Volume 6 Issue 1
Jun.  2022
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Juan Xie, Yun Yao, Chen Yang, Wei Liu, Xiaoyu Zhou, Mingshun Zhang. Erythrocyte immune system: beyond the gas transporter[J]. Blood&Genomics, 2022, 6(1): 1-11. doi: 10.46701/BG.2022012022009
Citation: Juan Xie, Yun Yao, Chen Yang, Wei Liu, Xiaoyu Zhou, Mingshun Zhang. Erythrocyte immune system: beyond the gas transporter[J]. Blood&Genomics, 2022, 6(1): 1-11. doi: 10.46701/BG.2022012022009

Erythrocyte immune system: beyond the gas transporter

doi: 10.46701/BG.2022012022009
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  • Corresponding author: Xiaoyu Zhou, Department of Transfusion, the First Affiliated Hospital of Nanjing Medical University, 300 Guangzhou Road, Nanjing, Jiangsu 210029, China. E-mail: deerzxy@163.com; Mingshun Zhang, Department of Immunology, Nanjing Medical University, 101 Longmian Avenue, Nanjing, Jiangsu 211166, China. E-mail: mingshunzhang@njmu.edu.cn
  • Received Date: 2022-05-15
  • Accepted Date: 2022-06-07
  • Rev Recd Date: 2022-06-04
  • Available Online: 2022-06-30
  • Publish Date: 2022-06-30
  • Accumulating research has revealed that erythrocytes play unique roles in the innate immune system. Once thought of as immunologically inert cells, erythrocytes are functional cells that exert diverse immunological effects. Although mature mammal erythrocytes lack internal organelles, they express various receptors, which provide an extraordinary ability for erythrocytes to clear or sequester circulating molecules that affect immune functions. In this review, we elucidate some crucial immunological molecules associated with erythrocytes, such as CR1, CD47, TLR9, and cytokines. CR1 acts as a bridge in clearing off immune complexes and an entrance gate for some pathogens. CD47, once bound to SIRPα, generates an inhibitory signal in macrophage phagocytosis. Reciprocally, erythrocyte CD47 undergoes a conformational change during oxidative stress-induced cellular senescence, subsequently activating phagocytic signals through binding to TSP-1. TLR9 recognizes unmethylated CpG-DNA present in viruses and bacteria. Erythrocyte TLR9 also binds to and eliminates mitochondrial DNA. Erythrocytes can recruit chemokines and modulate plasma chemokine levels through the Duffy antigen receptor for chemokines (DARC). Moreover, erythrocytes may exert immune functions by releasing danger-associated molecular patterns (DAMPs), i.e., heme, IL-33, ATP, and Hsp70. Heme bound with toll-like receptor 4 (TLR4) has the potential to trigger an inflammatory response. Similarly, IL-33, ATP, and Hsp70 from damaged erythrocytes may be involved in the innate immune response via diverse signaling mechanisms. This review provides novel insight into the immunological functions of erythrocytes, which play an irreplaceable role in innate immune responses. We argue that erythrocyte-involved immune function is a widespread area warranting intensive investigation.


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  • [1]
    Wicinski M, Liczner G, Cadelski K, et al. Anemia of chronic diseases: wider diagnostics-better treatment?[J]. Nutrients, 2020, 12(6): 1784. doi: 10.3390/nu12061784
    Moras M, Lefevre SD, Ostuni MA. From erythroblasts to mature red blood cells: organelle clearance in mammals[J]. Front Physiol, 2017, 8: 1076. doi: 10.3389/fphys.2017.01076
    Anderson HL, Brodsky IE, Mangalmurti NS. The evolving erythrocyte: red blood cells as modulators of innate immunity[J]. J Immunol, 2018, 201(5): 1343−1351. doi: 10.4049/jimmunol.1800565
    Tian XY, Tian J, Tang XY, et al. Long non-coding RNAs in the regulation of myeloid cells[J]. J Hematol Oncol, 2016, 9(1): 99. doi: 10.1186/s13045-016-0333-7
    Leslie M. Red blood cells may be immune sentinels[J]. Science, 2021, 374(6566): 383. doi: 10.1126/science.acx9389
    Siegel I, Liu TL, Gleicher N. The red-cell immune system[J]. Lancet, 1981, 2(8246): 556−559. doi: 10.1016/s0140-6736(81)90941-7
    Mendonça R, Silveira AA, Conran N. Red cell DAMPs and inflammation[J]. Inflamm Res, 2016, 65(9): 665−678. doi: 10.1007/s00011-016-0955-9
    Swann OV, Harrison EM, Opi DH, et al. No evidence that knops blood group polymorphisms affect complement receptor 1 clustering on erythrocytes[J]. Sci Rep, 2017, 7(1): 17825. doi: 10.1038/s41598-017-17664-9
    Fearon DT. Identification of the membrane glycoprotein that is the C3b receptor of the human erythrocyte, polymorphonuclear leukocyte, B lymphocyte, and monocyte[J]. J Exp Med, 1980, 152(1): 20−30. doi: 10.1084/jem.152.1.20
    Sandri TL, Lidani KCF, Andrade FA, et al. Human complement receptor type 1 (CR1) protein levels and genetic variants in chronic Chagas Disease[J]. Sci Rep, 2018, 8(1): 526. doi: 10.1038/s41598-017-18937-z
    Page MJ, Bester J, Pretorius E. The inflammatory effects of TNF-alpha and complement component 3 on coagulation[J]. Sci Rep, 2018, 8(1): 1812. doi: 10.1038/s41598-018-20220-8
    Qi XM, Ma JF. The role of amyloid beta clearance in cerebral amyloid angiopathy: more potential therapeutic targets[J]. Transl Neurodegener, 2017, 6: 22. doi: 10.1186/s40035-017-0091-7
    Birmingham DJ, Gavit KF, McCarty SM, et al. Consumption of erythrocyte CR1 (CD35) is associated with protection against systemic lupus erythematosus renal flare[J]. Clin Exp Immunol, 2006, 143(2): 274−280. doi: 10.1111/j.1365-2249.2005.02983.x
    Brancucci NM, Witmer K, Schmid C, et al. A var gene upstream element controls protein synthesis at the level of translation initiation in Plasmodium falciparum[J]. PLoS One, 2014, 9(6): e100183. doi: 10.1371/journal.pone.0100183
    Batinovic S, McHugh E, Chisholm SA, et al. An exported protein-interacting complex involved in the trafficking of virulence determinants in Plasmodium-infected erythrocytes[J]. Nat Commun, 2017, 8: 16044. doi: 10.1038/ncomms16044
    Mensah-Brown HE, Amoako N, Abugri J, et al. Analysis of erythrocyte invasion mechanisms of plasmodium falciparum clinical isolates across 3 malaria-endemic areas in Ghana[J]. J Infect Dis, 2015, 212(8): 1288−1297. doi: 10.1093/infdis/jiv207
    King C, Du P, Otieno W, et al. Use of mosquito preventive measures is associated with increased RBC CR1 levels in a malaria holoendemic area of western Kenya[J]. Am J Trop Med Hyg, 2015, 92(1): 34−38. doi: 10.4269/ajtmh.14-0342
    Lam LKM, Murphy S, Kokkinaki D, et al. DNA binding to TLR9 expressed by red blood cells promotes innate immune activation and anemia[J]. Sci Transl Med, 2021, 13(616): eabj1008. doi: 10.1126/scitranslmed.abj1008
    Lood C, Blanco LP, Purmalek MM, et al. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease[J]. Nat Med, 2016, 22(2): 146−153. doi: 10.1038/nm.4027
    Hotz MJ, Qing D, Shashaty MGS, et al. Red blood cells homeostatically bind mitochondrial DNA through TLR9 to maintain quiescence and to prevent lung injury[J]. Am J Respir Crit Care Med, 2018, 197(4): 470−480. doi: 10.1164/rccm.201706-1161OC
    Bajwa E, Pointer CB, Klegeris A. The role of mitochondrial damage-associated molecular patterns in chronic neuroinflammation[J]. Mediators Inflamm, 2019, 2019: 4050796. doi: 10.1155/2019/4050796
    Bordt EA, Shook LL, Atyeo C, et al. Maternal SARS-CoV-2 infection elicits sexually dimorphic placental immune responses[J]. Sci Transl Med, 2021, 13(617): eabi7428. doi: 10.1126/scitranslmed.abi7428
    Kazama R, Miyoshi H, Takeuchi M, et al. Combination of CD47 and signal-regulatory protein-alpha constituting the "don't eat me signal" is a prognostic factor in diffuse large B-cell lymphoma[J]. Cancer Sci, 2020, 111(7): 2608−2619. doi: 10.1111/cas.14437
    Gheibihayat SM, Cabezas R, Nikiforov NG, et al. CD47 in the brain and neurodegeneration: an update on the role in neuroinflammatory pathways[J]. Molecules, 2021, 26(13): 3943. doi: 10.3390/molecules26133943
    Oldenborg PA, Zheleznyak A, Fang YF, et al. Role of CD47 as a marker of self on red blood cells[J]. Science, 2000, 288(5473): 2051−2054. doi: 10.1126/science.288.5473.2051
    Nagaoka H, Sasaoka C, Yuguchi T, et al. PfMSA180 is a novel Plasmodium falciparum vaccine antigen that interacts with human erythrocyte integrin associated protein (CD47)[J]. Sci Rep, 2019, 9(1): 5923. doi: 10.1038/s41598-019-42366-9
    Della Pelle G, Delgado López A, Salord Fiol M, et al. Cyanine dyes for photo-thermal therapy: a comparison of synthetic liposomes and natural erythrocyte-based carriers[J]. Int J Mol Sci, 2021, 22(13): 6914. doi: 10.3390/ijms22136914
    Zhang KL, Wang YJ, Sun J, et al. Artificial chimeric exosomes for anti-phagocytosis and targeted cancer therapy[J]. Chem Sci, 2019, 10(5): 1555−1561. doi: 10.1039/c8sc03224f
    Navarathna DH, Stein EV, Lessey-Morillon EC, et al. CD47 promotes protective innate and adaptive immunity in a mouse model of disseminated candidiasis[J]. PLoS One, 2015, 10(5): e0128220. doi: 10.1371/journal.pone.0128220
    Myers DR, Abram CL, Wildes D, et al. Shp1 loss enhances macrophage effector function and promotes anti-tumor immunity[J]. Front Immunol, 2020, 11: 576310. doi: 10.3389/fimmu.2020.576310
    Hendriks MAJM, Ploeg EM, Koopmans I, et al. Bispecific antibody approach for EGFR-directed blockade of the CD47-SIRPalpha "don't eat me" immune checkpoint promotes neutrophil-mediated trogoptosis and enhances antigen cross-presentation[J]. Oncoimmunology, 2020, 9(1): 1824323. doi: 10.1080/2162402X.2020.1824323
    Tal MC, Torrez Dulgeroff LB, Myers L, et al. Upregulation of CD47 is a host checkpoint response to pathogen recognition[J]. mBio, 2020, 11(3): e01293−20. doi: 10.1128/mBio.01293-20
    Hayes BH, Tsai RK, Dooling LJ, et al. Macrophages show higher levels of engulfment after disruption of cis interactions between CD47 and the checkpoint receptor SIRPalpha[J]. J Cell Sci, 2020, 133(5): jcs237800. doi: 10.1242/jcs.237800
    Murata Y, Kotani T, Ohnishi H, et al. The CD47-SIRPalpha signalling system: its physiological roles and therapeutic application[J]. J Biochem, 2014, 155(6): 335−344. doi: 10.1093/jb/mvu017
    Burger P, Hilarius-Stokman P, de Korte D, et al. CD47 functions as a molecular switch for erythrocyte phagocytosis[J]. Blood, 2012, 119(23): 5512−5521. doi: 10.1182/blood-2011-10-386805
    Meinderts SM, Oldenborg PA, Beuger BM, et al. Human and murine splenic neutrophils are potent phagocytes of IgG-opsonized red blood cells[J]. Blood Adv, 2017, 1(14): 875−886. doi: 10.1182/bloodadvances.2017004671
    Romero PJ, Hernández-Chinea C. The action of red cell calcium ions on human erythrophagocytosis in vitro[J]. Front Physiol, 2017, 8: 1008. doi: 10.3389/fphys.2017.01008
    Hillary RF, Trejo-Banos D, Kousathanas A, et al. Multi-method genome- and epigenome-wide studies of inflammatory protein levels in healthy older adults[J]. Genome Med, 2020, 12(1): 60. doi: 10.1186/s13073-020-00754-1
    Lee JS, Wurfel MM, Matute-Bello G, et al. The Duffy antigen modifies systemic and local tissue chemokine responses following lipopolysaccharide stimulation[J]. J Immunol, 2006, 177(11): 8086−8094. doi: 10.4049/jimmunol.177.11.8086
    Rincon MR, Oppenheimer K, Bonney EA. Selective accumulation of Th2-skewing immature erythroid cells in developing neonatal mouse spleen[J]. Int J Biol Sci, 2012, 8(5): 719−730. doi: 10.7150/ijbs.3764
    Sennikov SV, Injelevskaya TV, Krysov SV, et al. Production of hemo- and immunoregulatory cytokines by erythroblast antigen+ and glycophorin A+ cells from human bone marrow[J]. BMC Cell Biol, 2004, 5(1): 39. doi: 10.1186/1471-2121-5-39
    Wei J, Zhao J, Schrott V, et al. Red blood cells store and release interleukin-33[J]. J Investig Med, 2015, 63(6): 806−810. doi: 10.1097/JIM.0000000000000213
    Bao GQ, Ju AZ. Signal pathways of eryptosis-review[J]. J Exp Hematol (in Chinese), 2009, 17(4): 1097–1100.https://pubmed.ncbi.nlm.nih.gov/19698269/
    Föller M, Huber SM, Lang F. Erythrocyte programmed cell death[J]. IUBMB Life, 2008, 60(10): 661−668. doi: 10.1002/iub.106
    Klarl BA, Lang PA, Kempe DS, et al. Protein kinase C mediates erythrocyte "programmed cell death" following glucose depletion[J]. Am J Physiol Cell Physiol, 2006, 290(1): C244−53. doi: 10.1152/ajpcell.00283.2005
    Lang F, Lang E, Föller M. Physiology and pathophysiology of eryptosis[J]. Transfus Med Hemother, 2012, 39(5): 308−314. doi: 10.1159/000342534
    Antonelou MH, Kriebardis AG, Papassideri IS. Aging and death signalling in mature red cells: from basic science to transfusion practice[J]. Blood Transfus, 2010, Suppl 3(Suppl 3): s39−47. doi: 10.2450/2010.007S
    Huang YX, Wu ZJ, Mehrishi J, et al. Human red blood cell aging: correlative changes in surface charge and cell properties[J]. J Cell Mol Med, 2011, 15(12): 2634−2642. doi: 10.1111/j.1582-4934.2011.01310.x
    Jeney V. Pro-inflammatory actions of red blood cell-derived DAMPs[J]. Exp Suppl, 2018, 108: 211−233. doi: 10.1007/978-3-319-89390-7_9
    Whitman JC, Paw BH, Chung J. The role of ClpX in erythropoietic protoporphyria[J]. Hematol Transfus Cell Ther, 2018, 40(2): 182−188. doi: 10.1016/j.htct.2018.03.001
    Fujiwara T, Harigae H. Biology of heme in mammalian erythroid cells and related disorders[J]. Biomed Res Int, 2015, 2015: 278536. doi: 10.1155/2015/278536
    Xu HH, Jiang ZH, Sun YT, et al. Differences in the hemolytic behavior of two isomers in ophiopogon japonicus in vitro and in vivo and their risk warnings[J]. Oxid Med Cell Longev, 2020, 2020: 8870656. doi: 10.1155/2020/8870656
    Schaer DJ, Buehler PW, Alayash AI, et al. Hemolysis and free hemoglobin revisited: exploring hemoglobin and hemin scavengers as a novel class of therapeutic proteins[J]. Blood, 2013, 121(8): 1276−1284. doi: 10.1182/blood-2012-11-451229
    Dutra FF, Alves LS, Rodrigues D, et al. Hemolysis-induced lethality involves inflammasome activation by heme[J]. Proc Natl Acad Sci U S A, 2014, 111(39): E4110−8. doi: 10.1073/pnas.1405023111
    Canesin G, Hejazi SM, Swanson KD, et al. Heme-derived metabolic signals dictate immune responses[J]. Front Immunol, 2020, 11: 66. doi: 10.3389/fimmu.2020.00066
    Fortes GB, Alves LS, de Oliveira R, et al. Heme induces programmed necrosis on macrophages through autocrine TNF and ROS production[J]. Blood, 2012, 119(10): 2368−2675. doi: 10.1182/blood-2011-08-375303
    Belcher JD, Chen C, Nguyen J, et al. Heme triggers TLR4 signaling leading to endothelial cell activation and vaso-occlusion in murine sickle cell disease[J]. Blood, 2014, 123(3): 377−390. doi: 10.1182/blood-2013-04-495887
    Wegiel B, Hauser CJ, Otterbein LE. Heme as a danger molecule in pathogen recognition[J]. Free Radic Biol Med, 2015, 89: 651−661. doi: 10.1016/j.freeradbiomed.2015.08.020
    Ghosh S, Adisa OA, Chappa P, et al. Extracellular hemin crisis triggers acute chest syndrome in sickle mice[J]. J Clin Invest, 2013, 123(11): 4809−4820. doi: 10.1172/JCI64578
    Bozza MT, Jeney V. Pro-inflammatory actions of heme and other hemoglobin-derived DAMPs[J]. Front Immunol, 2020, 11: 1323. doi: 10.3389/fimmu.2020.01323
    Frimat M, Boudhabhay I, Roumenina LT. Hemolysis derived products toxicity and endothelium: model of the second hit[J]. Toxins (Basel), 2019, 11(11): 660. doi: 10.3390/toxins11110660
    Simões RL, Arruda MA, Canetti C, et al. Proinflammatory responses of heme in alveolar macrophages: repercussion in lung hemorrhagic episodes[J]. Mediators Inflamm, 2013, 2013: 946878. doi: 10.1155/2013/946878
    Mooney JP, Barry A, Goncalves BP, et al. Haemolysis and haem oxygenase-1 induction during persistent "asymptomatic" malaria infection in Burkinabe children[J]. Malar J, 2018, 17(1): 253. doi: 10.1186/s12936-018-2402-6
    Liew FY, Girard JP, Turnquist HR. Interleukin-33 in health and disease[J]. Nat Rev Immunol, 2016, 16(11): 676−689. doi: 10.1038/nri.2016.95
    Kearley J, Silver JS, Sanden C, et al. Cigarette smoke silences innate lymphoid cell function and facilitates an exacerbated type I interleukin-33-dependent response to infection[J]. Immunity, 2015, 42(3): 566−579. doi: 10.1016/j.immuni.2015.02.011
    Drake LY, Kita H. IL-33: biological properties, functions, and roles in airway disease[J]. Immunol Rev, 2017, 278(1): 173−184. doi: 10.1111/imr.12552
    McSorley HJ, Smyth DJ. IL-33: a central cytokine in helminth infections[J]. Semin Immunol, 2021, 53: 101532. doi: 10.1016/j.smim.2021.101532
    Cayrol C, Girard JP. Interleukin-33 (IL-33): a nuclear cytokine from the IL-1 family[J]. Immunol Rev, 2018, 281(1): 154−168. doi: 10.1111/imr.12619
    Cayrol C, Girard JP. IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy[J]. Curr Opin Immunol, 2014, 31: 31−37. doi: 10.1016/j.coi.2014.09.004
    Byers DE, Alexander-Brett J, Patel AC, et al. Long-term IL-33-producing epithelial progenitor cells in chronic obstructive lung disease[J]. J Clin Invest, 2013, 123(9): 3967−3982. doi: 10.1172/JCI65570
    Tamagawa-Mineoka R, Okuzawa Y, Masuda K, et al. Increased serum levels of interleukin 33 in patients with atopic dermatitis[J]. J Am Acad Dermatol, 2014, 70(5): 882−888. doi: 10.1016/j.jaad.2014.01.867
    Raeiszadeh Jahromi S, Mahesh PA, Jayaraj BS, et al. Serum levels of IL-10, IL-17F and IL-33 in patients with asthma: a case-control study[J]. J Asthma, 2014, 51(10): 1004−13. doi: 10.3109/02770903.2014.938353
    Kasahara DI, Wilkinson JE, Cho Y, et al. The interleukin-33 receptor contributes to pulmonary responses to ozone in male mice: role of the microbiome[J]. Respir Res, 2019, 20(1): 197. doi: 10.1186/s12931-019-1168-x
    Nadafi R, Arens R. The curious case of IL-33 in homeostasis and infection[J]. Eur J Immunol, 2021, 51(1): 60−63. doi: 10.1002/eji.202049031
    Hoogerwerf JJ, Tanck MW, van Zoelen MA, et al. Soluble ST2 plasma concentrations predict mortality in severe sepsis[J]. Intensive Care Med, 2010, 36(4): 630−637. doi: 10.1007/s00134-010-1773-0
    Darbonne WC, Rice GC, Mohler MA, et al. Red blood cells are a sink for interleukin 8, a leukocyte chemotaxin[J]. J Clin Invest, 1991, 88(4): 1362−1369. doi: 10.1172/JCI115442
    Karsten E, Breen E, Herbert BR. Red blood cells are dynamic reservoirs of cytokines[J]. Sci Rep, 2018, 8(1): 3101. doi: 10.1038/s41598-018-21387-w
    Seeland S, Kettiger H, Murphy M, et al. ATP-induced cellular stress and mitochondrial toxicity in cells expressing purinergic P2X7 receptor[J]. Pharmacol Res Perspect, 2015, 3(2): e00123. doi: 10.1002/prp2.123
    Li Y, Zhou J, Burkovskiy I, et al. ATP in red blood cells as biomarker for sepsis in humans[J]. Med Hypotheses, 2019, 124: 84−86. doi: 10.1016/j.mehy.2019.02.014
    Kalan G, Derganc M, Primožič J. Phosphate metabolism in red blood cells of critically ill neonates[J]. Pflugers Arch, 2000, 440(5 Suppl): R109−11. doi: 10.1007/s004240000026
    Heming N, Salah A, Meng P, et al. Thiamine status and lactate concentration in sepsis: a prospective observational study[J]. Medicine (Baltimore), 2020, 99(7): e18894. doi: 10.1097/MD.0000000000018894
    Kirby BS, Crecelius AR, Voyles WF, et al. Impaired skeletal muscle blood flow control with advancing age in humans: attenuated ATP release and local vasodilation during erythrocyte deoxygenation[J]. Circ Res, 2012, 111(2): 220−230. doi: 10.1161/CIRCRESAHA.112.269571
    Yeung PK, Kolathuru SS, Mohammadizadeh S, et al. Adenosine 5'-triphosphate metabolism in red blood cells as a potential biomarker for post-exercise hypotension and a drug target for cardiovascular protection[J]. Metabolites, 2018, 8(2): 30. doi: 10.3390/metabo8020030
    Rocha M, Herance R, Rovira S, et al. Mitochondrial dysfunction and antioxidant therapy in sepsis[J]. Infect Disord Drug Targets, 2012, 12(2): 161−178. doi: 10.2174/187152612800100189
    Ferguson BS, Neidert LE, Rogatzki MJ, et al. Red blood cell ATP release correlates with red blood cell hemolysis[J]. Am J Physiol Cell Physiol, 2021, 321(5): C761−C769. doi: 10.1152/ajpcell.00510.2020
    Sikora J, Orlov SN, Furuya K, et al. Hemolysis is a primary ATP-release mechanism in human erythrocytes[J]. Blood, 2014, 124(13): 2150−2157. doi: 10.1182/blood-2014-05-572024
    Burnstock G. Purinergic signaling in the cardiovascular system[J]. Circ Res, 2017, 120(1): 207−228. doi: 10.1161/CIRCRESAHA.116.309726
    Song N, Ma J, Meng XW, et al. Heat shock protein 70 protects the heart from ischemia/reperfusion injury through inhibition of p38 MAPK signaling[J]. Oxid Med Cell Longev, 2020, 2020: 3908641. doi: 10.1155/2020/3908641
    Vacchina P, Norris-Mullins B, Carlson ES, et al. A mitochondrial HSP70 (HSPA9B) is linked to miltefosine resistance and stress response in Leishmania donovani[J]. Parasit Vectors, 2016, 9(1): 621. doi: 10.1186/s13071-016-1904-8
    Igarashi Y, Ohnishi K, Irie K, et al. Possible contribution of zerumbone-induced proteo-stress to its anti-inflammatory functions via the activation of heat shock factor 1[J]. PLoS One, 2016, 11(8): e0161282. doi: 10.1371/journal.pone.0161282
    Gromov PS, Celis JE. Identification of two molecular chaperons (HSX70, HSC70) in mature human erythrocytes[J]. Exp Cell Res, 1991, 195(2): 556−559. doi: 10.1016/0014-4827(91)90412-n
    Bhattacharya D, Saha S, Basu S, et al. Differential regulation of redox proteins and chaperones in HbEbeta-thalassemia erythrocyte proteome[J]. Proteomics Clin Appl, 2010, 4(5): 480−488. doi: 10.1002/prca.200900073
    Adewoye AH, Klings ES, Farber HW, et al. Sickle cell vaso-occlusive crisis induces the release of circulating serum heat shock protein-70[J]. Am J Hematol, 2005, 78(3): 240−242. doi: 10.1002/ajh.20292
    Molvarec A, Derzsy Z, Kocsis J, et al. Circulating anti-heat-shock-protein antibodies in normal pregnancy and preeclampsia[J]. Cell Stress Chaperones, 2009, 14(5): 491−498. doi: 10.1007/s12192-009-0102-4
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