stem cells-how the disease process impacts clinical considerations. Cytotherapy, 15(8), 893–904.
doi: 10.1016/j.jcyt.2013.01.218 pubmed: 23751203
Campbell, J. M., et al. (2021). Ageing human bone marrow mesenchymal stem cells have depleted NAD(P)H and distinct multispectral autofluorescence. Geroscience, 43(2), 859–868.
doi: 10.1007/s11357-020-00250-9 pubmed: 32789662
Sensebe, L., Bourin, P., & Tarte, K. (2011). Good manufacturing practices production of mesenchymal stem/stromal cells. Human Gene Therapy, 22(1), 19–26.
doi: 10.1089/hum.2010.197 pubmed: 21028982
Zhou, X., et al. (2020). Mesenchymal stem cell senescence and rejuvenation: Current Status and challenges. Frontiers in Cell and Developmental Biology, 8, 364.
doi: 10.3389/fcell.2020.00364 pubmed: 32582691 pmcid: 7283395
Yang, Y. K., et al. (2018). Changes in phenotype and differentiation potential of human mesenchymal stem cells aging in vitro. Stem Cell Research & Therapy, 9(1), 131.
doi: 10.1186/s13287-018-0876-3
Wang, Y. H., et al. (2021). Cell heterogeneity, rather than the cell storage solution, affects the behavior of mesenchymal stem cells in vitro and in vivo. Stem Cell Research & Therapy, 12(1), 391.
doi: 10.1186/s13287-021-02450-2
Murgia, A., et al. (2016). Potency Biomarker signature genes from multiparametric osteogenesis assays: Will cGMP Human Bone Marrow Mesenchymal stromal cells make bone? PLoS One, 11(10), e0163629.
doi: 10.1371/journal.pone.0163629 pubmed: 27711115 pmcid: 5053614
Chang, C. C., et al. (2018). Global MicroRNA profiling in human bone marrow skeletal-stromal or mesenchymal-stem cells identified candidates for bone regeneration. Molecular Therapy, 26(2), 593–605.
doi: 10.1016/j.ymthe.2017.11.018 pubmed: 29331291
Graneli, C., et al. (2014). Novel markers of osteogenic and adipogenic differentiation of human bone marrow stromal cells identified using a quantitative proteomics approach. Stem Cell Research, 12(1), 153–165.
doi: 10.1016/j.scr.2013.09.009 pubmed: 24239963
Kowal, J. M., et al. (2020). Single-cell high-content imaging parameters predict functional phenotype of cultured human bone marrow stromal stem cells. Stem Cells Transl Med, 9(2), 189–202.
doi: 10.1002/sctm.19-0171 pubmed: 31758755
Freeman, B. T., Jung, J. P., & Ogle, B. M. (2015). Single-cell RNA-Seq of bone marrow-derived mesenchymal stem cells reveals unique profiles of lineage priming. PLoS One, 10(9), e0136199.
doi: 10.1371/journal.pone.0136199 pubmed: 26352588 pmcid: 4564185
Lu, S., & Qiao, X. (2021). Single-cell profiles of human bone marrow-derived mesenchymal stromal cells after IFN-gamma and TNF-alpha licensing. Gene, 771, 145347.
doi: 10.1016/j.gene.2020.145347 pubmed: 33333228
Sun, C., et al. (2020). Single-cell RNA-seq highlights heterogeneity in human primary Wharton’s jelly mesenchymal stem/stromal cells cultured in vitro. Stem Cell Research & Therapy, 11(1), 149.
doi: 10.1186/s13287-020-01660-4
Campbell, J. M. (2023). Clinical applications of non-invasive multi and hyperspectral imaging of cell and tissue autofluorescence beyond oncology. Journal of Biophotonics,    e202200264.  https://doi.org/10.1002/jbio.202200264
Campbell, J. M., et al. (2019). Non-destructive, label free identification of cell cycle phase in cancer cells by multispectral microscopy of autofluorescence. BMC Cancer, 19(1), 1242.
doi: 10.1186/s12885-019-6463-x pubmed: 31864316 pmcid: 6925881
Campbell, J. M., et al. (2020). Multispectral characterisation of mesenchymal stem/stromal cells: Age, cell cycle, senescence, and pluripotency. LBIS, 11251, 112510F.
Kaluzny, J. (2016). Ex vivo confocal spectroscopy of autofluorescence in age-related macular degeneration. Plos One, 11(9), e0162869.
doi: 10.1371/journal.pone.0162869 pubmed: 27631087 pmcid: 5024989
Asfour, H., et al. (2018). Optimization of wavelength selection for multispectral image acquisition: A case study of atrial ablation lesions. Biomedical Optics Express, 9(5), 2189–2204.
doi: 10.1364/BOE.9.002189 pubmed: 29760980 pmcid: 5946781
Morgan, M. L., et al. (2021). Autofluorescence spectroscopy as a proxy for chronic white matter pathology. Multiple Sclerosis Journal, 27(7), 1046–1056.
doi: 10.1177/1352458520948221 pubmed: 32779553
Campbell, J. M., et al. (2023). Emerging clinical applications in oncology for non-invasive multi and hyperspectral imaging of cell and tissue autoflorescence. Journal of Biophotonics, 16(9), e202300105.
Habibalahi, A., et al. (2020). Non-invasive real-time imaging of reactive oxygen species (ROS) using multispectral auto-fluorescence imaging technique: A novel tool for redox biology. Redox biology.  https://doi.org/10.1101/2020.02.18.955112
Habibalahi, A., et al. (2020). Non-invasive real-time imaging of reactive oxygen species (ROS) using auto-fluorescence multispectral imaging technique: A novel tool for redox biology. Redox Biology, 34, 101561.
doi: 10.1016/j.redox.2020.101561 pubmed: 32526699 pmcid: 7287272
Tong, Y. (2016). Hyperspectral autofluorescence imaging of drusenand retinal pigment epithelium in donor eyes with age-related macular degeneration. Retina, 36 Suppl 1(Suppl 1), S127-s136.
Isenmann, S., et al. (2009). TWIST family of basic helix-loop-helix transcription factors mediate human mesenchymal stem cell growth and commitment. Stem Cells, 27(10), 2457–2468.
doi: 10.1002/stem.181 pubmed: 19609939
Shi, S., & Gronthos, S. (2003). Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. Journal of Bone and Mineral Research, 18(4), 696–704.
doi: 10.1359/jbmr.2003.18.4.696 pubmed: 12674330
Rasti, B., Ulfarsson, M. O., & Ghamisi, P. (2017). Automatic Hyperspectral Image Restoration using sparse and low-rank modeling. IEEE Geoscience and Remote Sensing Letters, 14(12), 2335–2339.
doi: 10.1109/LGRS.2017.2764059
Mahbub, S. B. (2017). Statistically strong label-free quantitative identification of native fluorophores in a biological sample. Scientific Reports, 7(1), 15792.
doi: 10.1038/s41598-017-15952-y pubmed: 29150629 pmcid: 5693869
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671.
doi: 10.1038/nmeth.2089 pubmed: 22930834 pmcid: 5554542
He, H., Bai, Y., Garcia, E. A., & Li, S. (2008). ADASYN: Adaptive synthetic sampling approach for imbalanced learning. In 2008 IEEE international joint conference on neural networks (IEEE world congress on computational intelligence) (pp. 1322–1328). https://doi.org/10.1109/IJCNN.2008.4633969
Peng, H., Long, F., & Ding, C. (2005). Feature selection based on mutual information: Criteria of max-dependency, max-relevance, and min-redundancy. Ieee Transactions on Pattern Analysis and Machine Intelligence, 27(8), 1226–1238.
doi: 10.1109/TPAMI.2005.159 pubmed: 16119262
Jombart, T., Devillard, S., & Balloux, F. (2010). Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. Bmc Genetics, 11, 94.
doi: 10.1186/1471-2156-11-94 pubmed: 20950446 pmcid: 2973851
Cover, T., & Hart, P. (1967). Nearest neighbor pattern classification. IEEE Transactions on Information Theory, 13(1), 21–27.
doi: 10.1109/TIT.1967.1053964
Yu, Z., et al. (2016). Hybrid k -Nearest neighbor classifier. IEEE Transactions on Cybernetics, 46(6), 1263–1275.
doi: 10.1109/TCYB.2015.2443857 pubmed: 26126291
Mandrekar, J. N. (2010). Receiver operating characteristic curve in diagnostic test assessment. Journal of Thoracic Oncology: Official Publication of the International Association for the Study of Lung Cancer, 5(9), 1315–1316.
doi: 10.1097/JTO.0b013e3181ec173d pubmed: 20736804
Tokumitsu, A., Wakitani, S., & Takagi, M. (2009). Noninvasive estimation of cell cycle phase and proliferation rate of human mesenchymal stem cells by phase-shifting laser microscopy. Cytotechnology, 59(3), 161–167.
doi: 10.1007/s10616-009-9209-9 pubmed: 19693683 pmcid: 2774568

Auteurs

Jared M Campbell (JM)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia. j.campbell@unsw.edu.au.

Abbas Habibalahi (A)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Adnan Agha (A)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Shannon Handley (S)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Aline Knab (A)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Xiaohu Xu (X)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Akanksha Bhargava (A)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Zhilin Lei (Z)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Max Mackevicius (M)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Yuan Tian (Y)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Saabah B Mahbub (SB)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Ayad G Anwer (AG)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Stan Gronthos (S)

Mesenchymal Stem Cell Laboratory, School of Biomedicine, Faculty of Health and Medical Sciences, University of Adelaide, Adelaide, South Australia, 5000, Australia.
South Australian Health and Medical Research Institute, Adelaide, South Australia, 5000, Australia.

Sharon Paton (S)

Mesenchymal Stem Cell Laboratory, School of Biomedicine, Faculty of Health and Medical Sciences, University of Adelaide, Adelaide, South Australia, 5000, Australia.
South Australian Health and Medical Research Institute, Adelaide, South Australia, 5000, Australia.

Shane T Grey (ST)

Garvan Institute of Medical Research, Darlinghurst, New South Wales, Australia.
Faculty of Medicine, University of New South Wales, Sydney, New South Wales, Australia.

Lindsay Wu (L)

School of Biomedical Sciences, UNSW Sydney, Sydney, NSW, Australia.

Robert B Gilchrist (RB)

School of Clinical Medicine, UNSW Sydney, Sydney, NSW, Australia.

Ewa M Goldys (EM)

Graduate School of Biomedical Engineering, University of New South Wales, Sydney, NSW, 2052, Australia.

Classifications MeSH