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Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

A Differential Protein Study on Bronchoalveolar Lavage Fluid at Different Stages of Silicosis

Author(s): Xiaoxuan Zhang, Ke Han, Linhui Kan, Zheng Zhang, Yihong Gong, Shuyu Xiao, Yuping Bai, Nan Liu, Chunyan Meng, Huisheng Qi* and Fuhai Shen*

Volume 27, Issue 16, 2024

Published on: 01 January, 2024

Page: [2366 - 2401] Pages: 36

DOI: 10.2174/0113862073260760231023055036

Price: $65

Abstract

Objectives: In this study, by comparing the difference in protein expression in bronchoalveolar lavage fluid between silicosis patients in different stages and healthy controls, the pathogenesis of pneumoconiosis was discussed, and a new idea for the prevention and treatment of pneumoconiosis was provided.

Methods: The lung lavage fluid was pretreated by 10 K ultrafiltration tube, Agilent 1100 conventional liquid phase separation, strong cation exchange column (SCX) HPLC pre-separation, and C18 reverse phase chromatography desalting purification, and protein was labeled with isotope. GO, KEGG pathway, and PPI analysis of differential proteins were conducted by bioinformatics, and protein types and corresponding signal pathways were obtained.

Results: Thermo Q-Exactive mass spectrometry identified 943 proteins. T-test analysis was used to evaluate the different significance of the results, and the different protein of each group was obtained by screening with the Ratio≥1.2 or Ratio≤0.83 and P<0.05. We found that there are 16 kinds of protein throughout the process of silicosis. There are different expressions of protein in stages III/control, stages II/control, stage I/control, stages III/ stages II, stages III/ stage I and stages II/ stage I groups. The results of ontology enrichment analysis of total differential protein genes show that KEGG pathway enrichment analysis of differential protein suggested that there were nine pathways related to silicosis.

Conclusion: The main biological changes in the early stage of silicosis are glycolysis or gluconeogenesis, autoimmunity, carbon metabolism, phagocytosis, etc., and microfibril-associated glycoprotein 4 may be involved in the early stage of silicosis. The main biological changes in the late stage of silicosis are autoimmunity, intercellular adhesion, etc. Calcium hippocampus binding protein may participate in the biological changes in the late stage of silicosis. It provides a new idea to understand the pathogenesis of silicosis and also raises new questions for follow-up research.

Graphical Abstract

[1]
Leung, C.C.; Yu, I.T.S.; Chen, W. Silicosis. Lancet, 2012, 379(9830), 2008-2018.
[http://dx.doi.org/10.1016/S0140-6736(12)60235-9] [PMID: 22534002]
[2]
Güngen, A.C.; Aydemir, Y.; Çoban, H.; Düzenli, H.; Tasdemir, C. Lung cancer in patients diagnosed with silicosis should be investigated. Respir. Med. Case Rep., 2016, 18, 93-95.
[http://dx.doi.org/10.1016/j.rmcr.2016.04.011] [PMID: 27330963]
[3]
Poinen-Rughooputh, S.; Rughooputh, M.S.; Guo, Y.; Rong, Y.; Chen, W. Occupational exposure to silica dust and risk of lung cancer: an updated meta-analysis of epidemiological studies. BMC Public Health, 2016, 16(1), 1137.
[http://dx.doi.org/10.1186/s12889-016-3791-5] [PMID: 27814719]
[4]
Jessop, F.; Hamilton, R.F.; Rhoderick, J.F.; Shaw, P.K.; Holian, A. Autophagy deficiency in macrophages enhances NLRP3 inflammasome activity and chronic lung disease following silica exposure. Toxicol. Appl. Pharmacol., 2016, 309, 101-110.
[http://dx.doi.org/10.1016/j.taap.2016.08.029] [PMID: 27594529]
[5]
Kawasaki, H. A mechanistic review of silica-induced inhalation toxicity. Inhal. Toxicol., 2015, 27(8), 363-377.
[http://dx.doi.org/10.3109/08958378.2015.1066905] [PMID: 26194035]
[6]
Lee, S.; Hayashi, H.; Mastuzaki, H.; Kumagai-Takei, N.; Otsuki, T. Silicosis and autoimmunity. Curr. Opin. Allergy Clin. Immunol., 2017, 17(2), 78-84.
[http://dx.doi.org/10.1097/ACI.0000000000000350] [PMID: 28177948]
[7]
Luna-Gomes, T.; Santana, P.T.; Coutinho-Silva, R. Silica-induced inflammasome activation in macrophages: Role of ATP and P2X7 receptor. Immunobiology, 2015, 220(9), 1101-1106.
[http://dx.doi.org/10.1016/j.imbio.2015.05.004] [PMID: 26024943]
[8]
Cordeiro, C.; Jones, J.; Alfaro, T.; Ferreira, A. Bronchoalveolar lavage in occupational lung diseases. Semin. Respir. Crit. Care Med., 2007, 28(5), 504-513.
[http://dx.doi.org/10.1055/s-2007-991523] [PMID: 17975778]
[9]
Jacobs, J.A.; Stobberingh, E.E.; Cornelissen, E.I.M.; Drent, M. Detection of Streptococcus pneumoniae antigen in bronchoalveolar lavage fluid samples by a rapid immunochromatographic membrane assay. J. Clin. Microbiol., 2005, 43(8), 4037-4040.
[http://dx.doi.org/10.1128/JCM.43.8.4037-4040.2005] [PMID: 16081947]
[10]
Wang, K.; Huang, C.; Nice, E. Recent advances in proteomics: Towards the human proteome. Biomed. Chromatogr., 2014, 28(6), 848-857.
[http://dx.doi.org/10.1002/bmc.3157] [PMID: 24861753]
[11]
American Thoracic Society Committee of the Scientific Assembly on Environmental and Occupational Health. Adverse effects of crystalline silica exposure. Am. J. Respir. Crit. Care Med., 1997, 155(2), 761-768.
[http://dx.doi.org/10.1164/ajrccm.155.2.9032226] [PMID: 9032226]
[12]
Forbess, L.J.; Rossides, M.; Weisman, M.H.; Simard, J.F. New-onset non-infectious pulmonary manifestations among patients with systemic lupus erythematosus in Sweden. Arthritis Res. Ther., 2019, 21(1), 48.
[http://dx.doi.org/10.1186/s13075-018-1804-8] [PMID: 30728079]
[13]
Lucas, C.D.; Amft, N.; Reid, P.T. Systemic lupus erythematosus complicating simple silicosis. Occup. Med., 2014, 64(5), 387-390.
[http://dx.doi.org/10.1093/occmed/kqu060] [PMID: 24919786]
[14]
Costallat, L.T.L.; De Capitani, E.M.; Zambon, L. Pulmonary silicosis and systemic lupus erythematosus in men: a report of two cases. Joint Bone Spine, 2002, 69(1), 68-71.
[http://dx.doi.org/10.1016/S1297-319X(01)00344-X] [PMID: 11858360]
[15]
Shtraichman, O.; Blanc, P.D.; Ollech, J.E.; Fridel, L.; Fuks, L.; Fireman, E.; Kramer, M.R. Outbreak of autoimmune disease in silicosis linked to artificial stone. Occup. Med., 2015, 65(6), 444-450.
[http://dx.doi.org/10.1093/occmed/kqv073] [PMID: 26070814]
[16]
Ricklin, D.; Reis, E.S.; Mastellos, D.C.; Gros, P.; Lambris, J.D. Complement component C3 – The “Swiss Army Knife” of innate immunity and host defense. Immunol. Rev., 2016, 274(1), 33-58.
[http://dx.doi.org/10.1111/imr.12500] [PMID: 27782325]
[17]
Tralau, T.; Meyer-Hoffert, U.; Schröder, J.M.; Wiedow, O. Human leukocyte elastase and cathepsin G are specific inhibitors of C5a-dependent neutrophil enzyme release and chemotaxis. Exp. Dermatol., 2004, 13(5), 316-325.
[http://dx.doi.org/10.1111/j.0906-6705.2004.00145.x] [PMID: 15140022]
[18]
Yang, J.; Roe, S.M.; Cliff, M.J.; Williams, M.A.; Ladbury, J.E.; Cohen, P.T.W.; Barford, D. Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. EMBO J., 2005, 24(1), 1-10.
[http://dx.doi.org/10.1038/sj.emboj.7600496] [PMID: 15577939]
[19]
Shang, Y.; Xu, X.; Duan, X.; Guo, J.; Wang, Y.; Ren, F.; He, D.; Chang, Z. Hsp70 and Hsp90 oppositely regulate TGF-β signaling through CHIP/Stub1. Biochem. Biophys. Res. Commun., 2014, 446(1), 387-392.
[http://dx.doi.org/10.1016/j.bbrc.2014.02.124] [PMID: 24613385]
[20]
Dong, H.; Le, Y.; Wang, Y.; Zhao, H.; Huang, C.; Hu, Y.; Luo, L.; Wan, X.; Wei, Y.; Chu, Z.; Li, W.; Cai, S. Extracellular heat shock protein 90α mediates HDM-induced bronchial epithelial barrier dysfunction by activating RhoA/MLC signaling. Respir. Res., 2017, 18(1), 111.
[http://dx.doi.org/10.1186/s12931-017-0593-y] [PMID: 28558721]
[21]
Hacker, S.; Lambers, C.; Hoetzenecker, K.; Pollreisz, A.; Aigner, C.; Lichtenauer, M.; Mangold, A.; Niederpold, T.; Zimmermann, M.; Taghavi, S.; Klepetko, W.; Ankersmit, H.J. Elevated HSP27, HSP70 and HSP90 alpha in chronic obstructive pulmonary disease: Markers for immune activation and tissue destruction. Clin. Lab., 2009, 55(1-2), 31-40.
[PMID: 19350847]
[22]
Low, R.B.; Adler, K.B.; Woodcock-Mitchell, J.; Giancola, M.S.; Vacek, P.M. Bronchoalveolar lavage lipids during development of bleomycin-induced fibrosis in rats. Relationship to altered epithelial cell morphology. Am. Rev. Respir. Dis., 1988, 138(3), 709-713.
[http://dx.doi.org/10.1164/ajrccm/138.3.709] [PMID: 2462382]
[23]
Goldmann, T.; Zissel, G.; Watz, H.; Drömann, D.; Reck, M.; Kugler, C.; Rabe, K.F.; Marwitz, S. Human alveolar epithelial cells type II are capable of TGFβ-dependent epithelial-mesenchymal-transition and collagen-synthesis. Respir. Res., 2018, 19(1), 138.
[http://dx.doi.org/10.1186/s12931-018-0841-9] [PMID: 30041633]
[24]
Hao, C.F.; Li, X.F.; Yao, W. Protein expression in silica dust-induced transdifferentiated rats lung fibroblasts. Biomed. Environ. Sci., 2013, 26(9), 750-758.
[PMID: 24099609]
[25]
Zuo, W.; Zhang, T.; Wu, D.Z.A.; Guan, S.P.; Liew, A.A.; Yamamoto, Y.; Wang, X.; Lim, S.J.; Vincent, M.; Lessard, M.; Crum, C.P.; Xian, W.; McKeon, F. p63+Krt5+ distal airway stem cells are essential for lung regeneration. Nature, 2015, 517(7536), 616-620.
[http://dx.doi.org/10.1038/nature13903] [PMID: 25383540]
[26]
Ma, J.; Bishoff, B.; Mercer, R.R.; Barger, M.; Schwegler-Berry, D.; Castranova, V. Role of epithelial-mesenchymal transition (EMT) and fibroblast function in cerium oxide nanoparticles-induced lung fibrosis. Toxicol. Appl. Pharmacol., 2017, 323, 16-25.
[http://dx.doi.org/10.1016/j.taap.2017.03.015] [PMID: 28315692]
[27]
Nica, I.; Stan, M.; Popa, M.; Chifiriuc, M.; Lazar, V.; Pircalabioru, G.; Dumitrescu, I.; Ignat, M.; Feder, M.; Tanase, L.; Mercioniu, I.; Diamandescu, L.; Dinischiotu, A. Interaction of new-developed TiO2-based photocatalytic nanoparticles with pathogenic microorganisms and human dermal and pulmonary fibroblasts. Int. J. Mol. Sci., 2017, 18(2), 249.
[http://dx.doi.org/10.3390/ijms18020249] [PMID: 28125053]
[28]
Maselli, A.; Conti, F.; Alessandri, C.; Colasanti, T.; Barbati, C.; Vomero, M.; Ciarlo, L.; Patrizio, M.; Spinelli, F.R.; Ortona, E.; Valesini, G.; Pierdominici, M. Low expression of estrogen receptor β in T lymphocytes and high serum levels of anti-estrogen receptor α antibodies impact disease activity in female patients with systemic lupus erythematosus. Biol. Sex Differ., 2016, 7(1), 3.
[http://dx.doi.org/10.1186/s13293-016-0057-y] [PMID: 26759713]
[29]
Khawaja, A.A.; Pericleous, C.; Ripoll, V.M.; Porter, J.C.; Giles, I.P. Autoimmune rheumatic disease IgG has differential effects upon neutrophil integrin activation that is modulated by the endothelium. Sci. Rep., 2019, 9(1), 1283.
[http://dx.doi.org/10.1038/s41598-018-37852-5] [PMID: 30718722]
[30]
Brown, J.M.; Archer, A.J.; Pfau, J.C.; Holian, A. Silica accelerated systemic autoimmune disease in lupus-prone New Zealand mixed mice. Clin. Exp. Immunol., 2003, 131(3), 415-421.
[http://dx.doi.org/10.1046/j.1365-2249.2003.02094.x] [PMID: 12605693]
[31]
Peng, B.; Huang, X.; Nakayasu, E.S.; Petersen, J.R.; Qiu, S.; Almeida, I.C.; Zhang, J.Y. Using immunoproteomics to identify alpha-enolase as an autoantigen in liver fibrosis. J. Proteome Res., 2013, 12(4), 1789-1796.
[http://dx.doi.org/10.1021/pr3011342] [PMID: 23458688]
[32]
Bogdanos, D.P.; Gilbert, D.; Bianchi, I.; Leoni, S.; Mitry, R.R.; Ma, Y.; Mieli-Vergani, G.; Vergani, D. Antibodies to soluble liver antigen and alpha-enolase in patients with autoimmune hepatitis. J. Autoimmune Dis., 2004, 1(1), 4.
[http://dx.doi.org/10.1186/1740-2557-1-4] [PMID: 15679947]
[33]
de Vries, J.J.V.; Chang, A.B.; Marchant, J.M. Comparison of bronchoscopy and bronchoalveolar lavage findings in three types of suppurative lung disease. Pediatr. Pulmonol., 2018, 53(4), 467-474.
[http://dx.doi.org/10.1002/ppul.23952] [PMID: 29405664]
[34]
Yip, Y.L.; Lin, W.; Deng, W.; Jia, L.; Lo, K.W.; Busson, P.; Vérillaud, B.; Liu, X.; Tsang, C.M.; Lung, M.L.; Tsao, S.W. Establishment of a nasopharyngeal carcinoma cell line capable of undergoing lytic Epstein–Barr virus reactivation. Lab. Invest., 2018, 98(8), 1093-1104.
[http://dx.doi.org/10.1038/s41374-018-0034-7] [PMID: 29769697]
[35]
Manipadam, M.T.; Sigamani, E.; Chandramohan, J.; Nair, S.; Chacko, G.; Thomas, M.; Mathew, L.G.; Pulimood, S. Lymphomatoid granulomatosis: A case series from South India. Indian J. Pathol. Microbiol., 2018, 61(2), 228-232.
[http://dx.doi.org/10.4103/IJPM.IJPM_471_17] [PMID: 29676363]
[36]
Liu, H.; Cheng, Y.; Yang, J.; Wang, W.; Fang, S.; Zhang, W.; Han, B.; Zhou, Z.; Yao, H.; Chao, J.; Liao, H. BBC3 in macrophages promoted pulmonary fibrosis development through inducing autophagy during silicosis. Cell Death Dis., 2017, 8(3), e2657.
[http://dx.doi.org/10.1038/cddis.2017.78] [PMID: 28277537]
[37]
Hidvegi, T.; Ewing, M.; Hale, P.; Dippold, C.; Beckett, C.; Kemp, C.; Maurice, N.; Mukherjee, A.; Goldbach, C.; Watkins, S.; Michalopoulos, G.; Perlmutter, D.H. An autophagy-enhancingdrug promotes degradation of mutant alpha1-antitrypsin Z and reduceshepatic fibrosis. Science, 2010, 329(5988), 229-232.
[http://dx.doi.org/10.1126/science.1190354]
[38]
Semren, N.; Welk, V.; Korfei, M.; Keller, I.E.; Fernandez, I.E.; Adler, H.; Günther, A.; Eickelberg, O.; Meiners, S. Regulation of 26S proteasome activity in pulmonary fibrosis. Am. J. Respir. Crit. Care Med., 2015, 192(9), 1089-1101.
[http://dx.doi.org/10.1164/rccm.201412-2270OC] [PMID: 26207697]
[39]
Majetschak, M.; Sorell, L.T.; Patricelli, T.; Seitz, D.H.; Knöferl, M.W. Detection and possible role of proteasomes in the bronchoalveolar space of the injured lung. Physiol. Res., 2009, 58(3), 363-372.
[http://dx.doi.org/10.33549/physiolres.931526] [PMID: 18637707]
[40]
Sato, S.; Fujita, N.; Tsuruo, T. Regulation of kinase activity of 3-phosphoinositide-dependent protein kinase-1 by binding to 14-3-3. J. Biol. Chem., 2002, 277(42), 39360-39367.
[http://dx.doi.org/10.1074/jbc.M205141200] [PMID: 12177059]
[41]
Yaffe, M.B.; Rittinger, K.; Volinia, S.; Caron, P.R.; Aitken, A.; Leffers, H.; Gamblin, S.J.; Smerdon, S.J.; Cantley, L.C. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell, 1997, 91(7), 961-971.
[http://dx.doi.org/10.1016/S0092-8674(00)80487-0] [PMID: 9428519]
[42]
Khorrami, A.; Sharif Bagheri, M.; Tavallaei, M.; Gharechahi, J. The functional significance of 14-3-3 proteins in cancer: Focus on lung cancer. Horm. Mol. Biol. Clin. Investig., 2017, 32(3)
[http://dx.doi.org/10.1515/hmbci-2017-0032] [PMID: 28779564]
[43]
Hartert, M.; Senbaklavacin, O.; Gohrbandt, B.; Fischer, B.M.; Buhl, R.; Vahld, C.F. Lung transplantation: A treatment option in end-stage lung disease. Dtsch. Arztebl. Int., 2014, 111(7), 107-116.
[PMID: 24622680]
[44]
Rosengarten, D.; Fox, B.D.; Fireman, E.; Blanc, P.D.; Rusanov, V.; Fruchter, O.; Raviv, Y.; Shtraichman, O.; Saute, M.; Kramer, M.R. Survival following lung transplantation for artificial stone silicosis relative to idiopathic pulmonary fibrosis. Am. J. Ind. Med., 2017, 60(3), 248-254.
[http://dx.doi.org/10.1002/ajim.22687] [PMID: 28145560]
[45]
Hayes, D., Jr; Hayes, K.T.; Hayes, H.C.; Tobias, J.D. Long-term survival after lung transplantation in patients with silicosis and other occupational lung disease. Lung, 2015, 193(6), 927-931.
[http://dx.doi.org/10.1007/s00408-015-9781-z] [PMID: 26267595]
[46]
Joubert, K.D.; Awori Hayanga, J.; Strollo, D.C.; Lendermon, E.A.; Yousem, S.A.; Luketich, J.D.; Ensor, C.R.; Shigemura, N. Outcomes after lung transplantation for patients with occupational lung diseases. Clin. Transplant., 2019, 33(1), e13460.
[http://dx.doi.org/10.1111/ctr.13460] [PMID: 30506808]
[47]
Lalmanach, G.; Saidi, A.; Marchand-Adam, S.; Lecaille, F.; Kasabova, M. Cysteine cathepsins and cystatins: From ancillary tasks to prominent status in lung diseases. Biol. Chem., 2015, 396(2), 111-130.
[http://dx.doi.org/10.1515/hsz-2014-0210] [PMID: 25178906]
[48]
Yoshioka, S.; Mukae, H.; Ishii, H.; Kakugawa, T.; Ishimoto, H.; Sakamoto, N.; Fujii, T.; Urata, Y.; Kondo, T.; Kubota, H.; Nagata, K.; Kohno, S. Alpha-defensin enhances expression of HSP47 and collagen-1 in human lung fibroblasts. Life Sci., 2007, 80(20), 1839-1845.
[http://dx.doi.org/10.1016/j.lfs.2007.02.014] [PMID: 17367817]
[49]
Müller, H.; Nagel, C.; Weiss, C.; Mollenhauer, J.; Poeschl, J. Deleted in malignant brain tumors 1 (DMBT1) elicits increased VEGF and decreased IL-6 production in type II lung epithelial cells. BMC Pulm. Med., 2015, 15(1), 32.
[http://dx.doi.org/10.1186/s12890-015-0027-x] [PMID: 25885541]
[50]
Lee, C.Y.; Hong, J.Y.; Lee, M.G.; Suh, I.B. Identification of 10 candidate biomarkers distinguishing tuberculous and malignant pleural fluid by proteomic methods. Yonsei Med. J., 2017, 58(6), 1144-1151.
[http://dx.doi.org/10.3349/ymj.2017.58.6.1144] [PMID: 29047238]
[51]
Zhou, X.J.; Cheng, F.J.; Zhu, L.; Lv, J.C.; Qi, Y.Y.; Hou, P.; Zhang, H. Association of systemic lupus erythematosus susceptibility genes with IgA nephropathy in a Chinese cohort. Clin. J. Am. Soc. Nephrol., 2014, 9(4), 788-797.
[http://dx.doi.org/10.2215/CJN.01860213] [PMID: 24458077]
[52]
Seto, S.; Tsujimura, K.; Koide, Y. Coronin-1a inhibits autophagosome formation around Mycobacterium tuberculosis-containing phagosomes and assists mycobacterial survival in macrophages. Cell. Microbiol., 2012, 14(5), 710-727.
[http://dx.doi.org/10.1111/j.1462-5822.2012.01754.x] [PMID: 22256790]
[53]
BoseDasgupta, S.; Pieters, J. Coronin 1 trimerization is essential to protect pathogenic mycobacteria within macrophages from lysosomal delivery. FEBS Lett., 2014, 588(21), 3898-3905.
[http://dx.doi.org/10.1016/j.febslet.2014.08.036] [PMID: 25217836]
[54]
Yang, J.; Goetz, D.; Li, J.Y.; Wang, W.; Mori, K.; Setlik, D.; Du, T.; Erdjument-Bromage, H.; Tempst, P.; Strong, R.; Barasch, J. An iron delivery pathway mediated by a lipocalin. Mol. Cell, 2002, 10(5), 1045-1056.
[http://dx.doi.org/10.1016/S1097-2765(02)00710-4] [PMID: 12453413]
[55]
Shields-Cutler, R.R.; Crowley, J.R.; Miller, C.D.; Stapleton, A.E.; Cui, W.; Henderson, J.P. Human metabolome-derived cofactors are required for the antibacterial activity of siderocalin in urine. J. Biol. Chem., 2016, 291(50), 25901-25910.
[http://dx.doi.org/10.1074/jbc.M116.759183] [PMID: 27780864]
[56]
Bao, G.; Clifton, M.; Hoette, T.M.; Mori, K.; Deng, S.X.; Qiu, A.; Viltard, M.; Williams, D.; Paragas, N.; Leete, T.; Kulkarni, R.; Li, X.; Lee, B.; Kalandadze, A.; Ratner, A.J.; Pizarro, J.C.; Schmidt-Ott, K.M.; Landry, D.W.; Raymond, K.N.; Strong, R.K.; Barasch, J. Iron traffics in circulation bound to a siderocalin (Ngal)–catechol complex. Nat. Chem. Biol., 2010, 6(8), 602-609.
[http://dx.doi.org/10.1038/nchembio.402] [PMID: 20581821]
[57]
Holmes, M.A.; Paulsene, W.; Jide, X.; Ratledge, C.; Strong, R.K. Siderocalin (Lcn 2) also binds carboxymycobactins, potentially defending against mycobacterial infections through iron sequestration. Structure, 2005, 13(1), 29-41.
[http://dx.doi.org/10.1016/j.str.2004.10.009] [PMID: 15642259]
[58]
Hoette, T.M.; Clifton, M.C.; Zawadzka, A.M.; Holmes, M.A.; Strong, R.K.; Raymond, K.N. Immune interference in Mycobacterium tuberculosis intracellular iron acquisition through siderocalin recognition of carboxymycobactins. ACS Chem. Biol., 2011, 6(12), 1327-1331.
[http://dx.doi.org/10.1021/cb200331g] [PMID: 21978368]
[59]
Michels, K.; Nemeth, E.; Ganz, T.; Mehrad, B. Hepcidin and host defense against infectious diseases. PLoS Pathog., 2015, 11(8), e1004998.
[http://dx.doi.org/10.1371/journal.ppat.1004998] [PMID: 26291319]
[60]
Wilson, B.R.; Bogdan, A.R.; Miyazawa, M.; Hashimoto, K.; Tsuji, Y. Siderophores in iron metabolism: From mechanism to therapy potential. Trends Mol. Med., 2016, 22(12), 1077-1090.
[http://dx.doi.org/10.1016/j.molmed.2016.10.005] [PMID: 27825668]
[61]
Jindal, H.K.; Vishwanatha, J.K. Functional identity of a primer recognition protein as phosphoglycerate kinase. J. Biol. Chem., 1990, 265(12), 6540-6543.
[http://dx.doi.org/10.1016/S0021-9258(19)39179-3] [PMID: 2324090]
[62]
Balamurugan, K. HIF-1 at the crossroads of hypoxia, inflammation, and cancer. Int. J. Cancer, 2016, 138(5), 1058-1066.
[http://dx.doi.org/10.1002/ijc.29519] [PMID: 25784597]
[63]
Lokmic, Z.; Musyoka, J.; Hewitson, T.D.; Darby, I.A. Hypoxia and hypoxia signaling in tissue repair and fibrosis. Int. Rev. Cell Mol. Biol., 2012, 296, 139-185.
[http://dx.doi.org/10.1016/B978-0-12-394307-1.00003-5] [PMID: 22559939]
[64]
Zhang, J.; Guo, H.; Zhu, J.S.; Yang, Y.C.; Chen, W.X.; Chen, N.W. Inhibition of phosphoinositide 3-kinase/Akt pathway decreases hypoxia inducible factor-1α expression and increases therapeutic efficacy of paclitaxel in human hypoxic gastric cancer cells. Oncol. Lett., 2014, 7(5), 1401-1408.
[http://dx.doi.org/10.3892/ol.2014.1963] [PMID: 24765145]
[65]
Erdely, A.; Liston, A.; Salmen-Muniz, R.; Hulderman, T.; Young, S.H.; Zeidler-Erdely, P.C.; Castranova, V.; Simeonova, P.P. Identification of systemic markers from a pulmonary carbon nanotube exposure. J. Occup. Environ. Med., 2011, 53(6), S80-S86.
[http://dx.doi.org/10.1097/JOM.0b013e31821ad724] [PMID: 21654424]
[66]
Chan, D.C.; Chen, M.M.; Ooi, E.M.M.; Watts, G.F. An ABC of apolipoprotein C-III: A clinically useful new cardiovascular risk factor? Int. J. Clin. Pract., 2008, 62(5), 799-809.
[http://dx.doi.org/10.1111/j.1742-1241.2007.01678.x] [PMID: 18201179]
[67]
Yao, Z.; Wang, Y. Apolipoprotein C-III and hepatic triglyceride-rich lipoprotein production. Curr. Opin. Lipidol., 2012, 23(3), 206-212.
[http://dx.doi.org/10.1097/MOL.0b013e328352dc70] [PMID: 22510806]
[68]
Royle, S.J.; Bright, N.A.; Lagnado, L. Clathrin is required for the function of the mitotic spindle. Nature, 2005, 434(7037), 1152-1157.
[http://dx.doi.org/10.1038/nature03502] [PMID: 15858577]
[69]
Booth, D.G.; Hood, F.E.; Prior, I.A.; Royle, S.J.A. TACC3/ch-TOG/clathrin complex stabilises kinetochore fibres by inter-microtubule bridging. EMBO J., 2011, 30(5), 906-919.
[http://dx.doi.org/10.1038/emboj.2011.15] [PMID: 21297582]
[70]
Cheeseman, L.P.; Harry, E.F.; McAinsh, A.D.; Prior, I.A.; Royle, S.J. Specific removal of TACC3/ch-TOG/clathrin at metaphase deregulates kinetochore fiber tension. J. Cell Sci., 2013, 126(Pt 9), jcs.124834.
[http://dx.doi.org/10.1242/jcs.124834] [PMID: 23532825]
[71]
Vergés, M.; Luton, F.; Gruber, C.; Tiemann, F.; Reinders, L.G.; Huang, L.; Burlingame, A.L.; Haft, C.R.; Mostov, K.E. The mammalian retromer regulates transcytosis of the polymeric immunoglobulin receptor. Nat. Cell Biol., 2004, 6(8), 763-769.
[http://dx.doi.org/10.1038/ncb1153] [PMID: 15247922]
[72]
Tabuchi, M.; Yanatori, I.; Kawai, Y.; Kishi, F. Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J. Cell Sci., 2010, 123(5), 756-766.
[http://dx.doi.org/10.1242/jcs.060574] [PMID: 20164305]
[73]
Mölleken, C.; Poschmann, G.; Bonella, F.; Costabel, U.; Sitek, B.; Stühler, K.; Meyer, H.E.; Schmiegel, W.H.; Marcussen, N.; Helmer, M.; Nielsen, O.; Hansen, S.; Schlosser, A.; Holmskov, U.; Sorensen, G.L. MFAP4: A candidate biomarker for hepatic and pulmonary fibrosis? Sarcoidosis Vasc. Diffuse Lung Dis., 2016, 33(1), 41-50.
[PMID: 27055835]
[74]
Holm, A.T.; Wulf-Johansson, H.; Hvidsten, S.; Jorgensen, P.T.; Schlosser, A.; Pilecki, B.; Ormhøj, M.; Moeller, J.B.; Johannsen, C.; Baun, C.; Andersen, T.; Schneider, J.P.; Hegermann, J.; Ochs, M.; Götz, A.A.; Schulz, H.; de Angelis, M.H.; Vestbo, J.; Holmskov, U.; Sorensen, G.L. Characterization of spontaneous air space enlargement in mice lacking microfibrillar-associated protein 4. Am. J. Physiol. Lung Cell. Mol. Physiol., 2015, 308(11), L1114-L1124.
[http://dx.doi.org/10.1152/ajplung.00351.2014] [PMID: 26033354]
[75]
Johansson, S.L.; Roberts, N.B.; Schlosser, A.; Andersen, C.B.; Carlsen, J.; Wulf-Johansson, H.; Sækmose, S.G.; Titlestad, I.L.; Tornoe, I.; Miller, B.; Tal-Singer, R.; Holmskov, U.; Vestbo, J.; Sorensen, G.L. Microfibrillar-associated protein 4: A potential biomarker of chronic obstructive pulmonary disease. Respir. Med., 2014, 108(9), 1336-1344.
[http://dx.doi.org/10.1016/j.rmed.2014.06.003] [PMID: 25022422]
[76]
Pilecki, B.; Schlosser, A.; Wulf-Johansson, H.; Trian, T.; Moeller, J.B.; Marcussen, N.; Aguilar-Pimentel, J.A.; de Angelis, M.H.; Vestbo, J.; Berger, P.; Holmskov, U.; Sorensen, G.L. Microfibrillar-associated protein 4 modulates airway smooth muscle cell phenotype in experimental asthma. Thorax, 2015, 70(9), 862-872.
[http://dx.doi.org/10.1136/thoraxjnl-2014-206609] [PMID: 26038533]
[77]
Schlosser, A.; Pilecki, B.; Hemstra, L.E.; Kejling, K.; Kristmannsdottir, G.B.; Wulf-Johansson, H.; Moeller, J.B.; Füchtbauer, E.M.; Nielsen, O.; Kirketerp-Møller, K.; Dubey, L.K.; Hansen, P.B.L.; Stubbe, J.; Wrede, C.; Hegermann, J.; Ochs, M.; Rathkolb, B.; Schrewe, A.; Bekeredjian, R.; Wolf, E.; Gailus-Durner, V.; Fuchs, H.; Hrabě de Angelis, M.; Lindholt, J.S.; Holmskov, U.; Sorensen, G.L. MFAP4 promotes vascular smooth muscle migration, proliferation and accelerates neointima formation. Arterioscler. Thromb. Vasc. Biol., 2016, 36(1), 122-133.
[http://dx.doi.org/10.1161/ATVBAHA.115.306672] [PMID: 26564819]
[78]
Schlosser, A.; Thomsen, T.; Shipley, J.M.; Hein, P.W.; Brasch, F.; Tornøe, I.; Nielsen, O.; Skjødt, K.; Palaniyar, N.; Steinhilber, W.; McCormack, F.X.; Holmskov, U. Microfibril-associated protein 4 binds to surfactant protein A (SP-A) and colocalizes with SP-A in the extracellular matrix of the lung. Scand. J. Immunol., 2006, 64(2), 104-116.
[http://dx.doi.org/10.1111/j.1365-3083.2006.01778.x] [PMID: 16867155]
[79]
Tang, W.; Morey, L.M.; Cheung, Y.Y.; Birch, L.; Prins, G.S.; Ho, S. Neonatal exposure to estradiol/bisphenol A alters promoter methylation and expression of Nsbp1 and Hpcal1 genes and transcriptional programs of Dnmt3a/b and Mbd2/4 in the rat prostate gland throughout life. Endocrinology, 2012, 153(1), 42-55.
[http://dx.doi.org/10.1210/en.2011-1308] [PMID: 22109888]
[80]
Wang, W.; Zhong, Q.; Teng, L.; Bhatnagar, N.; Sharma, B.; Zhang, X.; Luther, W., II; Haynes, L.P.; Burgoyne, R.D.; Vidal, M.; Volchenboum, S.; Hill, D.E.; George, R.E. Mutations that disrupt PHOXB interaction with the neuronal calcium sensor HPCAL1 impede cellular differentiation in neuroblastoma. Oncogene, 2014, 33(25), 3316-3324.
[http://dx.doi.org/10.1038/onc.2013.290] [PMID: 23873030]
[81]
Zhang, D.; Liu, X.; Xu, X.; Xu, J.; Yi, Z.; Shan, B.; Liu, B. HPCAL 1 promotes glioblastoma proliferation via activation of Wnt/β‐catenin signalling pathway. J. Cell. Mol. Med., 2019, 23(5), 3108-3117.
[http://dx.doi.org/10.1111/jcmm.14083] [PMID: 30843345]

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