Research progress on the mechanism of high mobility group box 1 in stroke_West China Medical Journal

Authors：

SHANG Wenzuo , BAI Xueling ,  WU Bo

Department of Neurology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

WU Bo, Email: dr.bowu@hotmail.com

Keywords：

Stroke; high mobility group box 1; inflammation

DOI：

10.7507/1002-0179.202304148

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

High mobility group box 1 (HMGB1) is widely expressed in mammalian tissues and cells which is involved in various pathophysiological processes such as inflammation, autophagy, and apoptosis, and plays an important role in maintaining cell survival and normal function. HMGB1 plays an important part in the development of stroke, which can affect the prognosis by inducing neuroinflammation and autophagy. HMGB1 may have a bidirectional effect in acute and chronic phases. Exploring the specific role and mechanism of HMGB1 in each stage of stroke may make it a new target for prevention and treatment in the future.

Citation： SHANG Wenzuo, BAI Xueling, WU Bo. Research progress on the mechanism of high mobility group box 1 in stroke. West China Medical Journal, 2023, 38(5): 729-733. doi: 10.7507/1002-0179.202304148 Copy

1.	Mo Y, Sun YY, Liu KY. Autophagy and inflammation in ischemic stroke. Neural Regen Res, 2020, 15(8): 1388-1396.
2.	Shi K, Tian DC, Li ZG, et al. Global brain inflammation in stroke. Lancet Neurol, 2019, 18(11): 1058-1066.
3.	Xi G, Strahle J, Hua Y, et al. Progress in translational research on intracerebral hemorrhage: is there an end in sight?. Prog Neurobiol, 2014, 115: 45-63.
4.	Keep RF, Hua Y, Xi G. Intracerebral haemorrhage: mechanisms of injury and therapeutic targets. Lancet Neurol, 2012, 11(8): 720-731.
5.	Wu S, Wu B, Liu M, et al. Stroke in China: advances and challenges in epidemiology, prevention, and management. Lancet Neurol, 2019, 18(4): 394-405.
6.	Zhu X, Messer JS, Wang Y, et al. Cytosolic HMGB1 controls the cellular autophagy/apoptosis checkpoint during inflammation. J Clin Invest, 2015, 125(3): 1098-1110.
7.	Chen R, Kang R, Tang D. The mechanism of HMGB1 secretion and release. Exp Mol Med, 2022, 54(2): 91-102.
8.	Kang R, Chen R, Zhang Q, et al. HMGB1 in health and disease. Mol Aspects Med, 2014, 40: 1-116.
9.	Liu L, Yang M, Kang R, et al. DAMP-mediated autophagy contributes to drug resistance. Autophagy, 2011, 7(1): 112-114.
10.	Xue J, Suarez JS, Minaai M, et al. HMGB1 as a therapeutic target in disease. J Cell Physiol, 2021, 236(5): 3406-3419.
11.	Wang S, Zhang Y. HMGB1 in inflammation and cancer. J Hematol Oncol, 2020, 13(1): 116.
12.	Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature, 2002, 418(6894): 191-195.
13.	Fan H, Tang HB, Chen Z, et al. Inhibiting HMGB1-RAGE axis prevents pro-inflammatory macrophages/microglia polarization and affords neuroprotection after spinal cord injury. J Neuroinflammation, 2020, 17(1): 295.
14.	Thakur V, Sadanandan J, Chattopadhyay M. High-mobility group box 1 protein signaling in painful diabetic neuropathy. Int J Mol Sci, 2020, 21(3): 881.
15.	Stevens NE, Chapman MJ, Fraser CK, et al. Therapeutic targeting of HMGB1 during experimental sepsis modulates the inflammatory cytokine profile to one associated with improved clinical outcomes. Sci Rep, 2017, 7(1): 5850.
16.	Sun Y, Chen H, Dai J, et al. Glycyrrhizin protects mice against experimental autoimmune encephalomyelitis by inhibiting high-mobility group box 1 (HMGB1) expression and neuronal HMGB1 release. Front Immunol, 2018, 9: 1518.
17.	Tang D, Kang R, Cheh CW, et al. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells. Oncogene, 2010, 29(38): 5299-5310.
18.	New J, Thomas SM. Autophagy-dependent secretion: mechanism, factors secreted, and disease implications. Autophagy, 2019, 15(10): 1682-1693.
19.	Kumariya S, Ubba V, Jha RK, et al. Autophagy in ovary and polycystic ovary syndrome: role, dispute and future perspective. Autophagy, 2021, 17(10): 2706-2733.
20.	Qu L, Chen C, Chen Y, et al. High-mobility group box 1 (HMGB1) and autophagy in acute lung injury (ALI): a review. Med Sci Monit, 2019, 25: 1828-1837.
21.	Frisardi V, Matrone C, Street ME. Metabolic syndrome and autophagy: focus on HMGB1 protein. Front Cell Dev Biol, 2021, 9: 654913.
22.	Foglio E, Pellegrini L, Germani A, et al. HMGB1-mediated apoptosis and autophagy in ischemic heart diseases. Vasc Biol, 2019, 1(1): H89-H96.
23.	Hayakawa K, Pham LD, Katusic ZS, et al. Astrocytic high-mobility group box 1 promotes endothelial progenitor cell-mediated neurovascular remodeling during stroke recovery. Proc Natl Acad Sci U S A, 2012, 109(19): 7505-7510.
24.	Zhao M, Zhang Y, Jiang Y, et al. YAP promotes autophagy and progression of gliomas via upregulating HMGB1. J Exp Clin Cancer Res, 2021, 40(1): 99.
25.	Gulmammadli N, Konukoğlu D, Merve Kurtuluş E, et al. Serum sirtuin-1, HMGB1-TLR4, NF-KB and IL-6 levels in Alzheimer’s: the relation between neuroinflammatory pathway and severity of dementia. Curr Alzheimer Res, 2022, 19(12): 841-848.
26.	Gao HM, Zhou H, Zhang F, et al. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci, 2011, 31(3): 1081-1092.
27.	Anderson G, Rodriguez M, Reiter RJ. Multiple sclerosis: melatonin, orexin, and ceramide interact with platelet activation coagulation factors and gut-microbiome-derived butyrate in the circadian dysregulation of mitochondria in glia and immune cells. Int J Mol Sci, 2019, 20(21): 5500.
28.	Kim SW, Lee JK. Role of HMGB1 in the interplay between NETosis and thrombosis in ischemic stroke: a review. Cells, 2020, 9(8): 1794.
29.	Vogel S, Bodenstein R, Chen Q, et al. Platelet-derived HMGB1 is a critical mediator of thrombosis. J Clin Invest, 2015, 125(12): 4638-4654.
30.	Essig F, Babilon L, Vollmuth C, et al. High mobility group box 1 protein in cerebral thromboemboli. Int J Mol Sci, 2021, 22(20): 11276.
31.	Shichita T, Ito M, Morita R, et al. MAFB prevents excess inflammation after ischemic stroke by accelerating clearance of damage signals through MSR1. Nat Med, 2017, 23(6): 723-732.
32.	Jayaraj RL, Azimullah S, Beiram R, et al. Neuroinflammation: friend and foe for ischemic stroke. J Neuroinflammation, 2019, 16(1): 142.
33.	Singh V, Roth S, Veltkamp R, et al. HMGB1 as a key mediator of immune mechanisms in ischemic stroke. Antioxid Redox Signal, 2016, 24(12): 635-651.
34.	Xie W, Zhu T, Dong X, et al. HMGB1-triggered inflammation inhibition of notoginseng leaf triterpenes against cerebral ischemia and reperfusion injury via MAPK and NF-κB signaling pathways. Biomolecules, 2019, 9(10): 512.
35.	Liang Y, Song P, Chen W, et al. Inhibition of caspase-1 ameliorates ischemia-associated blood-brain barrier dysfunction and integrity by suppressing pyroptosis activation. Front Cell Neurosci, 2021, 14: 540669.
36.	Shichita T. Molecular and cellular mechanisms underlying the sterile inflammation after ischemic stroke. Nihon Yakurigaku Zasshi, 2018, 151(1): 9-14.
37.	Gülke E, Gelderblom M, Magnus T. Danger signals in stroke and their role on microglia activation after ischemia. Ther Adv Neurol Disord, 2018, 11: 1756286418774254.
38.	Xiong X, Gu L, Wang Y, et al. Glycyrrhizin protects against focal cerebral ischemia via inhibition of T cell activity and HMGB1-mediated mechanisms. J Neuroinflammation, 2016, 13(1): 241.
39.	Ye Y, Zeng Z, Jin T, et al. The role of high mobility group box 1 in ischemic stroke. Front Cell Neurosci, 2019, 13: 127.
40.	Lu Q, Liu R, Sherchan P, et al. TREM (triggering receptor expressed on myeloid cells)-1 inhibition attenuates neuroinflammation via PKC (protein kinase C) δ/CARD9 (caspase recruitment domain family member 9) signaling pathway after intracerebral hemorrhage in mice. Stroke, 2021, 52(6): 2162-2173.
41.	Lei C, Li Y, Zhu X, et al. HMGB1/TLR4 induces autophagy and promotes neuroinflammation after intracerebral hemorrhage. Brain Res, 2022, 1792: 148003.
42.	Li D, Lei C, Zhang S, et al. Blockade of high mobility group box-1 signaling via the receptor for advanced glycation end-products ameliorates inflammatory damage after acute intracerebral hemorrhage. Neurosci Lett, 2015, 609: 109-119.
43.	Lei C, Geng J, Zhong L. The association between plasma HMGB1 and sRAGE and clinical outcome in intracerebral hemorrhage. J Neuroimmunol, 2020, 345: 577266.
44.	Pan G, Jin L, Shen W, et al. Treadmill exercise improves neurological function by inhibiting autophagy and the binding of HMGB1 to Beclin1 in MCAO juvenile rats. Life Sci, 2020, 243: 117279.
45.	Wang J, Han D, Sun M, et al. A combination of remote ischemic perconditioning and cerebral ischemic postconditioning inhibits autophagy to attenuate plasma HMGB1 and induce neuroprotection against stroke in rat. J Mol Neurosci, 2016, 58(4): 424-431.
46.	张列, 苗树船, 杨中鑫, 等. HMGB1 下调的作用: 通过抑制神经元细胞自噬和凋亡减轻大鼠脑出血后的神经元损伤. 南方医科大学学报, 2022, 42(7): 1050-1056.
47.	Chen H, Guan B, Wang B, et al. Glycyrrhizin prevents hemorrhagic transformation and improves neurological outcome in ischemic stroke with delayed thrombolysis through targeting peroxynitrite-mediated HMGB1 signaling. Transl Stroke Res, 2020, 11(5): 967-982.
48.	Tang D, Kang R, Livesey KM, et al. Endogenous HMGB1 regulates autophagy. J Cell Biol, 2010, 190(5): 881-892.
49.	Wu H, Chen Z, Chen JZ, et al. High mobility group B-1 (HMGB-1) promotes apoptosis of macrophage-derived foam cells by inducing endoplasmic reticulum stress. Cell Physiol Biochem, 2018, 48(3): 1019-1029.
50.	Zhang D, Ren J, Luo Y, et al. T cell response in ischemic stroke: from mechanisms to translational insights. Front Immunol, 2021, 12: 707972.
51.	Shi L, Sun Z, Su W, et al. Treg cell-derived osteopontin promotes microglia-mediated white matter repair after ischemic stroke. Immunity, 2021, 54(7): 1527-1542.
52.	Yang H, Gao X, Xiao W, et al. Minocycline alleviates white matter injury following intracerebral hemorrhage by regulating CD4⁺ T cell differentiation via notch1 signaling pathway. Oxid Med Cell Longev, 2022, 2022: 3435267.
53.	Lei C, Wu B, Cao T, et al. Activation of the high-mobility group box 1 protein-receptor for advanced glycation end-products signaling pathway in rats during neurogenesis after intracerebral hemorrhage. Stroke, 2015, 46(2): 500-506.

1. Mo Y, Sun YY, Liu KY. Autophagy and inflammation in ischemic stroke. Neural Regen Res, 2020, 15(8): 1388-1396.
2. Shi K, Tian DC, Li ZG, et al. Global brain inflammation in stroke. Lancet Neurol, 2019, 18(11): 1058-1066.
3. Xi G, Strahle J, Hua Y, et al. Progress in translational research on intracerebral hemorrhage: is there an end in sight?. Prog Neurobiol, 2014, 115: 45-63.
4. Keep RF, Hua Y, Xi G. Intracerebral haemorrhage: mechanisms of injury and therapeutic targets. Lancet Neurol, 2012, 11(8): 720-731.
5. Wu S, Wu B, Liu M, et al. Stroke in China: advances and challenges in epidemiology, prevention, and management. Lancet Neurol, 2019, 18(4): 394-405.
6. Zhu X, Messer JS, Wang Y, et al. Cytosolic HMGB1 controls the cellular autophagy/apoptosis checkpoint during inflammation. J Clin Invest, 2015, 125(3): 1098-1110.
7. Chen R, Kang R, Tang D. The mechanism of HMGB1 secretion and release. Exp Mol Med, 2022, 54(2): 91-102.
8. Kang R, Chen R, Zhang Q, et al. HMGB1 in health and disease. Mol Aspects Med, 2014, 40: 1-116.
9. Liu L, Yang M, Kang R, et al. DAMP-mediated autophagy contributes to drug resistance. Autophagy, 2011, 7(1): 112-114.
10. Xue J, Suarez JS, Minaai M, et al. HMGB1 as a therapeutic target in disease. J Cell Physiol, 2021, 236(5): 3406-3419.
11. Wang S, Zhang Y. HMGB1 in inflammation and cancer. J Hematol Oncol, 2020, 13(1): 116.
12. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature, 2002, 418(6894): 191-195.
13. Fan H, Tang HB, Chen Z, et al. Inhibiting HMGB1-RAGE axis prevents pro-inflammatory macrophages/microglia polarization and affords neuroprotection after spinal cord injury. J Neuroinflammation, 2020, 17(1): 295.
14. Thakur V, Sadanandan J, Chattopadhyay M. High-mobility group box 1 protein signaling in painful diabetic neuropathy. Int J Mol Sci, 2020, 21(3): 881.
15. Stevens NE, Chapman MJ, Fraser CK, et al. Therapeutic targeting of HMGB1 during experimental sepsis modulates the inflammatory cytokine profile to one associated with improved clinical outcomes. Sci Rep, 2017, 7(1): 5850.
16. Sun Y, Chen H, Dai J, et al. Glycyrrhizin protects mice against experimental autoimmune encephalomyelitis by inhibiting high-mobility group box 1 (HMGB1) expression and neuronal HMGB1 release. Front Immunol, 2018, 9: 1518.
17. Tang D, Kang R, Cheh CW, et al. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells. Oncogene, 2010, 29(38): 5299-5310.
18. New J, Thomas SM. Autophagy-dependent secretion: mechanism, factors secreted, and disease implications. Autophagy, 2019, 15(10): 1682-1693.
19. Kumariya S, Ubba V, Jha RK, et al. Autophagy in ovary and polycystic ovary syndrome: role, dispute and future perspective. Autophagy, 2021, 17(10): 2706-2733.
20. Qu L, Chen C, Chen Y, et al. High-mobility group box 1 (HMGB1) and autophagy in acute lung injury (ALI): a review. Med Sci Monit, 2019, 25: 1828-1837.
21. Frisardi V, Matrone C, Street ME. Metabolic syndrome and autophagy: focus on HMGB1 protein. Front Cell Dev Biol, 2021, 9: 654913.
22. Foglio E, Pellegrini L, Germani A, et al. HMGB1-mediated apoptosis and autophagy in ischemic heart diseases. Vasc Biol, 2019, 1(1): H89-H96.
23. Hayakawa K, Pham LD, Katusic ZS, et al. Astrocytic high-mobility group box 1 promotes endothelial progenitor cell-mediated neurovascular remodeling during stroke recovery. Proc Natl Acad Sci U S A, 2012, 109(19): 7505-7510.
24. Zhao M, Zhang Y, Jiang Y, et al. YAP promotes autophagy and progression of gliomas via upregulating HMGB1. J Exp Clin Cancer Res, 2021, 40(1): 99.
25. Gulmammadli N, Konukoğlu D, Merve Kurtuluş E, et al. Serum sirtuin-1, HMGB1-TLR4, NF-KB and IL-6 levels in Alzheimer’s: the relation between neuroinflammatory pathway and severity of dementia. Curr Alzheimer Res, 2022, 19(12): 841-848.
26. Gao HM, Zhou H, Zhang F, et al. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci, 2011, 31(3): 1081-1092.
27. Anderson G, Rodriguez M, Reiter RJ. Multiple sclerosis: melatonin, orexin, and ceramide interact with platelet activation coagulation factors and gut-microbiome-derived butyrate in the circadian dysregulation of mitochondria in glia and immune cells. Int J Mol Sci, 2019, 20(21): 5500.
28. Kim SW, Lee JK. Role of HMGB1 in the interplay between NETosis and thrombosis in ischemic stroke: a review. Cells, 2020, 9(8): 1794.
29. Vogel S, Bodenstein R, Chen Q, et al. Platelet-derived HMGB1 is a critical mediator of thrombosis. J Clin Invest, 2015, 125(12): 4638-4654.
30. Essig F, Babilon L, Vollmuth C, et al. High mobility group box 1 protein in cerebral thromboemboli. Int J Mol Sci, 2021, 22(20): 11276.
31. Shichita T, Ito M, Morita R, et al. MAFB prevents excess inflammation after ischemic stroke by accelerating clearance of damage signals through MSR1. Nat Med, 2017, 23(6): 723-732.
32. Jayaraj RL, Azimullah S, Beiram R, et al. Neuroinflammation: friend and foe for ischemic stroke. J Neuroinflammation, 2019, 16(1): 142.
33. Singh V, Roth S, Veltkamp R, et al. HMGB1 as a key mediator of immune mechanisms in ischemic stroke. Antioxid Redox Signal, 2016, 24(12): 635-651.
34. Xie W, Zhu T, Dong X, et al. HMGB1-triggered inflammation inhibition of notoginseng leaf triterpenes against cerebral ischemia and reperfusion injury via MAPK and NF-κB signaling pathways. Biomolecules, 2019, 9(10): 512.
35. Liang Y, Song P, Chen W, et al. Inhibition of caspase-1 ameliorates ischemia-associated blood-brain barrier dysfunction and integrity by suppressing pyroptosis activation. Front Cell Neurosci, 2021, 14: 540669.
36. Shichita T. Molecular and cellular mechanisms underlying the sterile inflammation after ischemic stroke. Nihon Yakurigaku Zasshi, 2018, 151(1): 9-14.
37. Gülke E, Gelderblom M, Magnus T. Danger signals in stroke and their role on microglia activation after ischemia. Ther Adv Neurol Disord, 2018, 11: 1756286418774254.
38. Xiong X, Gu L, Wang Y, et al. Glycyrrhizin protects against focal cerebral ischemia via inhibition of T cell activity and HMGB1-mediated mechanisms. J Neuroinflammation, 2016, 13(1): 241.
39. Ye Y, Zeng Z, Jin T, et al. The role of high mobility group box 1 in ischemic stroke. Front Cell Neurosci, 2019, 13: 127.
40. Lu Q, Liu R, Sherchan P, et al. TREM (triggering receptor expressed on myeloid cells)-1 inhibition attenuates neuroinflammation via PKC (protein kinase C) δ/CARD9 (caspase recruitment domain family member 9) signaling pathway after intracerebral hemorrhage in mice. Stroke, 2021, 52(6): 2162-2173.
41. Lei C, Li Y, Zhu X, et al. HMGB1/TLR4 induces autophagy and promotes neuroinflammation after intracerebral hemorrhage. Brain Res, 2022, 1792: 148003.
42. Li D, Lei C, Zhang S, et al. Blockade of high mobility group box-1 signaling via the receptor for advanced glycation end-products ameliorates inflammatory damage after acute intracerebral hemorrhage. Neurosci Lett, 2015, 609: 109-119.
43. Lei C, Geng J, Zhong L. The association between plasma HMGB1 and sRAGE and clinical outcome in intracerebral hemorrhage. J Neuroimmunol, 2020, 345: 577266.
44. Pan G, Jin L, Shen W, et al. Treadmill exercise improves neurological function by inhibiting autophagy and the binding of HMGB1 to Beclin1 in MCAO juvenile rats. Life Sci, 2020, 243: 117279.
45. Wang J, Han D, Sun M, et al. A combination of remote ischemic perconditioning and cerebral ischemic postconditioning inhibits autophagy to attenuate plasma HMGB1 and induce neuroprotection against stroke in rat. J Mol Neurosci, 2016, 58(4): 424-431.
46. 张列, 苗树船, 杨中鑫, 等. HMGB1 下调的作用: 通过抑制神经元细胞自噬和凋亡减轻大鼠脑出血后的神经元损伤. 南方医科大学学报, 2022, 42(7): 1050-1056.
47. Chen H, Guan B, Wang B, et al. Glycyrrhizin prevents hemorrhagic transformation and improves neurological outcome in ischemic stroke with delayed thrombolysis through targeting peroxynitrite-mediated HMGB1 signaling. Transl Stroke Res, 2020, 11(5): 967-982.
48. Tang D, Kang R, Livesey KM, et al. Endogenous HMGB1 regulates autophagy. J Cell Biol, 2010, 190(5): 881-892.
49. Wu H, Chen Z, Chen JZ, et al. High mobility group B-1 (HMGB-1) promotes apoptosis of macrophage-derived foam cells by inducing endoplasmic reticulum stress. Cell Physiol Biochem, 2018, 48(3): 1019-1029.
50. Zhang D, Ren J, Luo Y, et al. T cell response in ischemic stroke: from mechanisms to translational insights. Front Immunol, 2021, 12: 707972.
51. Shi L, Sun Z, Su W, et al. Treg cell-derived osteopontin promotes microglia-mediated white matter repair after ischemic stroke. Immunity, 2021, 54(7): 1527-1542.
52. Yang H, Gao X, Xiao W, et al. Minocycline alleviates white matter injury following intracerebral hemorrhage by regulating CD4⁺ T cell differentiation via notch1 signaling pathway. Oxid Med Cell Longev, 2022, 2022: 3435267.
53. Lei C, Wu B, Cao T, et al. Activation of the high-mobility group box 1 protein-receptor for advanced glycation end-products signaling pathway in rats during neurogenesis after intracerebral hemorrhage. Stroke, 2015, 46(2): 500-506.

Previous Article
Anesthesia management of pregnancy with moderate to severe scoliosis
Next Article
Research progress on hyperacute reperfusion therapies for patients with severe ischemic stroke

West China Medical Journal

Research progress on the mechanism of high mobility group box 1 in stroke

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content