Resolution-Associated Molecular Patterns (RAMPs) as Endogenous Regulators of Glia Functions in Neuroinflammatory Disease

Author(s): Tyler J. Wenzel, Evan Kwong, Ekta Bajwa, Andis Klegeris*

Journal Name: CNS & Neurological Disorders - Drug Targets
Formerly Current Drug Targets - CNS & Neurological Disorders

Volume 19 , Issue 7 , 2020


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Graphical Abstract:


Abstract:

Glial cells, including microglia and astrocytes, facilitate the survival and health of all cells within the Central Nervous System (CNS) by secreting a range of growth factors and contributing to tissue and synaptic remodeling. Microglia and astrocytes can also secrete cytotoxins in response to specific stimuli, such as exogenous Pathogen-Associated Molecular Patterns (PAMPs), or endogenous Damage-Associated Molecular Patterns (DAMPs). Excessive cytotoxic secretions can induce the death of neurons and contribute to the progression of neurodegenerative disorders, such as Alzheimer’s disease (AD). The transition between various activation states of glia, which include beneficial and detrimental modes, is regulated by endogenous molecules that include DAMPs, cytokines, neurotransmitters, and bioactive lipids, as well as a diverse group of mediators sometimes collectively referred to as Resolution-Associated Molecular Patterns (RAMPs). RAMPs are released by damaged or dying CNS cells into the extracellular space where they can induce signals in autocrine and paracrine fashions by interacting with glial cell receptors. While the complete range of their effects on glia has not been described yet, it is believed that their overall function is to inhibit adverse CNS inflammatory responses, facilitate tissue remodeling and cellular debris removal. This article summarizes the available evidence implicating the following RAMPs in CNS physiological processes and neurodegenerative diseases: cardiolipin (CL), prothymosin α (ProTα), binding immunoglobulin protein (BiP), heat shock protein (HSP) 10, HSP 27, and αB-crystallin. Studies on the molecular mechanisms engaged by RAMPs could identify novel glial targets for development of therapeutic agents that effectively slow down neuroinflammatory disorders including AD.

Keywords: αB-crystallin, astrocytes, cardiolipin, DAMPs, heat shock proteins, microglia, prothymosin, toll-like receptors.

[1]
Dukay B, Csoboz B, Tóth ME. Heat-shock proteins in neuroinflammation. Front Pharmacol 2019; 10: 920.
[http://dx.doi.org/10.3389/fphar.2019.00920] [PMID: 31507418]
[2]
Paudel YN, Shaikh MF, Chakraborti A, et al. HMGB1: a common biomarker and potential target for TBI, neuroinflammation, epilepsy, and cognitive dysfunction. Front Neurosci 2018; 12: 628.
[http://dx.doi.org/10.3389/fnins.2018.00628] [PMID: 30271319]
[3]
Wang S, Song R, Wang Z, Jing Z, Wang S, Ma J. S100A8/A9 in Inflammation. Front Immunol 2018; 9: 1298.
[http://dx.doi.org/10.3389/fimmu.2018.01298] [PMID: 29942307]
[4]
Andersson U, Yang H, Harris H. High-Mobility Group Box 1 protein (HMGB1) operates as an alarmin outside as well as inside cells. Semin Immunol 2018; 38: 40-8.
[http://dx.doi.org/10.1016/j.smim.2018.02.011] [PMID: 29530410]
[5]
Jhang KA, Lee EO, Kim HS, Chang KA, Suh Y-H, Chong YH. S100A9 exacerbates the A(beta)1-42-mediated innate immunity in human THP-1 monocytes. CNS Neurol Disord Drug Targets 2016; 15(8): 910-7.
[http://dx.doi.org/10.2174/1871527315666160815161922] [PMID: 27577740]
[6]
Bortolotto V, Grilli M. Every cloud has a silver lining: proneurogenic effects of Aβ; oligomers and HMGB-1 via activation of the RAGE-NF-κB axis. CNS Neurol Disord Drug Targets 2017; 16(10): 1066-79.
[http://dx.doi.org/10.2174/1871527315666160803153459] [PMID: 27488419]
[7]
Pointer CB, Wenzel TJ, Klegeris A. Extracellular cardiolipin regulates select immune functions of microglia and microglia-like cells. Brain Res Bull 2019; 146: 153-63.
[http://dx.doi.org/10.1016/j.brainresbull.2019.01.002] [PMID: 30625370]
[8]
Gouveia A, Bajwa E, Klegeris A. Extracellular cytochrome c as an intercellular signaling molecule regulating microglial functions. Biochim Biophys Acta, Gen Subj 2017; 1861(9): 2274-81.
[http://dx.doi.org/10.1016/j.bbagen.2017.06.017] [PMID: 28652078]
[9]
Wenzel TJ, Bajwa E, Klegeris A. Cytochrome c can be released into extracellular space and modulate functions of human astrocytes in a toll-like receptor 4-dependent manner. Biochim Biophys Acta, Gen Subj 2019; 1863(11)129400
[http://dx.doi.org/10.1016/j.bbagen.2019.07.009] [PMID: 31344401]
[10]
Venegas C, Heneka MT. Danger-associated molecular patterns in Alzheimer’s disease. J Leukoc Biol 2017; 101(1): 87-98.
[http://dx.doi.org/10.1189/jlb.3MR0416-204R] [PMID: 28049142]
[11]
Kakimura J ichi, Kitamura Y, Taniguchi T, Shimohama S, Gebicke-Haerter PJ. BiP/GRP78-induced production of cytokines and uptake of amyloid-β(1-42) peptide in microglia. Biochem Biophys Res Commun 2001; 281: 6-10.
[http://dx.doi.org/10.1006/bbrc.2001.4299]
[12]
Guo Y shun, Liang P zhou, Lu S zhao, Chen R, Yin Y qing, Zhou J wei. Extracellular αB-crystallin modulates the inflammatory responses. Biochem Biophys Res Commun 2019; 508: 282-8.
[13]
Wakida NM, Cruz GMS, Ro CC, et al. Phagocytic response of astrocytes to damaged neighboring cells. PLoS One 2018; 13(4)e0196153
[http://dx.doi.org/10.1371/journal.pone.0196153] [PMID: 29708987]
[14]
Renz A, Berdel WE, Kreuter M, Belka C, Schulze-Osthoff K, Los M. Rapid extracellular release of cytochrome c is specific for apoptosis and marks cell death in vivo. Blood 2001; 98(5): 1542-8.
[http://dx.doi.org/10.1182/blood.V98.5.1542] [PMID: 11520805]
[15]
Ahlemeyer B, Klumpp S, Krieglstein J. Release of cytochrome c into the extracellular space contributes to neuronal apoptosis induced by staurosporine. Brain Res 2002; 934(2): 107-16.
[http://dx.doi.org/10.1016/S0006-8993(02)02365-X] [PMID: 11955473]
[16]
Madeira JM, Little JP, Klegeris A. Microglia secretome: from neurotoxins to neurotrophins. In:Microglia: Biology, Functions and Roles in Disease New York: Nova Science Publishers pp. 73-92.
[17]
Hashioka S, Klegeris A, Schwab C, McGeer PL. Interferon-γ-dependent cytotoxic activation of human astrocytes and astrocytoma cells. Neurobiol Aging 2009; 30(12): 1924-35.
[http://dx.doi.org/10.1016/j.neurobiolaging.2008.02.019] [PMID: 18375019]
[18]
Brown GC, Vilalta A. How microglia kill neurons. Brain Res 2015; 1628(Pt B): 288-97.
[http://dx.doi.org/10.1016/j.brainres.2015.08.031] [PMID: 26341532]
[19]
Czeh M, Gressens P, Kaindl AM. The yin and yang of microglia. Dev Neurosci 2011; 33(3-4): 199-209.
[http://dx.doi.org/10.1159/000328989] [PMID: 21757877]
[20]
Amor S, Peferoen LAN, Vogel DYS, et al. Inflammation in neurodegenerative diseases--an update. Immunology 2014; 142(2): 151-66.
[http://dx.doi.org/10.1111/imm.12233] [PMID: 24329535]
[21]
Maeda S, Sasaki K, Halder SK, Fujita W, Ueda H. Neuroprotective DAMPs member prothymosin alpha has additional beneficial actions against cerebral ischemia-induced vascular damages. J Pharmacol Sci 2016; 132(1): 100-4.
[http://dx.doi.org/10.1016/j.jphs.2016.05.006] [PMID: 27543170]
[22]
Franco FJ, Diaz C, Barcia M, et al. Synthesis and apparent secretion of prothymosin α by different subpopulations of calf and rat thymocytes. Immunology 1989; 67(2): 263-8.
[PMID: 2787781]
[23]
Shields AM, Panayi GS, Corrigall VM. Resolution-Associated Molecular Patterns (RAMP): RAMParts defending immunological homeostasis? Clin Exp Immunol 2011; 165(3): 292-300.
[http://dx.doi.org/10.1111/j.1365-2249.2011.04433.x] [PMID: 21671907]
[24]
Starossom SC, Mascanfroni ID, Imitola J, et al. Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity 2012; 37(2): 249-63.
[http://dx.doi.org/10.1016/j.immuni.2012.05.023] [PMID: 22884314]
[25]
Tóth ME, Szegedi V, Varga E, et al. Overexpression of Hsp27 ameliorates symptoms of Alzheimer’s disease in APP/PS1 mice. Cell Stress Chaperones 2013; 18(6): 759-71.
[http://dx.doi.org/10.1007/s12192-013-0428-9] [PMID: 23605646]
[26]
Yang Y, Turner RS, Gaut JR. The chaperone BiP/GRP78 binds to amyloid precursor protein and decreases Abeta40 and Abeta42 secretion. J Biol Chem 1998; 273(40): 25552-5.
[http://dx.doi.org/10.1074/jbc.273.40.25552] [PMID: 9748217]
[27]
Ordóñez-Gutiérrez L, Re F, Bereczki E, et al. Repeated intraperitoneal injections of liposomes containing phosphatidic acid and cardiolipin reduce amyloid-β levels in APP/PS1 transgenic mice. Nanomedicine (Lond) 2015; 11(2): 421-30.
[http://dx.doi.org/10.1016/j.nano.2014.09.015] [PMID: 25461285]
[28]
Vanags D, Williams B, Johnson B, et al. Therapeutic efficacy and safety of chaperonin 10 in patients with rheumatoid arthritis: a double-blind randomised trial. Lancet 2006; 368(9538): 855-63.
[http://dx.doi.org/10.1016/S0140-6736(06)69210-6] [PMID: 16950363]
[29]
Kirkham B, Chaabo K, Hall C, et al. Safety and patient response as indicated by biomarker changes to binding immunoglobulin protein in the phase I/IIA RAGULA clinical trial in rheumatoid arthritis. Rheumatology (Oxford) 2016; 55(11): 1993-2000.
[http://dx.doi.org/10.1093/rheumatology/kew287] [PMID: 27498355]
[30]
van Noort JM, Bsibsi M, Nacken PJ, Verbeek R, Venneker EHG. Therapeutic intervention in multiple sclerosis with alpha B-crystallin: a randomized controlled phase IIa trial. PLoS One 2015; 10(11)e0143366
[http://dx.doi.org/10.1371/journal.pone.0143366] [PMID: 26599332]
[31]
Renkawek K, Voorter CEM, Bosman GJCGM, van Workum FPA, de Jong WW. Expression of α B-crystallin in Alzheimer’s disease. Acta Neuropathol 1994; 87(2): 155-60.
[http://dx.doi.org/10.1007/BF00296185] [PMID: 8171966]
[32]
Birmpilis AI, Karachaliou C-E, Samara P, et al. Antitumor reactive T-cell responses are enhanced in vivo by DAMP prothymosin alpha and its C-terminal decapeptide. Cancers (Basel) 2019; 11(11): 1764.
[http://dx.doi.org/10.3390/cancers11111764] [PMID: 31717548]
[33]
Chen GY, Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 2010; 10(12): 826-37.
[http://dx.doi.org/10.1038/nri2873] [PMID: 21088683]
[34]
Broere F, van der Zee R, van Eden W. Heat shock proteins are no DAMPs, rather ‘DAMPERs’. Nat Rev Immunol 2011; 11(8): 565.
[http://dx.doi.org/10.1038/nri2873-c1] [PMID: 21785457]
[35]
Samara P, Ioannou K, Neagu M, et al. The C-terminal decapeptide of prothymosin α is responsible for its stimulatory effect on the functions of human neutrophils in vitro. Int Immunopharmacol 2013; 15(1): 50-7.
[http://dx.doi.org/10.1016/j.intimp.2012.11.011] [PMID: 23201434]
[36]
Sahara N, Maeda S, Yoshiike Y, et al. Molecular chaperone-mediated tau protein metabolism counteracts the formation of granular tau oligomers in human brain. J Neurosci Res 2007; 85(14): 3098-108.
[http://dx.doi.org/10.1002/jnr.21417] [PMID: 17628496]
[37]
Kundel F, De S, Flagmeier P, et al. Hsp70 inhibits the nucleation and elongation of tau and sequesters tau aggregates with high affinity. ACS Chem Biol 2018; 13(3): 636-46.
[http://dx.doi.org/10.1021/acschembio.7b01039] [PMID: 29300447]
[38]
Pointer CB, Klegeris A. Cardiolipin in central nervous system physiology and pathology. Cell Mol Neurobiol 2017; 37(7): 1161-72.
[http://dx.doi.org/10.1007/s10571-016-0458-9] [PMID: 28039536]
[39]
Minkler PE, Hoppel CL. Separation and characterization of cardiolipin molecular species by reverse-phase ion pair high-performance liquid chromatography-mass spectrometry. J Lipid Res 2010; 51(4): 856-65.
[http://dx.doi.org/10.1194/jlr.D002857] [PMID: 19965604]
[40]
Sorice M, Circella A, Misasi R, et al. Cardiolipin on the surface of apoptotic cells as a possible trigger for antiphospholipids antibodies. Clin Exp Immunol 2000; 122(2): 277-84.
[http://dx.doi.org/10.1046/j.1365-2249.2000.01353.x] [PMID: 11091286]
[41]
Deguchi H, Fernandez JA, Hackeng TM, Banka CL, Griffin JH. Cardiolipin is a normal component of human plasma lipoproteins. Proc Natl Acad Sci USA 2000; 97(4): 1743-8.
[http://dx.doi.org/10.1073/pnas.97.4.1743] [PMID: 10677528]
[42]
Balasubramanian K, Maeda A, Lee JS, et al. Dichotomous roles for externalized cardiolipin in extracellular signaling: Promotion of phagocytosis and attenuation of innate immunity. Sci Signal 2015; 8(395): ra95.
[http://dx.doi.org/10.1126/scisignal.aaa6179] [PMID: 26396268]
[43]
Sato K. Effects of microglia on neurogenesis. Glia 2015; 63(8): 1394-405.
[http://dx.doi.org/10.1002/glia.22858] [PMID: 26010551]
[44]
Elkabes S, DiCicco-Bloom EM, Black IB. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 1996; 16(8): 2508-21.
[http://dx.doi.org/10.1523/JNEUROSCI.16-08-02508.1996] [PMID: 8786427]
[45]
Curtis J, Kim G, Wehr NB, Levine RL. Group B streptococcal phospholipid causes pulmonary hypertension. Proc Natl Acad Sci 2003; 100: 5087-90.
[46]
Leitner GR, Wenzel TJ, Marshall N, Gates EJ, Klegeris A. Targeting toll-like receptor 4 to modulate neuroinflammation in central nervous system disorders. Expert Opin Ther Targets 2019; 23(10): 865-82.
[http://dx.doi.org/10.1080/14728222.2019.1676416] [PMID: 31580163]
[47]
Cao D, Luo J, Chen D, et al. CD36 regulates lipopolysaccharide-induced signaling pathways and mediates the internalization of Escherichia coli in cooperation with TLR4 in goat mammary gland epithelial cells. Sci Rep 2016; 6: 23132-44.
[http://dx.doi.org/10.1038/srep23132] [PMID: 26976286]
[48]
Erdman LK, Cosio G, Helmers AJ, Gowda DC, Grinstein S, Kain KC. CD36 and TLR interactions in inflammation and phagocytosis: implications for malaria. J Immunol 2009; 183(10): 6452-9.
[http://dx.doi.org/10.4049/jimmunol.0901374] [PMID: 19864601]
[49]
Uhlén M, Fagerberg L, Hallström BM, et al. Tissue-based map of the human proteome Science (80-) 2015; 347: 12604191.
[http://dx.doi.org/10.1126/science.1260419]
[50]
Eschenfeldt WH, Berger SL. The human prothymosin alpha gene is polymorphic and induced upon growth stimulation: evidence using a cloned cDNA. Proc Natl Acad Sci USA 1986; 83(24): 9403-7.
[http://dx.doi.org/10.1073/pnas.83.24.9403] [PMID: 3467312]
[51]
Smith MR, al-Katib A, Mohammad R, et al. Prothymosin α gene expression correlates with proliferation, not differentiation, of HL-60 cells. Blood 1993; 82(4): 1127-32.
[http://dx.doi.org/10.1182/blood.V82.4.1127.1127] [PMID: 8353279]
[52]
Panneerselvam C, Haritos AA, Caldarella J, Horecker BL. Prothymosin alpha in human blood. Proc Natl Acad Sci USA 1987; 84(13): 4465-9.
[http://dx.doi.org/10.1073/pnas.84.13.4465] [PMID: 3474615]
[53]
Mosoian A, Teixeira A, Burns CS, et al. Prothymosin-alpha inhibits HIV-1 via Toll-like receptor 4-mediated type I interferon induction. Proc Natl Acad Sci USA 2010; 107(22): 10178-83.
[http://dx.doi.org/10.1073/pnas.0914870107] [PMID: 20479248]
[54]
Skopeliti M, Kratzer U, Altenberend F, et al. Proteomic exploitation on prothymosin α-induced mononuclear cell activation. Proteomics 2007; 7(11): 1814-24.
[http://dx.doi.org/10.1002/pmic.200600870] [PMID: 17474146]
[55]
Kakimura J, Kitamura Y, Takata K, et al. Microglial activation and amyloid-β clearance induced by exogenous heat-shock proteins. FASEB J 2002; 16(6): 601-3.
[http://dx.doi.org/10.1096/fj.01-0530fje] [PMID: 11919167]
[56]
Fujita R, Ueda H. Prothymosin-α1 prevents necrosis and apoptosis following stroke. Cell Death Differ 2007; 14(10): 1839-42.
[http://dx.doi.org/10.1038/sj.cdd.4402189] [PMID: 17599097]
[57]
Lucke-Wold BP, Turner RC, Logsdon AF, et al. Common mechanisms of Alzheimer’s disease and ischemic stroke: the role of protein kinase C in the progression of age-related neurodegeneration. J Alzheimers Dis 2015; 43(3): 711-24.
[http://dx.doi.org/10.3233/JAD-141422] [PMID: 25114088]
[58]
van Noort JM, Bugiani M, Amor S. Heat shock proteins: old and novel roles in neurodegenerative diseases in the central nervous system. CNS Neurol Disord Drug Targets 2017; 16(3): 244-56.
[http://dx.doi.org/10.2174/1871527315666161031125317] [PMID: 27804858]
[59]
Rayner K, Chen YX, McNulty M, et al. Extracellular release of the atheroprotective heat shock protein 27 is mediated by estrogen and competitively inhibits acLDL binding to scavenger receptor-A. Circ Res 2008; 103(2): 133-41.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.172155] [PMID: 18566345]
[60]
Murshid A, Theriault J, Gong J, Calderwood SK. Investigating receptors for extracellular heat shock proteins. Methods Mol Biol 2011; 787: 289-302.
[http://dx.doi.org/10.1007/978-1-61779-295-3_22] [PMID: 21898244]
[61]
Thériault JR, Adachi H, Calderwood SK. Role of scavenger receptors in the binding and internalization of heat shock protein 70. J Immunol 2006; 177(12): 8604-11.
[http://dx.doi.org/10.4049/jimmunol.177.12.8604] [PMID: 17142759]
[62]
Molteni M, Gemma S, Rossetti C. The role of toll-like receptor 4 in infectious and noninfectious inflammation. Mediators Inflamm 2016; 20166978936
[http://dx.doi.org/10.1155/2016/6978936] [PMID: 27293318]
[63]
Cohen-Sfady M, Nussbaum G, Pevsner-Fischer M, et al. Heat shock protein 60 activates B cells via the TLR4-MyD88 pathway. J Immunol 2005; 175(6): 3594-602.
[http://dx.doi.org/10.4049/jimmunol.175.6.3594] [PMID: 16148103]
[64]
Fang H, Wu Y, Huang X, et al. Toll-Like Receptor 4 (TLR4) is essential for Hsp70-like protein 1 (HSP70L1) to activate dendritic cells and induce Th1 response. J Biol Chem 2011; 286(35): 30393-400.
[http://dx.doi.org/10.1074/jbc.M111.266528] [PMID: 21730052]
[65]
Undisclosed. Chaperonin 10 as a putative modulator of multiple toll-like receptors for the treatment of inflammatory diseases. Expert Opin Ther Pat 2007; 17: 1299-308.
[http://dx.doi.org/10.1517/13543776.17.10.1299]
[66]
Mohammadi F, Nezafat N, Negahdaripour M, et al. Neuroprotective effects of heat shock protein70. CNS Neurol Disord Drug Targets 2018; 17(10): 736-42.
[http://dx.doi.org/10.2174/1871527317666180827111152] [PMID: 30147017]
[67]
Wang M, Wey S, Zhang Y, Ye R, Lee AS. Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders. Antioxid Redox Signal 2009; 11(9): 2307-16.
[http://dx.doi.org/10.1089/ars.2009.2485] [PMID: 19309259]
[68]
Corrigall VM, Bodman-Smith MD, Brunst M, Cornell H, Panayi GS. Inhibition of antigen-presenting cell function and stimulation of human peripheral blood mononuclear cells to express an antiinflammatory cytokine profile by the stress protein BiP: relevance to the treatment of inflammatory arthritis. Arthritis Rheum 2004; 50(4): 1164-71.
[http://dx.doi.org/10.1002/art.20134] [PMID: 15077298]
[69]
Aksoy MO, Kim V, Cornwell WD, et al. Secretion of the endoplasmic reticulum stress protein, GRP78, into the BALF is increased in cigarette smokers. Respir Res 2017; 18(1): 78.
[http://dx.doi.org/10.1186/s12931-017-0561-6] [PMID: 28464871]
[70]
Delpino A, Castelli M. The 78 kDa glucose-regulated protein (GRP78/BIP) is expressed on the cell membrane, is released into cell culture medium and is also present in human peripheral circulation. Biosci Rep 2002; 22(3-4): 407-20.
[http://dx.doi.org/10.1023/A:1020966008615] [PMID: 12516782]
[71]
Qin K, Ma S, Li H, et al. GRP78 impairs production of lipopolysaccharide-induced cytokines by interaction with CD14. Front Immunol 2017; 8: 579.
[http://dx.doi.org/10.3389/fimmu.2017.00579] [PMID: 28588578]
[72]
Corrigall VM, Bodman-Smith MD, Fife MS, et al. The human endoplasmic reticulum molecular chaperone BiP is an autoantigen for rheumatoid arthritis and prevents the induction of experimental arthritis. J Immunol 2001; 166: 1492-8.
[73]
Brownlie RJ, Myers LK, Wooley PH, et al. Treatment of murine collagen-induced arthritis by the stress protein BiP via interleukin-4-producing regulatory T cells: a novel function for an ancient protein. Arthritis Rheum 2006; 54(3): 854-63.
[http://dx.doi.org/10.1002/art.21654] [PMID: 16508967]
[74]
Yoshida K, Ochiai A, Matsuno H, Panayi GS, Corrigall VM. Binding immunoglobulin protein resolves rheumatoid synovitis: a xenogeneic study using rheumatoid arthritis synovial membrane transplants in SCID mice. Arthritis Res Ther 2011; 13(5): R149-9.
[http://dx.doi.org/10.1186/ar3463] [PMID: 21914218]
[75]
Nomura F, Akashi S, Sakao Y, et al. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J Immunol 2000; 164(7): 3476-9.
[http://dx.doi.org/10.4049/jimmunol.164.7.3476] [PMID: 10725699]
[76]
Jia H, Halilou AI, Hu L, Cai W, Liu J, Huang B. Heat shock protein 10 (Hsp10) in immune-related diseases: one coin, two sides. Int J Biochem Mol Biol 2011; 2(1): 47-57.
[PMID: 21969171]
[77]
Shamaei-Tousi A, D’Aiuto F, Nibali L, et al. Differential regulation of circulating levels of molecular chaperones in patients undergoing treatment for periodontal disease. PLoS One 2007; 2(11)e1198
[http://dx.doi.org/10.1371/journal.pone.0001198] [PMID: 18030332]
[78]
Johnson BJ, Le TTT, Dobbin CA, et al. Heat shock protein 10 inhibits lipopolysaccharide-induced inflammatory mediator production. J Biol Chem 2005; 280(6): 4037-47.
[http://dx.doi.org/10.1074/jbc.M411569200] [PMID: 15546885]
[79]
Focosi D. Chaperonin 10 for rheumatoid arthritis. Lancet 2006; 368(9551): 1961-2.
[http://dx.doi.org/10.1016/S0140-6736(06)69799-7] [PMID: 17141697]
[80]
Athanasas-Platsis S, Zhang B, Hillyard NC, et al. Early pregnancy factor suppresses the infiltration of lymphocytes and macrophages in the spinal cord of rats during experimental autoimmune encephalomyelitis but has no effect on apoptosis. J Neurol Sci 2003; 214(1-2): 27-36.
[http://dx.doi.org/10.1016/S0022-510X(03)00170-9] [PMID: 12972385]
[81]
Zhang B, Walsh MD, Nguyen KB, et al. Early pregnancy factor treatment suppresses the inflammatory response and adhesion molecule expression in the spinal cord of SJL/J mice with experimental autoimmune encephalomyelitis and the delayed-type hypersensitivity reaction to trinitrochlorobenzene in normal BALB/c mice. J Neurol Sci 2003; 212(1-2): 37-46.
[http://dx.doi.org/10.1016/S0022-510X(03)00103-5] [PMID: 12809997]
[82]
Vidyasagar A, Wilson NA, Djamali A. Heat shock protein 27 (HSP27): biomarker of disease and therapeutic target. Fibrogenesis Tissue Repair 2012; 5(1): 7.
[http://dx.doi.org/10.1186/1755-1536-5-7] [PMID: 22564335]
[83]
Batulan Z, Pulakazhi Venu VK, Li Y, et al. Extracellular release and signaling by heat shock protein 27: Role in modifying vascular inflammation. Front Immunol 2016; 7: 285.
[http://dx.doi.org/10.3389/fimmu.2016.00285] [PMID: 27507972]
[84]
Ce P, Erkizan O, Gedizlioglu M. Elevated HSP27 levels during attacks in patients with multiple sclerosis. Acta Neurol Scand 2011; 124(5): 317-20.
[http://dx.doi.org/10.1111/j.1600-0404.2010.01475.x] [PMID: 21208199]
[85]
Jin C, Cleveland JC, Ao L, et al. Human myocardium releases heat shock protein 27 (HSP27) after global ischemia: the proinflammatory effect of extracellular HSP27 through toll-like receptor (TLR)-2 and TLR4. Mol Med 2014; 20: 280-9.
[http://dx.doi.org/10.2119/molmed.2014.00058] [PMID: 24918749]
[86]
Salari S, Seibert T, Chen YX, et al. Extracellular HSP27 acts as a signaling molecule to activate NF-κB in macrophages. Cell Stress Chaperones 2013; 18(1): 53-63.
[http://dx.doi.org/10.1007/s12192-012-0356-0] [PMID: 22851137]
[87]
Yusuf N, Nasti TH, Huang C-M, et al. Heat shock proteins HSP27 and HSP70 are present in the skin and are important mediators of allergic contact hypersensitivity. J Immunol 2009; 182(1): 675-83.
[http://dx.doi.org/10.4049/jimmunol.182.1.675] [PMID: 19109201]
[88]
Muchowski PJ, Bassuk JA, Lubsen NH, Clark JI. Human alphaB-crystallin. Small heat shock protein and molecular chaperone. J Biol Chem 1997; 272(4): 2578-82.
[http://dx.doi.org/10.1074/jbc.272.4.2578] [PMID: 8999975]
[89]
Sreekumar PG, Kannan R, Kitamura M, et al. αβ crystallin is apically secreted within exosomes by polarized human retinal pigment epithelium and provides neuroprotection to adjacent cells. PLoS One 2010; 5(10)e12578
[http://dx.doi.org/10.1371/journal.pone.0012578] [PMID: 20949024]
[90]
Holtman IR, Bsibsi M, Gerritsen WH, et al. Identification of highly connected hub genes in the protective response program of human macrophages and microglia activated by alpha B-crystallin. Glia 2017; 65(3): 460-73.
[http://dx.doi.org/10.1002/glia.23104] [PMID: 28063173]
[91]
van Noort JM, Bsibsi M, Nacken PJ, et al. Activation of an immune-regulatory macrophage response and inhibition of lung inflammation in a mouse model of COPD using heat-shock protein alpha B-crystallin-loaded PLGA microparticles. Biomaterials 2013; 34(3): 831-40.
[http://dx.doi.org/10.1016/j.biomaterials.2012.10.028] [PMID: 23117214]
[92]
Triantafilou M, Gamper FGJ, Haston RM, et al. Membrane sorting of Toll-Like Receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J Biol Chem 2006; 281(41): 31002-11.
[http://dx.doi.org/10.1074/jbc.M602794200] [PMID: 16880211]
[93]
Peri F, Calabrese V. Toll-like receptor 4 (TLR4) modulation by synthetic and natural compounds: an update. J Med Chem 2014; 57(9): 3612-22.
[http://dx.doi.org/10.1021/jm401006s] [PMID: 24188011]
[94]
Ribes S, Ebert S, Regen T, et al. Toll-like receptor stimulation enhances phagocytosis and intracellular killing of nonencapsulated and encapsulated Streptococcus pneumoniae by murine microglia. Infect Immun 2010; 78(2): 865-71.
[http://dx.doi.org/10.1128/IAI.01110-09] [PMID: 19933834]
[95]
van Brummelen EMJ, Ros W, Wolbink G, Beijnen JH, Schellens JHM. New drug development and clinical pharmacology antidrug antibody formation in oncology: Clinical relevance and challenges. Oncologist 2016; 21(10): 1260-8.
[http://dx.doi.org/10.1634/theoncologist.2016-0061] [PMID: 27440064]
[96]
Pratt KP. Anti-drug antibodies: Emerging approaches to predict, reduce or reverse biotherapeutic immunogenicity. Antibodies (Basel) 2018; 7(2): 1-19.
[http://dx.doi.org/10.3390/antib7020019] [PMID: 31544871]
[97]
Krishna M, Nadler SG. Immunogenicity to biotherapeutics - The role of anti-drug immune complexes. Front Immunol 2016; 7: 21.
[http://dx.doi.org/10.3389/fimmu.2016.00021] [PMID: 26870037]
[98]
Radic M, Pattanaik D. Cellular and molecular mechanisms of anti-phospholipid syndrome. Front Immunol 2018; 9: 969.
[http://dx.doi.org/10.3389/fimmu.2018.00969] [PMID: 29867951]
[99]
Ousman SS, Tomooka BH, van Noort JM, et al. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 2007; 448(7152): 474-9.
[http://dx.doi.org/10.1038/nature05935] [PMID: 17568699]
[100]
Carson MJ, Thrash JC, Walter B. The cellular response in neuroinflammation: the role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin Neurosci Res 2006; 6(5): 237-45.
[http://dx.doi.org/10.1016/j.cnr.2006.09.004] [PMID: 19169437]
[101]
Wenzel TJ, Klegeris A. Novel multi-target directed ligand-based strategies for reducing neuroinflammation in Alzheimer’s disease. Life Sci 2018; 207: 314-22.
[http://dx.doi.org/10.1016/j.lfs.2018.06.025] [PMID: 29940242]


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VOLUME: 19
ISSUE: 7
Year: 2020
Published on: 02 July, 2020
Page: [483 - 494]
Pages: 12
DOI: 10.2174/1871527319666200702143719
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