CD36 and metabolic inflammatory diseases_West China Medical Journal

Authors：

TU Rong , GONG Ting , CAO Juan , PENG Qing ,  ZHOU Jingqun

Department of Cardiovascular Medicine, Renhe Hospital Affiliated to China Three Gorges University, Yichang, Hubei 443002, P. R. China;

Corresponding author：

ZHOU Jingqun, Email: jingqun zhou@163.com

Keywords：

Metabolic inflammatory disease; Scavenger receptor CD36; Macrophage

DOI：

10.7507/1002-0179.202003142

Video：

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Scavenger receptor CD36 is a transmembrane protein as well as pattern recognition receptor expressed on the surfaces of multiple types of cells such as monocytes, macrophages, microvascular endothelial cells, smooth muscle cells, and platelets. In recent years, studies have found that the expression of CD36 is increased in some diseases, including type 2 diabetes, atherosclerosis, non-alcoholic fatty liver, and obesity. This paper collates the latest progress in the studies of scavenger receptor CD36, illuminates the role of CD36 receptor in metabolic inflammatory diseases by inflammation control, endoplasmic reticulum stress, macrophage phenotype transformation, and insulin resistance, and briefly introduces that CD36 can be a serum marker of metabolic inflammatory diseases, in order to provide potential therapeutic targets for treatment of metabolic inflammatory diseases.

Citation： TU Rong, GONG Ting, CAO Juan, PENG Qing, ZHOU Jingqun. CD36 and metabolic inflammatory diseases. West China Medical Journal, 2021, 36(6): 821-825. doi: 10.7507/1002-0179.202003142 Copy

1.	胡仁明, 谢颖, 鹿斌, 等. 2型糖尿病患者高发“代谢性炎症综合征”. 中华内分泌代谢杂志, 2016, 32(1): 27-32.
2.	Fitzgibbons TP, Czech MP. Emerging evidence for beneficial macrophage functions in atherosclerosis and obesity-induced insulin resistance. J Mol Med (Berl), 2016, 94(3): 267-275.
3.	Luiken JJ, Chanda D, Nabben M, et al. Post-translational modifications of CD36: implications for regulation of myocellular fatty acid uptake. Biochim Biophys Acta, 2016, 1862(SR/B2): 2253-2258.
4.	Lubura M, Hesse D, Kraemer M, et al. Diabetes prevalence in NZO females depends on estrogen action on liver fat content. Am J Physiol Endocrinol Metab, 2015, 309(12): E968-E980.
5.	Kim HJ, Moon JS, Park IR, et al. A novel index using soluble CD36 is associated with the prevalence of type 2 diabetes mellitus: comparison study with triglyceride-glucose index. Endocrinol Metab (Seoul), 2017, 32(3): 375-382.
6.	Grewal T, Enrich C, Rentero C, et al. Annexins in adipose tissue: novel players in obesity. Int J Mol Sci, 2019, 20(14): 3449.
7.	Tian K, Xu Y, Sahebkar A, et al. CD36 in atherosclerosis: pathophysiological mechanisms and therapeutic implications. Curr Atheroscler Rep, 2020, 22(10): 59.
8.	Jiang Y, Wang M, Huang K, et al. Oxidized low-density lipoprotein induces secretion of interleukin-1β by macrophages via reactive oxygen species-dependent NLRP3 inflammasome activation. Biochem Biophys Res Commun, 2012, 425(2): 121-126.
9.	Raghavan S, Singh NK, Gali S, et al. Protein kinase Cθ via activating transcription factor 2-Mediated CD36 expression and foam cell formation of Ly6C(hi) cells contributes to atherosclerosis. Circulation, 2018, 138(21): 2395-2412.
10.	Liu J, Yang P, Zuo G, et al. Long-chain fatty acid activates hepatocytes through CD36 mediated oxidative stress. Lipids Health Dis, 2018, 17(1): 153.
11.	Koonen DP, Jensen MK, Handberg A. Soluble CD36: a marker of the (pathophysiological) role of CD36 in the metabolic syndrome?. Arch Physiol Biochem, 2011, 117(2): 57-63.
12.	Kim EK, Choi EJ. Compromised MAPK signaling in human diseases: an update. Arch Toxicol, 2015, 89(6): 867-882.
13.	Zhang Q, Sun X, Xiao X, et al. 649 Effects of maternal chromium restriction on the long-term programming in MAPK signaling pathway of lipid metabolism in mice. Nutrients, 2016, 8: E488.
14.	Zhang C, Luo X, Chen J, et al. Osteoprotegerin promotes liver steatosis by targeting the ERK-PPAR-γ-CD36 pathway. Diabetes, 2019, 68(10): 1902-1914.
15.	Wei S, Zhang L, Wang BL, et al. ALDH2 deficiency inhibits Ox-LDL induced foam cell formation via suppressing CD36 expression. Biochem Biophys Res Commun, 2019, 512(1): 41-48.
16.	Adorni MP, Cipollari E, Favari E, et al. Inhibitory effect of PCSK9 on Abca1 protein expression and cholesterol efflux in macrophages. Atherosclerosis, 2017, 256: 1-6.
17.	He J, Zhang G, Pang Q, et al. SIRT6 reduces macrophage foam cell formation by inducing autophagy and cholesterol efflux under ox-LDL condition. FEBS J, 2017, 284(9): 1324-1337.
18.	Chen Y, Yang LX, Guo RW, et al. The role of FAK in the secretion of MMP9 after CD147 stimulation in macrophages. Int Heart J, 2018, 59(2): 394-398.
19.	Biedroń R, Peruń A, Józefowski S. CD36 differently regulates macrophage responses to smooth and rough lipopolysaccharide. PLoS One, 2016, 11(4): e0153558.
20.	He C, Zhang G, Ouyang H, et al. Effects of β2/aβ2 on oxLDL-induced CD36 activation in THP-1 macrophages. Life Sci, 2019, 239: 117000.
21.	Sasi USS, Ganapathy S, Palayyan SR, et al. Mitochondria associated membranes (MAMs): emerging drug targets for diabetes. Curr Med Chem, 2020, 27(20): 3362-3385.
22.	Rieusset J. Role of endoplasmic reticulum-mitochondria communication in type 2 diabetes. Adv Exp Med Biol, 2017, 997: 171-186.
23.	Geng J, Xu H, Fu W, et al. Rosuvastatin protects against endothelial cell apoptosis in vitro and alleviates atherosclerosis in ApoE^-/- mice by suppressing endoplasmic reticulum stress. Exp Ther Med, 2020, 20(1): 550-560.
24.	Nègre-Salvayre A, Augé N, Camaré C, et al. Dual signaling evoked by oxidized LDLs in vascular cells. Free Radic Biol Med, 2017, 106: 118-133.
25.	Widenmaier SB, Snyder N, Nguyen TB, et al. NRF1 is an ER membrane sensor that is central to cholesterol homeostasis. Cell, 2017, 171(5): 1094-1109. e15.
26.	Chen Y, Yang M, Huang W, et al. Mitochondrial metabolic reprogramming by CD36 signaling drives macrophage inflammatory responses. Circ Res, 2019, 125(12): 1087-1102.
27.	Yang S, Yuan HQ, Hao YM, et al. Macrophage polarization in atherosclerosis. Clin Chim Acta, 2020, 501: 142-146.
28.	Ma Z, Ketelhuth D, Wirström T, et al. Increased uptake of oxLDL does not exert lipotoxic effects in insulin-secreting cells. J Mol Endocrinol, 2019, 62(4): 159-168.
29.	Krenkel O, Hundertmark J, Abdallah AT, et al. Myeloid cells in liver and bone marrow acquire a functionally distinct inflammatory phenotype during obesity-related steatohepatitis. Gut, 2020, 69(3): 551-563.
30.	Rao X, Zhao S, Braunstein Z, et al. Oxidized LDL upregulates macrophage DPP4 expression via TLR4/TRIF/CD36 pathways. EBioMedicine, 2019, 41: 50-61.
31.	Oh H, Park SH, Kang MK, et al. Asaronic acid attenuates macrophage activation toward M1 phenotype through inhibition of NF-κB pathway and JAK-STAT signaling in glucose-loaded murine macrophages. J Agric Food Chem, 2019, 67(36): 10069-10078.
32.	Ekici M, Kisa U, Arikan Durmaz S, et al. Fatty acid transport receptor soluble CD36 and dietary fatty acid pattern in type 2 diabetic patients: a comparative study. Br J Nutr, 2018, 119(2): 153-162.
33.	Tsai S, Clemente-Casares X, Zhou AC, et al. Insulin receptor-mediated stimulation boosts T cell immunity during inflammation and infection. Cell Metab, 2018, 28(6): 922-934. e4.
34.	Beverly JK, Budoff MJ. Atherosclerosis: pathophysiology of insulin resistance, hyperglycemia, hyperlipidemia, and inflammation. J Diabetes, 2020, 12(2): 102-104.
35.	Yang N, Li S, Liu S, et al. Insulin resistance-related proteins are overexpressed in patients and rats treated with olanzapine and are reverted by pueraria in the rat model. J Clin Psychopharmacol, 2019, 39(3): 214-219.
36.	张爱军, 郭宏伟, 冯琼, 等. 清道夫受体CD36基因缺陷对正常高值血压患者动态血压节律及代谢指标的影响研究. 中国全科医学, 2020, 23(23): 2890-2894.
37.	Balkaya M, Kim ID, Shakil F, et al. CD36 deficiency reduces chronic BBB dysfunction and scar formation and improves activity, hedonic and memory deficits in ischemic stroke. J Cereb Blood Flow Metab, 2021, 41(3): 486-501.
38.	Badrnya S, Schrottmaier WC, Kral JB, et al. Platelets mediate oxidized low-density lipoprotein-induced monocyte extravasation and foam cell formation. Arterioscler Thromb Vasc Biol, 2014, 34(3): 571-580.

1. 胡仁明, 谢颖, 鹿斌, 等. 2型糖尿病患者高发“代谢性炎症综合征”. 中华内分泌代谢杂志, 2016, 32(1): 27-32.
2. Fitzgibbons TP, Czech MP. Emerging evidence for beneficial macrophage functions in atherosclerosis and obesity-induced insulin resistance. J Mol Med (Berl), 2016, 94(3): 267-275.
3. Luiken JJ, Chanda D, Nabben M, et al. Post-translational modifications of CD36: implications for regulation of myocellular fatty acid uptake. Biochim Biophys Acta, 2016, 1862(SR/B2): 2253-2258.
4. Lubura M, Hesse D, Kraemer M, et al. Diabetes prevalence in NZO females depends on estrogen action on liver fat content. Am J Physiol Endocrinol Metab, 2015, 309(12): E968-E980.
5. Kim HJ, Moon JS, Park IR, et al. A novel index using soluble CD36 is associated with the prevalence of type 2 diabetes mellitus: comparison study with triglyceride-glucose index. Endocrinol Metab (Seoul), 2017, 32(3): 375-382.
6. Grewal T, Enrich C, Rentero C, et al. Annexins in adipose tissue: novel players in obesity. Int J Mol Sci, 2019, 20(14): 3449.
7. Tian K, Xu Y, Sahebkar A, et al. CD36 in atherosclerosis: pathophysiological mechanisms and therapeutic implications. Curr Atheroscler Rep, 2020, 22(10): 59.
8. Jiang Y, Wang M, Huang K, et al. Oxidized low-density lipoprotein induces secretion of interleukin-1β by macrophages via reactive oxygen species-dependent NLRP3 inflammasome activation. Biochem Biophys Res Commun, 2012, 425(2): 121-126.
9. Raghavan S, Singh NK, Gali S, et al. Protein kinase Cθ via activating transcription factor 2-Mediated CD36 expression and foam cell formation of Ly6C(hi) cells contributes to atherosclerosis. Circulation, 2018, 138(21): 2395-2412.
10. Liu J, Yang P, Zuo G, et al. Long-chain fatty acid activates hepatocytes through CD36 mediated oxidative stress. Lipids Health Dis, 2018, 17(1): 153.
11. Koonen DP, Jensen MK, Handberg A. Soluble CD36: a marker of the (pathophysiological) role of CD36 in the metabolic syndrome?. Arch Physiol Biochem, 2011, 117(2): 57-63.
12. Kim EK, Choi EJ. Compromised MAPK signaling in human diseases: an update. Arch Toxicol, 2015, 89(6): 867-882.
13. Zhang Q, Sun X, Xiao X, et al. 649 Effects of maternal chromium restriction on the long-term programming in MAPK signaling pathway of lipid metabolism in mice. Nutrients, 2016, 8: E488.
14. Zhang C, Luo X, Chen J, et al. Osteoprotegerin promotes liver steatosis by targeting the ERK-PPAR-γ-CD36 pathway. Diabetes, 2019, 68(10): 1902-1914.
15. Wei S, Zhang L, Wang BL, et al. ALDH2 deficiency inhibits Ox-LDL induced foam cell formation via suppressing CD36 expression. Biochem Biophys Res Commun, 2019, 512(1): 41-48.
16. Adorni MP, Cipollari E, Favari E, et al. Inhibitory effect of PCSK9 on Abca1 protein expression and cholesterol efflux in macrophages. Atherosclerosis, 2017, 256: 1-6.
17. He J, Zhang G, Pang Q, et al. SIRT6 reduces macrophage foam cell formation by inducing autophagy and cholesterol efflux under ox-LDL condition. FEBS J, 2017, 284(9): 1324-1337.
18. Chen Y, Yang LX, Guo RW, et al. The role of FAK in the secretion of MMP9 after CD147 stimulation in macrophages. Int Heart J, 2018, 59(2): 394-398.
19. Biedroń R, Peruń A, Józefowski S. CD36 differently regulates macrophage responses to smooth and rough lipopolysaccharide. PLoS One, 2016, 11(4): e0153558.
20. He C, Zhang G, Ouyang H, et al. Effects of β2/aβ2 on oxLDL-induced CD36 activation in THP-1 macrophages. Life Sci, 2019, 239: 117000.
21. Sasi USS, Ganapathy S, Palayyan SR, et al. Mitochondria associated membranes (MAMs): emerging drug targets for diabetes. Curr Med Chem, 2020, 27(20): 3362-3385.
22. Rieusset J. Role of endoplasmic reticulum-mitochondria communication in type 2 diabetes. Adv Exp Med Biol, 2017, 997: 171-186.
23. Geng J, Xu H, Fu W, et al. Rosuvastatin protects against endothelial cell apoptosis in vitro and alleviates atherosclerosis in ApoE^-/- mice by suppressing endoplasmic reticulum stress. Exp Ther Med, 2020, 20(1): 550-560.
24. Nègre-Salvayre A, Augé N, Camaré C, et al. Dual signaling evoked by oxidized LDLs in vascular cells. Free Radic Biol Med, 2017, 106: 118-133.
25. Widenmaier SB, Snyder N, Nguyen TB, et al. NRF1 is an ER membrane sensor that is central to cholesterol homeostasis. Cell, 2017, 171(5): 1094-1109. e15.
26. Chen Y, Yang M, Huang W, et al. Mitochondrial metabolic reprogramming by CD36 signaling drives macrophage inflammatory responses. Circ Res, 2019, 125(12): 1087-1102.
27. Yang S, Yuan HQ, Hao YM, et al. Macrophage polarization in atherosclerosis. Clin Chim Acta, 2020, 501: 142-146.
28. Ma Z, Ketelhuth D, Wirström T, et al. Increased uptake of oxLDL does not exert lipotoxic effects in insulin-secreting cells. J Mol Endocrinol, 2019, 62(4): 159-168.
29. Krenkel O, Hundertmark J, Abdallah AT, et al. Myeloid cells in liver and bone marrow acquire a functionally distinct inflammatory phenotype during obesity-related steatohepatitis. Gut, 2020, 69(3): 551-563.
30. Rao X, Zhao S, Braunstein Z, et al. Oxidized LDL upregulates macrophage DPP4 expression via TLR4/TRIF/CD36 pathways. EBioMedicine, 2019, 41: 50-61.
31. Oh H, Park SH, Kang MK, et al. Asaronic acid attenuates macrophage activation toward M1 phenotype through inhibition of NF-κB pathway and JAK-STAT signaling in glucose-loaded murine macrophages. J Agric Food Chem, 2019, 67(36): 10069-10078.
32. Ekici M, Kisa U, Arikan Durmaz S, et al. Fatty acid transport receptor soluble CD36 and dietary fatty acid pattern in type 2 diabetic patients: a comparative study. Br J Nutr, 2018, 119(2): 153-162.
33. Tsai S, Clemente-Casares X, Zhou AC, et al. Insulin receptor-mediated stimulation boosts T cell immunity during inflammation and infection. Cell Metab, 2018, 28(6): 922-934. e4.
34. Beverly JK, Budoff MJ. Atherosclerosis: pathophysiology of insulin resistance, hyperglycemia, hyperlipidemia, and inflammation. J Diabetes, 2020, 12(2): 102-104.
35. Yang N, Li S, Liu S, et al. Insulin resistance-related proteins are overexpressed in patients and rats treated with olanzapine and are reverted by pueraria in the rat model. J Clin Psychopharmacol, 2019, 39(3): 214-219.
36. 张爱军, 郭宏伟, 冯琼, 等. 清道夫受体CD36基因缺陷对正常高值血压患者动态血压节律及代谢指标的影响研究. 中国全科医学, 2020, 23(23): 2890-2894.
37. Balkaya M, Kim ID, Shakil F, et al. CD36 deficiency reduces chronic BBB dysfunction and scar formation and improves activity, hedonic and memory deficits in ischemic stroke. J Cereb Blood Flow Metab, 2021, 41(3): 486-501.
38. Badrnya S, Schrottmaier WC, Kral JB, et al. Platelets mediate oxidized low-density lipoprotein-induced monocyte extravasation and foam cell formation. Arterioscler Thromb Vasc Biol, 2014, 34(3): 571-580.

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