Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Adipocyte and Cell Biology

The capacity of differentiation of stromal vascular fraction cells into beige adipocytes is markedly reduced in subjects with overweight/obesity and insulin resistance: effect of genistein

International Journal of Obesity volume 45, pages 2471–2481 (2021)Cite this article

Subjects

A Correction to this article was published on 09 March 2022

This article has been updated

Abstract

Background

Dietary bioactive compounds have been demonstrated to produce several health benefits. Genistein, an isoflavone of soy protein, and resveratrol, a polyphenol from grapes, have been shown to improve insulin sensitivity and to stimulate white adipose tissue (WAT) browning, leading to increased energy expenditure. However, it has not been demonstrated in humans whether genistein or resveratrol have the capacity to stimulate the differentiation of stromal vascular fraction (SVF) cells from white fat into beige adipocytes.

Subjects/methods

With this aim, we assessed whether stromal vascular fraction cells obtained from biopsies of the subdermal fat depots of subjects with normal body weight (NW) or from subjects with overweight/obesity with (OIR) or without (OIS) insulin resistance were able to differentiate into the beige adipose tissue lineage in vitro, by exposing the cells to genistein, resveratrol, or the combination of both.

Results

The results showed that SVF cells obtained from NW or OIS subjects were able to differentiate into beige adipocytes according to an increased expression of beige biomarkers including UCP1, PDRM-16, PGC1α, CIDEA, and SHOX2 upon exposure to genistein. However, SVF cells from OIR subjects were unable to differentiate into beige adipocytes with any of the inducers. Exposure to resveratrol or the combination of resveratrol/genistein did not significantly stimulate the expression of browning markers in any of the groups studied. We found that the non-responsiveness of the SVF from subjects with obesity and insulin resistance to any of the inducers was associated with an increase in the expression of endoplasmic reticulum stress markers.

Conclusion

Consumption of genistein may stimulate WAT browning mainly in NW or OIS subjects. Thus, obesity associated with insulin resistance may be considered as a condition that prevents some beneficial effects of some dietary bioactive compounds.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Overweight/obesity and insulin resistance inhibit the browning process of SVF cells upon pioglitazone/T3 treatment.
Fig. 2: Effect of pioglitazone/T3 and genistein on protein expression of adipocyte beige/brite markers in SVF cells.
Fig. 3: Genistein promotes browning of human SVF cells from subcutaneous fat and its effects are blunted by overweight/obesity and insulin resistance.
Fig. 4: Resveratrol has a mild effect on SVF cell browning and prevents the stimulatory effect of Genistein.
Fig. 5: Principal component analysis.

Similar content being viewed by others

Change history

References

  1. Taylor VH, Forhan M, Vigod SN, McIntyre RS, Morrison KM. The impact of obesity on quality of life. Best Pract Res Clin Endocrinol Metab. 2013;27:139–46.

    Article  PubMed  Google Scholar 

  2. Choe SS, Huh JY, Hwang IJ, Kim JI, Kim JB. Adipose tissue remodeling: its role in energy metabolism and metabolic disorders. Front Endocrinol. 2016;7:30.

    Article  Google Scholar 

  3. Sethi JK, Vidal-Puig AJ. Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J Lipid Res. 2007;48:1253–62.

    Article  CAS  PubMed  Google Scholar 

  4. Vargas-Castillo A, Fuentes-Romero R, Rodriguez-Lopez LA, Torres N, Tovar AR. Understanding the biology of thermogenic fat: is browning a new approach to the treatment of obesity? Arch Med Res. 2017;48:401–13.

    Article  CAS  PubMed  Google Scholar 

  5. Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M, Kristiansen K, et al. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am J Physiol Endocrinol Metab. 2010;298:E1244–53.

    Article  CAS  PubMed  Google Scholar 

  6. Wu J, Cohen P, Spiegelman BM. Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev. 2013;27:234–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Granneman JG, Burnazi M, Zhu Z, Schwamb LA. White adipose tissue contributes to UCP1-independent thermogenesis. Am J Physiol Endocrinol Metab. 2003;285:E1230–6.

    Article  CAS  PubMed  Google Scholar 

  8. Ikeda K, Kang Q, Yoneshiro T, Camporez JP, Maki H, Homma M, et al. UCP1-independent signaling involving SERCA2b-mediated calcium cycling regulates beige fat thermogenesis and systemic glucose homeostasis. Nat Med. 2017;23:1454–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Nedergaard J, Cannon B. The browning of white adipose tissue: some burning issues. Cell Metab. 2014;20:396–407.

    Article  CAS  PubMed  Google Scholar 

  10. Wang W, Seale P. Control of brown and beige fat development. Nat Rev Mol Cell Biol. 2016;17:691–702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Wu Y, Kinnebrew MA, Kutyavin VI, Chawla A. Distinct signaling and transcriptional pathways regulate peri-weaning development and cold-induced recruitment of beige adipocytes. Proc Natl Acad Sci U S A. 2020;117:6883–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kim HJ, Choi EJ, Kim HS, Choi CW, Choi SW, Kim SL, et al. Germinated soy germ extract ameliorates obesity through beige fat activation. Food Funct. 2019;10:836–48.

    Article  CAS  PubMed  Google Scholar 

  13. Wu L, Zhang L, Li B, Jiang H, Duan Y, Xie Z, et al. AMP-activated protein kinase (AMPK) regulates energy metabolism through modulating thermogenesis in adipose tissue. Front Physiol. 2018;9:122.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Zou T, Wang B, Li S, Liu Y, You J. Dietary apple polyphenols promote fat browning in high-fat diet-induced obese mice through activation of adenosine monophosphate-activated protein kinase alpha. J Sci Food Agric. 2020;100:2389–98.

    Article  CAS  PubMed  Google Scholar 

  15. Bartelt A, Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol. 2014;10:24–36.

    Article  CAS  PubMed  Google Scholar 

  16. Fernandez-Verdejo R, Marlatt KL, Ravussin E, Galgani JE. Contribution of brown adipose tissue to human energy metabolism. Mol Aspects Med. 2019;68:82–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Longo M, Spinelli R, D’Esposito V, Zatterale F, Fiory F, Nigro C, et al. Pathologic endoplasmic reticulum stress induced by glucotoxic insults inhibits adipocyte differentiation and induces an inflammatory phenotype. Biochim Biophys Acta. 2016;1863:1146–56.

    Article  CAS  PubMed  Google Scholar 

  18. Shimada T, Hiramatsu N, Okamura M, Hayakawa K, Kasai A, Yao J, et al. Unexpected blockade of adipocyte differentiation by K-7174: implication for endoplasmic reticulum stress. Biochem Biophys Res Commun. 2007;363:355–60.

    Article  CAS  PubMed  Google Scholar 

  19. Cnop M, Foufelle F, Velloso LA. Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med. 2012;18:59–68.

    Article  CAS  PubMed  Google Scholar 

  20. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004;306:457–61.

    Article  PubMed  Google Scholar 

  21. Grossini E, Farruggio S, Raina G, Mary D, Deiro G, Gentilli S. Effects of genistein on differentiation and viability of human visceral adipocytes. Nutrients. 2018;10:1–18.

    Article  Google Scholar 

  22. Wang S, Liang X, Yang Q, Fu X, Rogers CJ, Zhu M, et al. Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) alpha1. Int J Obes. 2015;39:967–76.

    Article  CAS  Google Scholar 

  23. Zou T, Chen D, Yang Q, Wang B, Zhu MJ, Nathanielsz PW, et al. Resveratrol supplementation of high-fat diet-fed pregnant mice promotes brown and beige adipocyte development and prevents obesity in male offspring. J Physiol. 2017;595:1547–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mendez-del Villar M, Gonzalez-Ortiz M, Martinez-Abundis E, Perez-Rubio KG, Lizarraga-Valdez R. Effect of resveratrol administration on metabolic syndrome, insulin sensitivity, and insulin secretion. Metab Syndr Relat Disord. 2014;12:497–501.

    Article  CAS  PubMed  Google Scholar 

  25. Konings E, Timmers S, Boekschoten MV, Goossens GH, Jocken JW, Afman LA, et al. The effects of 30 days resveratrol supplementation on adipose tissue morphology and gene expression patterns in obese men. Int J Obes. 2014;38:470–3.

    Article  CAS  Google Scholar 

  26. Lan F, Weikel KA, Cacicedo JM, Ido Y. Resveratrol-induced AMP-activated protein kinase activation is cell-type dependent: lessons from basic research for clinical application. Nutrients. 2017;9:1–14.

    Article  Google Scholar 

  27. Carey AL, Vorlander C, Reddy-Luthmoodoo M, Natoli AK, Formosa MF, Bertovic DA, et al. Reduced UCP-1 content in in vitro differentiated beige/brite adipocytes derived from preadipocytes of human subcutaneous white adipose tissues in obesity. PLoS ONE. 2014;9:e91997.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol. 2008;9:367–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.

    Article  CAS  PubMed  Google Scholar 

  30. World Health Organization. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organization Technical Report Series, vol. 894. World Health Organization. Geneva, Switzerland; 2000. p. i–xii, 1–253.

  31. Mehlem A, Hagberg CE, Muhl L, Eriksson U, Falkevall A. Imaging of neutral lipids by oil red O for analyzing the metabolic status in health and disease. Nat Protoc. 2013;8:1149–54.

    Article  PubMed  Google Scholar 

  32. Galgani JE, Moro C, Ravussin E. Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab. 2008;295:E1009–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wosnitza M, Hemmrich K, Groger A, Graber S, Pallua N. Plasticity of human adipose stem cells to perform adipogenic and endothelial differentiation. Differentiation. 2007;75:12–23.

    Article  CAS  PubMed  Google Scholar 

  34. Loh RKC, Formosa MF, Eikelis N, Bertovic DA, Anderson MJ, Barwood SA, et al. Pioglitazone reduces cold-induced brown fat glucose uptake despite induction of browning in cultured human adipocytes: a randomised, controlled trial in humans. Diabetologia. 2018;61:220–30.

    Article  CAS  PubMed  Google Scholar 

  35. Palacios-Gonzalez B, Vargas-Castillo A, Velazquez-Villegas LA, Vasquez-Reyes S, Lopez P, Noriega LG, et al. Genistein increases the thermogenic program of subcutaneous WAT and increases energy expenditure in mice. J Nutr Biochem. 2019;68:59–68.

    Article  CAS  PubMed  Google Scholar 

  36. Yuliana A, Daijo A, Jheng HF, Kwon J, Nomura W, Takahashi H, et al. Endoplasmic reticulum stress impaired uncoupling protein 1 expression via the suppression of peroxisome proliferator-activated receptor gamma binding activity in mice beige adipocytes. Int J Mol Sci. 2019;20:1–15.

    Article  Google Scholar 

  37. Cuthbertson DJ, Steele T, Wilding JP, Halford JC, Harrold JA, Hamer M, et al. What have human experimental overfeeding studies taught us about adipose tissue expansion and susceptibility to obesity and metabolic complications? Int J Obes. 2017;41:853–65.

    Article  CAS  Google Scholar 

  38. Kyrou I, Chrousos GP, Tsigos C. Stress, visceral obesity, and metabolic complications. Ann N Y Acad Sci. 2006;1083:77–110.

    Article  CAS  PubMed  Google Scholar 

  39. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature. 2006;444:840–6.

    Article  CAS  PubMed  Google Scholar 

  40. Karpe F, Dickmann JR, Frayn KN. Fatty acids, obesity, and insulin resistance: time for a reevaluation. Diabetes. 2011;60:2441–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Qatanani M, Lazar MA. Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev. 2007;21:1443–55.

    Article  CAS  PubMed  Google Scholar 

  42. Vazquez-Vela ME, Torres N, Tovar AR. White adipose tissue as endocrine organ and its role in obesity. Arch Med Res. 2008;39:715–28.

    Article  CAS  PubMed  Google Scholar 

  43. Hutley LJ, Herington AC, Shurety W, Cheung C, Vesey DA, Cameron DP, et al. Human adipose tissue endothelial cells promote preadipocyte proliferation. Am J Physiol Endocrinol Metab. 2001;281:E1037–44.

    Article  CAS  PubMed  Google Scholar 

  44. Rodriguez AM, Elabd C, Delteil F, Astier J, Vernochet C, Saint-Marc P, et al. Adipocyte differentiation of multipotent cells established from human adipose tissue. Biochem Biophys Res Commun. 2004;315:255–63.

    Article  CAS  PubMed  Google Scholar 

  45. Kajimura S, Spiegelman BM, Seale P. Brown and beige fat: physiological roles beyond heat generation. Cell Metab. 2015;22:546–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Shabalina IG, Petrovic N, de Jong JM, Kalinovich AV, Cannon B, Nedergaard J. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 2013;5:1196–203.

    Article  CAS  PubMed  Google Scholar 

  47. Azhar Y, Parmar A, Miller CN, Samuels JS, Rayalam S. Phytochemicals as novel agents for the induction of browning in white adipose tissue. Nutr Metab. 2016;13:89.

    Article  Google Scholar 

  48. Arzola-Paniagua MA, Garcia-Salgado Lopez ER, Calvo-Vargas CG, Guevara-Cruz M. Efficacy of an orlistat-resveratrol combination for weight loss in subjects with obesity: a randomized controlled trial. Obesity. 2016;24:1454–63.

    Article  CAS  PubMed  Google Scholar 

  49. Faghihzadeh F, Adibi P, Rafiei R, Hekmatdoost A. Resveratrol supplementation improves inflammatory biomarkers in patients with nonalcoholic fatty liver disease. Nutr Res. 2014;34:837–43.

    Article  CAS  PubMed  Google Scholar 

  50. Poulsen MM, Vestergaard PF, Clasen BF, Radko Y, Christensen LP, Stodkilde-Jorgensen H, et al. High-dose resveratrol supplementation in obese men: an investigator-initiated, randomized, placebo-controlled clinical trial of substrate metabolism, insulin sensitivity, and body composition. Diabetes. 2013;62:1186–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Timmers S, Konings E, Bilet L, Houtkooper RH, van de Weijer T, Goossens GH, et al. Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab. 2011;14:612–22.

    Article  CAS  PubMed  Google Scholar 

  52. Chachay VS, Macdonald GA, Martin JH, Whitehead JP, O’Moore-Sullivan TM, Lee P, et al. Resveratrol does not benefit patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2014;12:2092–103.e1–6.

    Article  CAS  PubMed  Google Scholar 

  53. Yoshino J, Conte C, Fontana L, Mittendorfer B, Imai S, Schechtman KB, et al. Resveratrol supplementation does not improve metabolic function in nonobese women with normal glucose tolerance. Cell Metab. 2012;16:658–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Alberdi G, Rodriguez VM, Miranda J, Macarulla MT, Churruca I, Portillo MP. Thermogenesis is involved in the body-fat lowering effects of resveratrol in rats. Food Chem. 2013;141:1530–5.

    Article  CAS  PubMed  Google Scholar 

  55. Asnani-Kishnani M, Rodriguez AM, Serrano A, Palou A, Bonet ML, Ribot J. Neonatal resveratrol and nicotinamide riboside supplementations sex-dependently affect beige transcriptional programming of preadipocytes in mouse adipose tissue. Front Physiol. 2019;10:83.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Aziz SA, Wakeling LA, Miwa S, Alberdi G, Hesketh JE, Ford D. Metabolic programming of a beige adipocyte phenotype by genistein. Mol Nutr Food Res. 2017;61:1–10.

    Article  Google Scholar 

  57. Zhang M, Ikeda K, Xu JW, Yamori Y, Gao XM, Zhang BL. Genistein suppresses adipogenesis of 3T3-L1 cells via multiple signal pathways. Phytother Res. 2009;23:713–8.

    Article  CAS  PubMed  Google Scholar 

  58. Contreras C, Gonzalez-Garcia I, Seoane-Collazo P, Martinez-Sanchez N, Linares-Pose L, Rial-Pensado E, et al. Reduction of hypothalamic endoplasmic reticulum stress activates browning of white fat and ameliorates obesity. Diabetes. 2017;66:87–99.

    Article  CAS  PubMed  Google Scholar 

  59. Onate B, Vilahur G, Ferrer-Lorente R, Ybarra J, Diez-Caballero A, Ballesta-Lopez C, et al. The subcutaneous adipose tissue reservoir of functionally active stem cells is reduced in obese patients. FASEB J. 2012;26:4327–36.

    Article  CAS  PubMed  Google Scholar 

  60. Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Peault B, Rubin JP, et al. Stromal vascular progenitors in adult human adipose tissue. Cytometry A. 2010;77:22–30.

    PubMed  PubMed Central  Google Scholar 

  61. Banyard DA, Sarantopoulos CN, Borovikova AA, Qiu X, Wirth GA, Paydar KZ, et al. Phenotypic analysis of stromal vascular fraction after mechanical shear reveals stress-induced progenitor populations. Plast Reconstr Surg. 2016;138:237e–47e.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kim WS, Park BS, Kim HK, Park JS, Kim KJ, Choi JS, et al. Evidence supporting antioxidant action of adipose-derived stem cells: protection of human dermal fibroblasts from oxidative stress. J Dermatol Sci. 2008;49:133–42.

    Article  CAS  PubMed  Google Scholar 

  63. Torre-Villalvazo I, Bunt AE, Aleman G, Marquez-Mota CC, Diaz-Villasenor A, Noriega LG, et al. Adiponectin synthesis and secretion by subcutaneous adipose tissue is impaired during obesity by endoplasmic reticulum stress. J Cell Biochem. 2018;119:5970–84.

    Article  CAS  PubMed  Google Scholar 

  64. Boden G, Duan X, Homko C, Molina EJ, Song W, Perez O, et al. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes. 2008;57:2438–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Hotamisligil GS. Inflammation and endoplasmic reticulum stress in obesity and diabetes. Int J Obes. 2008;32 Suppl 7:S52–4.

    Article  CAS  Google Scholar 

  66. Sage AT, Holtby-Ottenhof S, Shi Y, Damjanovic S, Sharma AM, Werstuck GH. Metabolic syndrome and acute hyperglycemia are associated with endoplasmic reticulum stress in human mononuclear cells. Obesity. 2012;20:748–55.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Council of Science and Technology Mexico (CONACYT) (Grant Number 261843 to ART) and supported by the National Institute of Medical Sciences and Nutrition S.Z. Leonardo Rodriguez-López received a CONACYT scholarship for the Basic Biomedical Research program (Investigacion Biomedica Basica), UNAM.

Author information

Authors and Affiliations

  1. Department of Physiology of Nutrition, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México CDMX, México

    Leonardo A. Rodriguez-López, Ivan Torre-Villalvazo, Gabriela Aleman-Escondrillas, Adriana Flores-López, Martha Guevara-Cruz, Mónica Sánchez-Tapia, Erik A. Torre-Anaya, Sarai Vasquez-Reyes, Nimbe Torres & Armando R. Tovar

  2. Tissue Engineering, Cell Therapy and Regenerative Medicine Unit, Instituto Nacional de Rehabilitacion Luis Guillermo Ibarra Ibarra, México CDMX, México

    Valentín Martínez-López

  3. Department Experimental Surgery, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México CDMX, México

    Gonzalo M. Torres-Villalobos

  4. Instituto de Neurobiología, Universidad Nacional Autónoma de México, Juriquilla, Mexico

    Yazmín Macotela

Authors
  1. Leonardo A. Rodriguez-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivan Torre-Villalvazo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriela Aleman-Escondrillas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adriana Flores-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martha Guevara-Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mónica Sánchez-Tapia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Erik A. Torre-Anaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Valentín Martínez-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sarai Vasquez-Reyes
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gonzalo M. Torres-Villalobos
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yazmín Macotela
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Nimbe Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Armando R. Tovar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LAR-L: experimental work and analysis; IT-V: experimental design; GA-E: experimental work and writing; AF-L and MG-C: clinical and experimental work; MS-T, EAT-A, VM-L, and SV-R: experimental work; GMT-V: surgical process; YM: data analysis; NT: experimental design and writing; ART: experimental concept, design, analysis, and writing.

Corresponding author

Correspondence to Armando R. Tovar.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodriguez-López, L.A., Torre-Villalvazo, I., Aleman-Escondrillas, G. et al. The capacity of differentiation of stromal vascular fraction cells into beige adipocytes is markedly reduced in subjects with overweight/obesity and insulin resistance: effect of genistein. Int J Obes 45, 2471–2481 (2021). https://doi.org/10.1038/s41366-021-00921-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-021-00921-3

Search

Advanced search

Quick links