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Effect of Lemon Verbena Polyphenol on Glycerol Channel Aquaporin 7 Expression in 3T3-L1 Adipocytes

Year 2024, Volume: 14 Issue: 2, 102 - 109, 26.08.2024
https://doi.org/10.26650/experimed.1479944

Abstract

Objective: Polyphenols are of great interest in obesity prevention approaches. The aquaglyceroporin 7 (AQP7) channel is involved in the transport of glycerol across cell membranes in adipose tissue. This study aimed to explore how lemon verbena (LV) polyphenols affect the expression of the glycerol channels AQP7 and perilipin 1 (PLIN1) in 3T3-L1 hypertrophic adipocytes.
Materials and Methods: Hypertrophic adipocyte cells (H) were treated with LV at two different doses of 200 µg/mL (H-LV200) and 400 µg/mL (H-LV400). In addition, 0.1 µM β3-AR agonist (CL316243) and 0.1 µM β3-AR antagonist (L7483337) were applied to the cells at both doses. AQP7 and PLIN1 gene expressions were determined by real time-polymerase chain reaction (RT-PCR), and glycerol levels were determined by enzyme-linked immunosorbent assay (ELISA).
Results: Hypertrophic adipocytes showed increased AQP7 and PLIN1 gene expression and glycerol content compared with the control group. H-LV200 and CL316243 treatment together increased AQP7 gene expression, whereas H-LV400 and L7483337 treatment together decreased AQP7 gene expression.
Conclusion: The data indicated that both doses of LV inhibited glycerol production by suppressing AQP7 and PLIN1 gene expression. Approaches to regulate AQP7 gene expression in adipose tissue using plant-derived polyphonic compounds are considered a healthy and innovative approach to combat and manage metabolic diseases, including obesity.

Ethical Statement

Ethical approval is not applicable as a cell line is used.

Supporting Institution

Trakya University Scientific Research Projects Unit

Project Number

TUBAP 2021/11

Thanks

We would like to thank TUBAP for their support of project number 2021-11.

References

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  • 3. Herranz-Lopez M, Fernandez-Arroyo S, Perez-Sanchez A, Barrajon-Catalan E, Beltran-Debon R, Menendez JA, et al. Synergism of plant-derived polyphenols in adipogenesis: perspectives and implications. Phytomedicine 2012; 19(3-4): 253-61. google scholar
  • 4. Fernandez-Arroyo S, Herranz-Lopez M, Beltran-Debon R, Borras-Linares I, Barrajon-Catalan E, Joven J et al. Bioavailability of a polyphenol-enriched extract of Hibiscus sabdariffa in rats and associated antioxidant status. Mol Nutr Food Res 2012; 56(10): 1590-5. google scholar
  • 5. Herranz-Lopez M, Olivares-Vicente M, Boix-Castejon M, Caturla N, Roche E, Micol V. Differential effects of a combination of Hibiscus sabdariffa and Lippia citriodora polyphenols in overweight/obese subjects: A randomised controlled trial. Sci Rep 2019; 9(1): 2999. google scholar
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  • 7. Sânchez-Marzo N, Lozano-Sânchez J, Câdiz-Gurrea MdlL, Herranz-Löpez M, Micol V, Segura-Carretero A. Relationships between the chemical structure and antioxidant activity of phytocompounds isolated from lemon verbena. Antioxidants 2019; 8(8): 324. google scholar
  • 8. Joven J, Rull A, Rodriguez-Gallego E, Camps J, Riera-Borrull M, Hernândez-Aguilera A et al. Multifunctional targets of dietary polyphenols in diseases: A case study of the chemokine network and energy metabolism. Food Chem Toxicol 2013; 51: 267-79. google scholar
  • 9. Herranz-Löpez M, Barrajön-Catalân E, Segura-Carretero A, Menendez JA, Joven J, Micol V. Lemon verbena (Lippia citriodora) polyphenols alleviate obesity-related disturbances in hypertrophic adipocytes through AMPK-dependent mechanisms. Phytomedicine 2015; 22(6): 605-14. google scholar
  • 10. da Silva IV, Rodrigues JS, Rebelo I, Miranda JPG, Soveral G. Revisiting metabolic syndrome: the emerging role of aquaglyceroporin. Cell Mol Life Sci 2018; 75(11): 1973-88. google scholar
  • 11. Frühbeck G, Catalân V, Gömez-Ambrosi J, Rodnguez A. Aquaporin-7 and glycerol permeability as novel obesity drug-target pathways. Trends Pharmacol Sci 2006; 27(7): 345-7. google scholar
  • 12. K. Ishibashi, S. Hara, and S. Kondo. Aquaporin water channels in mammals. Clin Exp Nephrol 2009; 13: 107-17. google scholar
  • 13. Verkman AS, Anderson MO, Papadopoulos MC. Aquaporins: important but elusive drug targets. Nat Rev Drug Discov 2014; 13(4): 259-77. google scholar
  • 14. da Silva IV, Soveral G. Aquaporins in obesity. In: Yang B, editor. Aquaporins. Advances in Experimental Medicine and Biology, vol 1398. Springer, Singapore; 2023.p.289-302. google scholar
  • 15. Iena FM, Lebeck J. Implications of aquaglyceroporin 7 in energy metabolism. Int J Mol Sci 2018; 19(1): 154. google scholar
  • 16. Brasaemle DL. The perilipin family of structural lipid droplet proteins: stabilisation of lipid droplets and control of lipolysis. J Lipid Res 2007; 48(12): 2547-59. google scholar
  • 17. MacDougald OA, Burant CF. Obesity and metabolic perturbations after the loss of aquaporin 7, an adipose glycerol transporter. PNAS 2005; 102(31): 10759-60. google scholar
  • 18. Rodriguez A, Catalan V, Gomez-Ambrosi J, Fruhbeck G. Role of aquaporin-7 in the pathophysiological control of fat accumulation in mice. FEBS Lett 2006; 580(20): 4771-6. google scholar
  • 19. Fiorentini D, Zambonin L, Vieceli Dalla Sega F, Hrelia S. Polyphenols as modulators of aquaporin family in health and disease. Oxid Med Cell Longev 2015: 2015: 196914. google scholar
  • 20. Boque N, de la Iglesia R, de la Garza AL, Milagro FI, Olivares M, Banuelos O, et al. Prevention of diet induced obesity by apple polyphenols in W istar rats via regulation of adipocyte gene expression and DNA methylation patterns. Mol Nutr Food Res 2013; 57(8): 1473-8. google scholar
  • 21. Funes L, Laporta O, Cerdân-Calero M, Micol V. Effects of verbascoside, a phenylpropanoid glycoside from lemon verbena, on phospholipid model membranes. Chem Phys Lipids 2010; 163(2): 190-9. google scholar
  • 22. Green H, Kehinde O. Establishment of a preadipose cell line and its differentiation in culture II. Factors affecting the adipose conversion. Cell 1975; 5(1): 19-27. google scholar
  • 23. Han CY, Kargi AY, Omer M, Chan CK, Wabitsch M, O’Brien KD, et al. Differential effects of saturated and unsaturated free fatty acids on the generation of monocyte adhesion and chemotactic factors by adipocytes: dissociation of adipocyte hypertrophy from inflammation. Diabetes 2010; 59(2): 386-96. google scholar
  • 24. Tsukatani T, Suenaga H, Shiga M, Ikegami T, Ishiyama M, Ezoe T et al. Rapid susceptibility testing of slowly growing nontuberculous mycobacteria using colorimetric microbial viability assays based on reduced water-soluble tetrazolium WST-1. Eur J Clin Microbiol Infect Dis 2015; 34(10): 1965-73. google scholar
  • 25. Ji E, Jung M, Park J, Kim S, Seo C, Park K et al. Inhibition of adipogenesis in 3T3-L1 cells and suppression of abdominal fat accumulation in high-fat diet fed C57BL/6J mice after downregulation of hyaluronic acid. Int J Obes 2014; 38(8): 1035-43. google scholar
  • 26. Han CY, Subramanian S, Chan CK, Omer M, Chiba T, Wight TN, et al. Adipocyte-derived serum amyloid A3 and hyaluronan play roles in monocyte recruitment and adhesion. Diabetes 2007; 56(9): 2260-73. google scholar
  • 27. Shen FX, Gu X, Pan W, Li WP, Li W, Ye J, et al. Over-expression of AQP7 contributes to improve insulin resistance in adipocytes. Exp Cell Res 2012; 318(18): 2377-84. google scholar
  • 28. Kishida K, Kuriyama H, Funahashi T, Shimomura I, Kihara S, Ouchi N et al. Aquaporin adipose, a putative glycerol channel in adipocytes. J Biol Chem 2000; 275(27): 20896-902. google scholar
  • 29. Ardevol A, Blade C, Salvado MJ, Arola L. Changes in lipolysis and hormone-sensitive lipase expression caused by procyanidins in 3T3-L1 adipocytes. Int J Obes Relat Metab Disord 2000; 24(3): 319-24. google scholar
  • 30. Pan R, Zhu X, Maretich P, Chen Y. Combating obesity with thermogenic fat: Current challenges and advancements. Front Endocrinol (Lausanne) 2020; 11: 185. google scholar
  • 31. Mund RA, Frishman WH. Brown adipose tissue thermogenesis: beta3-adrenoreceptors as potential targets for the treatment of obesity in humans. Cardiol Rev 2013; 21(6): 265-9. google scholar
  • 32. Ghorbani M, Himms-Hagen, J. Appearance of brown adipocytes in white adipose tissue during CL 316,243-induced reversal of obesity and diabetes in Zucker fa/fa rats. Int J Obes Relat Metab Disord 1997; 21(6): 465-75. google scholar
  • 33. Clookey SL, Welly RJ, Shay D, Woodford ML, Fritsche KL, Rector RS, et al. Beta-3 adrenergic receptor activation rescues metabolic dysfunction in female estrogen receptor alpha-null mice. Front Physiol 2019; 10:9. google scholar
  • 34. Kishida K, Shimomura I, Nishizawa H, Maeda N, Kuriyama H, Kondo H et al. Enhancement of the aquaporin adipose gene expression by a peroxisome proliferator-activated receptor gamma. J Biol Chem 2001; 276(51): 48572-9. google scholar
  • 35. Fasshauer M, Klein J, Lossner U, Klier M, Kralisch S, Paschke R. Suppression of aquaporin adipose gene expression by isoproterenol, TNFalpha, and dexamethasone. Horm Metab Res 2003; 35(4): 222-7. google scholar
  • 36. Nakazato K, Song H, Waga T. Effects of dietary apple polyphenol on adipose tissues weights in Wistar rats. Experimental Animals 2006; 55(4): 383-9. google scholar
  • 37. Sugiyama H, Akazome Y, Shoji T, Yamaguchi A, Yasue M, Kanda T, et al. Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption. J Agric Food Chem 2007; 55(11): 4604-9. google scholar
  • 38. Joven J, Micol V, Segura-Carretero A, Alonso-Villaverde C, Menendez JA. Bioactive food components p. polyphenols and the modulation of gene expression pathways: can we the danger of chronic disease? Crit Rev Food Sci Nutr 2014; 54(8): 985-1001. google scholar
Year 2024, Volume: 14 Issue: 2, 102 - 109, 26.08.2024
https://doi.org/10.26650/experimed.1479944

Abstract

Project Number

TUBAP 2021/11

References

  • 1. Zukiewicz-Sobczak W, Wröblewska P, Zwolinski J, Chmielewska-Badora J, Adamczuk P, Krasowska E et al. Obesity and poverty paradox in developed countries. Ann Agric Environ Med 2014; 21(3): 590-4. google scholar
  • 2. Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev 2013; 93(1): 359-404. google scholar
  • 3. Herranz-Lopez M, Fernandez-Arroyo S, Perez-Sanchez A, Barrajon-Catalan E, Beltran-Debon R, Menendez JA, et al. Synergism of plant-derived polyphenols in adipogenesis: perspectives and implications. Phytomedicine 2012; 19(3-4): 253-61. google scholar
  • 4. Fernandez-Arroyo S, Herranz-Lopez M, Beltran-Debon R, Borras-Linares I, Barrajon-Catalan E, Joven J et al. Bioavailability of a polyphenol-enriched extract of Hibiscus sabdariffa in rats and associated antioxidant status. Mol Nutr Food Res 2012; 56(10): 1590-5. google scholar
  • 5. Herranz-Lopez M, Olivares-Vicente M, Boix-Castejon M, Caturla N, Roche E, Micol V. Differential effects of a combination of Hibiscus sabdariffa and Lippia citriodora polyphenols in overweight/obese subjects: A randomised controlled trial. Sci Rep 2019; 9(1): 2999. google scholar
  • 6. Amiot MJ, Riva C, Vinet A. Effects of dietary polyphenols on metabolic syndrome in humans: a systematic review. Obes Rev 2016; 17(7): 573-86. google scholar
  • 7. Sânchez-Marzo N, Lozano-Sânchez J, Câdiz-Gurrea MdlL, Herranz-Löpez M, Micol V, Segura-Carretero A. Relationships between the chemical structure and antioxidant activity of phytocompounds isolated from lemon verbena. Antioxidants 2019; 8(8): 324. google scholar
  • 8. Joven J, Rull A, Rodriguez-Gallego E, Camps J, Riera-Borrull M, Hernândez-Aguilera A et al. Multifunctional targets of dietary polyphenols in diseases: A case study of the chemokine network and energy metabolism. Food Chem Toxicol 2013; 51: 267-79. google scholar
  • 9. Herranz-Löpez M, Barrajön-Catalân E, Segura-Carretero A, Menendez JA, Joven J, Micol V. Lemon verbena (Lippia citriodora) polyphenols alleviate obesity-related disturbances in hypertrophic adipocytes through AMPK-dependent mechanisms. Phytomedicine 2015; 22(6): 605-14. google scholar
  • 10. da Silva IV, Rodrigues JS, Rebelo I, Miranda JPG, Soveral G. Revisiting metabolic syndrome: the emerging role of aquaglyceroporin. Cell Mol Life Sci 2018; 75(11): 1973-88. google scholar
  • 11. Frühbeck G, Catalân V, Gömez-Ambrosi J, Rodnguez A. Aquaporin-7 and glycerol permeability as novel obesity drug-target pathways. Trends Pharmacol Sci 2006; 27(7): 345-7. google scholar
  • 12. K. Ishibashi, S. Hara, and S. Kondo. Aquaporin water channels in mammals. Clin Exp Nephrol 2009; 13: 107-17. google scholar
  • 13. Verkman AS, Anderson MO, Papadopoulos MC. Aquaporins: important but elusive drug targets. Nat Rev Drug Discov 2014; 13(4): 259-77. google scholar
  • 14. da Silva IV, Soveral G. Aquaporins in obesity. In: Yang B, editor. Aquaporins. Advances in Experimental Medicine and Biology, vol 1398. Springer, Singapore; 2023.p.289-302. google scholar
  • 15. Iena FM, Lebeck J. Implications of aquaglyceroporin 7 in energy metabolism. Int J Mol Sci 2018; 19(1): 154. google scholar
  • 16. Brasaemle DL. The perilipin family of structural lipid droplet proteins: stabilisation of lipid droplets and control of lipolysis. J Lipid Res 2007; 48(12): 2547-59. google scholar
  • 17. MacDougald OA, Burant CF. Obesity and metabolic perturbations after the loss of aquaporin 7, an adipose glycerol transporter. PNAS 2005; 102(31): 10759-60. google scholar
  • 18. Rodriguez A, Catalan V, Gomez-Ambrosi J, Fruhbeck G. Role of aquaporin-7 in the pathophysiological control of fat accumulation in mice. FEBS Lett 2006; 580(20): 4771-6. google scholar
  • 19. Fiorentini D, Zambonin L, Vieceli Dalla Sega F, Hrelia S. Polyphenols as modulators of aquaporin family in health and disease. Oxid Med Cell Longev 2015: 2015: 196914. google scholar
  • 20. Boque N, de la Iglesia R, de la Garza AL, Milagro FI, Olivares M, Banuelos O, et al. Prevention of diet induced obesity by apple polyphenols in W istar rats via regulation of adipocyte gene expression and DNA methylation patterns. Mol Nutr Food Res 2013; 57(8): 1473-8. google scholar
  • 21. Funes L, Laporta O, Cerdân-Calero M, Micol V. Effects of verbascoside, a phenylpropanoid glycoside from lemon verbena, on phospholipid model membranes. Chem Phys Lipids 2010; 163(2): 190-9. google scholar
  • 22. Green H, Kehinde O. Establishment of a preadipose cell line and its differentiation in culture II. Factors affecting the adipose conversion. Cell 1975; 5(1): 19-27. google scholar
  • 23. Han CY, Kargi AY, Omer M, Chan CK, Wabitsch M, O’Brien KD, et al. Differential effects of saturated and unsaturated free fatty acids on the generation of monocyte adhesion and chemotactic factors by adipocytes: dissociation of adipocyte hypertrophy from inflammation. Diabetes 2010; 59(2): 386-96. google scholar
  • 24. Tsukatani T, Suenaga H, Shiga M, Ikegami T, Ishiyama M, Ezoe T et al. Rapid susceptibility testing of slowly growing nontuberculous mycobacteria using colorimetric microbial viability assays based on reduced water-soluble tetrazolium WST-1. Eur J Clin Microbiol Infect Dis 2015; 34(10): 1965-73. google scholar
  • 25. Ji E, Jung M, Park J, Kim S, Seo C, Park K et al. Inhibition of adipogenesis in 3T3-L1 cells and suppression of abdominal fat accumulation in high-fat diet fed C57BL/6J mice after downregulation of hyaluronic acid. Int J Obes 2014; 38(8): 1035-43. google scholar
  • 26. Han CY, Subramanian S, Chan CK, Omer M, Chiba T, Wight TN, et al. Adipocyte-derived serum amyloid A3 and hyaluronan play roles in monocyte recruitment and adhesion. Diabetes 2007; 56(9): 2260-73. google scholar
  • 27. Shen FX, Gu X, Pan W, Li WP, Li W, Ye J, et al. Over-expression of AQP7 contributes to improve insulin resistance in adipocytes. Exp Cell Res 2012; 318(18): 2377-84. google scholar
  • 28. Kishida K, Kuriyama H, Funahashi T, Shimomura I, Kihara S, Ouchi N et al. Aquaporin adipose, a putative glycerol channel in adipocytes. J Biol Chem 2000; 275(27): 20896-902. google scholar
  • 29. Ardevol A, Blade C, Salvado MJ, Arola L. Changes in lipolysis and hormone-sensitive lipase expression caused by procyanidins in 3T3-L1 adipocytes. Int J Obes Relat Metab Disord 2000; 24(3): 319-24. google scholar
  • 30. Pan R, Zhu X, Maretich P, Chen Y. Combating obesity with thermogenic fat: Current challenges and advancements. Front Endocrinol (Lausanne) 2020; 11: 185. google scholar
  • 31. Mund RA, Frishman WH. Brown adipose tissue thermogenesis: beta3-adrenoreceptors as potential targets for the treatment of obesity in humans. Cardiol Rev 2013; 21(6): 265-9. google scholar
  • 32. Ghorbani M, Himms-Hagen, J. Appearance of brown adipocytes in white adipose tissue during CL 316,243-induced reversal of obesity and diabetes in Zucker fa/fa rats. Int J Obes Relat Metab Disord 1997; 21(6): 465-75. google scholar
  • 33. Clookey SL, Welly RJ, Shay D, Woodford ML, Fritsche KL, Rector RS, et al. Beta-3 adrenergic receptor activation rescues metabolic dysfunction in female estrogen receptor alpha-null mice. Front Physiol 2019; 10:9. google scholar
  • 34. Kishida K, Shimomura I, Nishizawa H, Maeda N, Kuriyama H, Kondo H et al. Enhancement of the aquaporin adipose gene expression by a peroxisome proliferator-activated receptor gamma. J Biol Chem 2001; 276(51): 48572-9. google scholar
  • 35. Fasshauer M, Klein J, Lossner U, Klier M, Kralisch S, Paschke R. Suppression of aquaporin adipose gene expression by isoproterenol, TNFalpha, and dexamethasone. Horm Metab Res 2003; 35(4): 222-7. google scholar
  • 36. Nakazato K, Song H, Waga T. Effects of dietary apple polyphenol on adipose tissues weights in Wistar rats. Experimental Animals 2006; 55(4): 383-9. google scholar
  • 37. Sugiyama H, Akazome Y, Shoji T, Yamaguchi A, Yasue M, Kanda T, et al. Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption. J Agric Food Chem 2007; 55(11): 4604-9. google scholar
  • 38. Joven J, Micol V, Segura-Carretero A, Alonso-Villaverde C, Menendez JA. Bioactive food components p. polyphenols and the modulation of gene expression pathways: can we the danger of chronic disease? Crit Rev Food Sci Nutr 2014; 54(8): 985-1001. google scholar
There are 38 citations in total.

Details

Primary Language English
Subjects Biochemistry and Cell Biology (Other)
Journal Section Research Article
Authors

Orkide Palabıyık 0000-0002-3488-3740

Emine Kılıç Toprak 0000-0002-8795-0185

Deniz Şumnulu 0009-0009-0693-3569

Jülide Tozkır 0000-0002-8436-8309

Ayşegül Çört 0000-0001-8946-7173

Project Number TUBAP 2021/11
Publication Date August 26, 2024
Submission Date May 7, 2024
Acceptance Date July 24, 2024
Published in Issue Year 2024 Volume: 14 Issue: 2

Cite

Vancouver Palabıyık O, Kılıç Toprak E, Şumnulu D, Tozkır J, Çört A. Effect of Lemon Verbena Polyphenol on Glycerol Channel Aquaporin 7 Expression in 3T3-L1 Adipocytes. Experimed. 2024;14(2):102-9.