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Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1

Year 2023, , 105 - 115, 15.03.2023

Salih Tunç Kaya

https://doi.org/10.18521/ktd.1214575

Abstract

Objective: Cellular and physiological functions may be affected in an age- and sex-specific manner. The aim of this study is to investigate sex- and age-specific differences in the serum levels of Total Antioxidant Status (TAS), Total Oxidant Status (TOS), Oxidative Stress Index (OSI), Toll-like Receptor 2 (TLR2), Toll-Like Receptor 4 (TLR4), Heat Shock Protein 60 (HSP60), Heat Shock Protein 90 (HSP90), and High Mobility Group Box 1 (HMGB1) as well as to examine the correlation between them.
Methods: Four groups of mice, each including seven animals, were used in the present study: young males and females (6 months old); old males and females (24 months old). Blood samples were taken from the heart and serum was used to assay the levels of TLR2, TLR4, HSP60, HSP90, HMGB1, TAS and TOS.
Results: HGMB1, TOS and OSI were higher in old females than in young females (p<0.05). TLR2 and TLR4 levels were higher in young females than in young males; however, HSP60 was lower in young females than in young males (p<0.01). HSP60 was lower in old males than in young males (p<0.05). Positive correlations were present between TLR2, TLR4 and HMGB1 (p=0.001, r=0.096; p=0.012, r=0.867; p=0.002, r=0.935, respectively) as well as between HMGB1 and HSP60 (p=0.049, r=0.756) in young females. A negative correlation was detected between HSP90 and TLR4 in young males (p=0.000, r=-0,982), and between HSP60 and TLR2, OSI in old males (p=0.014, r=-0.856; p=0.042, r=-0.772, respectively).
Conclusions: The results of present study indicated that age and sex could be important factors for the serum levels of TLR2, TLR4, HSP60, HSP90, HMGB1 and OSI as well as the correlation between them.

Keywords

Sex Age High Mobility Group Box 1 Heat Shock Proteins Toll Like Receptors Oxidative Stress

Supporting Institution

Duzce University

Project Number

BAP- 2021.05.01.1262.

Thanks

I would like to thank to Dr. Kağan Ağan for his technical contribution.

References

  • 1. Ghimire A, Howlett SE. An acute estrogen receptor agonist enhances protective effects of cardioplegia in hearts from aging male and female mice. Exp Gerontol. 2020;141:111093.
  • 2. Rubin JB, Lagas JS, Broestl L, et al. Sex differences in cancer mechanisms. Biol Sex Differ. 2020;11(1):17.
  • 3. Brand BA, de Boer JN, Sommer IEC. Estrogens in schizophrenia: progress, current challenges and opportunities. Curr Opin Psychiatry. 2021;34(3):228-37.
  • 4. Connelly PJ, Azizi Z, Alipour P, et al. The Importance of Gender to Understand Sex Differences in Cardiovascular Disease. Can J Cardiol. 2021;37(5):699-710.
  • 5. Luo J, Mills K, le Cessie S, Noordam R, van Heemst D. Ageing, age-related diseases and oxidative stress: What to do next? Ageing Res Rev. 2020;57:100982.
  • 6. Kander MC, Cui Y, Liu Z. Gender difference in oxidative stress: a new look at the mechanisms for cardiovascular diseases. J Cell Mol Med. 2017;21(5):1024-32.
  • 7. Tang D, Kang R, Zeh HJ, 3rd, Lotze MT. High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal. 2011;14(7):1315-35.
  • 8. Szyller J, Bil-Lula I. Heat Shock Proteins in Oxidative Stress and Ischemia/Reperfusion Injury and Benefits from Physical Exercises: A Review to the Current Knowledge. Oxid Med Cell Longev. 2021;2021:6678457.
  • 9. Tsan MF. Heat shock proteins and high mobility group box 1 protein lack cytokine function. J Leukoc Biol. 2011;89(6):847-53.
  • 10. Huang J, Xie Y, Sun X, et al. DAMPs, ageing, and cancer: The 'DAMP Hypothesis'. Ageing Res Rev. 2015;24(Pt A):3-16.
  • 11. Ooboshi H, Shichita T. [DAMPs (damage-associated molecular patterns) and inflammation]. Nihon Rinsho. 2016;74(4):573-8.
  • 12. Li X, Jiang S, Tapping RI. Toll-like receptor signaling in cell proliferation and survival. Cytokine. 2010;49(1):1-9.
  • 13. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85.
  • 14. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11.
  • 15. Kosecik M, Erel O, Sevinc E, Selek S. Increased oxidative stress in children exposed to passive smoking. Int J Cardiol. 2005;100(1):61-4.
  • 16. Yumru M, Savas HA, Kalenderoglu A, et al. Oxidative imbalance in bipolar disorder subtypes: a comparative study. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33(6):1070-4.
  • 17. Brunelli E, Domanico F, La Russa D, Pellegrino D. Sex differences in oxidative stress biomarkers. Curr Drug Targets. 2014;15(8):811-5.
  • 18. Sanchez-Rodriguez MA, Mendoza-Nunez VM. Oxidative Stress Indexes for Diagnosis of Health or Disease in Humans. Oxid Med Cell Longev. 2019;2019:4128152.
  • 19. Lian YJ, Gong H, Wu TY, et al. Ds-HMGB1 and fr-HMGB induce depressive behavior through neuroinflammation in contrast to nonoxid-HMGB1. Brain Behav Immun. 2017;59:322-32.
  • 20. Kan M, Song L, Zhang X, Zhang J, Fang P. Circulating high mobility group box-1 and toll-like receptor 4 expressions increase the risk and severity of epilepsy. Braz J Med Biol Res. 2019;52(7):e7374.
  • 21. Raucci A, Di Maggio S, Scavello F, et al. The Janus face of HMGB1 in heart disease: a necessary update. Cell Mol Life Sci. 2019;76(2):211-29.
  • 22. Chen L, Zhu H, Su S, et al. High-Mobility Group Box-1 Is Associated With Obesity, Inflammation, and Subclinical Cardiovascular Risk Among Young Adults: A Longitudinal Cohort Study. Arterioscler Thromb Vasc Biol. 2020;40(11):2776-84.
  • 23. Fu GX, Chen AF, Zhong Y, Zhao J, Gu YJ. Decreased serum level of HMGB1 and MyD88 during human aging progress in healthy individuals. Aging Clin Exp Res. 2016;28(2):175-80.
  • 24. Umit EG, Baysal M, Bas V, et al. Value of Extracellular High Mobility Group Box 1 (HMGB1) in the Clinical Context of Immune Thrombocytopenia. Journal of Clinical and Experimental Investigations. 2019;10(2).
  • 25. Giuliano JS, Jr., Lahni PM, Wong HR, Wheeler DS. Pediatric Sepsis - Part V: Extracellular Heat Shock Proteins: Alarmins for the Host Immune System. Open Inflamm J. 2011;4:49-60.
  • 26. Purandhar K, Jena PK, Prajapati B, Rajput P, Seshadri S. Understanding the role of heat shock protein isoforms in male fertility, aging and apoptosis. World J Mens Health. 2014;32(3):123-32.
  • 27. Ocana GJ, Sims EK, Watkins RA, et al. Analysis of serum Hsp90 as a potential biomarker of beta cell autoimmunity in type 1 diabetes. PLoS One. 2019;14(1):e0208456.
  • 28. Pawlik-Gwozdecka D, Gorska-Ponikowska M, Adamkiewicz-Drozynska E, Niedzwiecki M. Serum heat shock protein 90 as a future predictive biomarker in childhood acute lymphoblastic leukemia. Cent Eur J Immunol. 2021;46(1):63-7.
  • 29. Murshid A, Eguchi T, Calderwood SK. Stress proteins in aging and life span. Int J Hyperthermia. 2013;29(5):442-7.
  • 30. Njemini R, Lambert M, Demanet C, Kooijman R, Mets T. Basal and infection-induced levels of heat shock proteins in human aging. Biogerontology. 2007;8(3):353-64.
  • 31. Rea IM, McNerlan S, Pockley AG. Serum heat shock protein and anti-heat shock protein antibody levels in aging. Exp Gerontol. 2001;36(2):341-52.
  • 32. Kim YS, Koh JM, Lee YS, et al. Increased circulating heat shock protein 60 induced by menopause, stimulates apoptosis of osteoblast-lineage cells via up-regulation of toll-like receptors. Bone. 2009;45(1):68-76.
  • 33. Koh JM, Lee YS, Kim YS, et al. Heat shock protein 60 causes osteoclastic bone resorption via toll-like receptor-2 in estrogen deficiency. Bone. 2009;45(4):650-60.
  • 34. Benini R, Nunes PRP, Orsatti CL, Portari GV, Orsatti FL. Influence of sex on cytokines, heat shock protein and oxidative stress markers in response to an acute total body resistance exercise protocol. Journal of Exercise Science & Fitness. 2015;13(1):1-7.
  • 35. Voss MR, Stallone JN, Li M, et al. Gender differences in the expression of heat shock proteins: the effect of estrogen. Am J Physiol Heart Circ Physiol. 2003;285(2):H687-92.
  • 36. El-Zayat SR, Sibaii H, Mannaa FA. Toll-like receptors activation, signaling, and targeting: an overview. Bulletin of the National Research Centre. 2019;43(1):187.
  • 37. El-Kharashy G, Gowily A, Okda T, Houssen M. Association between serum soluble Toll-like receptor 2 and 4 and the risk of breast cancer. Mol Clin Oncol. 2021;14(2):38.
  • 38. Paarnio K, Tuomisto A, Vayrynen SA, et al. Serum TLR2 and TLR4 levels in colorectal cancer and their association with systemic inflammatory markers, tumor characteristics, and disease outcome. APMIS. 2019;127(8):561-9.
  • 39. Hossain MJ, Morandi E, Tanasescu R, et al. The Soluble Form of Toll-Like Receptor 2 Is Elevated in Serum of Multiple Sclerosis Patients: A Novel Potential Disease Biomarker. Front Immunol. 2018;9:457.
  • 40. Li T, Jing JJ, Yang J, et al. Serum levels of matrix metalloproteinase 9 and toll-like receptor 4 in acute aortic dissection: a case-control study. BMC Cardiovasc Disord. 2018;18(1):219.
  • 41. Liu S, Wang X, Kai Y, et al. Clinical significance of high mobility group box 1/toll-like receptor 4 in obese diabetic patients. Endocr J. 2021.
  • 42. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol. 2005;5(6):446-58.
  • 43. Iram N, Mildner M, Prior M, et al. Age-related changes in expression and function of Toll-like receptors in human skin. Development. 2012;139(22):4210-9.
  • 44. Staller S, Lindsay AK, Ramos ED, Thomas P, Srinivasan M. Changes in salivary microbial sensing proteins CD14 and TLR2 with aging. Clin Oral Investig. 2020;24(7):2523-8.
  • 45. Scotland RS, Stables MJ, Madalli S, Watson P, Gilroy DW. Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood. 2011;118(22):5918-27.
  • 46. Koupenova M, Mick E, Mikhalev E, et al. Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors. Arterioscler Thromb Vasc Biol. 2015;35(4):1030-7.
  • 47. Shaw AC, Panda A, Joshi SR, et al. Dysregulation of human Toll-like receptor function in aging. Ageing Res Rev. 2011;10(3):346-53.
  • 48. Yu Y, Tang D, Kang R. Oxidative stress-mediated HMGB1 biology. Front Physiol. 2015;6:93.
  • 49. Chen R, Kang R, Tang D. The mechanism of HMGB1 secretion and release. Exp Mol Med. 2022;54(2):91-102.
  • 50. Abdulmahdi W, Patel D, Rabadi MM, et al. HMGB1 redox during sepsis. Redox Biology. 2017;13:600-7.
  • 51. Walker LE, Sills GJ, Jorgensen A, et al. High-mobility group box 1 as a predictive biomarker for drug-resistant epilepsy: A proof-of-concept study. Epilepsia. 2022;63(1):e1-e6.
  • 52. Devaraj S, Dasu MR, Park SH, Jialal I. Increased levels of ligands of Toll-like receptors 2 and 4 in type 1 diabetes. Diabetologia. 2009;52(8):1665-8.
  • 53. Calderwood SK, Mambula SS, Gray PJ, Jr. Extracellular heat shock proteins in cell signaling and immunity. Ann N Y Acad Sci. 2007;1113:28-39. 54. Hori M, Nishida K. Toll-like receptor signaling: defensive or offensive for the heart? Circ Res. 2008;102(2):137-9. 55. Milani A, Basirnejad M, Bolhassani A. Heat-shock proteins in diagnosis and treatment: an overview of different biochemical and immunological functions. Immunotherapy. 2019;11(3):215-39.

TAS, TOS, TLR2, TLR4, HSP60, HSP90 ve HMGB1 Serum Düzeylerinde Yaşa ve Cinsiyete Bağlı Değişiklikler

Year 2023, , 105 - 115, 15.03.2023

Salih Tunç Kaya

https://doi.org/10.18521/ktd.1214575

Abstract

Amaç: Hücresel ve fizyolojik fonksiyonlar yaşa ve cinsiyete özgü bir şekilde etkilenebilir. Bu çalışmanın amacı, Toplam Antioksidan Durumu (TAS), Toplam Oksidan Durumu (TOS), Oksidatif Stres İndeksi (OSI), Toll-Benzeri Reseptör 2 (TLR2), Toll-Benzeri Reseptör 4 (TLR4), Isı Şok Protein 60 (HSP60), Isı Şok Protein 90 (HSP90) ve Yüksek Mobilite Grup Kutusu 1 (HMGB1) serum seviyelerindeki cinsiyete ve yaşa özgü farklılıkları ve aralarındaki korelasyonu incelemektir.
Gereç ve Yöntem: Bu çalışmada her biri yedi hayvan içeren dört fare grubu kullanıldı: genç erkekler ve dişiler (6 aylık); yaşlı erkekler ve dişiler (24 aylık). Kan örnekleri Kalpten alındı ve TLR2, TLR4, HSP60, HSP90, HMGB1, TAS ve TOS seviyelerini değerlendirmek için serum kullanıldı.
Bulgular: HGMB1, TOS ve OSI yaşlı dişilerde genç dişilere göre daha yüksekti (p<0.05). TLR2 ve TLR4 seviyeleri genç dişilerde genç erkeklerden daha yüksekti; ancak HSP60 genç dişilerde genç erkeklere göre daha düşüktü (p<0.01). HSP60 yaşlı erkeklerde genç erkeklere göre daha düşüktü (p<0.05). Genç dişilerde TLR2, TLR4 ve HMGB1 arasında (sırasıyla p=0,001, r=0,096; p=0,012, r=0,867; p=0,002, r=0,935) ve HMGB1 ile HSP60 arasında (p=0,049, r=0,756) pozitif korelasyonlar mevcuttu. Genç erkeklerde HSP90 ile TLR4 arasında (p=0.000, r=-0,982), yaşlı erkeklerde HSP60 ile TLR2 ve OSI arasında negatif korelasyon saptandı (sırasıyla (p=0,014, r=-0,856; p=0,042, r=-0,772)
Sonuç: Bu çalışmanın sonuçları, TLR2, TLR4, HSP60, HSP90, HMGB1 ve OSI'nin serum düzeyleri ve aralarındaki korelasyon için yaş ve cinsiyetin önemli faktörler olabileceğini göstermiştir.

Keywords

Cinsiyet Yaş Yüksek Mobilite Grup Kutusu 1 Isı Şok Proteinleri Toll Benzeri Reseptörler Oksidatif Stres

Project Number

BAP- 2021.05.01.1262.

References

  • 1. Ghimire A, Howlett SE. An acute estrogen receptor agonist enhances protective effects of cardioplegia in hearts from aging male and female mice. Exp Gerontol. 2020;141:111093.
  • 2. Rubin JB, Lagas JS, Broestl L, et al. Sex differences in cancer mechanisms. Biol Sex Differ. 2020;11(1):17.
  • 3. Brand BA, de Boer JN, Sommer IEC. Estrogens in schizophrenia: progress, current challenges and opportunities. Curr Opin Psychiatry. 2021;34(3):228-37.
  • 4. Connelly PJ, Azizi Z, Alipour P, et al. The Importance of Gender to Understand Sex Differences in Cardiovascular Disease. Can J Cardiol. 2021;37(5):699-710.
  • 5. Luo J, Mills K, le Cessie S, Noordam R, van Heemst D. Ageing, age-related diseases and oxidative stress: What to do next? Ageing Res Rev. 2020;57:100982.
  • 6. Kander MC, Cui Y, Liu Z. Gender difference in oxidative stress: a new look at the mechanisms for cardiovascular diseases. J Cell Mol Med. 2017;21(5):1024-32.
  • 7. Tang D, Kang R, Zeh HJ, 3rd, Lotze MT. High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal. 2011;14(7):1315-35.
  • 8. Szyller J, Bil-Lula I. Heat Shock Proteins in Oxidative Stress and Ischemia/Reperfusion Injury and Benefits from Physical Exercises: A Review to the Current Knowledge. Oxid Med Cell Longev. 2021;2021:6678457.
  • 9. Tsan MF. Heat shock proteins and high mobility group box 1 protein lack cytokine function. J Leukoc Biol. 2011;89(6):847-53.
  • 10. Huang J, Xie Y, Sun X, et al. DAMPs, ageing, and cancer: The 'DAMP Hypothesis'. Ageing Res Rev. 2015;24(Pt A):3-16.
  • 11. Ooboshi H, Shichita T. [DAMPs (damage-associated molecular patterns) and inflammation]. Nihon Rinsho. 2016;74(4):573-8.
  • 12. Li X, Jiang S, Tapping RI. Toll-like receptor signaling in cell proliferation and survival. Cytokine. 2010;49(1):1-9.
  • 13. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85.
  • 14. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11.
  • 15. Kosecik M, Erel O, Sevinc E, Selek S. Increased oxidative stress in children exposed to passive smoking. Int J Cardiol. 2005;100(1):61-4.
  • 16. Yumru M, Savas HA, Kalenderoglu A, et al. Oxidative imbalance in bipolar disorder subtypes: a comparative study. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33(6):1070-4.
  • 17. Brunelli E, Domanico F, La Russa D, Pellegrino D. Sex differences in oxidative stress biomarkers. Curr Drug Targets. 2014;15(8):811-5.
  • 18. Sanchez-Rodriguez MA, Mendoza-Nunez VM. Oxidative Stress Indexes for Diagnosis of Health or Disease in Humans. Oxid Med Cell Longev. 2019;2019:4128152.
  • 19. Lian YJ, Gong H, Wu TY, et al. Ds-HMGB1 and fr-HMGB induce depressive behavior through neuroinflammation in contrast to nonoxid-HMGB1. Brain Behav Immun. 2017;59:322-32.
  • 20. Kan M, Song L, Zhang X, Zhang J, Fang P. Circulating high mobility group box-1 and toll-like receptor 4 expressions increase the risk and severity of epilepsy. Braz J Med Biol Res. 2019;52(7):e7374.
  • 21. Raucci A, Di Maggio S, Scavello F, et al. The Janus face of HMGB1 in heart disease: a necessary update. Cell Mol Life Sci. 2019;76(2):211-29.
  • 22. Chen L, Zhu H, Su S, et al. High-Mobility Group Box-1 Is Associated With Obesity, Inflammation, and Subclinical Cardiovascular Risk Among Young Adults: A Longitudinal Cohort Study. Arterioscler Thromb Vasc Biol. 2020;40(11):2776-84.
  • 23. Fu GX, Chen AF, Zhong Y, Zhao J, Gu YJ. Decreased serum level of HMGB1 and MyD88 during human aging progress in healthy individuals. Aging Clin Exp Res. 2016;28(2):175-80.
  • 24. Umit EG, Baysal M, Bas V, et al. Value of Extracellular High Mobility Group Box 1 (HMGB1) in the Clinical Context of Immune Thrombocytopenia. Journal of Clinical and Experimental Investigations. 2019;10(2).
  • 25. Giuliano JS, Jr., Lahni PM, Wong HR, Wheeler DS. Pediatric Sepsis - Part V: Extracellular Heat Shock Proteins: Alarmins for the Host Immune System. Open Inflamm J. 2011;4:49-60.
  • 26. Purandhar K, Jena PK, Prajapati B, Rajput P, Seshadri S. Understanding the role of heat shock protein isoforms in male fertility, aging and apoptosis. World J Mens Health. 2014;32(3):123-32.
  • 27. Ocana GJ, Sims EK, Watkins RA, et al. Analysis of serum Hsp90 as a potential biomarker of beta cell autoimmunity in type 1 diabetes. PLoS One. 2019;14(1):e0208456.
  • 28. Pawlik-Gwozdecka D, Gorska-Ponikowska M, Adamkiewicz-Drozynska E, Niedzwiecki M. Serum heat shock protein 90 as a future predictive biomarker in childhood acute lymphoblastic leukemia. Cent Eur J Immunol. 2021;46(1):63-7.
  • 29. Murshid A, Eguchi T, Calderwood SK. Stress proteins in aging and life span. Int J Hyperthermia. 2013;29(5):442-7.
  • 30. Njemini R, Lambert M, Demanet C, Kooijman R, Mets T. Basal and infection-induced levels of heat shock proteins in human aging. Biogerontology. 2007;8(3):353-64.
  • 31. Rea IM, McNerlan S, Pockley AG. Serum heat shock protein and anti-heat shock protein antibody levels in aging. Exp Gerontol. 2001;36(2):341-52.
  • 32. Kim YS, Koh JM, Lee YS, et al. Increased circulating heat shock protein 60 induced by menopause, stimulates apoptosis of osteoblast-lineage cells via up-regulation of toll-like receptors. Bone. 2009;45(1):68-76.
  • 33. Koh JM, Lee YS, Kim YS, et al. Heat shock protein 60 causes osteoclastic bone resorption via toll-like receptor-2 in estrogen deficiency. Bone. 2009;45(4):650-60.
  • 34. Benini R, Nunes PRP, Orsatti CL, Portari GV, Orsatti FL. Influence of sex on cytokines, heat shock protein and oxidative stress markers in response to an acute total body resistance exercise protocol. Journal of Exercise Science & Fitness. 2015;13(1):1-7.
  • 35. Voss MR, Stallone JN, Li M, et al. Gender differences in the expression of heat shock proteins: the effect of estrogen. Am J Physiol Heart Circ Physiol. 2003;285(2):H687-92.
  • 36. El-Zayat SR, Sibaii H, Mannaa FA. Toll-like receptors activation, signaling, and targeting: an overview. Bulletin of the National Research Centre. 2019;43(1):187.
  • 37. El-Kharashy G, Gowily A, Okda T, Houssen M. Association between serum soluble Toll-like receptor 2 and 4 and the risk of breast cancer. Mol Clin Oncol. 2021;14(2):38.
  • 38. Paarnio K, Tuomisto A, Vayrynen SA, et al. Serum TLR2 and TLR4 levels in colorectal cancer and their association with systemic inflammatory markers, tumor characteristics, and disease outcome. APMIS. 2019;127(8):561-9.
  • 39. Hossain MJ, Morandi E, Tanasescu R, et al. The Soluble Form of Toll-Like Receptor 2 Is Elevated in Serum of Multiple Sclerosis Patients: A Novel Potential Disease Biomarker. Front Immunol. 2018;9:457.
  • 40. Li T, Jing JJ, Yang J, et al. Serum levels of matrix metalloproteinase 9 and toll-like receptor 4 in acute aortic dissection: a case-control study. BMC Cardiovasc Disord. 2018;18(1):219.
  • 41. Liu S, Wang X, Kai Y, et al. Clinical significance of high mobility group box 1/toll-like receptor 4 in obese diabetic patients. Endocr J. 2021.
  • 42. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol. 2005;5(6):446-58.
  • 43. Iram N, Mildner M, Prior M, et al. Age-related changes in expression and function of Toll-like receptors in human skin. Development. 2012;139(22):4210-9.
  • 44. Staller S, Lindsay AK, Ramos ED, Thomas P, Srinivasan M. Changes in salivary microbial sensing proteins CD14 and TLR2 with aging. Clin Oral Investig. 2020;24(7):2523-8.
  • 45. Scotland RS, Stables MJ, Madalli S, Watson P, Gilroy DW. Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood. 2011;118(22):5918-27.
  • 46. Koupenova M, Mick E, Mikhalev E, et al. Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors. Arterioscler Thromb Vasc Biol. 2015;35(4):1030-7.
  • 47. Shaw AC, Panda A, Joshi SR, et al. Dysregulation of human Toll-like receptor function in aging. Ageing Res Rev. 2011;10(3):346-53.
  • 48. Yu Y, Tang D, Kang R. Oxidative stress-mediated HMGB1 biology. Front Physiol. 2015;6:93.
  • 49. Chen R, Kang R, Tang D. The mechanism of HMGB1 secretion and release. Exp Mol Med. 2022;54(2):91-102.
  • 50. Abdulmahdi W, Patel D, Rabadi MM, et al. HMGB1 redox during sepsis. Redox Biology. 2017;13:600-7.
  • 51. Walker LE, Sills GJ, Jorgensen A, et al. High-mobility group box 1 as a predictive biomarker for drug-resistant epilepsy: A proof-of-concept study. Epilepsia. 2022;63(1):e1-e6.
  • 52. Devaraj S, Dasu MR, Park SH, Jialal I. Increased levels of ligands of Toll-like receptors 2 and 4 in type 1 diabetes. Diabetologia. 2009;52(8):1665-8.
  • 53. Calderwood SK, Mambula SS, Gray PJ, Jr. Extracellular heat shock proteins in cell signaling and immunity. Ann N Y Acad Sci. 2007;1113:28-39. 54. Hori M, Nishida K. Toll-like receptor signaling: defensive or offensive for the heart? Circ Res. 2008;102(2):137-9. 55. Milani A, Basirnejad M, Bolhassani A. Heat-shock proteins in diagnosis and treatment: an overview of different biochemical and immunological functions. Immunotherapy. 2019;11(3):215-39.
There are 53 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Articles
Authors

Salih Tunç Kaya 0000-0002-4133-407X

Project Number BAP- 2021.05.01.1262.
Publication Date March 15, 2023
Acceptance Date February 20, 2023
Published in Issue Year 2023

Cite

APA Kaya, S. T. (2023). Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1. Konuralp Medical Journal, 15(1), 105-115. https://doi.org/10.18521/ktd.1214575
AMA Kaya ST. Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1. Konuralp Medical Journal. March 2023;15(1):105-115. doi:10.18521/ktd.1214575
Chicago Kaya, Salih Tunç. “Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1”. Konuralp Medical Journal 15, no. 1 (March 2023): 105-15. https://doi.org/10.18521/ktd.1214575.
EndNote Kaya ST (March 1, 2023) Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1. Konuralp Medical Journal 15 1 105–115.
IEEE S. T. Kaya, “Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1”, Konuralp Medical Journal, vol. 15, no. 1, pp. 105–115, 2023, doi: 10.18521/ktd.1214575.
ISNAD Kaya, Salih Tunç. “Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1”. Konuralp Medical Journal 15/1 (March 2023), 105-115. https://doi.org/10.18521/ktd.1214575.
JAMA Kaya ST. Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1. Konuralp Medical Journal. 2023;15:105–115.
MLA Kaya, Salih Tunç. “Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1”. Konuralp Medical Journal, vol. 15, no. 1, 2023, pp. 105-1, doi:10.18521/ktd.1214575.
Vancouver Kaya ST. Age- and Sex- Dependent Changes in Serum Levels of TAS, TOS, TLR2, TLR4, HSP60, HSP90, and HMGB1. Konuralp Medical Journal. 2023;15(1):105-1.