The Potential of Receptor for Advanced Glycation End Products (RAGE) as a Therapeutic Target for Lung Associated Diseases

Page: [679 - 689] Pages: 11

  • * (Excluding Mailing and Handling)

Abstract

The receptor for advanced glycation end products (RAGE) is a multi-ligand pattern recognition receptor that is highly expressed in lung epithelial cells. It helps alveolar epithelial cells to maintain their morphology and specific architecture. However, in various pathophysiological conditions, pulmonary tissues express a supraphysiological level of RAGE and its ligands including advanced glycation end products, high mobility group box 1 proteins, and S100 proteins. On interaction with RAGE, these ligands stimulate downstream signaling that generates inflammation and oxidative stress leading to asthma, chronic obstructive pulmonary disease, lung cancers, idiopathic pulmonary fibrosis, acute lung injury, pneumonia, bronchopulmonary dysplasia, cystic fibrosis, and sepsis. Thus, pharmacological agents that can either suppress the production of RAGE or block its biological activity would offer promising therapeutic value against pathogenesis of the aforementioned lungassociated diseases. This review presents a comprehensive overview of the recent progress made in defining the functions of RAGE in lung-associated diseases.

Keywords: Lung, RAGE, inflammation, pulmonary diseases, anti-RAGE therapy, lung epithelial cells.

Graphical Abstract

[1]
Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 2008; 8: 183-92.
[2]
Sukkar MB, Ullah MA, Gan WJ, et al. RAGE a new frontier in chronic airways disease. Br J Pharmacol 2012; 167: 1161-76.
[3]
Lambrecht BN, Hammad H. The role of dendritic and epithelial cells as master regulators of allergic air way inflammation. Lancet 2010; 376: 835-43.
[4]
Mukherjee TK, Mukhopadhyay S, Hoidal JR. Implication of receptor for advanced glycation end product (RAGE) in pulmonary health and pathophysiology. Respir Physiol Neurobiol 2008; 162: 210-5.
[5]
Buckley ST, Ehrhardt C. The receptor for advanced glycation end products (RAGE) and the lung. J Biomed Biotechnol 2010; 2010: 917108.
[6]
Neeper M, Schmidt AM, Brett J, et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 1992; 267: 14998-5004.
[7]
Ramasamy R, Yan SF, Schmidt AM. RAGE therapeutic target and biomarker of the inflammatory response--the evidence mounts. J Leukoc Biol 2009; 86: 505-12.
[8]
Mukherjee TK, Reynolds PR, Hoidal JR. Differential effect of estrogen receptor alpha and beta agonists on the receptor for advanced glycation end product expression in human microvascular endothelial cells. Biochim Biophys Acta 2005; 1745: 300-9.
[9]
Xie J, Mendez JD, Mendez-Valenzuela V, Aguilar-Hernandez MM. Cellular signaling of the receptor for advanced glycation end products (RAGE). Cell Signal 2013; 25: 2185-97.
[10]
Malik P, Chaudhry N, Mittal R, Mukherjee TK. Role of receptor for advanced glycation end products in the complication and progression of various types of cancers. Biochim Biophys Acta 2015; 1850: 1898-904.
[11]
Li J, Schmidt AM. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J Biol Chem 1997; 272: 16498-506.
[12]
Oczypok EA, Perkins TN, Oury TD. All the “RAGE” in lung disease: The receptor for advanced glycation endproducts (RAGE) is a major mediator of pulmonary inflammatory responses. Paediatr Respir Rev 2017; 23: 40-9.
[13]
Smith DJ, Yerkovich ST, Towers MA, Carroll ML, Thomas R, Upham JW. Reduced soluble receptor for advanced glycation end products in chronic obstructive pulmonary disease. Eur Respir J 2010; 37: 516-22.
[14]
Kanazawa H, Tochino Y, Asai K, et al. Validity of HMGB1 measurement in epithelial lining fluid in patients with COPD. Eur J Clin Invest 2012; 42: 419-26.
[15]
Chuah YK, Basir R, Talib H, Tie TH, Nordin N. Receptor for Advanced Glycation End Products and Its Involvement in Inflammatory Diseases. Int J Inflamm 2013; 2013: 403460.
[16]
Wautier MP, Chappey O, Corda S, et al. Activation of NADPH oxidase by AGE links oxidative stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 2001; 280: E685-94.
[17]
Busse WW, Lemanske RF. Asthma and the hygiene hypothesis. N Engl J Med 2001; 344: 350-62.
[18]
He M, Kubo H, Morimoto K, et al. Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Reports 2011; 12: 358-64.
[19]
Oczypok EA, Milutinovic PS, Alcorn JF, et al. Pulmonary receptor for advanced glycationend-products promotes asthma pathogenesis through IL-33 and accumulation of group 2 innate lymphoid cells. J Allergy Clin Immunol 2015; 136: 747-56.
[20]
Hou C, Zhao H, Liu L, et al. High mobility group protein B1 (HMGB1) in asthma comparison of patients with chronic obstructive pulmonary disease and healthy controls. Mol Med 2011; 17: 807-15.
[21]
Hancock DB, Eijgelsheim M, Wilk JB, et al. Meta-analyses of genome-wide association studies identify multiple loci associated with pulmonary function. Nat Genet 2010; 42: 45-52.
[22]
Akirav EM, Henegariu O, Preston-Hurlburt P, et al. The receptor for advanced glycation end products (RAGE) affects T cell differentiation in OVA induced asthma. PLoS One 2014; 9: e95678.
[23]
Yao L, Zhao H, Tang H, et al. The receptor for advanced glycation end products is required for β-catenin stabilization in a chemical-induced asthma model. Br J Pharmacol 2016; 173: 2600-13.
[24]
Xiong J, Zhao WQ, Huang GH, et al. Receptor for advanced glycation end products upregulates MUC5AC expression and promotes mucus overproduction in mice with toluene diisocyanate-induced asthma. Nan Fang Yi Ke Da Xue Xue Bao 2017; 37: 1301-7.
[25]
Ullah MA, Loh Z, Gan WJ, et al. Receptor for advanced glycation end products and its ligand high-mobility group box-1 mediate allergic airway sensitization and airway inflammation. J Allergy Clin Immunol 2014; 134: 440-50.
[26]
Li R, Wang J, Zhu F, et al. HMGB regulates T helper 2 and T helper17 cell differentiation both directly and indirectly in asthmatic mice. Mol Immunol 2018; 97: 45-55.
[27]
Zhou Y, Jiang YQ, Wang WX, et al. HMGB1 and RAGE levels in induced sputum correlate with asthma severity and neutrophil percentage. Hum Immunol 2012; 73: 1171-4.
[28]
Halayko AJ, Ghavami S. S100A8/A9: a mediator of severe asthma pathogene-sis, morbidity? Can J Physiol Pharmacol 2009; 87: 743-55.
[29]
Yang Z, Yan WX, Cai H, et al. S100A12 provokes mast cell activation: a potential amplification pathway in asthma and innate immunity. J Allergy Clin Immunol 2007; 119: 106-14.
[30]
El-Seify MY, Fouda EM, Nabih ES. Serum level of soluble receptor for advanced glycation end products in asthmatic children and its correlation to severity and pulmonary functions. Clin Lab 2014; 60: 957-62.
[31]
Lyu Y, Zhao H, Ye Y, et al. Decreased soluble RAGE in neutrophilic asthma is correlated with disease severity and RAGE G82S variants. Mol Med Rep 2018; 17: 4131-7.
[32]
Bediwy AS, Hassan SM, El-Najjar MR. Receptor of advanced glycation end products in childhood asthma exacerbation. Egyptian Journal of Chest Diseases and Tuberculosis 2016; 65: 15-8.
[33]
Zhang F, Su X, Huang G, et al. sRAGE alleviates neutrophilic asthma by blocking HMGB1/RAGE signaling in airway dendritic cells. Sci Rep 2017; 7: 14268.
[34]
Li M, Guo L, Wang H, et al. RAGE-ligands axis A new ‘driving force’ for cigarette smoke-induced airway inflammation in COPD? Respirology 2015; 20: 998-9.
[35]
Lewis JB, Hirschi KM, Arroyo JA, et al. Plausible roles for rage in conditions exacerbated by direct and indirect (Second hand) smoke exposure. Int J Mol Sci 2017; 18: E652.
[36]
Lee H, Lee J, Hong SH, Rahman I, Yang SR. Inhibition of RAGE Attenuates Cigarette Smoke-Induced Lung Epithelial Cell Damage via RAGE-Mediated Nrf2/DAMP Signaling. Front Pharmacol 2018; 9: 684.
[37]
Chen L, Wang T, Guo L, et al. Overexpression of RAGE contributes to cigarette smoke-induced nitric oxide generation in COPD. Lung 2014; 192: 267-75.
[38]
Chen L, Liu L, Wang T, Shen YC, Wen FQ. Receptor for advanced glycation end products a new theraputic target for chronic obstructive pulmonary disease? Arch Med Res 2013; 44: 75-6.
[39]
Gangemi S, Casciaro M, Trapani G, et al. COPD A Systematic Review Mediators Inflamm 2015; Association between HMGB1 and 2015: 164913
[40]
Reimann S, Fink L, Wilhelm J, et al. Increased S100A4 expression in the vasculature of lungs and murine model of smoke-induced emphysema. Respir Res 2015; COPD human 16:: 127.
[41]
Chen M, Wang T, Shen Y, et al. Knockout of RAGE ameliorates mainstream cigarette smoke-induced airway inflammation in mice. Int Immunopharmacol 2017; 50: 230-5.
[42]
Sambamurthy N, Leme AS, Oury TD, Shapiro SD. The receptor for advanced glycation end products (RAGE) contributes to the progression of emphysema in mice. PLoS One 2015; 10: e0118979.
[43]
Wolf L, Herr C, Niederstraber J, Beisswenger C, Bals R. Receptor for advanced glycation endproducts (RAGE) maintains pulmonary structure and regulates the response to cigarette smoke. PLoS One 2017; 12: e0180092.
[44]
Zhang Y1, Li S1, Wang G1, et al. Changes of HMGB1 and sRAGE during the recovery of COPD exacerbation. J Thorac Dis 2014; 6: 734-41.
[45]
Cheng DT, Kim DK, Cockayne DA, et al. Systemic soluble receptor for advanced glycation end products is a biomarker of emphysema and associated with AGER genetic variants in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2013; 188: 948-57.
[46]
Wood TT, Winden DR, Marlor DR, et al. Acute secondhand smoke-induced pulmonary inflammation is diminished in RAGE knockout mice. Am J Physiol Lung Cell Mol Physiol 2014; 307: L758-64.
[47]
Yonchuk JG, Silverman EK, Bowler RP, et al. Circulating soluble receptor for advanced glycation end products (srage) as a biomarker of emphysema and the rage axis in the lung. Am J Respir Crit Care Med 2015; 192: 785-92.
[48]
Miller S, Henry AP, Hodge E, et al. The ser82 rage variant affects lung function and serum rage in smokers and srage production in vitro. PLoS One 2016; 11: e0164041.
[49]
Lee H, Park JR, Kim WJ, et al. Blockade of RAGE ameliorates elastase-induced emphysema development and progression via RAGE-DAMP signaling. FASEB J 2017; 31: 2076-89.
[50]
Guo WA, Knight PR, Raghavendran K. The receptor for advanced glycation end products and acute lung injury/acute respiratory distress syndrome. Intensive Care Med 2012; 38: 1588-98.
[51]
Bernard GR, Artigas A, Brigham KL, et al. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 1994; 149: 818-24.
[52]
McElroy MC, Kasper M. The use of alveolar epithelial type I cell-selective markers to investigate lung injury and repair. Eur Respir J 2004; 24: 664-73.
[53]
Uchida T, Shirasawa M, Ware LB, et al. Receptor for advanced glycation end-products is a marker of type I cell injury in acute lung injury. Am J Respir Crit Care Med 2006; 173: 1008-15.
[54]
Calfee CS, Ware LB, Eisner MD, et al. Plasma receptor for advanced glycation end products and clinical outcomes in acute lung injury. Thorax 2008; 63: 1083-9.
[55]
Su X, Looney MR, Gupta N, Matthay MA. Receptor for advanced glycation end-products (RAGE) is an indicator of direct lung injury in models of experimental lung injury. Am J Physiol Lung Cell Mol Physiol 2008; 297: L1-5.
[56]
Zhang Z, Zhou J, Liao C, et al. RAGE deficiency attenuates the protective effect of Lidocaine against sepsis-induced acute lung injury. Inflammation 2017; 40: 601-11.
[57]
Li Y, Wu R, Zhao S, et al. RAGE/NF-κB pathway mediates lipopolysaccharide-induced inflammation in alveolar type I epithelial cells isolated from neonate rats. Inflammation 2014; 37: 1623-9.
[58]
Reynolds PR, Schmitt RE, Kasteler SD, et al. Receptors for advanced glycation end-products targeting protect against Inflammation hyperoxia-induced lung injury in mice. Am J Respir Cell Mol Biol 2010; 42: 545-51.
[59]
Wang G, Liu L, Zhang Y, et al. Activation of PPARγ attenuates LPS-induced acute lung injury by inhibition of HMGB1-RAGE levels. Eur J Pharmacol 2014; 726: 27-32.
[60]
Wang G, Han D, Zhang Y, et al. A novel hypothesis up-regulation of HO-1 by activation of PPARγ inhibits HMGB1-RAGE signaling pathway and ameliorates the development of ALI/ARDS. J Thorac Dis 2013; 5: 706-10.
[61]
Ueno H, Matsuda T, Hashimoto S, et al. Contributions of high mobility group box protein in experimental and clinical acute lung injury. Am J Respir Crit Care Med 2004; 170: 1310-6.
[62]
Cohen MJ, Brohi K, Calfee CS, et al. Early release of high mobility group box nuclear protein 1 after severe trauma in humans: role of injury severity and tissue hypoperfusion. Crit Care 2009; 13: R174.
[63]
Fu J, Lin SH, Wang CJ, et al. HMGB1 regulates IL-33 expression in acute respiratory distress syndrome. Int Immunopharmacol 2016; 38: 267-74.
[64]
He M, Kubo H, Ishizawa K, et al. The role of the receptor for advanced glycation end-products in lung fibrosis. Am J Physiol Lung Cell Mol Physiol 2007; 293: L1427-36.
[65]
Wittkowski H, Sturrock A, van Zoelen MA, et al. Neutrophil-derived S100A12 in acute lung injury and respiratory distress syndrome. Crit Care Med 2007; 35: 1369-75.
[66]
Zhang H, Tasaka S, Shiraishi Y, et al. Role of soluble receptor for advanced glycation end products on endotoxin-induced lung injury. Am J Respir Crit Care Med 2008; 178: 356-62.
[67]
Weber DJ, Gracon AS, Ripsch MS, et al. The HMGB1-RAGE axis mediates traumatic brain injury-induced pulmonary dysfunction in lung transplantation. Sci Transl Med 2014; 6: 252ra124.
[68]
Jabaudon M, Blondonnet R, Roszyk L, et al. Constantin, soluble receptor for advanced glycation end-products predicts impaired alveolar fluid clearance in acute respiratory distress syndrome. Am J Respir Crit Care Med 2015; 192: 191-9.
[69]
Wang HC, Bloom O, Zhang MH, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Sci 1999; 285: 248-51.
[70]
Laubach VE, Sharma AK. Mechanisms of lung ischemia-reperfusion injury. Curr Opin Organ Transplant 2016; 21: 246-52.
[71]
Cui T, Zhu G. Ulinastatin attenuates brain edema after traumatic brain injury in rats. Cell Biochem Biophys 2015; 71: 595-600.
[72]
Wolfson RK, Chiang ET, Garcia JGN. HMGB1 induces human lung endothelial cell cytoskeletal rearrangement and barrier disruption. Microvasc Res 2011; 81: 189-97.
[73]
Venereau E, Schiraldi M, Uguccioni M, Bianchi ME. HMGB1 and leukocyte migration during trauma and sterile inflammation. Mol Immunol 2013; 55: 76-82.
[74]
Zandarashvili L, Sahu D, Lee K, et al. Real-time kinetics of high-mobility group box 1 (HMGB1) oxidation in extracellular fluids studied by in situ protein NMR spectroscopy. J Biol Chem 2013; 288: 11621-7.
[75]
Wu X, Mi Y, Yang H, et al. The activation of HMGB1 as a progression factor on inflammation response in normal human bronchial epithelial cells through RAGE/JNK/NF- kB pathway. Mol Cell Biochem 2013; 380: 249-57.
[76]
Luan ZG, Zhang H, Yang PT, et al. HMGB1 activates nuclear factor- kB signaling by RAGE and increases the production of TNF-α in human umbilical vein endothelial cells. Immunobiol 2010; 215: 956-62.
[77]
Todd JL, Christie JD, Palmer SM. Update in lung transplantation 2013. Am J Respir Crit Care Med 2014; 190: 19-24.
[78]
Shah RJ, Bellamy SL, Lee JC, et al. Early plasma soluble receptor for advanced glycation end-product levels are associated with bronchiolitis obliterans syndrome. Am J Transplant 2013; 13: 754-9.
[79]
Selman M, Pardo A. Role of epithelial cells in idiopathic pulmonary fibrosis from innocent targets to serial killers. Proc Am Thorac Soc 2006; 3: 364-72.
[80]
Song JS, Kang CM, Park CK, et al. Inhibitory effect of receptor for advanced glycation end products (RAGE) on the TGF-β-induced alveolar epithelial to mesenchymal transition. Exp Mol Med 2011; 43: 517-24.
[81]
Hackett TL, Warner SM, Stefanowicz D, et al. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-beta1. Am J Respir Crit Care Med 2009; 180: 122-33.
[82]
Kyung SY, Byun KH, Yoon JY, et al. Advanced glycation end-products and receptor for advanced glycation end-products expression in patients with idiopathic pulmonary fibrosis and NSIP. Int J Clin Exp Pathol 2014; 7: 221-8.
[83]
Chen L, Wang T, Wang X, et al. Blockade of advanced glycation end product formation attenuates bleomycin-induced pulmonary fibrosis in rats. Respir Res 2009; 10: 55.
[84]
Aoki Y, Maeno T, Aoyagi K, et al. Pioglitazone, a peroxisome proliferator- activated receptor gamma ligand, suppresses blemycin-induced acute lung injury and fibrosis. Respiration 2009; 77: 311-9.
[85]
Stitt AW. lassara HV. Advanced glycation end products impact on diabetic complications In: Current Perspectives in diabetes. Betteridge DJ, Ed London Martin Dunitz 1999; pp. 67-C92.
[86]
Zhang L, Ji Y, Kang Z, Lv C, Jiang W. Protocatechuic aldehyde ameliorates experimental pulmonary fibrosis by modulating HMGB1/RAGE pathway. Toxicol Appl Pharmacol 2015; 283: 50-6.
[87]
Yamaguchi K, Iwamoto H, Horimasu Y, et al. AGER gene polymorphisms and soluble receptor for advanced glycation end product in patients with idiopathic pulmonary fibrosis. Respirol 2017; 22: 965-71.
[88]
Manichaikul A, Sun L, Borczuk AC, et al. Plasma soluble receptor for advanced glycation end products in idiopathic pulmonary fibrosis. Ann Am Thorac Soc 2017; 4: 628-35.
[89]
Englert JM, Hanford LE, Kaminski N, et al. A role for the receptor for advanced glycation end products in idiopathic pulmonary fibrosis. Am J Pathol 2008; 172: 583-91.
[90]
Foell D, Seeliger S, Vogl T, et al. Expression of S100A12 (EN-RAGE) in cystic fibrosis. Thorax 2003; 58: 613-7.
[91]
Hasegawa K, Mansbach JM, Teach SJ, et al. Multicenter study of viral etiology and relapse in hospitalized children with bronchiolitis. Pediatr Infect Dis J 2014; 33: 809-13.
[92]
Papadopoulos NG, Moustaki M, Tsolia M, et al. Association of rhinovirus infection with increased disease severity in acute bronchiolitis. Am J Respir Crit Care Med 2002; 165: 1285-9.
[93]
Garcia-Salido A, Onoro G, Melen GJ, et al. Serums RAGE as a potential biomarker for pediatric bronchiolitis a pilot study. Lung 2015; 193: 19-23.
[94]
Egron C, Roszyk L, Rochette E, et al. Serum soluble receptor for advanced glycation end-products during acute bronchiolitis in infant: Prospective study in 93 cases. Pediatr Pulmonol 2018; 53: 1429-35.
[95]
Levy MM, Fink MP, Marshall JC, et al. SCCM/ESICM/ ACCP/ATS/SIS international sepsis definitions conference. Crit Care Med 2003; 31: 1250-6.
[96]
Creagh-Brown BC, Quinlan GJ, Evans TW, Burke-Gaffney A. The RAGE axis in systemic inflammation, acute lung injury and myocardial dysfunction: an important therapeutic target? Intensive Care Med 2010; 36: 1644-56.
[97]
Liliensiek B, Weigand MA, Bierhaus A, et al. Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J Clin Invest 2004; 113: 1641-50.
[98]
Lutterloh EC, Opal SM, Pittman DD, et al. Inhibition of the RAGE products increases survival in experimental models of severe sepsis and systemic infection. Critical Care 2007; 11: R122.
[99]
Hu H, Shi D, Hu C, et al. Dexmedetomidine mitigates CLP-stimulated acute lung injury via restraining the RAGE pathway. Am J Transl Res 2017; 9: 5245-58.
[100]
Zhao X, Liao YN, Huang Q. The impact of RAGE inhibition in animal models of bacterial sepsis: a systematic review and meta-analysis. J Int Med Res 2018; 46: 11-21.
[101]
van Zoelen MA, Laterre PF, van Veen SQ, et al. Systemic and local high mobility group box 1 concentrations during severe infection. Crit Care Med 2007; 35: 2799-804.
[102]
Yang H1, Ochani M, Li J, et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 2004; 101: 296-301.
[103]
Matsumoto H, Matsumoto N, Ogura H, et al. The clinical significance of circulating soluble RAGE in patients with severe sepsis. J Trauma Acute Care Surg 2015; 78: 1086-93.
[104]
Wu S, Mao L, Li Y, et al. RAGE may act as a tumour suppressor to regulate lung cancer development. Gene 2018; 651: 86-93.
[105]
Marinakis E, Bagkos G, Piperi C, Roussou P, Diamanti-Kandarakis E. Critical role of RAGE in lung physiology and tumorigenesis a potential target of therapeutic intervention? Clin Chem Lab Med 2014; 52: 189-200.
[106]
Palanissami G, Paul SFD. RAGE and its ligands: Molecular interplay between glycation, inflammation, and hallmarks of cancer-a review. Horm Cancer 2018; 9: 295-325.
[107]
Leclerc E, Vetter SW. The role of S100 proteins and their receptor RAGE in pancreatic cancer. Biochim Biophys Acta 2015; 1852: 2706-11.
[108]
Zhang QY, Wu LQ, Zhang T, Han YF, Lin X. Autophagy-mediated HMGB1 release promotes gastric cancer cell survival via RAGE activation of extracellular signal-regulated kinases 1/2. Oncol Rep 2015; 33: 1630-8.
[109]
Taguchi A, Blood DC, del Toro G, et al. Blockade of RAGE–amphoterin signaling suppresses tumour growth and metastases. Nature 2000; 405: 354-60.
[110]
Radia AM, Yaser AM, Ma X, et al. Specific siRNA targeting receptor for advanced glycation end products (RAGE) decreases proliferation in human breast cancer cell lines. Int J Mol Sci 2013; 14: 7959-78.
[111]
Hardaway AL, Podgorski I. IL-1β, RAGE and FABP4: targeting the dynamic trio in metabolic inflammation and related pathologies. Future Med Chem 2013; 5: 1089-108.
[112]
Matsubara D, Niki T, Ishikawa S, et al. Differential expression of S100A2 and S100A4 in lung adenocarcinomas: clinicopathological significance, relationship to p53 and identification of their target genes. Cancer Sci 2005; 96: 844-57.
[113]
Lin J, Yang Q, Wilder PT, Carrier F, Weber DJ. The calcium-binding protein S100B down-regulates p53 and apoptosis in malignant melanoma. J Biol Chem 2010; 285: 27487-98.
[114]
Stav D, Bar I, Sandbank J. Usefulness of CDK5RAP3, CCNB2, and RAGE genes for the diagnosis of lung adenocarcinoma. Int J Biol Markers 2007; 22: 108-13.
[115]
Bartling B, Hofmann HS, Weigle B, Silber RE, Simm A. Down-regulation of the receptor for advanced glycation end-products (RAGE) supports non-small cell lung carcinoma. Carcinogenesis 2005; 26: 293-301.
[116]
Kobayashi S, Kubo H, Suzuki T, et al. Endogenous secretory receptor for advanced glycation end products in non-small cell lung carcinoma. Am J Respir Crit Care Med 2007; 175: 184-9.
[117]
Stav D, Bar I, Sandbank J. Usefulness of CDK5RAP3, CCNB2, and RAGE genes for the diagnosis of lung adenocarcinoma. Int J Biol Markers 2007; 22: 108-13.
[118]
Bartling B, Demling N, Silber RE, Simm A. Proliferative stimulus of lung fibroblasts on lung cancer cells is impaired by the receptor for advanced glycation end-products. Am J Respir Cell Mol Biol 2006; 34: 83-91.
[119]
Miyazaki N, Abe Y, Oida Y, et al. Poor outcome of patients with pulmonary adenocarcinoma showing decreased E-cadherin combined with increased S100A4 expression. Int J Oncol 2006; 28: 1369-74.
[120]
Zhang YB, He FL, Fang M, et al. Increased expression of Toll-like receptors 4 and 9 in human lung cancer. Mol Biol Rep 2009; 361: 1475-81.
[121]
Jing R, Cui M, Wang J, Wang H. Receptor for advanced glycation end products (RAGE) soluble form (sRAGE) a new biomarker for lung cancer. Neoplasma 2010; 57: 55-61.
[122]
Blondonnet R, Audard J, Belville C, et al. RAGE inhibition reduces acute lung injury in mice. Sci Rep 2017; 7: 7208.
[123]
Lee S, Piao C, Kim G, et al. Production and application of HMGB1 derived recombinant RAGE-antagonist peptide for anti-inflammatory therapy in acute lung injury. Eur J Pharm Sci 2018; 114: 275-84.