Free Fatty Acids from Type 2 Diabetes Mellitus Serum Remodel Mesenchymal Stem Cell Lipids, Hindering Differentiation into Primordial Germ Cells.
Diabetes Mellitus
Fatty Acids
Germ Cells
Mesenchymal Stem Cells
Phospholipids
Triglycerides
Journal
Applied biochemistry and biotechnology
ISSN: 1559-0291
Titre abrégé: Appl Biochem Biotechnol
Pays: United States
ID NLM: 8208561
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
accepted:
21
10
2022
medline:
4
5
2023
pubmed:
11
12
2022
entrez:
10
12
2022
Statut:
ppublish
Résumé
Type 2 diabetes mellitus (T2DM) adversely affects the essential characteristics of adipose tissue-derived mesenchymal stem cells (AdMSCs). Given that T2DM is associated with an altered serum free fatty acid (FFA) profile, we examined whether diabetic serum FFAs influence the viability, differentiation, and fatty acid composition of the major lipid fractions of human AdMSCs in vitro. Serum FFAs were isolated from 7 diabetic and 10 healthy nondiabetic female individuals. AdMSCs were cultured and differentiated into primordial germ cell-like cells (PGCLCs) in the presence of either diabetic or nondiabetic FFAs. Cell viability was assessed using trypan blue staining. Cell differentiation was evaluated by measuring the PGCLC transcriptional markers Blimp1 and Stella. Lipid fractionation and fatty acid quantification were performed using thin-layer chromatography and gas-liquid chromatography, respectively. Both diabetic and nondiabetic FFAs significantly reduced the viability of PGCLCs. The gene expression of both differentiation markers was significantly lower in cells exposed to diabetic FFAs than in those treated with nondiabetic FFAs. Saturated fatty acids were significantly increased and linoleic acid was significantly decreased in the cellular phospholipid fraction after exposure to diabetic FFAs. In contrast, monounsaturated fatty acids were reduced and linoleic acid was elevated in the cellular triglyceride fraction in response to diabetic FFAs. Such an altered serum FFA profile in patients with T2DM reduces the proliferation and differentiation potential of AdMSCs, presumably due to the aberrant distribution of fatty acids into cell phospholipids and triglycerides.
Identifiants
pubmed: 36495376
doi: 10.1007/s12010-022-04204-z
pii: 10.1007/s12010-022-04204-z
doi:
Substances chimiques
Fatty Acids, Nonesterified
0
Fatty Acids
0
Linoleic Acids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3011-3026Subventions
Organisme : Tabriz University of Medical Sciences
ID : 59420
Organisme : Tabriz University of Medical Sciences
ID : 66852
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Roden, M., & Shulman, G. I. (2019). The integrative biology of type 2 diabetes. Nature, 576(7785), 51–60.
pubmed: 31802013
doi: 10.1038/s41586-019-1797-8
Association, A. D. (2014). Diagnosis and classification of diabetes mellitus. Diabetes care, 37(Supplement_1), S81–S90.
doi: 10.2337/dc14-S081
Deshpande, A. D., Harris-Hayes, M., & Schootman, M. (2008). Epidemiology of diabetes and diabetes-related complications. Physical therapy, 88(11), 1254–1264.
pubmed: 18801858
pmcid: 3870323
doi: 10.2522/ptj.20080020
Guariguata, L., et al. (2011). The International Diabetes Federation diabetes atlas methodology for estimating global and national prevalence of diabetes in adults. Diabetes research and clinical practice, 94(3), 322–332.
pubmed: 22100977
doi: 10.1016/j.diabres.2011.10.040
Thong, E. P., et al. (2020). Diabetes: A metabolic and reproductive disorder in women. The Lancet Diabetes & Endocrinology, 8(2), 134–149.
doi: 10.1016/S2213-8587(19)30345-6
Vander Borght, M., & Wyns, C. (2018). Fertility and infertility: Definition and epidemiology. Clinical biochemistry, 62, 2–10.
pubmed: 29555319
doi: 10.1016/j.clinbiochem.2018.03.012
Fayezi, S., et al. (2018). Primary Culture of Human Cumulus Cells Requires Stearoyl-Coenzyme A Desaturase 1 Activity for Steroidogenesis and Enhancing Oocyte In Vitro Maturation. Reproductive Sciences, 25(6), 844–853.
pubmed: 28345489
doi: 10.1177/1933719117698578
Cena, H., Chiovato, L., & Nappi, R. E. (2020). Obesity, polycystic ovary syndrome, and infertility: A new avenue for GLP-1 receptor agonists. The Journal of Clinical Endocrinology & Metabolism, 105(8), e2695–e2709.
doi: 10.1210/clinem/dgaa285
Broughton, D. E., & Moley, K. H. (2017). Obesity and female infertility: Potential mediators of obesity’s impact. Fertility and sterility, 107(4), 840–847.
pubmed: 28292619
doi: 10.1016/j.fertnstert.2017.01.017
Jungheim, E. S., & Moley, K. H. (2010). Current knowledge of obesity’s effects in the pre-and periconceptional periods and avenues for future research. American journal of obstetrics and gynecology, 203(6), 525–530.
pubmed: 20739012
pmcid: 3718032
doi: 10.1016/j.ajog.2010.06.043
Mehdizadeh, A., et al. (2011). Correlation between the level of cholesteryl ester transfer protein in follicular fluid with fertilization rates in IVF/ ICSI cycles. Iranian Journal of Reproductive Medicine, 9(3), 193–198.
pubmed: 26396563
pmcid: 4575753
Baksh, D., Song, L., & Tuan, R. S. (2004). Adult mesenchymal stem cells: Characterization, differentiation, and application in cell and gene therapy. Journal of cellular and molecular medicine, 8(3), 301–316.
pubmed: 15491506
pmcid: 6740223
doi: 10.1111/j.1582-4934.2004.tb00320.x
Goenka, V., et al. (2020). Therapeutic potential of mesenchymal stem cells in treating both types of diabetes mellitus and associated diseases. Journal of Diabetes & Metabolic Disorders, 19(2), 1979–1993.
doi: 10.1007/s40200-020-00647-5
Horwitz, E. M., Andreef, M., & Frassoni, F. (2006). Mesenchymal stromal cells. Current opinion in hematology, 13(6), 419.
pmcid: 3365862
doi: 10.1097/01.moh.0000245697.54887.6f
Kariminekoo, S., et al. (2016). Implications of mesenchymal stem cells in regenerative medicine. Artificial cells, nanomedicine, and biotechnology, 44(3), 749–757.
pubmed: 26757594
doi: 10.3109/21691401.2015.1129620
Smith, A. N., et al. (2012). Unsaturated fatty acids induce mesenchymal stem cells to increase secretion of angiogenic mediators. Journal of cellular physiology, 227(9), 3225–3233.
pubmed: 22105830
pmcid: 3305849
doi: 10.1002/jcp.24013
Lupette, J., & Benning, C. (2020). Human health benefits of very-long-chain polyunsaturated fatty acids from microalgae. Biochimie, 178, 15–25.
pubmed: 32389760
doi: 10.1016/j.biochi.2020.04.022
Hirano, T. (2018). Pathophysiology of diabetic dyslipidemia. Journal of Atherosclerosis and Thrombosis, 25(9), 771–782.
Seigneur, M., et al. (1994). Serum fatty acid profiles in type I and type II diabetes: Metabolic alterations of fatty acids of the main serum lipids. Diabetes research and clinical practice, 23(3), 169–177.
pubmed: 7924877
doi: 10.1016/0168-8227(94)90101-5
Hosseini, V., et al. (2021). A small molecule modulating monounsaturated fatty acids and Wnt signaling confers maintenance to induced pluripotent stem cells against endodermal differentiation. Stem Cell Research & Therapy, 12(1), 550.
doi: 10.1186/s13287-021-02617-x
Sessler, A. M., & Ntambi, J. M. (1998). Polyunsaturated fatty acid regulation of gene expression. The Journal of nutrition, 128(6), 923–926.
pubmed: 9614148
doi: 10.1093/jn/128.6.923
Fayyazpour, P., et al. (2022). Fatty acids of type 2 diabetic serum decrease the stemness properties of human adipose derived mesenchymal stem cells. Journal of Cellular Biochemistry, 123(7), 1157–1170.
Kim, K., et al. (2019). Associations between preconception plasma fatty acids and pregnancy outcomes. Epidemiology (Cambridge, Mass.), 30(Suppl 2), S37.
pubmed: 31569151
doi: 10.1097/EDE.0000000000001066
Zarezadeh, R., et al. (2021). Fatty acids of follicular fluid phospholipids and triglycerides display distinct association with IVF outcomes. Reproductive BioMedicine Online, 42(2), 301–309.
pubmed: 33279420
doi: 10.1016/j.rbmo.2020.09.024
Maharlouei, N., et al. (2021). Prevalence and pattern of infertility in Iran: A systematic review and meta-analysis study. Women’s Health Bulletin, 8(2), 63–71.
Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian journal of biochemistry and physiology, 37(8), 911–917.
pubmed: 13671378
doi: 10.1139/o59-099
Alizadeh, E., et al. (2016). The effect of dimethyl sulfoxide on hepatic differentiation of mesenchymal stem cells. Artificial cells, nanomedicine, and biotechnology, 44(1), 157–164.
pubmed: 24978442
doi: 10.3109/21691401.2014.928778
Shirzeily, M. H., et al. (2013). Comparison of differentiation potential of male mouse adipose tissue and bone marrow derived-mesenchymal stem cells into germ cells. Iranian journal of reproductive medicine, 11(12), 965.
Lepage, G., & Roy, C. C. (1986). Direct transesterification of all classes of lipids in a one-step reaction. Journal of lipid research, 27(1), 114–120.
pubmed: 3958609
doi: 10.1016/S0022-2275(20)38861-1
Qi, Y., et al. (2019). Applicability of adipose-derived mesenchymal stem cells in treatment of patients with type 2 diabetes. Stem cell research & therapy, 10(1), 1–13.
doi: 10.1186/s13287-019-1362-2
Horiguchi, M., et al. (2021). Characterizing the degeneration of nuclear membrane and mitochondria of adipose-derived mesenchymal stem cells from patients with type II diabetes. Journal of Cellular and Molecular Medicine, 25(9), 4298–4306.
pubmed: 33759360
pmcid: 8093988
doi: 10.1111/jcmm.16484
Alicka, M., et al. (2019). Adipose-derived mesenchymal stem cells isolated from patients with type 2 diabetes show reduced “stemness” through an altered secretome profile, impaired anti-oxidative protection, and mitochondrial dynamics deterioration. Journal of Clinical Medicine, 8(6), 765.
pubmed: 31151180
pmcid: 6617220
doi: 10.3390/jcm8060765
Abu-Shahba, N., et al. (2021). Impact of type 2 diabetes mellitus on the immunoregulatory characteristics of adipose tissue-derived mesenchymal stem cells. The international journal of biochemistry & cell biology, 140, 106072.
doi: 10.1016/j.biocel.2021.106072
Sobczak, A. I. S., Blindauer, C. A., & Stewart, A. J. (2019). Changes in plasma free fatty acids associated with type-2 diabetes. Nutrients, 11(9), 2022.
doi: 10.3390/nu11092022
Ma, Y., et al. (2021). Potential biomarker in serum for predicting susceptibility to type 2 diabetes mellitus: Free fatty acid 22: 6. Journal of diabetes investigation, 12(6), 950–962.
pubmed: 33068491
doi: 10.1111/jdi.13443
Sobczak, A. I., et al. (2021). Lipidomic profiling of plasma free fatty acids in type-1 diabetes highlights specific changes in lipid metabolism. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1866(1), 158823.
pubmed: 33010452
Chandra, K., et al. (2020). Effect of augmented glycation in mobilization of plasma free fatty acids in type 2 diabetes mellitus. Diabetes & Metabolic Syndrome: Clinical Research & Reviews, 14(5), 1385–1389.
doi: 10.1016/j.dsx.2020.07.028
Lu, J., et al. (2012). Palmitate causes endoplasmic reticulum stress and apoptosis in human mesenchymal stem cells: Prevention by AMPK activator. Endocrinology, 153(11), 5275–5284.
pubmed: 22968644
doi: 10.1210/en.2012-1418
Gillet, C., et al. (2015). Oleate abrogates palmitate-induced lipotoxicity and proinflammatory response in human bone marrow-derived mesenchymal stem cells and osteoblastic cells. Endocrinology, 156(11), 4081–4093.
pubmed: 26327577
doi: 10.1210/en.2015-1303
Yaghooti, H., Mohammadtaghvaei, N., & Mahboobnia, K. (2019). Effects of palmitate and astaxanthin on cell viability and proinflammatory characteristics of mesenchymal stem cells. International Immunopharmacology, 68, 164–170.
pubmed: 30639962
doi: 10.1016/j.intimp.2018.12.063
Qu, B., et al. (2018). MiR-449 overexpression inhibits osteogenic differentiation of bone marrow mesenchymal stem cells via suppressing Sirt1/Fra-1 pathway in high glucose and free fatty acids microenvironment. Biochemical and biophysical research communications, 496(1), 120–126.
pubmed: 29305863
doi: 10.1016/j.bbrc.2018.01.009
Qu, B., et al. (2020). MiR-155 inhibition alleviates suppression of osteoblastic differentiation by high glucose and free fatty acids in human bone marrow stromal cells by upregulating SIRT1. Pflügers Archiv-European Journal of Physiology, 472(4), 473–480.
pubmed: 32248286
doi: 10.1007/s00424-020-02372-7
Kang, J. X., Wan, J. B., & He, C. (2014). Concise review: Regulation of stem cell proliferation and differentiation by essential fatty acids and their metabolites. Stem Cells, 32(5), 1092–1098.
pubmed: 24356924
doi: 10.1002/stem.1620
Wiesenfeld, P. W., Babu, U. S., & O’Donnell, M. W. (2001). Effect of long-chain fatty acids in the culture medium on fatty acid composition of WEHI-3 and J774A. 1 cells. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 128(1), 123–134.
doi: 10.1016/S1096-4959(00)00305-5
Huot, P. S., Sarkar, B., & Ma, D. W. (2010). Conjugated linoleic acid alters caveolae phospholipid fatty acid composition and decreases caveolin-1 expression in MCF-7 breast cancer cells. Nutrition research, 30(3), 179–185.
pubmed: 20417878
doi: 10.1016/j.nutres.2010.02.003
Zhang, C., et al. (2015). Growth inhibitory effect of polyunsaturated fatty acids (PUFAs) on colon cancer cells via their growth inhibitory metabolites and fatty acid composition changes. PLoS ONE, 10(4), e0123256.
pubmed: 25886460
pmcid: 4401647
doi: 10.1371/journal.pone.0123256
Belal, S. A., et al. (2019). Effect of long chain fatty acids on triacylglycerol accumulation, fatty acid composition and related gene expression in primary cultured bovine satellite cells. Animal Biotechnology, 30(4), 323–331.
pubmed: 30179065
doi: 10.1080/10495398.2018.1496925
Weijers, R. N. (2015). Membrane flexibility, free fatty acids, and the onset of vascular and neurological lesions in type 2 diabetes. Journal of Diabetes & Metabolic Disorders, 15(1), 1–8.
doi: 10.1186/s40200-016-0235-9
Song, Y., & Jensen, M. D. (2021). Red blood cell triglycerides—a unique pool that incorporates plasma-free fatty acids and relates to metabolic health. Journal of Lipid Research, 62, 100131.